Obligate symbionts of arthropods, attached by a holdfast structure to
the
lining of the hindgut, midgut, or foregut. Thalli simple or branched,
vegetative parts coenocytic or uninucleate, septate or nonseptate.
Reproducing
asexually by sporangiospores, deciduous appendaged sporangia
(trichospores),
arthrospores, or sexually by biconical zygospores.
Consisting of the orders Harpellales, Asellariales, Eccrinales. [The
protozoan order Amoebidiales, whose species live in the hindgut or on
the
exoskeleton of insects and crustaceans (producing sporangiospores
and/or
amoeboid cells and cystospores), are also treated in this chapter.]
Lichtwardt & Manier, 1978
Thalli unbranched or branched, producing basipetal series of trichospores. Zygospores biconical. Attached to the gut lining of aquatic larvae of Insecta or (rarely) Isopoda.
Consisting of the families Harpellaceae and Legeriomycetaceae.
The ordinal name was first used, but not validly published, by
Duboscq,
Léger, and Tuzet in 1948, and included two families of unbranched
Trichomycetes,
the Harpellaceae and Palavasciaceae. The latter family is now
considered to
belong to the Eccrinales. The first use of the name Harpellales in the
present
sense was by Manier (1962b), but she did not formally establish the
order at
that time.
Léger
& Duboscq,
1929, ex P.M. Kirk & P.F. Cannot, 2007
Thalli unbranched, attached to the peritrophic membrane (or rarely to the hindgut lining) of the host. Five genera.
Type genus: Harpella Léger & Duboscq.
Carouxella
Manier, Rioux & Whisler ex Manier & Lichtwardt, 1969 (1968)
[ = Carouxella Manier, Rioux & Whisler, 1961, nom. nud.]
Modified trichospores remain attached to generative cells, which disarticulate like arthrospores. Zygospores attached at one pole. On peritrophic membrane or hindgut cuticle of larval Ceratopogonidae (Diptera). Three species.
Type species: Carouxella scalaris Manier, Rioux & Whisler ex Manier & Lichtwardt.
The original publication by Manier et al. (1961) had neither a Latin
diagnosis nor a type for the species. These same authors in 1965
provided a
genus-species description in Latin. The genus and species were
validated by
Manier and Lichtwardt in 1969 by citing a nomenclatural type (Art. 37).
Carouxella coemeteriensis Lichtwardt, López Lastra & Ferrington, 1999
Unbranched thalli attached to hindgut cuticle, up to 800 µm long by about 7 µm diam, base not incurved. Producing generative cells that do not easily disarticulate. Trichospores short-cylindrical with a slight median bulge, 27-38 x 5.5-7.5 µm, remaining attached to generative cell.
Illustrations: Fig. 11.58.
Host: Dasyhelea necrophila Spinelli & Rodríguez (Diptera, Ceratopogonidae).
Distribution: Buenos Aires Province, Argentina
The ceratopogonid hosts were found in flower vases in the La Plata cemetery. The host was a new species of Dasyhelea, the only genus known to harbor Carouxella spp.
Reference: Lichtwardt et al., 1999.
Carouxella
scalaris Manier, Rioux &
Whisler ex Manier & Lichtwardt, 1969 (1968)
[= Carouxella scalaris Manier, Rioux & Whisler, 1961, nom.
nud.]
Thalli unbranched, attached to the peritrophic membrane by a holdfast located inside the incurved basal cell. Producing 5-30 generative cells from which develop cylindrical trichospores slightly swollen in the middle, 25-(32)-37 µm long by 4.5-(5.3)-7 µm diam. Trichospores remain attached to the disarticulated generative cells. Appendages unknown. Scalariform conjugation of two thalli gives rise to elongate-pyriform zygospores, 35 x 5.7 µm, attached at the broader end and produced laterally from one of the conjugated pairs. Type species.
Illustrations: Fig. 11.1; Fig. 11.2; Fig. 11.3.
Host: On peritrophic membrane or hindgut cuticle of aquatic larvae of Dasyhelea lithotelmatica Strenzk and Dasyhelea sp. (Diptera, Ceratopogonidae) living in troughs, potholes, and rocky fissures containing algae and decomposing vegetation.
Distribution: Departments of Hérault and Pyrénées-Orientales, France; New South Wales, Australia.
The disarticulating generative cell-trichospore unit of this unusual species has a remarkable resemblance to the arthrospores of Asellaria ligiae with their subsequently developing trichospore-like outgrowths (Manier, 1969b; Lichtwardt, 1973a). This reproductive unit in C. scalaris is apparently the primary means of dissemination from host to host. In their original paper of 1961, in which the species was invalidly published, Manier et al. suggested that the released generative cell-trichospore units (diaspores) may also develop in situ without passing out of the gut. Thalli producing trichospores and zygospores simultaneously have been observed. The zygospores are similar to those of Zygopolaris (Type IV).
According to Manier et al. (1961), the peritrophic membrane of Dasyhelea lithotelmatica extends well into the hindgut, and the thalli of C. scalaris attach to the membrane in the region of the Malphighian tubules and develop within the anterior hindgut. Lichtwardt in 1983 (unpublished) collected larvae of an unnamed and probably endemic species of Dasyhelea (not D. lithotelmatica) in potholes along the Georges River south of Sydney, Australia. Some of these larvae were infested with a fungus identical to C. scalaris, but reproducing only asexually. The Australian C. scalaris was attached to the hindgut cuticle, and not to the peritrophic membrane. Some of these larvae, like Dasyhelea spp. in France, also had Smittium culisetae growing in the hindgut. Another point to note is that Manier (1969b, p. 642) stated that D. lithotelmatica is a carnivore, a questionable statement which we have not been able to confirm in the literature. The Australian Dasyhelea sp. larvae were clearly feeding on algae, and gave no indication of predaceousness or of having had a carnivorous diet.
References: Manier et al., 1961; Manier et al., 1965; Manier and
Lichtwardt,
1968 (1969); Lichtwardt, 1973a; Manier, 1969b (1970b).
Harpella
Léger & Duboscq, 1929
Cylindrical trichospores curved to coiled, sometimes straight, without a collar; appendages (3-)4. Biconical zygospores attached perpendicularly to zygosporophores, which arise from one of the two conjugated cells. On peritrophic membrane of larval Simuliidae (Diptera). Five species.
Type species: Harpella melusinae Léger & Duboscq.
Harpella amazonica Ríos-Velásquez, Lichtwardt, Hamada & Alencar, 2003
Narrow and short thalli, about 104-150 µm long by 3-4 µm diam. Base rounded with holdfast less diameter than the thallus. Curved to almost coiled trichospores 33-52 x 3-4 µm, with about 4 very fine appendages. Thalli producing very few trichospores (only 2-3 per thallus). Zygospores unknown.
Illustration: Fig. 11.256.
Host: Simulium rorotaense Floch & Abonnenc larvae.
Distribution: Amazonas, Brazil. Dominican Republic.
Reference: Alencar, Ríos-Velásquez, Lichtwardt, and Hamada,
2003. Valle and Cafaro, 2010.
Harpella
asiana Hapsari, M.M. White, & K.D. Hyde, 2009
Thalli unbranched, slightly curved or straight, 125-250 x 4-5 µm
long and 4-5 µm in diameter. Attached to the peritrophic matrix with a
tapered secreted holdfast structure. Thalli producing 2 to 4
generative cells, each producing one curved to tightly coiled
trichospore (50-75 x 4-5 µm). Four helical appendages seen through the
thallus prior to detachment.
Illustration: Fig. 11.360.
Host: Simuliidae larvae.
Distribution: Thailand.
Reference: Hapsari et al., 2008.
Harpella leptosa Lichtwardt & Moss, 1980 (in Moss
and
Lichtwardt, 1980)
Immature thalli often sinuous. Mature thalli 250-450 µm long and 4-6 µm wide, producing 2-5 coiled or curved trichospores 110-150 µm long and 4.5 µm diam with 3 (or 4) appendages. Basal generative cell tapered only immediately above the short holdfast. Zygospores unknown.
Illustrations: Fig. 11.192.
Hosts: On peritrophic membrane of aquatic (lotic) larvae of Simuliidae (Diptera), including Simulium canonicolum (Dyar & Shannon) and S. venustum complex, among other Simuliidae..
Distribution: Northwest Montana, Idaho, USA.
The smaller dimensions of the thalli and spores, as well as the more abrupt tapering of the thallus base just above the short holdfast, distinguish Harpella leptosa from the much more common and widespread type species, H. melusinae. Electron micrographs have shown that there are considerable differences in the fine structure of the trichospore appendages and the holdfasts of the two species, but the light microscope is sufficient for identification. A few individual larvae have been found with both species attached simultaneously to the hosts' peritrophic membrane. It is probable that H. leptosa is more widely distributed geographically than the present records indicate. No zygospores have been found in H. leptosa, although conjugations between thalli have been seen. Trichospores with 3 appendages have been observed, but it is possible the normal number is 4.
Reference: Moss and Lichtwardt, 1980. Beach and White, 2012.
Harpella melusinae Léger & Duboscq, 1929b
Thalli slightly arched or undulate, up to 750 µm long and 6-10 µm, diam, narrowing at the base to form a tapered holdfast that flares at the area of contact with the peritrophic membrane. Trichospores curved to tightly coiled, occasionally straight, 2-10 per thallus, approximately 150 µm long and as wide as the thallus, with 4 very finely transversely banded appendages. Biconical zygospores attached medially and perpendicularly to zygosporophores, which arise from one of the conjugants opposite the zone of conjugation. Zygospores 38-97 µm long by 10-15 µm diam. Zygosporophore 16-25 x 9-15 µm. Type species.
Illustrations: Fig.. 7.9; Fig. 7.10; Fig. 7.17; Fig. 11.1; Fig. 11.2; Fig. 11.4.
Hosts: On peritrophic membrane of many species of aquatic (lotic) larvae of Simuliidae (Diptera). Host genera include Simulium, Prosimulium, Austrosimulium, and Cnephia.
Distribution: Probably worldwide wherever Simuliidae occur. Reports
(some
unpublished) include lotic stations throughout the USA; eastern Canada
(Newfoundland, Labrador, Ontario, Prince Edward Island); Europe from
Abisko, Sweden, and
Norway to the
Mediterranean;
England; New Zealand; Australia; and Japan. Armenia, Malasia, Thailand,
China. Mexico.
Harpella melusinae is one of the most widespread species of Harpellales. The authors have found it in the majority of populations of blackflies examined. Although the trichospores are normally curved to coiled, in larvae of some populations they are occasionally perfectly straight. Sometimes mature thalli with straight spores are found side by side with thalli bearing coiled spores. The fine structure of the holdfast is unusual, consisting of a chamber at the base of the thallus that excretes a cementing substance around some finger-like projections or digits (Fig. 7.10B). These digits can be discerned with the light microscope in good preparations. The appendages also are unique: They have a very fine, regularly recurrent banding pattern barely visible with the light microscope, but clearly seen in electron micrographs (Fig. 7.17C). This periodic banding is not found in H. leptosa.
Rarely have zygospores been seen in H. melusinae, perhaps only in about 6 or 7 larvae. Yet, conjugations of thalli are very common in some populations of larvae (see Chapter 7). The length of the zygospores appears to vary considerably, but measurements are based on few specimens. The shorter lengths are measurements of zygospores that developed in water on slide cultures (Lichtwardt, 1967), and may be somewhat abnormal; the more usual length may be 60-95 mm. The side of the biconical zygospore where attachment to the zygosporophore occurs is often flattened. Sometimes the arms of the zygospore are bent slightly toward the zygosporophore. Rizzo and Pang (2005) reported that ovarian cysts attached to simuliid egg masses produced one to multiple outgrowth from whcih developed zygospores measuring 15-20 x 4-6 µm, rather than trichospores as previously reported (Labeyrie et al., 1996; Lichtwardt et al., 2001).
Tuzet and Manier (1955a) once used the name H. melusinae var. eyziesi (nom. nud.) for some specimens they studied, but this was later not recognized as a distinct variety (Manier, 1969b)
References: Léger and Duboscq, 1929b; Léger and Gauthier, 1935b;
Manier,
1950 (1951), 1969b (1970b); Tuzet and Manier, 1955a; Lichtwardt, 1967;
Moss,
1970; Frost and Manier, 1971; Brassard et al., 1971; Reichle and
Lichtwardt,
1972; Crosby, 1974; Moss and Lichtwardt, 1977; Labeyrie, Molloy and
Lichtwardt, 1996, Adler et al., 1996, Takaoka and Adler, 1997,
Lichtwardt, White and Colbo, 2001, White and
Lichtwardt,
2004; White, Siri, and Lichtwardt, 2006, Rizzo and Pang, 2005, Nelder
et al., 2005, Strongman and White, 2008. Strongman, 2007. Valle et al.,
2011. Beach and White, 2012.
Harpella meridianalis Lichtwardt & Arenas, 1996
Thalli about 200-320 mm long by 7-9 µm diam. Base rounded with a broad secreted holdfast. Trichospores curved to coiled, 80-100 x 4-8 µm. Zygospores unknown.
Illustrations: Fig. 11.105.
Hosts: Simulium spp. (Diptera, Simuliidae)
Distribution: Chile, Argentina.
References: Lichtwardt and Arenas, 1996; Lichtwardt et al., 1998;
Lichtwardt
et al., 2000; López Lastra et al., 2005.
Harpella tica Lichtwardt, 1997
Mature thalli 180-380 x 6-9 µm, normally with about 8 generative cells but ranging from 4-46 per thallus. Base rounded with a holdfast about same diameter as the thallus. Trichospores sigmoid, more rarely curved to almost coiled, (98-)130(-140) x 3-4 µm, with 2 or 4 appendages. Zygospores unknown.
Illustrations: Fig. 11.127.
Distribution: Costa Rica, Argentina, Puerto Rico. Dominican
Republic, Mexico. Possibly Thailand.
Hosts: Simuliidae (Diptera).
References: Lichtwardt, 1997; Lichtwardt et al., 1998; White et al., 2000; López Lastra et al., 2005. Valle and Cafaro, 2010. Valle et al., 2011.
Harpella torus Bench &
M.M. White, 2012
Thalli straight to flexuous (325-)430-615(-800) x (6-)7-8(-11) µm,
occasionally intertwining when in proximity. Typically shorer thalli
are straight, whereas longer thalli often flexuous. Basal cell not
evenly tapered, with simple, disk-shaped holdfast offset at base of
thallus. A protuberance develops on the basal cell adjacent to the
hodfast, enlarging as the thallus elongates (to 6 µm) and usually
appearing collapsed in mature thalli. Thalli, producing (5-)11-15 but
with as many as 42, straight to circinate cylindrical trichsores,
(67-)77-95(-124) x (3-)4-5 µm, with four fine appendages. Generative
cells, (8-)18-35(-60) x (6-)8-10(-12) µm, more variable in size when
the thallus produces trichsoore numbers that exceed the typical number.
Zygospores unknown.
Illustrations: Fig. 379.
Distribution: Idaho, USA.
Host: Simuliidae.
Reference: Beach and White, 2012.
Harpellomyces
Lichtwardt & Moss, 1984b
Thalli unbranched, producing distally a series of collarless trichospores with 3 appendages, or conjugating and producing zygospores attached obliquely and submedially to the zygosporophore. Attached to hindgut cuticle, and possibly the peritrophic membrane, of Thaumaleidae (Diptera) larvae. Three species.
Type species: Harpellomyces eccentricus Lichtwardt &
Moss.
Harpellomyces abruptus Lichtwardt, White & Colbo
Thalli 6-7 µm diam, often branched at the base, producing long series of ellipsoidal trichospores 20-33 x 7-11 µm that bear 2-5 appendages upon release. Zygospores unknown.
Illustration: Fig. 11.246.
Host: Thaumalea verralli Edwards (Diptera, Thaumaleidae).
Distribution: Newfoundland and Ontario, Canada.
Reference: Lichtwardt et al., 2001; Strongman and White, 2008.
Harpellomyces
eccentricus Lichtwardt &
Moss, 1984b
Unbranched thalli up to 1 mm or more long, generally 6-8 µm diam, but with segments sometimes as narrow as 1.5 µm diam. Holdfast a short basal disk. Distal fertile tips producing series of a few or up to more than 30 generative cells of variable lengths. Trichospores oval to slightly ovoid, 20-25 x 6-8 µm, attached eccentrically to the generative cell, on release having 3 broad appendages usually 40-60 µm long, sometimes split at their ends. Zygospores biconical, 48-58 x 10-11 µm, attached obliquely and submedially to a zygosporophore 20-30 x 11-12 µm, both remaining together upon release. Type species.
Illustrations: Fig. 11.1; Fig. 11.2; Fig. 11.5.
Hosts: In hindgut of larval Thaumalea sp. and another Thaumaleidae species (Diptera), and possibly growing but not sporulating within the peritrophic membrane of the midgut.
Distribution: In a small stream in northern Sweden, seepy cliffs in Norway, and from seeping waters on a steep coastal cliff in Wales.
This species of Harpellaceae, although unbranched, grows and sporulates in the hindgut of its larval hosts and produces spores only on the distal portion of the thallus, and thus has some characters found in the Legeriomycetaceae.
Reference:
Lichtwardt
and Moss, 1984b; White and Lichtwardt, 2004.
Harpellomyces montanus White, Siri & Lichtwardt, 2006
Thalli branched near the base, producing long series of ellipsoidal trichospores 17-21 x 5.5-7 µm, usually bearing two appendages upon release. Zygospores biconical, 35 x 9.5 µm, attached obliquely and submedially to a zygosporophore 20 x 9.5 µm, both remaining together upon release. In hindgut of Thaumaleidae larvae.
Illustration: Fig. 11.281.Distribution: Great Smoky Mountains National Park, USA.
The distinctive features of Harpellomyces montanus, other than the trichospore dimensions, are the greater branching near the base than other species of this genus, and the fewer appendages (normally two) at the base of trichospores.
Reference: White, Siri and Lichtwardt,
2006.
Thalli
unbranched, often with a sterile basal
cell, attached to the peritrophic matrix of Chironomidae, generative
cells
disarticulating after production of trichospores which remain attached
to their
generative cells. Zygospores biconical, attached medially and at right
angles
to the zygosporophore (Type I, Moss et al. 1975). Monotypic.
Type species: Klastostachys reflexa
Lichtwardt, Williams, & White.
Klastostachys
reflexa Lichtwardt, Williams, & White.
= Stachylina reflexa
Lichtwardt & Williams, 1988
Thalli 80-160 µm long, 8-10 µm diam, attached to the peritrophic membrane of Chironomidae larvae by means of an inconspicuous holdfast. Thalli producing 1-7 generative cells, plus a short (4 µm long) sterile basal cell. Trichospores long ellipsoidal, (21-)33(-41) x (5-)6(-8) µm, without an appendage, remaining attached to their generative cells which disarticulate singly or in units of 2-4. Terminal trichospore typically reflexed, with its axis oriented backward at an angle to the first outgrowth from the terminal generative cell to which the trichospore is attached. Zygospores biconical, 49-55 x 7-8 µm, attached laterally and perpendicularly midway between the poles to a short (4-5 µm long) zygosporophore.
Illustrations: Fig. 11.115.
Host: Cryptochironomus sp. (Diptera, Chironomidae).
Distribution: Colorado USA.
Stachylina reflexa is the only species in the genus that is
known to
produce zygospores. Features that are unusual, in addition to the
production of
zygospores, are the disarticulation of the generative cells with their
trichospores remaining attached (in a manner very similar to the
generative
cells of Carouxella scalaris and the disarticulating
arthrosporesof Asellaria
ligiae), and the sterile cell at the base of the thallus. These
differences
would later warrant the establishment of a new genus, and Lichtwardt,
Williams, and White (2011) made a new combination (basionym Stachylina reflexa).
Stachylina
Léger and Gauthier, 1932
Unbranched thalli cylindrical to fusiform. Trichospores oval to almost biconical, (with or) without a collar, bearing a single appendage. Biconical zygospores [in one species (S. reflexa)] attached perpendicularly to zygosporophore. On peritrophic membrane (base of thallus sometimes penetrating the membrane) of larval Chironomidae and Psychodidae (Diptera). Thirty species.
Type species: Stachylina macrospora Léger & Gauthier.
Stachylina acutobasilaris White & Lichtwardt, 2004
Thalli 78-155 x 10-18 µm, basal cell tapering to a small holdfast, producing 4-8 or more trichospores. Trichospores ellipsoidal with a slight median swelling, without a collar, 15-23 x 5-7 µm.
Illustration: Fig. 11.277.
Host: Brillia cf. longifurca Kieffer larvae (Diptera, Chironomidae).
Distribution: Norway.
Reference: White and Lichtwardt, 2004.
Stachylina ceratopogonidarum Lichtwardt & Arenas, 1996.
Thallus long-fusiform, 90-120 x 6-8 µm, with a small secreted holdfast. Trichospores elongate-ovoid 17-20 x 5-8 µm, without a collar. Zygospores unknown.
Illustrations: Fig. 11.107.
Host: Forcypomyia(?) sp. (Diptera, Ceratopogonidae).
Distribution: Chile.
Reference: Lichtwardt and Arenas, 1996.
Stachylina
chironomidarum Lichtwardt, 1972
Mature thalli usually 180-250 µm long by 4-5 µm diam, attached to peritrophic membrane by an inconspicuous disklike holdfast, producing 2-6 (or more) generative cells that are usually longer than the trichospores. Trichospores long-ellipsoidal, 35-49 x 4-5 µm, with a collar 1-2 mm long and a single appendage. Zygospores unknown.
Illustrations: Fig. 11.191.
Host: On peritrophic membrane of unidentified lentic bloodworms (Diptera, Chironomidae).
Distribution: In a pond near Gothic, Gunnison Co., Colorado, USA.
The very slender, collared trichospores of S. chironomidarum distinguish this Stachylina species from all others.
Reference: Lichtwardt, 1972.
Stachylina dolichospora Ferrington, Hayford & Lichtwardt
Thalli 8-11 µm diam. by more than 400 µm long. Trichospores (78-)93(-108) x 8-10 µm, with a collar about 2 µm long, and a short, stout appendage with a terminal knob.
Illustration: Fig.
11.304.
Host: In hindgut of Riethia sp. larvae (Chironomidae).
Distribution: Tasmania, Australia.
Reference: Ferrington, Lichtwardt, Hayford, and Williams, 2005.
Stachylina euthena Manier & Coste, 1971
Thalli 130-150(-200) mm long by 7-8 µm diam, attached to peritrophic membrane by a small disklike holdfast. Trichospores 8 per thallus, fusiform with a median swelling, 25-35 x 7-8 µm, with an ephemeral collar 2.5-3 µm long and a single prominent appendage. Zygospores unknown.
Illustrations: Fig. 11.203.
Hosts: In Chironomus plumosus complex and Psectrotanypus varius Fabr. larvae (Diptera, Chironomidae) collected in roadside ponds and watering places.
Distribution: Department of Hérault, France, Spain.
Stachylina euthena wasdescribed and illustrated in Coste-Mathiez's 1970 thesis under the name S. chironomi (nom. provis.), priorto its valid publication. The species most closely resembles S. grandispora, but has shorter trichospores.
References: Manier and Coste, 1971; Coste-Mathiez, 1970; Valle, 2007.
Stachylina forantipes Strongman, 2010.
Thalli 35-50 x 6-9 µm, with a small bulbous holdfast
penetrating the peritrophic membrane of the host. Trichospores,
2-4 spores per thallus, ovoid, 17.5-21 x 7-8 µm with a strong medial
swelling, no collar. Zygospores unknown.
Illustration: Fig. 11.372.
Host: Chironomidae larvae.
Stachylina grandispora Lichtwardt, 1972
Mature thalli less than 100 µm to more than 250 µm long by 6-10 µm diam, attached to peritrophic membrane by an inconspicuous holdfast. Trichospores 2-16 (or more) per thallus, long-ellipsoidal, 40-72 x 6-10 (or more) µm, upon release having a collar 1-3 µm long and a single, prominent and very long appendage. Zygospores unknown.
Illustrations: Fig. 11.6; Fig. 11.190.
Hosts: Various lotic or lentic Chironomidae (Diptera) larvae, including species of Tanytarsus, Tendipes, Paratendipes, Polypedilum, Chironomus, and Cricotopus.
Distribution: Several states of the USA, including Great Smoky
Mountains National Park, Idaho, and Hawaii; Canada, England;
Sweden;
Australia; New Zealand. Spain. Dominican Republic, Mexico.
Although the thallial and trichospore lengths are variable, S. grandispora is easily identified by its large collared trichospores and the long appendages measuring up to 200 mm or more in length. The fine structure of the appendage and septum has been studied in this species (Moss, 1972, 1976; Moss and Young, 1977, 1978). Moss (1972) was able to infest species of seven additional chironomid genera by exposing them to naturally infested larvae (see Chapter 6). Conjugations between thalli have been observed (Lichtwardt, 1972; Moss, 1972), but not zygospores.
Lichtwardt in 1983 (unpublished) found S. grandispora growing in the endemic New Zealand bloodworm, Chironomus zealandicus Hudson, as well as in an undetermined species of Chironomus in Queensland, Australia. A bloodworm host species from Hawaii, Chironomus hawaiensis Grimshaw, may be endemic to that island group (Lichtwardt, 1963, unpublished). These data indicate that S. grandispora has a remarkable record of dispersal.
References: Lichtwardt, 1972, 1976;
Moss, 1972,
1974, 1976, 1979; Moss and Young, 1977, 1978; White, Siri and
Lichtwardt, 2006; Valle, 2007, Strongman and White, 2008, Strongman,
2007. Valle and Cafaro, 2010. Strongman, 2010. Valle et al., 2011.
Beach and White, 2012.
Stachylina gravicaudata Siri, White & Lichtwardt, 2006
Thalli about 160-250 µm long by 5-10 µm diameter, bearing 4-8 trichospores, 25-31 x 4-5 µm, with a short collar and one heavy appendage.
Illustration: Fig. 11.251.
Host: Paralauterbornielle sp. (Chironomidae) larvae.
Distribution: Great Smoky Mountains National Park, USA.
This species is distinguished from other Stachylinas by thallial and trichospore sizes, and the heavy trichospore appendages.
Reference: White, Siri & Lichtwardt, 2006.
Stachylina
jujuyensis Mazzucchelli, López
Lastra & Lichtwardt, 2000
(in Lichtwardt, López Lastra and Mazzucchelli, 2000)
Thalli about 10 µm diam with a tapered base and small secreted holdfast. Producing numerous ellipsoidal trichospores measuring 30-37 x 8-9 µm.
Illustrations: Fig. 11.56.
Hosts: Chironomidae (Diptera).
Distribution: Argentina.
Reference: Lichtwardt, López Lastra and Mazzucchelli, 2000
Stachylina lentica White & Lichtwardt, 2004
Thalli 50-150 x 4-9 µm, with a small, rounded holdfast at the base, producing 1-2(-4) trichospores. Trichospores long-ellipsoidal, (22-)35(-50) x (4-)5-6(-7) µm, with a very short collar, and a very long and fine appendage.
Illustration: Fig. 11.278.
Host: Chironomus sp. larvae, and Brillia cf. longifurca Kieffer, Polypedilum sp. Metriocnemus eryngiotelmatus Donato & Paggi larvae (Diptera, Chironomidae).
Distribution: Norway, Argentina.
Reference: White and Lichtwardt, 2004.; Siri,
Marti, and Lopez Lastra, 2008. Siri and Lopez Lastra, 2010.
.
Stachylina litoralis Lichtwardt, White & Colbo
Thalli 135-200 x 10-12 µm, attached to the peritrophic membrane by a slightly bulbous base; 4-8 trichospores produced per thallus, 39-47 x10-12 µm, without a collar.
Illustration: Fig. 11.248.
Host: Telmatogeton japonicus
Tokunaga (Diptera, Chironomidae); Crozetia
seguyi Beaucornu-Saguez & Vernon (Diptera, Simuliidae).
Distribution: Newfoundland, Canada; Crozet Islands (Indian Ocean).
Reference: Lichtwardt et al., 2001; Reeves, Beard & Craig, 2004.
Stachylina longa Léger & Gauthier, 1932
Thalli 100 mm or more long by 9-10 µm diam, bearing 6-8 trichospores 25 x 5-6 µm, without a collar. Zygospores unknown.
Illustration: None available.
Host: On peritrophic membrane of larval Tanytarsus sp. (Diptera, Chironomidae).
Distribution: Alpine streams, France.
Stachylina longa was originally poorly described, along with the type species, S. macrospora, when the genus Stachylina was established. In 1961 Gauthier provided a slightly more complete-but not very satisfactory-description. Neither publication presented illustrations, thus leaving in question the form of the thallial base, trichospore shape, range of trichospore lengths, and other such features. To date this has presented no problem, since all subsequently described species have different trichospore dimensions.
References: Léger and Gauthier, 1932; Gauthier, 1961.
Stachylina lotica Williams & Lichtwardt, 1984
Mature thalli up to 100 µm long by 8-10 µm diam, producing up to 8 trichospores. Holdfast generally with a smaller diameter than the thallus. Trichospores ellipsoidal to subbiconical, 24-32 x 8-10 µm, with appendage up to 10 times spore length, without a collar. Generative cells commonly 8-10 µm long. Zygospores unknown.
Illustration: Fig. 11.6.
Host: On peritrophic membrane of larval Maruina sp. (Diptera, Psychodidae).
Distribution: In stream just south of Glacier National Park,
Montana, USA. Argentina.
This is the only species of Stachylina known in Psychodidae larvae. All other species are in Chironomidae.
Reference: Williams and Lichtwardt, 1984. Siri and Lopez Lastra,
2010.
Stachylina
macrospora Léger &
Gauthier, 1932
[= Stachylina intermedia Poisson, 1936, nom. nud.]
Mature thalli usually 100-200 µm long by 8-10 µm diam, attached to peritrophic membrane by a broad holdfast disk; bearing (2-)4-8 long-ovoid trichospores 40-50 x 7-8 µm, upon release having no collar and a single appendage several times the length of the trichospore. Zygospores unknown. Type species.
Illustrations: Fig. 11.202.
Host: On peritrophic membrane of larval Diamesinae (Diptera, Chironomidae), including Diamesa sp. and Syndiamesa macronyx Kieff.
Distribution: In alpine streams and fountain waters in France; possibly also in streams near Peters Lake and a pond near Barrow, Alaska.
Stachylina macrospora and S. longa were briefly described by Léger and Gauthier in 1932 when they established the new genus Stachylina. Manier and Lichtwardt (1968) selected S. macrospora as the type species, because it was the only species of the two to be illustrated (later) by Léger and Gauthier (1935b). Gauthier in 1961 published a somewhat better description of S. macrospora. The species description above is a slight modification of Gauthier's so as to accommodate Poisson's (1936) description of S. intermedia Poisson (nom. nud.), which appears to be a synonym of S. macrospora (Manier, 1969b; Kobayasi et al., 1969; Lichtwardt, 1972). The original collections were from larvae of Diamesa sp. in alpine streams, presumably near Grenoble, France, whereas Poisson's collections came from larval Syndiamesa macronyx collected in fountains at Besse-en-Chandesse, Puy-de-Dôme, France.
Kobayasi (in Kobayasi et al., 1967, 1969) reported finding S. macrospora in unidentified chironomid larvae in Alaska. But the basal cell of his specimens, as drawn, are tapered and almost pointed, a feature not in accord with either Léger and Gauthier's (1935b) or Poisson's (1936) drawings, which leaves a question as to the correct identification of the Alaskan specimens. Coste-Mathiez (1970) and Manier and Coste (1971) tentatively identified as S. macrospora a Stachylina sp. from larvae of Syncrotopus rufiventris Meig., but it appears from their photomicrographs and descriptions to be some other, peritrophic membrane-penetrating species, and not S. macrospora.
References: Léger and Gauthier, 1932, 1935b; Poisson, 1936;
Gauthier, 1961;
Kobayasi et al., 1967, 1969; Manier, 1969b (1970b); Manier and
Lichtwardt,
1968; Manier and Coste, 1971; Coste-Mathiez, 1970.
Stachylina
magna Indoh, Lichtwardt &
Kobayasi, 1988 (1987)
[in Lichtwardt, Kobayasi and Indoh, 1988 (1987)]
Mature thalli 400-900 µm long, 14-25 µm in diam, producing 40-65 generative cells with 11-18 trichospores attached at one time. Trichospores long ellipsoidal, (30-)56(-80) x (6.5-)11(-15) µm, without a collar. Zygospores unknown.
Illustrations: Fig. 11.145.
Host: Chironomidae (Diptera).
Distribution: Japan. Idaho, USA.
Reference: Lichtwardt, Kobayasi and Indoh, 1987. Beach and White,
2012.
Stachylina manicata Williams & Lichtwardt, 1984
Thalli up to 100 µm long by 6.5-8 µm diam, producing up to 8 trichospores. Holdfast disklike, with a diameter smaller than the thallus. Trichospores ellipsoidal to subbiconical, 17.5-20 x 4.5 µm, with a small sleevelike collar 1-1.5 x 0.5 µm surrounding the single appendage, which narrows toward the distal end and is generally at least 5 times the spore length. Generative cell usually shorter than the trichospore. Zygospores unknown.
Illustration: Fig. 11.6.
Host: On peritrophic membrane of larval Polypedilum sp. and/or Pseudochironomus sp. (Diptera, Chironomidae).
Distribution: In a cattail swamp bordering Flathead Lake, Montana, USA.
Reference: Williams and Lichtwardt, 1984.
Stachylina minima Williams & Lichtwardt, 1990 (in Lichtwardt and Williams, 1990)
Thalli 32-46 x 6-8 µm, with a bulbous base that penetrates the peritrophic membrane, producing 1-4 trichospores. Trichospores ovoid, (11-)14(-18) x 6-8 µm, without a collar. The most distal trichospore produced subterminally. Zygospores unknown.
Illustrations: Fig. 11.143.
Hosts: Orthocladiinae (Diptera, Chironomidae).
Distribution: South Island, New Zealand, Argentina.
Reference: Lichtwardt and Williams, 1990; Lňpez Lastra et al., 2005.
Stachylina
minuta Gauthier ex Lichtwardt,
1984a
[= Stachylina minuta, Gauthier, 1961, nom. nud.]
Fusiform thalli 30-55 µm long by 5-6 µm diam, attached by a bulbous base that penetrates the peritrophic membrane, bearing 1-4 trichospores; terminal cell sterile. Trichospores ellipsoidal, 15-16 x 5-6 µm, produced on a narrow cylindrical outgrowth from the generative cell, upon detachment having a single short appendage and no collar. Zygospores unknown.
Illustrations: Fig. 11.112.
Host: On peritrophic membrane of Tanytarsini larvae (Diptera, Chironomidae).
Distribution: In small streams around Grenoble, France.
Among the distinctive features of Stachylina minuta are the sterile terminal cell or compartment and the long, narrow outgrowth from the generative cell on which the trichospore is produced.
References: Lichtwardt, 1984a; Gauthier, 1961.
Stachylina nana Lichtwardt, 1984a
Thalli cymbiform to fusiform, 60-80 µm long, attached by a small holdfast disk. Producing 2-4 oval to biconical trichospores, (25-)30(-40) x (7-)8.5(-10) µm, with a single ribbon-like (near the base) appendage and no collar. Zygospores unknown.
Illustrations: Fig. 11.200.
Hosts: On peritrophic membrane of unidentified Chironomidae (Diptera).
Distribution: In the Dranse River east of Thonon-les-Bains near Lake
Léman,
France; Ontario and Prince Edward Island, Canada. Thailand. Idaho, USA.
Reference: Lichtwardt, 1984a. Strongman and White, 2008.
Strongman, 2007, Strongman,2010. Beach and White, 2012.
Stachylina paludosa Lichtwardt 1994
Thalli 80-150 x 7-9 µm, producing about 8 generative cells, holdfast 1 x 2 µm. Trichospores long-ellipsoidal with a slight median bulge, 31-40 x 6-8 µm, with a collar about 1 µm long. Zygospores unknown.
Illustrations: Fig. 11.148.
Hosts: Polypedilum sp. and Chironomus sp. (Diptera, Chironomidae).
Distribution: Costa Rica.
Reference: Lichtwardt 1994.
Stachylina paucispora
Lichtwardt, 2003
Thallus fusiform ~70-80 x 6-7 µm. Long-ellipsoidal trichospores 29-40 x
6-8 µm with a single appendage and without a collar. One or two
trichospores per
thallus.
Conjugations of thalli, but zygospores unknown.
Illustration:
Fig. 11.258.
Host: Cricotopus sp. larva (Chironomidae, Orthocladiinae).
Distribution: Amazonas, Brazil. Mexico.
Reference: Alencar, Ríos-Velásquez, Lichtwardt, and Hamada, 2003. Valle
et al., 2011.
Stachylina
pedifer Williams &
Lichtwardt, 1983 (in Lichtwardt and Williams, 1983a).
Host: On peritrophic membrane of larval Boreoheptagyia lurida (Garrett)
(Diptera, Chironomidae) living in fast-flowing streams; bloodworm
(Chironomidae).
Distribution: In and near Glacier National Park, Montana, Oconce
County in South Carolina, and Great
Smoky Mountains National Park USA; Ontario and Prince Edward Island,
Canada; Norway, Spain.
Stachylina pedifer occurs in the same host species as Smittium
dimorphum (located in the hindgut). The most noticeable features
of S.
pedifer are the footlike base of the thallus, which penetrates
through
the peritrophic membrane, and the commonly subapical placement of the
terminal
trichospore. Zygospores were produced by Beard and Adler in the
laboratory by placing peritrophic matrices in Ph 10 KOH BHI medium
Reference: Lichtwardt and Williams, 1983a; White and Lichtwardt,
2004; White, Siri and Lichtwardt, 2006 Beard and Adler, 2003; Valle,
2007, Strongman and White, 2008, Strongman, 2007.
Stachylina penetralis Lichtwardt, 1984a
Thalli 70-180 x 8-10 µm, attached by a bulbous base that penetrates the peritrophic membrane. Producing (2-)4-12 long-ellipsoidal trichospores, 30-50 x 8-12 µm, with a single appendage and no collar. Zygospores unknown.
Illustration: Fig. 11.6.
Host: On peritrophic membrane of Diamesa spp. larvae (Diptera, Chironomidae) and other Chironomidae..
Distribution: In small streams, waterfalls, and a water tank; Island
of
Honshu, Japan, Ontario, Canada, and in French and Swiss Alps. Spain.
Argentina.
Like Stachylina pedifer and S. minuta, the base of the thallus of S. penetralis penetrates the peritrophic membrane of the host. Each of the 3 species, however, is morphologically distinct.
References: Lichtwardt, 1973a, 1984a; Valle, 2007, Strongman and
White, 2008. Siri and Lopez Lastra, 2010.
Stachylina
platensis López Lastra,
Lichtwardt & Ferrington, 1999
(in Lichtwardt, Ferrington and López Lastra, 1999)
Thalli 6-10 µm diam, consisting of 4 to more than 32 generative cells; generative cells may be very short when numerous. Trichospores ellipsoidal with a slight median bulge, 25-36 x 5-7.8 µm, with a very short collar and one appendage that sometimes appears to split into two. Zygospores unknown.
Illustrations: Fig. 11.62.
Host: Chironomus sp. (Chironomidae).
Distribution: Argentina.
Reference: Lichtwardt et al., 1999.
Stachylina prolifica Lichtwardt, Kobayasi & Indoh, 1988 (1987)
Thalli up to 450 µm long by 8-12 µm in diam, producing up to 50 ellipsoidal trichospores 22-36 x 5-5.5 µm without a collar.
Illustrations: Fig. 11.144.
Host: Chironomus sp. (Diptera, Chironomidae).
Distribution: Japan, Spain.
Reference: Lichtwardt et al., 1987; Valle, 2007.
Stachylina
queenslandiae Lichtwardt, 1990
(in Lichtwardt and Williams, 1990)
Thalli 60-100 x 7-8 µm with a bulbous base that penetrates the peritrophic membrane, producing up to 16 trichospores per thallus. Trichospores oval, 20-30 x 8-9 µm, with apical trichospore borne subterminally. Zygospores unknown.
Illustrations: Fig. 11.96.
Host: Orthocladiinae (Diptera, Chironomidae).
Distribution: Queensland, Australia.
Reference: Lichtwardt and Williams, 1990.
Stachylina reflexa Lichtwardt & Williams, 1988
See Klastostachys
reflexa, comb. nov.
Lichtwardt, Williams & White, 2011.
Stachylina robusta Lichtwardt & Williams, 1999
Thallus 12-14 µm diam with a small discoid secreted holdfast, producing 15 or more generative cells. Trichospores ellipsoidal with a slight median bulge, 30-37 x 8-9 µm, collarless. Zygospores unknown.
Illustrations: Fig. 11.111.
Host: Psectrocladius sp. (Chironomidae).
Distribution: Colorado, USA. Spain.
Stachylina stenospora Siri, White and Lichtwardt, 2006
Thalli 4.5-7 µm diameter, producing 1-4 subcylindrical trichospores with a slight median bulge, 42-70 x 4-7 µm, with a short collar. Zygospores unknown.
Illustration: Fig. 11.252.
Host: Larval Phaenopsectra
sp. (Chironomidae).
Distribution: Great Smoky Mountains National Park, USA..
Stachylina stenospora resembles the more common and widespread S. grandispora, but the thalli are narrower as are the trichospores.
Reference: White, Siri and Lichtwardt, 2006.
Stachylina thaumaleidarum Lichtwardt & Williams, 1990
Mature thalli commonly 75-200 µm long, 5-8 µm diam, producing 2-16 generative cells, the terminal one slightly tapered. Trichospores elongate-ovoid, (20-)26(-38) x (5.5-)7(-8) µm, without a collar, the apical trichospore arising subterminally from the generative cell. Zygospores unknown.
Illustrations: Fig. 11.95.
Host: Austrothaumalea sp. (Diptera, Thaumaleidae).
Distribution: Victoria, Australia.
Reference: Lichtwardt and Williams, 1990.
Stachylina
tianensis J. Wang, S.Q. Xu & Strongman, 2010
Thallus 130-350 x 10-15 µm, with a lobulate, bulbous base that penetrates the peritrophic matrix, producing 4-25 trichospores. Trichospores long-ellipsoidal, 55-90 x 7-10 µm, with a single appendage and a short collar, produced on small lateral projections from the generative cell, near a septum. Zygospores unknown. On peritrophic matrix of Chironomidae larvae.
Illustrations: Fig. 11-350
Host: Chironomidae larvae.
Distribution:: Xinjiang, China.
Reference: Wang, Xu, and Strongman, 2010.
Stachylinoides
Ferrington, Lichtwardt & López Lastra, 1999
Unbranched thallus not fertile near basal end, producing trichospores without a collar and with a single appendage. In Chironomidae larvae. Monotypic.
Type species: Stachylinoides arctata Ferrington, Lichtwardt
&
López Lastra, 1999
Stachylinoides
arctata Ferrington, Lichtwardt
& López Lastra, 1999
(in Lichtwardt, Ferrington and López Lastra, 1999).
Unbranched thalli may be more than 800 µm long by 8-10 µm diam. Base of thalli rounded without a discernable secreted holdfast. Trichospores produced on terminal half of thallus, oval, 10-15(-19) x 5-7(-9) µm.
Illustrations: Fig. 11.54.
Hosts: Thienemanniella sp. (Chironomidae).
Distribution: Argentina.
Reference: Lichtwardt et al., 1999.
Pouzar,
1972
= Genistellaceae Léger & Gauthier, 1932
Thalli branched and septate, eucarpic, attached to the hindgut lining of the host. Sixteen genera.
Type genus: Legeriomyces Pouzar (= Genistella Léger & Gauthier, 1932).
Pouzar erected the new family name, Legeriomycetaceae, because the former type genus, Genistella, was a later homonym of Genistella Ortega 1773, a genus that Ortega had assigned to the legume family Papilionaceae Giseke.
Williams & Lichtwardt, 1993
Zygospores (Type I) biconical, formed on a cylindrical
zygosporophore
attached subapically to an extension of one of the conjugants; may be
homothallic. Trichospores subcylindrical with a bulge below midregion,
with a
collarette and single appendage. Allantoid auxiliary spores formed from
generative cells, without an appendage, germinating within same gut
where
formed. In hindgut of Caenidae (Ephemeroptera) nymphs.
Type species: Allantomyces caenidarum Williams &
Lichtwardt.
Allantomyces caenidarum Williams & Lichtwardt, 1993
Trichospores (11-)13(-16) x (2.5-)3(-4)µm,
subcylindrical with a bulge below midregion, with a short and flared
collarette
and single long appendage. Zygospores (34-)42(-46) x (4-)5(-6) µm, upon
release bearing a
cylindrical collar
about 12 x 2 mm. Allantoid
auxiliary
spores (18-)25(-30) x (2.5-)4.5(-5.5) µm. Two species.
Illustrations: Fig. 11.41.
Host: Tasmanocoenis sp. (Ephemeroptera, Caenidae), in silted, slow-flowing streams.
Distribution: Western Australia, Australia.
The most unusual feature of this species is the production of allantoid auxiliary spores that grow from generative cells and which, after release, are capable of germinating within the gut where they were produced, thus increasing the number of thalli endogenously. Normal trichospores and zygospores are also produced.
Reference: Williams and Lichtwardt, 1993.
Allantomyces
zopilotei L.G. Valle, M.M. White, and Cafaro, 2008
Thalli pinnately branched, sometimes with di- and trichotomous
branching at distal ends. Many axis cells 14-20 µm diam at the proximal
end, decreasing to 3 µm at distal branches. Holdfast cell tapered
to a point in young specimens, variable with maturity ranging from
nondifferentiated with a thin holdfast secretion to lobulate, usually
with proximal lateral branches. Trichospores ovate-ellipsoidal to
subcylindrical with a submedial swelling, and a wide range in
lengths, 9-24 x 3.5-5 µm, with an outflared collar 3-5(-7) x 2.5 µm
(sometimes absent), and a single, fine, slightly curled appendage.
Generative cells (1-)4-8 per fertile branch, variable in length.
Zygospores Type I, perpendicular to and straight or slightly bent at
the medial point of attachment, 53-65 x 5.5-7 µm, collarless. A scar is
visible on the released zygospore, where it was attached to the
zygosporophore. Zygosporophore not clearly delimited from the
conjugating hyphae, arranged in a V- (or Y-) shaped pattern, the
zygospore emerging from the vertex of conjugating hyphae. No auxiliary
allantoid spores observed.
Illustrations: Fig. 11.330
Host: Attached to hindgut lining of Tricorythodes sp. (Ephemeroptera,
Leptohyphidae) nymphs.
Distribution: Veracruz, Mexico.
Austrosmittium
Lichtwardt & Williams, 1990
Trichospores oval or ellipsoidal, small (<16 µm long), with a basal collar 1/3-1/2 as long as the spore body, one appendage. Zygospores biconical, but noticeably swollen in the middle, small (<36 µm long), with an oblique collar located at the edge of the medial swelling and one appendage. Thalli branched. In hindgut of Chironomidae (Diptera) larvae. Four species.
Type species: Austrosmittium kiwiorum Williams &
Lichtwardt
Austrosmittium
aussiorum Williams &
Lichtwardt, 1990
(in Lichtwardt and Williams, 1990)
Thalli with 2-6 generative cells producing oval trichospores 11-16 x 5-8 µm, collar 6-7 x 3.5 µm, with a single, coarse appendage. Zygospores biconical with a pronounced median swelling, 20-25 x 6-8 µm, and with a long collar at an oblique angle, bearing a single, coarse appendage. Conjugations among thalli scalariform.
Illustrations: Fig. 11.99.
Hosts: Orthocladiinae near Kiefferophyes and Paratrichocladius pluriserialis (Diptera, Chironomidae).
Distribution: Victoria and Tasmania, Australia.
Reference: Lichtwardt and Williams, 1990.
Austrosmittium
biforme Williams &
Lichtwardt, 1992
(in Lichtwardt and Williams, 1992)
Trichospores ellipsoidal, either (18-)22-29 x 7.2-8 µm with a collar 8-14 x 4-4.5 mm or (8.4-)10-15 x 4.2-5.6 µm with a collar 4.2-7.6 x 3.2 µm, and a single coarse appendage. Thallus less than 500 µm long, basal cells producing numerous dentate projections, some serving as auxiliary holdfasts. Zygospores unknown.
Illustrations: Fig. 11.93.
Hosts: Orthocladiinae (Diptera, Chironomidae).
Distribution: Tasmania, Australia.
Reference: Lichtwardt and Williams, 1992.
Austrosmittium kiwiorum Williams & Lichtwardt, 1990 (type species)
Trichospores oval, (11-)14(-15) x (6.5-)8(-9) µm, with an obvious collar narrowed where the single, fine appendage emerges, borne 1-3 per fertile branch. Zygospores (27-)32(-35) x 10-12 µm, produced following scalariform conjugations of branches, upon release bearing a collar approximately 18 x 4 µm attached about 8 µm from one end. Type species.
Illustrations: Fig. 11.42.
Hosts: Orthocladiinae (Diptera, Chironomidae).
Distribution: South Island, New Zealand.
Reference: Williams and Lichtwardt, 1990.
Austrosmittium lenticum
Siri, 2010
Thalli up to 120 µm long, with a ramified main axis, 2-4
trichsopores per fertile branch and a secreted holdfast. Oval to
ellipsoidal trichospores (10-)12(-17) x 5-6 µm, collar 2-3 µm,
appendage not apparent. Detached biconical zygospores (Type II)
(23-)26(-28) x 10-12 µm, with a median bulge and an oblique collar
10-12 x 2-3 µm. Zygosporophores 34-38 x 6-7 µm
Illustration: Fig. 11.357.
Host: Corynoneura sp..
larva.
Distribution: Argentina.
Reference: Siri and Lňpez Lastra, 2010
Austrosmittium norinsulare Lichtwardt, 1990 (in Williams and Lichtwardt, 1990)
Trichospores oval, 10-14 x 5-6.5 µm, collar 5-7 µm long, with a single, very fine appendage, borne 2-4 per fertile branch. Zygospores 19-20 x 8-9 µm.
Illustrations: Fig. 11.139.
Hosts: Orthocladiinae (Diptera, Chironomidae) larvae.
Distribution: North Island, New Zealand.
Reference: Williams and Lichtwardt, 1990.
Austrosmittium
patagonicum Siri, 2010
Branched thalli less than 300 µm long, basal structure
consisting of cells arranged in a ring around a holdfast from which
branches arise. Ellipsoidal trichospores (24-)28(-31) x 7 µm, with a
thin and long appendage, collar 9-13 µm long. Biconical zygospores
(Type II) with a pronounced median bulge, (47-)54(-62) x (21-)24(-28)
µm, and an oblique collar; zygosporophore 40 x 12 µm arising from
scalariform conjugations betwen thalli.
Illustrations: Fig. 11..358.
Host:: Parochlus sp
(Diptera, Chironomidae) larva.
Distribution: Argentina.
Reference: Siri and Lňpez Lastra, 2010.
Baetimyces
Valle & Santamaria, 2004a
Trichospores subcylindrical, bearing two thick appendages, one elongated and the other short. Appendages helically oriented within the generative cell before trichospore release. Zygospores biconical, perpendicularly and medially attached to zygosporophore. Thalli irregularly branched. More than one holdfast per thallus, in lateral and terminal positions. Attached to hindgut cuticle of Baetis (Ephemeroptera, Baetidae) nymphs. Monotypic.
Type species: Baetimyces ancorae Valle & Santamaria
Baetimyces ancorae Valle & Santamaria, 2002a
Thalli sparsely branched, attached to the hindgut lining of Baetis nymphs by laterally secreted, cup-like holdfasts, one of them in terminal position at the end of a sinuous basal cell. The presence of a main axis is not always evident due to the variable direction of projecting branches. Hyphal cells 3.5-5 µm diam. Fertile branches bearing 3-5 trichospores each. Trichospores subcylindrical, (40-)50(-58.5) x (3.5-)4.5(-5.5) µm, straight to slightly arcuate. Generative cells 12-18 x 5-7 µm, distally swollen at the trichospore-formation area. After release, the trichospores show two thick appendages: an elongated appendage, slightly wider at the proximal end, and a small, short appendage which contacts at the basal area and continues with the longest appendage. A very small and inconspicuous collar can be seen in trichospore base. Both appendages are helically oriented within the generative cell before trichospore release, appearing as broad oblique bands. Zygospores biconical, (34-)45(-54) x 7-9 µm, perpendicularly and medially attached to the zygosporophore (Type I). The zygosporophore subtending a mature zygospore, when preserved and stained with lactophenol cotton-blue contains cytoplasmic material restricted to a well-defined central zone showing cytoplasmic contractions with lateral expansions in the overall shape of an anchor. Conjugations scalariform, with zygospores arising from a distal end of cells of either conjugating branches. After release, zygospores have an empty collar and no appendages.
Illustration: Fig. 11.269.
Host: Baetis sp. (Ephemeroptera, Baetidae).
Distribution: Spain.
Reference:
Valle and
Santamaria, 2002a
Barbatospora
White, Siri & Lichtwardt, 2005
Branched thalli producing cylindrical trichospores without a collar but
with
multiple fine appendages at their base; trichospores may bear a
cylindrical
sleeve or wall at their terminal end that, upon dehiscence, may reveal
appendage-like filaments. Monotypic.
Type species. Barbatospora ambicaudata White, Siri & Lichtwardt
Barbatospora ambicaudata
M.M. White, Siri & Lichtwardt, 2006
Thalli with a basal cell 8-12 µm diameter, branched near the base, and bearing a cup-shaped holdfast. Branchlets producing 1-4 cylindrical trichospores 38-42 x 3-4 µm with non-persistent fine multiple appendages at their base. Trichospores may sometimes have appendage-like filaments at their terminal end that are initially concealed by a cylindrical sleeve or wall 6-13 x 2.5-4 µm. Zygospores unknown. Type species.
Illustrations: Fig. 11.279.
Host: Simulium vandalicum Dyer & Shannon larvae (Simuliidae).
Distribution: Great Smoky Mountains National Park, USA.
Barbatospora ambicaudata is unusual in the development of its cylindrical trichospores that results in some of them having appendage-like filaments at both ends. The ontogeny of these structures is not clearly understood. An axenic culture, TN-49-W2(A), was obtained.
Reference: White, Siri and Lichtwardt, 2006.
Bojamyces
Longcore, 1989, emend. L.G.
Valle & Santam., 2004
Thallus with sparse and indeterminate branching, attached to the
host hindgut cuticle. Generative cells scattered on the thallus,
interspersed with vegetative cells. Trichospores elongate-ellipsoidal,
with or without a single appendage and with a flared collar. Zygospores
perpendicularly and medially attached to the zygosporophore (Type I
[Moss et al., 1975]}, with a collar. In ephemeropteran nymphs. Three
species.
Type species: Bojamyces repens Longcore
Bojamyces olmecensis M.M. White, L.G. Valle & Cafaro, 2008
Thalli sparsely branched, 3.5-5 µm diam. Holdfast cell
undifferentiated, simple with a thin layer of secreted holdfast
material. Ellipsoidally elongate trichospores, 30-35 x 3.5-5 µm diam,
with a collar of convergent margins 3.5-5 x 2-2.5 µm and a single,
filiform appendage. Trichospores develop with random orientation on
thalli. Generative cells scattered along the entire thallus, variable
in length, sometimes longer than the trichospores. Zygospores
biconical, Type I at maturity, 50-60 x 5-7 µm, medially and
perpendicularly attached to the zygosporophore, formed in the vicinity
of the scalariform conjugations between adjacent branches.
Zygosporophore cone shaped, about 7.5 µm long, with a swollen base
tapering at the attachment point of the zygospore.
Illustrations: Fig. 11.331.
Host: On hindgut lining of Leptophlebiidae nymphs
(Ephemeroptera).
Distribution: Veracruz, Mexico.
Reference: Valle, White, and Cafaro, 2008.
Bojamyces repens Longcore, 1989
Thallus sparsely branched, indeterminate, attached to cuticle of hindgut of host. Generative cells scattered on thallus, interspersed with vegetative cells. Trichospores elongate-ellipsoidal with collar; lacking appendages. Zygospores unknown. Trichospores (30-)45(-77) x 6-8 µm, collar 3-5 x 3-5 µm. Thallus disarticulating at irregular intervals.
Illustrations: Fig. 11.44.
Hosts: Leptophlebia intermedia (Ephemeroptera,
Leptophlebiidae) and
possibly Siphlonurus sp. (Siphlonuridae). Habroleptoides confusa Artori &
Jacob (Leptophlebiidae) (in Spain).
Distribution: USA (Maine); Spain.
Lichtwardt and Williams (1992) reported and illustrated a fungus very similar to B. repens living in nymphs of Australonousia sp. (Leptophlebiidae) in Tasmania, Australia. However, insufficient specimens did not allow a determination of the genus or species.
References: Longcore, 1989; Lichtwardt and Williams, 1992; Valle and
Santamaria, 2004b.
Bojamyces
transfuga L.G. Valle & Santam., 2004
Trichospores (24-)30(-36) x 5-6 µm, with a 1.5-2.5 µm long and 2-2.5 µm broad collar with a single appendage, visible inside the generative cell before the trichospore release. After trichospore release, the appendage appears compactly folded. Trichospores arise from generative cells without a definite direction. Zygospores (27-)42(-50) x 8-9 µm, perpendicularly and medially attached to the zygosporophore, which is inflated at the lower part. Once released, a 7-7.5 µm long flared collar and a single filiform appendage can be observed. Later, typical scalariform conjugation bridges develop, and zygospores grow from the proximities of these bridges, from one of the conjugants.
Illustration: Fig. 11.306.
Host:: Caenis luctuosa
Burmeister (Ephemeroptera, Caenidae) nymphs.
Distribution: Spain.
Reference: Valle and Santamaria, 2004b.
Capniomyces
Peterson & Lichtwardt, 1983
Trichospores elongate-ovoid with 1-6 very broad appendages, collar
lacking.
Zygospores biconical, point of attachment to the zygosporophore.
submedian and
the angle oblique. In hindgut of larval Capniidae (Plecoptera). Two
species.
Type species: Capniomyces stellatus Peterson &
Lichtwardt.
Capniomyces
celatus L.G. Valle, 2007
Thalli sparsely ramified from the basal cell. Basal cell wider than
the upper ones, showing fine coating of secreted holdfast material.
Trichospore 10.5 x 3 µm, ovoid-ellipsoidal, without a collar, carrying
an undetermined number of wide petaloid appendages observable inside
the corresponding generative cell. Generative cells 4-8 x 2-3.5 µm,
with 6-12 cells per fertile branch. Zygospores 35-38 x 5-6 µm, Type II,
regularly biconical and developing directly from the conjugation tube
or near it. Zygosporophore 16-20 x 3-4.5(-5) µm, released with the
zygospore as a collar once mature. In hindgut of Nemouridae nymphs.
Illustrations: Fig. 11.317.
Host: Nemoura cinerea
Retzius (Plecoptera, Nemouridae) nymphs.
Distribution: Spain.
Reference: Valle, 2007.
Capniomyces
sasquachoides M.M. White & Bench, 2012
Thallus densely branched, emanating from a prominent basal cell (approx. 55-75 x 18-20 µm), which is attached to the hindgut cuticle with a disk-like holdfast and adhesive. At maturity holdfast may possess accessory, lobe-like extensions for gut attachment. Basal cell may collapse after thallus maturation and spore release. Trichospores elongate-obpyriform (28-)34(-39) x (6-)7.2(-8.1) µm, up to 2-4 per fertile branchlet, without a collar and with two appendages. Zygosporophores (14-22 x 4-5 µm) arising from the extension of a cell near two conjugating thalli. Zygospores biconical (41-)45(-60) x (8-)9.4(-12) µm, attached below their middle to the zygosporophore at an oblique angle. Upon detachment of zygospores a single appendage may be present in the hindgut of immature Taeniopterygidae (Plecoptera).
Illustration: Fig. 11,378
Host: Taenionema sp.
(Taenioperygidae, Plecoptera).
Distribution: Idaho, USA.
Reference: Bench and White, 2012.
Capniomyces stellatus Peterson & Lichtwardt, 1983
Attached to the hindgut cuticle by a discrete pad of secreted holdfast material. Trichospores elongate-ovoid, (10-)15(-19) x 4-6 µm, with 1-6 very broad basal appendages 40-150 x 2-6 µm. Generative cells 10-20 x 4-7 µm, forming a series of 3-4 trichospores on terminal branches. Zygospores biconical, (42-)52(-64) x 7-9 µm, point of attachment to the zygosporophore submedian and the angle oblique. Zygosporophores 10-15 x 2-3 µm, arising from the conjugation tube between two hyphae, or from a swollen hemispherical region of a fertile hypha distant from any conjugations of branches. In hindgut of larval Capniidae and Taeniopterygidae (Plecoptera). Type species.
Illustrations: Fig. 11.7; Fig. 11.8; Fig. 11.77.
Host: In hindgut of larval Allocapnia spp., including A.
granulata
(Claassen) and A. vivipara (Claassen) (Plecoptera, Capniidae),
in leaf
packs, on sticks, and under stones in flowing streams. Also in
Nemouridae (?). In Strophopterix
limata (Frison) nymphs (Plecoptera, Taeniopterygidae)
Distribution: USA (Kansas, Arkansas, Missouri, Indiana, Great Smoky Mountains National Park).
The variable number (1-6; median 4) of very broad (2-6 mm) and gelatinous-like appendages make this species easily identifiable. Another unique feature is the sexual apparatus: Zygospores arise by hyphal conjugations, as in most other harpellids, but as well from the juncture of two adjacent cells on a hypha. The species has been cultured axenically by Peterson.
References: Peterson and Lichtwardt, 1983; Peterson, 1984; White,
Siri, and Lichtwardt, 2006.
Caudomyces
Lichtwardt, Kobayasi & Indoh, 1988 (1987)
Trichospores produced on a long extension of the generative cell
which, upon
release, remains attached to the trichospore. Trichospores without
appendages.
Thalli branched. In hindgut of Tipulidae (Diptera) larvae. Two species.
Type species; Caudomyces japonicus Lichtwardt, Kobayasi
& Indoh.
Caudomyces japonicus Lichtwardt, Kobayasi & Indoh, 1988 (1987)
Trichospores long-ellipsoidal, 25-30 x 3-3.5 µm, produced on narrow extensions (45-66 µm long) of generative cells. Upon release trichospores retaining the extensions, bearing no appendages. Thalli sparsely branched except at the base.
Illustrations: Fig. 11.45.
Host: Antocha sp. larva (Diptera, Tipulidae).
Distribution: Japan., China..
Strongman and Xu found in
the Qualing Mountains, Shaanxi Province, China, specimens in Antocha sp. larvae that match C. japonicus.
Reference: Lichtwardt et al., 1988 (1987).
Caudomyces
longicollis Strongman, 2007.
Host: Antocha sp.
larvae (Diptera, Tipulidae).
Distribution: Mill Creek, Prince Edward Island, Canada.
Reference: Strongman, 2007.
Coleopteromyces
Ferrington, Lichtwardt & López Lastra, 1999
Thalli with a main axis, sparsely branched, in hindgut of larvae of Scirtidae (Coleoptera). Trichospores long-ellipsoidal with a small collar and single appendage. Zygospores unknown. Monotypic.
Type species: Coleopteromyces amnicus Ferrington, Lichtwardt
&
López Lastra.
Coleopteromyces
amnicus Ferrington,
Lichtwardt & López Lastra, 1999
(in Lichtwardt, Ferrington and López Lastra, 1999)
Thalli up to 2 µm long with a sparsely branched main axis producing several fertile branches 4-8 µm diameter. Some sterile branches as narrow as 2 µm diameter. Up to 12 generative cells per branch, producing long-ellipsoidal trichospores (28-)33(-37) x 6-7 µm, upon release having a small collar attached by a narrow connection to the trichospore body, with a single appendage. Zygospores unknown. Monotypic.
Illustrations: Fig. 11.46.
Host: Scirtidae (Coleoptera) larva.
Distribution: On submerged logs in streams in Patagonia, Argentina.
This is the only known Harpellales in a beetle.
Reference: Lichtwardt et al., 1999.
Dacryodiomyces
Lichtwardt,
2011
Zygospores
elongate-ovoid, attached at wide end
to a long collarlike extension of the zygosporophore, Trichospores
subcylindrical with a collar and one appendage. Attached to hindgut
cuticle of
Chironomidae (Diptera) larvae. Monotypic.
Type species:
Dacryodiomyces oklahomensis
Lichtwardt.
Dacryodiomyces
oklahomensis Lichtwardt, 2011
Thalli
compact with numerous branches arising
from the basal area. Zygospores elongate-ovoid, Type IV (Moss et al.
1975),
60--63 x 12--15 µm, arising from a collarlike basal cell 23--30 x 5--7
µm.
Trichospores subcylindrical, 25--31 x 3.5--5 µm, with a collar 3--9 µm
long,
and one fine appendage. In hindgut of Cricotopus
sp. larvae (Diptera: Chironomidae).
Illustrations:
Fig. 11.375.
Host: Cricotopus sp. (Diptera,
Chironomidae).
Distribution:
Oklahoma, USA.
Reference:
Lichtwardt, 2011.
Ejectosporus
Peterson, Lichtwardt & Williams, 1991
See Strongman’s revision of Ejectosporus below.
Ejectosporus magnus Peterson, Lichtwardt & Williams, 1991
See Ejectosporus spica that combines Ejectosporus
magnus
and Simuliomyces spica.
Ejectosporus
Peterson, Lichtwardt & Williams emend. Strongman, 2005
Three spore types produced. Trichospores bearing 2 appendages, typically 8-16 spores produced at the distal ends of thin, fertile branches. Vegetative spores produced on thicker branches (4-6 per branch), extruding sporangiospores in situ with the sporangial and spore wall remaining attached to the branch. Zygospores biconical, tips co-linear or slightly bent toward the zygosporophore when mature, zygosporophores slightly swollen at the point of attachment to the spore, medially, at right angles to the zygospore (Type I).. Two species.
Strongman (2005)
discovered that Ejectosporus magnus and Simuliomyces spica
are
conspecific, the former being a vegetative state of reproduction whose
spores
germinate within the gut where produced, thus augmenting the number of
thalli.
The name Ejectosporus takes precedence over Simuliomyces.
= Simuliomyces spica S.W. Peterson & Lichtw. Mycologia 75(2) 1983 pp. 246-247
= Ejectosporus magnus S.W. Peterson, Lichtw. & M.C. Williams Mycologia 83(4) 1991 pp. 389-390
Thallus branched, from a prostrate central axis, branches form either elongate-ellipsoidal trichospores 12-14(-16) x 2 µm, no collar, with 2 short, stiff appendages, or, nondeciduous, vegetative spores, clavate to elongate-ellipsoidal 50-85 x 8-10 µm. Zygospores biconical, 36-43 x 7-10 µm, attached to zygosporophores medially, at right angles (Type I), zygosporophore slightly swollen, formed from swellings along one of the pair of hyphae undergoing scalariform conjugations, resulting often in a row of zygospores produced. Attached to hindgut of Allocapnia sp. (Plecoptera: Capniidae) nymphs.
Illustration: Fig. 11.282.
Hosts: Allocapnia spp. (Plecoptera, Capniidae).
Distribution: Midwestern and Southern USA states (Missouri,
Oklahoma, Texas,
Arkansas, Alabama); Great Smoly Mountains National Park.
References: Lichtwardt et al., 1993; Strongman, 2005; White, Siri,
and Lichtwardt, 2006.
Ejectosporus trisporus Strongman, 2005.
Thallus branched, sometimes from a prostrate central axis, branches form either trichospores 12-18.5 x 2-4.5 µm with 2 short, stiff appendages and no collar, or nondeciduous, vegetative spores, elongate-ellipsoidal 72-86 x 8-11.5 µm when fully mature. Branches forming trichospores thin (3-5 µm wide at base) with 8-16 trichospores forming along one side of the fertile tip. Vegetative spores formed on thicker (5-8 µm) branches. Zygospores biconical, 54-71 x 9-12.5(-14) µm attached to the zygosporophore medially at right angles (Type I) with tips slightly bent toward the zygosporophore, zygosporophore slightly swollen, 24-32.5 x 5-6.5 (-8.5) µm, formed from swellings along one of the pair of hyphae undergoing scalariform conjugations, resulting often in a row of zygospores produced. Rarely, zygospores are released without the zygosporophore attached. Attached to the hindgut of Allocapnia (Plecoptera: Capniidae) nymphs.
Illustration: Fig. 11.283.
Host: Allocapnia pygmaea (Plecoptera, Capniidae).
Distribution: Eastern Canada.
Reference: Strongman, 2005, 2007.
Ephemerellomyces
White & Lichtwardt, 2004
Trichospores long-ovoid with two or three very long appendages. Trichospores may germinate on hindgut cuticle to produce a cell bearing one terminal trichospore. Attached to hindgut of Ephemeroptera nymphs. Monotypic.
Type species: Ephemerellomyces aquilonius White & Lichtwardt
Ephemerellomyces aquilonius White & Lichtwardt, 2004
Trichospores long-ovoid, (30-)45(-50) x 8-10 µm, with 2, occasionally 3, very long appendages. Trichospores may attach and germinate on the hindgut cuticle and produce a fertile cell 75-110 µm long bearing one terminal trichospore. Zygospores unknown.
Illustration: Fig. 11.270.
Host: Ephemerella aurivillii (Bengtsson) nymph (Ephemeroptera).
Distribution: Norway.
Reference: White and Lichtwardt, 2004.
Furculomyces
Lichtwardt & Williams, 1992
Thalli homothallic, conjugating branches fusing at their tips and swelling to form a furcula-like structure from which a zygospore develops. Zygospores (Type II) biconical, bent near the middle away from the point of attachment and bearing a collar upon release. Trichospores almost cylindrical, with a collar and a single appendage upon release. Holdfast a horseshoe-shaped cell with outwardly radiating primary branches. In hindgut of Chironomidae (Diptera) larvae. Three species.
Type species: Furculomyces boomerangus Lichtwardt &
Williams.
Furculomyces
boomerangus (Williams &
Lichtwardt) Williams & Lichtwardt, 1992
= Smittium boomerangum Williams & Lichtwardt, 1990.
Holdfast developing into a horseshoe-shaped cell with outwardly radiating primary branches and sparse, narrow secondary branches; 2-6 generative cells per fertile branch. Trichospores almost cylindrical, but with a median swelling, (20-)25(-30) x (3.0-)3.6(-4.2) µm, with a short, indistinct appendage; collar approx. 1.5 x 1.5-2.0 µm long. Zygospores 87-111 x 11-14 µm, collar 6-12 x 4.0-4.5 µm attached at an angle near the midregion, with a pronounced bend or depression opposite the collar, such that it may resemble a boomerang in side view. Zygospores commonly forming homothallically from a pair of conjugated primary branches arising from the curved basal holdfast cell.
Illustrations: Fig. 11.103.
Hosts: Chironomus oppositus Walker, Procladius paludicola Skuse, Aspectrotanypus maculosa (Freeman), Tanytarsus nr. inextentus (Diptera, Chironomidae).
Distribution: Victoria and Tasmania, Australia.
References: Lichtwardt and Williams, 1990; Lichtwardt and Williams,
1992.
Furculomyces septentrionalis Misra, White & Lichtwardt, 1999
Trichospores subcylindrical, (26-)33(-39) x (4.6-)4.9(-5.5) µm, collar about 2-3 mm long, with a fine appendage. Zygospores 86-121 x 9-14 µm, with a conspicuous depression opposite the collar. Attached to hindgut cuticle of Chironomidae larvae.
Illustrations: Fig. 11.63.
Host: Chironomus sp. (Chironomidae).
Distribution: Rocky Mountains, Colorado, USA.
Furculomyces was thought to be an Australian genus until the discovery of F. septentrionalis in Colorado.
Reference: Misra et al., 1999.
Furculomyces westraliensis Williams & Lichtwardt, 1992
Trichospores nearly cylindrical, 36-40 x 2.3-3.0 µm, often produced singly on a fertile branch. Zygospores 97-109 x 10-11 µm, bent near the middle, produced at the point of fusion of two swollen conjugating branches that grow from different branches of a thallus or from the same branch.
Illustrations: Fig. 11.48.
Host: Chironomus oppositus group (Diptera, Chironomidae).
Distribution: Western Australia, Australia.
References: Lichtwardt and Williams, 1992.
Gauthieromyces
Lichtwardt, 1983
Thallus arbusculate, bearing horseshoe-shaped trichospores attached
eccentrically (basolaterally) to their generative cells. In hindgut of
Baetidae
(Ephemeroptera) nymphs. Three species.
Gauthieromyces indicus Misra & Tiwari, 2008
Thallus arbusculate, up to 297 µm long, with a broad basal holdfast, 12-18 µm diam and a stout dichotomously branched main axis, tapering from the base to an apex 2.5-5 µm diam. Secondary branches not tapering, 2.5 µm diam. Fertile branches 25-60 x 2.5-5 µm, bearing 3-15 irregular, horseshoe-shaped trichospores approximately 10 x 2.5 µm, attached eccentrically to generative cells of 2.5-7.5 x 2.5 µm with fine appendages that may twist together. Zygospores unknown.
Illustrations: Fig. 11.334.
Host: Baetis sp. nymphs
(Ephemeroptera, Baetidae).
Distribution: Streams in India.
Reference: Misra & Tiwari, 2008.
Gauthieromyces
microsporus Lichtwardt,
1983a
[= Genistella microspora Gauthier, 1960, nom. nud.]
Arbusculate thallus up to 300 µm long, main axis and primary branches stout (15-20 µm diam), secondary branches narrower (3-6 µm diam), with a prominent basal holdfast. Trichospores horseshoe-shaped, overall shape ~10-12 µm, attached laterally near base, up to 4 per fertile branch. Trichospore appendages and zygospores unknown. Type species.
Illustrations: Fig. 11.7; Fig. 11.64.
Host: Larval hindgut of Baetis pumilus (Burm.) (Ephemeroptera, Baetidae).
Distribution: Streams (Bresson, Tavernolles) located near Grenoble, France.
The species is apparently quite rare, for it is reported only once in the literature. Lichtwardt was not able to find it in 1968 in mountain streams in the general vicinity where Gauthier originally collected it. She reported that G. microsporus occurred together with Legeriomyces ramosus in the same host hindguts. Gauthier incorrectly assigned this fungus to Genistella (now Legeriomyces); the trichospores of the two genera are not similar. Gauthieromyces and Orphella are the only Legeriomycetaceae with curved trichospores, but the reproductive branches of the latter are distinctly different and the two genera are readily separable on this basis.
References: Gauthier, 1960; Lichtwardt, 1983a.
Gauthieromyces
viviparus L.G. Valle, M.M. White & Cafaro, 2008.
Thalli up to 260 µm long, diversely branched, presenting dichotomous
sections, with an enlarged basal cell narrowing abruptly to long
branches. Holdfast cell 20-45 x 10-21 µm, sometimes with lateral and
basal branches. Trichospores an extended V-shape, with an arc length of
7-9 x 2.5-3 µm, attached to the generative cell at the proximal end, no
collar, with a single filiform appendage on release. Generative cells
up to 25 per fertile branch, 3-6 x 2.5-3.5 µm. Outgrowths, which
we refer to as propagule-like structures, can form on the basal and
second cell of the thallus and start growing before being detached from
the main (parent) thallus. Zygospores not found.
Illustrations: Fig. 11.332.
Host: On hindgut of Baetodes
sp. and Baetis sp.
(Ephemeroptera, Baetidae) nymphs.
Distribution: Veracruz, Mexico.
Reference: Valle, White, and Cafaro, 2008.
Genistelloides
Peterson, Lichtwardt & Horn, 1981
Trichospores obpyriform, without a collar, bearing 2 appendages. Zygospores attached medially and perpendicularly to the zygosporophore. In hindgut of nymphal Capniidae (Plecoptera). Four species.
Type species: Genistelloides hibernus Peterson, Lichtwardt & Horn.
The trichospores of this genus resemble those of Legeriomyces.
However, the zygospores of Genistelloides are Type I, rather
than Type
II as in Legeriomyces.
Genistelloides amplispora White & Lichtwardt, 2004
Trichospores long-ellipsoidal, 50-60 x 9-10 µm. Biconical zygospores (Type I) 26-28 x 4-4.5 µm, zygosporophores 17-20 x 4-5 µm.
Illustration: Fig. 11.271.
Host: Amphinemura sulcicollis (Stephens) nymph (Plecoptera, Nemouridae).
Distribution: Norway.
Reference: White and Lichtwardt, 2004.
Genistelloides communis White & Lichtwardt, 2004
Trichospores long-obpyriform, 31-38 x 5.5-6.5 µm, bearing two long, initially helical appendages upon release. Zygospores unknown.
Illustration: Fig. 11.272.
Host: Nemoura cinerea (Retzius) nymph (Plecoptera, Nemouridae).
Distribution: Norway.
Reference: White and Lichtwardt, 2004.
Genistelloides helicoides Williams & Lichtwardt, 1987
Elongate-ovoid trichospores 2(-4) per fertile branch, (42-)51(-62) x (7.5-)8.7(-10) µm, upon release lacking a collar and bearing 2 distinct long appendages (helically oriented immediately upon release). Multiple lateral branches are formed near the base of a principal axial cell. Lateral branches from the axial cell tend to form a more alternate than opposite branching pattern Lateral branches may branch again, often near the base. Frequently 3-4 perpendicular lateral branches may be observed from the first lateral branch; however, branching of these perpendicular lateral branches generally does not occur until later in the developmental process. Zygospores unknown.
Illustrations: Fig. 11.149.
Hosts: Zapada haysi, Z. cintipes, Malenka fluxura (Plecoptera, Nemouridae).
Distribution: USA (Colorado and more eastern states).
Though placed in Genistelloides because of the plecopteran host and the two appendages, the heavy appendages of G. helicoides are different from those of the type species. The generic placement of this species would be confirmed if zygospores are found and match those of the type species.
Reference: Williams and Lichtwardt, 1987.
Genistelloides hibernus Peterson, Lichtwardt & Horn, 1981
Young thalli attached to hindgut cuticle by a more or less pointed basal holdfast, often with a unilateral bulbous swelling just above the point of attachment. Long fertile branches producing 3(-7) generative cells that become distally swollen in the region where trichospores are produced. Trichospores obpyriform, (23-)29(-34) x (6-)8(-10) µm, with two distinct long appendages. Zygospores (22-)26(-30) x (4-)4.5(-6) µm which develops in most cases directly from the conjugation tube. Upon release, the zygosporophore usually remains attached to the zygospore. Type species.
Illustrations: Fig. 11.7; Fig. 11.8; Fig. 11.9.
Hosts: In hindgut of Allocapnia vivipara (Claassen), A. granulata (Claassen), A. rickeri (Frison), A. pygmaea, Mesocapnia sp. (Plecoptera, Capniidae) nymphs.
Distribution: USA (Kansas, Missouri, Arkansas, Indiana, Great Smoky
Mountains National Park). Prince Edward Island, Canada.
This species from winter-emerging stonefly nymphs resembles Legeriomyces spp. from mayfly nymphs in the basic features of its trichospores, but produces a different type of zygospore. Manier (1969b) showed a photomicrograph (her Fig. 1, Plate IX) of a "Legeriomyces sp." from Capnia bifrons, which conceivably is a species of Genistelloides on the basis of the Capniidae host; however, zygospores would have to be available in order to determine its generic placement. Several axenic isolates of Genistelloides hibernus have been obtained by both Peterson and Lichtwardt.
References: Peterson et al., 1981; Peterson, 1984; White, Siri, and
Lichtwardt, 2006, Strongman, 2007.
Genistellospora
Lichtwardt, 1972
Trichospores ovoid, without a collar, bearing about 6 appendages. Zygospores produced without hyphal conjugations, borne parallel to axis of zygosporophore, to which they are attached medially. In hindgut of larval Simuliidae (Diptera). Six species.
Type species: Genistellospora homothallica Lichtwardt.
Genistellospora
dorsicaudata L.G. Valle, M.M. White & Cafaro,
2011
Thalli alternately branched basally and sparsely to vertically branched at distal portions. Basal cell slightly wider at the proximal end, with a simple discoid holdfast and 3-6 pairs of lateral branches originating from it. Trichospores ovate-ellipsoidal to elongate-ellipsoidal, slightly asymmetrical, 32-38 x 8-12.5 µm, with the maximum diameter about one-third the distance from the base, narrowing (to 6-7 µm diam) at the apex. On release of the trichospores 4(-6) uncurled appendages are visible. Biconical symmetric zygospores 85-105 x 15-20 µm, parallel to the corresponding zygosporophore, formed immediately without conjugations. Zygosporophores are 30-45 x 10-14 µm, with the maximum diameter at the distal portion. The intermediate cell (60-85 x 6-8.5 µm bears a proximal zygosporophore on a short extension on the intermediate cell, and a terminal cell, a projection (25-30 x 5 µm) composed of two cells when fully developed. Of the two cells making up a terminal cell the lower one is slightly globose at the bottom while the upper one is cylindrical. This extension grows upward nearly parallel to the intermediate cell or more rarely retroflex, pointing downward. Attached to the hindgut lining of
Simuliidae (Diptera) larvae.
Illustrations: Fig. 11.376.
Hosts: Simulium iriarti, S..
(Psilopelmia) sp.,, S. metallicum complex (Simuliidae).
Distribution: Veracruz, Mexico.
Genistellospora guanacastensis Lichtwardt, 1997
Thallus with a main axis usually 150-250 µm long from which lateral and sometimes terminal branches arise. Trichospores long-oval, 50-61 x (8-)10(-13) µm, bearing 4(-6) partially coiled appendages. Zygospores 85-105 x 14-18(-20) µm, zygosporophore 50-70 x 7-14 µm, with the distal region slightly wider than the proximal end. Intermediate cell (below zygosporophore) 75-85 µm long with an apical terminal cell, about 30 µm long, wider at the base
Illustrations: Fig.
11.129, Fig. 11.377.
Host: Simulium sp., S. virgatum group (Diptera, Simuliidae).
Distribution: Costa Rica, Mexico.
Reference: Lichtwardt, 1997. Valle et al., 2011.
Genistellospora homothallica Lichtwardt, 1972
Thalli generally less than 1 mm long, with moderate to prolific branching, usually with a main axis attached by a small but prominent secreted holdfast. Trichospores ovoid, (24-)30(-41) x (8-)10(-13) µm, bearing (5-)6(-7) very fine appendages, without a collar. Generative cells typically several times longer than the trichospores; lateral trichospores borne on short branchlike extensions of the generative cells. Zygospores (77-)100(-113) x (15-)20(-22) µm, produced without conjugation, attached medially and oriented parallel to the axis of the zygosporophore. Zygosporophores about (39-)40(-48) x (10-)15(-17) µm. Supporting cell (below zygosporophore) with a straight or reflexed, thumblike branch terminating in a cell. Type species.
Illustrations: Fig. 7.7; Fig. 7.16; Fig. 7.18; Fig. 11.7; Fig. 11.8; Fig. 11.10.
Hosts: In hindgut of many species of larval Simulium and Prosimulium (Diptera, Simuliidae).
Distribution: Widespread in lotic habitats in the USA. Common in
(but not
restricted to) many blackfly populations in the Rocky Mountains and
other
mountain streams. Idaho, USA. One unpublished report (Moss and
Lichtwardt) from
southern
England in Bere Stream, East Stoke, Wareham. Also known from Puerto
Rico, Costa
Rica, Chile, and Argentina. Armenia. Ontario, Canada. Dominican
Republic. Mexico.
This species is easily identified on the basis of its blackfly host, prominent secreted holdfast, growth habit, and especially the distinctive homothallic zygospore apparatus. The trichospores most closely resemble those of several species of Pennella, also encountered in blackfly guts. Like G. homothallica, Pennella spp. have Type III zygospores, but conjugations of thallial branches are clearly seen in Pennella. Furthermore, Pennella thalli attach to the gut cuticle by a general secretion of mucilage along a tapered, forked, or lobed basal cell, and consequently do not present a clearly defined holdfast structure as in G. homothallica. Thalli of G. homothallica not infrequently are found with attached thalli of Simuliomyces microsporus. Trichospore formation and holdfast structure of G. homothallica have been studied with the electron microscope (Preisner, 1973; Moss and Lichtwardt, 1974; Mayfield and Lichtwardt, 1980).
References: Lichtwardt, 1972; Preisner, 1973; Mayfield and
Lichtwardt, 1980;
Moss, 1975; Moss and Lichtwardt, 1976; White et al., 2000; López Lastra
et al., 2005, Nelder et al., 2005, Strongman and White, 2008. Valle and
Cafaro, 2010. Valle et al., 2011. Beach and White, 2012.
Genistellospora nubila Lichtwardt, 1997
Thallus 400-1200 µm with a small secreted holdfast. Trichospores ovoid, 38-41 x 10-14 µm, attached eccentrically to generative cell, on release having 4(-6) appendages. Zygospores unknown.
Illustrations: Fig. 11.130.
Host: Simulium spp. (Diptera, Simuliidae).
Distribution: Costa Rica.
Reference: Lichtwardt, 1997.
Genistellospora tepidaria Lichtwardt, 1997
Base of thallus with a prominent secreted holdfast. Thallus with few to numerous branches. Trichospores ovoid, 21-31 x 9-11 µm, with 6(-8) fine appendages. Zygospores produced without conjugations, 58-70 x 10-15 µm. Zygosporophores 29-30 x 8-11 µm.
Illustrations: Fig. 11.131.
Host: Simuliidae (Diptera).
Distribution: Costa Rica.
Reference: Lichtwardt, 1997.
Genistellospora tropicalis Ríos-Velásquez, Alencar, Lichtwardt & Hamada, 2003
Branched thalli with a main axis 114-343 µm long from which lateral branches arise. Holdfast may be shaped like a horseshoe. Ovoid trichospores 20-27 x (3-)6(-8) µm without a collar, each with about 6 fine appendages, produced in high numbers. Zygospores 50-60 x 8-10 µm attached medially and oriented parallel to the axis of the zygosporophore. Zygosporophores about 40-50 x 7-8 µm. Supporting cell (below zygosporophore) with a straight or thumblike lateral extension.
Illustration: Fig.11.255.
Host: Larvae of Simulium goeldii Cerqueira & Nunes de Mello, S. ulyssesi Py-Daniel & Coscarón, S. trombetense Hamada, Py-Daniel & Adler.
Distribution: Amazonas, Brazil.
Reference: Alencar, Ríos-Velásquez, Lichtwardt, and Hamada, 2003.
Glotzia
Gauthier ex Manier & Lichtwardt, 1969 (1968)
[= Glotzia Gauthier, 1936, nom. nud.]
Thalli with one or more holdfasts attached laterally to a prominent basal cell. Trichospores cylindrical, collarless, with 2 short divergent appendages and 1 long, finer appendage. Zygospores attached obliquely and submedially to a zygosporophore arising from the area of conjugation between two cells. In hindgut of Baetidae (Ephemeroptera) nymphs and Plecoptera nymphs (one species). Seven species.
Type species: Glotzia centroptili Gauthier ex Manier & Lichtwardt.
Gauthier's (1936) illegitimate genus was monotypic when Manier and Lichtwardt validated it by providing a Latin diagnosis; Manier (1969b) later "validated" the type species with a Latin diagnosis, which was unnecessary according to Art. 42 of the Code. Tuzet and Manier in 1955(a) described Glotzia grassei (nom. nud.) from larvae of a species of blackfly, but it was later transferred to the genus Pennella; see Pennella grassei.
In 1971 Lichtwardt collected in northern Sweden what is apparently
an
undescribed species of Glotzia with long-obpyriform
trichospores and
zygospores with 2 appendages. Further studies will probably require a
slight
modification of the above generic description.
Glotzia
centroptili Gauthier ex Manier
& Lichtwardt, 1969 (1968)
[= Glotzia centroptili Gauthier, 1936, nom. nud.]
Thalli often clustered, 1-2 mm long, the slightly swollen and branched basal cell of each thallus with one lateral holdfast. Trichospores cylindrical, 6-7 per fertile branch, 40 x 4 µm, with a terminal refractive cap, and bearing 1 long fine appendage initially spiraled around 2 short (10 µm), broader, divergent, and rigid appendages. Zygospores 50-60 x 15 µm. Type species.
Illustrations: Fig. 11.174.
Host: In hindgut of Centroptilum luteolum M. nymphs (Ephemeroptera, Baetidae).
Distribution: Cold pools and streams of the Dauphiné French Alps.
References: Gauthier, 1936; Manier and Lichtwardt, 1968 (1969);
Manier,
1969b (1970b).
Glotzia coloradense Williams & Lichtwardt, 1999 (in Lichtwardt and Williams, 1999)
Trichospores almost cylindrical, (55-)69(-79) x (3.7-)4.5(-5.8) µm, collarless, with a terminal refractive cap, bearing one long fine central appendage with two short broader divergent appendages. Zygospores 52-54 x 7-9 µm.
Illustrations: Fig. 11.160.
Host: Baetis tricaudatus (Ephemeroptera, Baetidae).
Distribution: Colorado, USA.
Reference: Lichtwardt and Williams, 1999.
Glotzia ephemeridarum Lichtwardt, 1972
Basal cell of thalli unbranched or irregularly branched, when mature having a series of peglike secreted holdfasts. Trichospores cylindrical, 45-70 x 4.5-7 µm, tip sometimes refractive, usually with three appendages, the two outer ones short, broad and often divergent, the central one at an angle to the two others, broad at the base but tapering to a long fine filament. Zygospores 28-37 x 7.5-10 µm, flattened or incurved on the side of attachment; attachment to zygosporophore submedial and oblique; upon detachment bearing a small collar. Zygosporophore about 16-19 x 3-5 µm
Illustrations: Fig. 7.10; Fig. 11.11.
Hosts: In hindgut of Baetis tricaudatus Dodds nymphs, and possibly other Baetidae (Ephemeroptera).
Distribution: Streams in Wasatch Co., Utah; Mission Creek and
tributary near
National Bison Range, Wolf Creek, and N. Fork Bond Creek, Lake, Co.,
Montana, Idaho, and Great Smoky Mountains National Park,
USA.; Feng Yu River western China.
Glotzia
incilis Strongman & M.M. White, 2008
Thallus attached to hindgut lining by a bulbous basal cell, branches arising from the basal cell dividing sparingly, to give fertile branches distally. Six to eight generative cells per fertile branch, each producing a trichospore. Trichospores elliptical-elongate, with a slight median swelling, 21.5-26.5 x 3.5-4.5 µm with 2 short appendages (less than helf the spore length) and a third appendage longer than the trichospore, no collar. Trichospores with a refractive apex in both stained and unstained preparations. No zygospores found.
Illustrations: Fig. 11.336.
Host: Meniscus midges (Diptera, Dixidae).
Distribution: Ditch in Algonquin Provincial Park, Ontario, Canada.
Reference: Strongman and White, 2008.
Glotzia plecopterorum Lichtwardt, 1990 (in Williams and Lichtwardt, 1990)
Trichospores elongate-ellipsoidal, almost cylindrical, 39-50 x 6-8 µm, with two broad appendages circa 20 µm long and one very fine appendage many times the length of the trichospore. Thallus initially sparsely branched, becoming densely branched with up to 15 generative cells per fertile branch. Holdfast a bulbous, sometimes striated growth from the main branch. Zygospores unknown.
Illustrations: Fig. 11.140.
Hosts: Zelandoperla decorata, Z. fenestrata, and Acroperla spiniger (Plecoptera, Gripopterygidae).
Distribution: North Island, New Zealand.
Reference: Williams and Lichtwardt, 1990.
Glotzia stenospora White & Lichtwardt, 2004
Trichospores cylindrical, 60-68 x 3-5 µm. Zygospores (Type II) 61-72 x 11-14 µm. Zygosporophores 30-38 x 8-10 µm.
Illustration: Fig. 11.273.
Host: Centroptilum luteolum (Müller) nymph (Ephemeroptera, Baetidae).
Distribution: Norway.
Reference: White and Lichtwardt, 2004.
Glotzia tasmaniensis Lichtwardt & Williams, 1990
Basal cell of thallus with a simple basal holdfast, cells of sporulating branchlets sometimes swollen. Trichospores cylindrical, straight or bent or slightly sigmoid, with a slightly bulbous refractive apex, (30-)46(-78) x (3.2-)4.0(-6.0) µm. Zygospores unknown.
Illustrations: Fig. 11.100.
Host: Baetis sp. (Ephemeroptera, Baetidae).
Distribution: Tasmania, Australia.
Reference: Lichtwardt and Williams, 1990.
Graminella
Léger & Gauthier ex Manier, 1962
[= Graminella Léger & Gauthier, 1937, nom. nud.]
Thalli with a bulbous base and sparsely branched main axis,
producing
long series of small ovoid trichospores with a single appendage and no
collar. Zygospores with an oblique, median collar. May reproduce
endogenously
within the gut by means of specialized vegetative propagules. In
hindgut of
nymphal Baetidae (Ephemeroptera). Three species.
Type species: Graminella bulbosa Léger & Gauthier ex
Manier.
Both species of Graminella are unusual Harpellales because
of their
production of vegetative propagules; these are ontogenetically
different in the
two species.
Graminella
bulbosa Léger & Gauthier ex
Manier, 1962a
[= Graminella bulbosa Léger & Gauthier, 1937, nom. nud.]
Thalli up to 500-600 µm long, lower branches few and short, terminal ones fertile and producing a unilateral series of up to 40 ovoid trichospores 10-17 x 2-3 µm having 1 appendage and no collar. Bulbous base of thallus 8-10 µm wide, terminal branches 2-3 µm wide. Thalli often formed side by side and arranged in parallel rows. Vegetative production of new thalli occurs by means of a small bulbous detachable outgrowth from a thallus base. Zygospores unknown. Type species.
Illustrations: Fig. 11.172.
Hosts: In hindgut of Baetis sp. (Ephemeroptera, Baetidae) nymphs.
Distribution: Streams near Grenoble (Department of lsčre) and in the Néouvieille Mountains (Department of Hautes-Pyrénées), France. Spain..
References: Léger and Gauthier, 1937; Manier, 1962a; Valle, 2007.
Graminella ophiuroidea M.M. White, L.G. Valle & Cafaro, 2008.
Thalli 200-300 x 4-10 µm, sparsely branched, sometimes dichotomous. Main axis cells 4-6 µm diam. Basal cell oblong, 25-35 x 8-14 µm, attached to the hindgut lining by a secreted holdfast, with a main axis arising apically, and other axes emerging basally or laterally from the basal cells. Trichospores ovate-ellipsoidal, 8-12 x 2.5-3.5 µm, with a single thin appendage and no collar. Generative cells up to 20 per fertile branch, variable in length, also produced in the axial hypha below distal dichotomous fertile branch ramifications. Zygospores not found. Vegetative propagules formed from the basal cell.
Illustrations: Fig. 11.333.
Host: On hindgut lining of Baetidae (Ephemeroptera) nymphs.
Distribution: Veracruz, Mexico.
Reference: Valle, White, and Cafaro, 2008.
Graminella microspora Moss & Lichtwardt, 1981 (in Lichtwardt and Moss, 1981)
Thalli sparsely branched, up to 300 µm long with a bulbous base up to 11-18 µm diam. Terminal branches 2.5-3 µm diam, some producing long series of 10-20 lateral, ovoid trichospores 6-8.5 µm long by 2-2.5 µm diam, with a single appendage and no collar upon detachment. Conjugating branches producing from one of the conjugated cells biconical zygospores 32-43 x 6-8 µm, each with an oblique, median collar 5-8 µm long upon detachment. Reproduction is also by single clavate to ovoid cells, which emerge from the bulbous basal cells or other swollen cells of the thallus, attach to the gut cuticle, and develop into new thalli.
Illustrations: Fig. 11.12.
Hosts: In hindgut of Baetis tricaudatus Dodds nymphs, and unidentified nymphs of other Baetidae species (Ephemeroptera).
Distribution: N. Fork Bond Creek, Lake Co., Montana, and Great Smoky
Mountains National Park, USA; and at base
of
Mürrenbach Falls near Stechelberg, Switzerland. Chile; Norway. Ontario
and Newfoundland
Canada.
Reference: Lichtwardt and Moss, 1981; White and Lichtwardt, 2004;
White, Siri, and Lichtwardt, 2006, Strongman and White, 2008.
Strongman, 2010.
Graminelloides
Lichtwardt 1997
Thalli with few branches; base tapered to a point, without mucilage. Trichospores biconical, collarless, with a single appendage. Entire thallus may become reproductive except for the very basal cells. In hindgut of Simuliidae (Diptera) larvae. Monotypic.
Type species: Graminelloides biconica Lichtwardt
Graminelloides biconica Lichtwardt, 1997
Mature thalli up to 350 µm long by 5-8 µm diameter, with sparse branching. Immature thalli fusiform. Base tapered, without mucilage. Thalli often fascicled, sometimes consisting of more than 24 thalli in a cluster. Trichospores biconical, 10-16 x 4-5 µm, without a collar, and with one short appendage. Zygospores unknown.
Illustrations: Fig. 11.49.
Host: Simuliidae (Diptera).
Distribution: Costa Rica. Possibly Thailand.
Trichospores elongate-ovoid, lacking a collar and bearing two
distinct long
appendages. Thallus consisting of a main axis bearing multiple
pinnately
arranged branches. Zygospores lance-shaped. In hindgut of Nemouridae
(Plecoptera) nymphs.
Trichospores of Lancisporomyces resemble those of Genistelloides which also infest Plecoptera nymphs. However, the unique lance-shaped zygospores are unusual. A single specimen of another species of Lancisporomyces was found earlier in a Nemouridae nymph in Arkansas, USA, but it remains undescribed.
Type species: Lancisporomyces vernalis Santamaria
Lancisporomyces anguilliformis Strongman & M.M. White, 2006
Thallus extensively branched, holdfast
inconspicuous, 2-4 trichospores produced per fertile tip. Trichospores
ellipsoidal, swollen in mid-region (23.4-32.5 x 4-6 µm), with two
short, thick appendages not coiled within the generative cell, no
collar. Zygospores are produced in series, arising from swellings along
a thallus branch. Individual zygospores occur on a clavate
zygosporophore (25-34.5 x 8-9.5 µm), and are slightly sigmoid (125-151
µm in length, the base (3-5 µm wide) is delineated from the
zygosporophore by a septum, the zygospore is uniform through the middle
(4.5-5 µm wide) to the tip (5-5.5 µm wide) which has a thickened wall,
tapering abruptly to a point. Four species.
Illustrations: Fig. 11.310.
Host: Allocapnia pygmaea Burmeister nymph (Plecoptera, Capniidae).
Distribution:
Reference: Strongman and White, 2006, Strongman,
2007.
Lancisporomyces falcatus Strongman & M.M. White, 2006.
Thallus with a central axis, primary branches large, arising regularly along the axis, tapering to finer branches bearing 2-4 trichospores that arise from small projections on the side of the fertile tips of terminal branches. Trichospores long-ellipsoidal, 31-39.4 x 4-6 µm, slightly swollen in midregion (4-6 µm in width), tapered at the distal end (3-4 µm wide), two appendages, one long and relatively thick, the other short and thin or sometimes missing. The appendages are not coiled within the generative cell, and the spores have no collar. Zygospores sickle-shaped (119-)132-177 µm long, produced singly on a zygosporophore arising from a bulbous conjugation cell. A septum delineates the zygospore from the zygosporophore, the base of the zygospore is 3-5.5 µm wide, then it swells along the mid-region (6.5-10 µm wide) and gradually tapers at the tip to 3-5 µm wide, with a conspicuously thickened wall at the distal end.
Illustrations: Fig. 11.309.
Host: Paracapnia angulata Hanson (Plecoptera, Capniidae).
Distribution:
Lancisporomyces nemouridarum Strongman & M.M. White, 2006
Thallus with a central axis, large primary branches forming regularly along the axis with sparse secondary branching, typically 1-2 trichospores on the fertile ends of secondary branches, often with one spore produced apically on a branch. Trichospores long-ellipsoidal (33-56 x 5.5-9 µm), slightly swollen in the midregion, with two long, thin appendages coiled within the generative cell prior to release. Zygospores lanceolate, 141-205 µm long, developing on a zygosporophore arising from a swollen conjugation cell, a septum delineates the base (3.5-5 µm wide) of the zygospore, which is swollen at the apical region (44-47 x 8-9 µm) tapering abruptly at the distal end, the wall is conspicuously thick-ended at the tip.
Illustrations: Fig. 11.308.
Host: Amphinemura nigritta
(Plecoptera, Nemouridae). In Mexico, in Nemouridae nymphs.
Distribution:
Reference: Strongman and White, 2006; Valle,
White, and Cafaro, 2008.
Lancisporomyces vernalis Santamaria, 1997
Trichospores elongate-ovoid, (17-)23(-31) x (3.6)-4.5(-5.5) µm, (2-)4(-7) per fertile branch, lacking a collar and bearing two distinct long appendages, which are helically oriented within the generative cell before their release. Thallus consisting of a main axis composed of very elongated cells. Basal cell long, bearing multiple pinnately arranged branches, laterally adnate to the hindgut cuticle and adhering to it by a series of small pits. Holdfast small and pointed. Multiple branches appearing from all parts of the thallus, including opposite and verticillate branches. Bulbs and swellings observed along the branches before new ramifications appear at these points. Zygospores lance-shaped (67-79 µm long), consisting of a broadened head (36-41 x 5.4-7.2 µm) with a thickened distal wall, and an elongated narrow base (3-3.6 µm diam). Zygosporophore undifferentiated, thus the zygospores are directly supported by the conjugated cell or are formed at some distance from the conjugation. Conjugations scalariform.
Illustrations: Fig. 11.161.
Host: Nemoura sp. (Plecoptera, Nemouridae).
Distribution: Spain (Barcelona).
Reference: Santamaria, 1997.
Legerioides
White, 1999
Trichospores obpyriform, without a collar, bearing two appendages. Conjugations may be homothallic. Conjugation occurs between an extension of a swollen cell and a branch. Zygosporophore borne on a swollen cell. Zygospores biconical, attached submedially and obliquely to the zygosporophore. Attached to hindgut lining of freshwater Isopoda. Monotypic.
Type species: Legerioides tumidus White.
Legerioides tumidus White, 1999
Septate thalli with main axis of 2-3 or more elongate cells (100-)134(-155) x (9-)11(-17) µm. Main axis branched at intervals. Base cupped initially, producing broad and blunt lobelike processes at maturity. Trichospores long-obpyriform to nearly cylindrical, (37.2-)41(-43.7) x (6.9-)7.6(-8.3) µm, with two long appendages; appendages broader near the spore, upon detachment arranged like a helix but later uncoiling. Conjugation occurs between extension of a swollen cell and a non-swollen branch. Non-swollen branches may connect to extensions of more than one swollen cell. Zygosporophore (25-)30(-37) x 5-6 µm borne on a swollen cell. Zygospores biconical (75-)88(-106) x (8.8-)10(-13) µm, attached submedially and obliquely.
Illustrations: Fig. 11.50.
Host: Caecidotea communis (Isopoda). This is the only species of Harpellales known from isopods.
Distribution: Massachusetts, USA.
Reference: White, 1999.
Legeriomyces
Pouzar, 1972
= Genistella Léger & Gauthier, 1932
Trichospores obpyriform, without a collar, bearing 2 appendages. Zygospores biconical, attached submedially and obliquely to the zygosporophore, upon detachment retaining a collar and a single appendage. In hindgut of larval Ephemeroptera. Seven species.
Type species: Legeriomyces ramosus Pouzar.
Five illegitimate species of Legeriomyces have been
described under
the name Genistella: G. chironomi Tuzet & Manier,
1953 (now Smittium
chironomi); G. choanifera Tuzet & Manier, 1953
(probably a Smittium
sp.); G. mailleti Tuzet & Manier, 1955 (probably L.
ramosus);
G. microspora Gauthier, 1960 (now Gauthieromyces microsporus);
and G. rhitrogenae Tuzet & Manier, 1955 (insufficiently
described).
Legeriomyces aenigmaticus Lichtwardt & Williams, 1983b
Thalli highly branched, sometimes in dense tufts or clumps with a mass of contorted cells in the holdfast region, producing one or more of three trichospore sizes: (1) 14-23 x 3.5-5 µm; (2) 30-36 x 6-8 µm; (3) 40-49 x 7-9 µm. Trichospores long-obpyriform, with two appendages; appendages unusually broad (3-7 µm) in the two larger spore sizes, progressively narrowing towards their free ends. Smallest trichospores most common, borne in series of up to 15 per fertile branch. The two larger size trichospores borne 2-4 per fertile branch, with one or both larger types on the same thalli that produce the smallest spores. Zygospores unknown.
Illustrations: Fig. 11.175.
Host: In hindgut of Drunella spinifera Needham (Ephemeroptera, Ephemerellidae) nymphs.
Distribution: Known from one small stream, Johnson Creek, draining into Swan Lake in northwestern Montana, USA.
The unusual feature of this species is the three class sizes into which the trichospores fall. The only known host species was found in fair abundance, mostly on silted substrates, in the otherwise clear mountain stream. At least nine other trichomycetes have been collected in the lotic insect fauna of Johnson Creek, which is also the type locality for Harpella leptosa.
Reference: Lichtwardt and Williams, 1983b.
Legeriomyces
algonquinensis Strongman & M.M. White, 2008
Thallus sparse, no conspicuous holdfast, fertile branches with 4-8
generative cells per branch, each producing a slightly obpyriform
trichospore 19.5-21.5 x 4.5-5.5 µm, with two appendages, no collar. No
zygospores found.
Illustrations: Fig. 11.337.
Host: In hindgut of Arthroplea
bipunctata McDunnough nymphs (Ephemeroptera, Heptageniidae).
Distribution: Standing water in a ditch, Algonquin Provincial
Park, Ontario, Canada.
Reference: Strongman and White, 2008.
Legeriomyces
dolabrae Valle, 2007
Thalli sparsely ramified from the base, with an axial filament
diameter of 6-7.5 µm. Basal cell slightly broadened, with a conical
secreted holdfast. Trichospores 36-43 x 8.5-9.5 µm, elongate-obpyriform
without a collar but with two appendages differing in length.
Appendages wider at the proximal end, helically coiled inside the
generative cell. Generative cells measuring 6-7.5 µm diameter, variable
in length occurring in a series of 2-5 cells per fertile branch.
Zygospores 39-43 x 9-9.5 µm, biconical, obliquely attached to the
zygosporophore and markedly asymmetrical. The proximal end (9-12 µm) is
curved toward the zygosporophore, whereas the longer end (26-30 µm) is
straight. Zygosporophore 12-13.5 x 5-6 µm, with a dense cytoplasm that
aggregates into a slender conical shape after staining with LPCB. The
zygospore on release has a collar (11-13.5 x 5-6 µm) at its base. In
hindgut of Baetidae (Ephemeroptera) larvae.
Illustrations: Fig. 11.318.
Host: In hindgut of Baetis
rhodani (Pictet) (Ephemeroptera, Baetidae) nymphs.
Distribution: Spain.
Legeriomyces
minae Strongman, 2007
Thallus attached to the hindgut by a conspicuous, pigmented, knobby
holdfast, multiple thalli can be fused together at the holdfast.
Branches (2-6) originate from the holdfast and secondary branching is
profuse. Trichospores are dimorphic with large spores measuring 33.5-37
x 6.5-8 µm, ellipsoidal with a slight submedial swelling, bearing two
long, broad appendages, no collar. Small trichospores, 9.5-11 x 3-3.5
µm, with sligiht submedial swelling, bearing two broad appendages that
can either be long or short (2 x the length of spores), no collar.
Trichospores produced on the generative cell, with the appendages
coiled within the generative cell prior to spore formation. Both, or
only one form of trichospore, can occur on a single thallus, but
typically only small spores are produced on thalli with zygospores.
Zygospores (Type II) biconical, 50.5-71 x 9.5-11 µm, 4.5 µm wide at
both ends where the spore begins to taper, with a short collar and
single appendage upon release. Zygospores attached submedially and
obliquely to the zygosporophore (19.5-22.5 x 5.5-6 µm), which arises
from a cell formed by two conjugated branches. In hindgut of mayflies
(Ephemerellidae).
Illustrations: Fig. 11.327.
Host: Ephemerella invaria
(Ephemeroptera, Ephemerellidae) nymphs.
Distribution: Trout River near Tyne Valley, Prince Edward Island,
Canada.
Legeriomyces
ramosus Pouzar, 1972
= Genistella ramosa Léger & Gauthier, 1932
Trichospores long-obpyriforrn, 31-49 x 6-10 µm, with 2 long appendages. Biconical zygospores 41-70 x 7-10 µm, upon detachment with a collar and a single appendage. Type species.
Illustrations: Fig. 11.13.
Hosts: In hindgut of Ephemeroptera nymphs, including Baetis rhodani Pict. and B. bioculatus L. (Baetidae), and Ephemerella infrequens McDunnough (Ephemerellidae).
Distribution: Streams in the French and Swiss Alps, French Pyrénées,
Spain,
Norway,
and
Montana, USA; possibly also in the foothills of the Sierra Nevada
Mountains,
California, USA. (Whisler, 1963) and England (Moss, 1979).
Newfoundland, Canada.
This appears to be primarily a European species, and Baetidae nymphs are the usual host. The appendages of L. ramosus can be seen forming within the generative cell before trichospore outgrowth commences. Upon initial release of the mature trichospore the 2 appendages are intricately wound around each other, then they separate, straighten out, and become somewhat divergent. The appendages are often broad near the trichospore body; they were unusually broad in one collection in Montana (Lichtwardt and Williams, 1983b). Infrequently, 1 appendage may be noticeably shorter than the other (Moss, 1979; Lichtwardt, unpublished). Manier (1973a) has published an electronmicrographic study of the species.
References: Léger and Gauthier, 1932, 1935; Manier, 1962, 1973a;
Whisler,
1961, 1963; Moss, 1979; Lichtwardt and Williams, 1983b; White and
Lichtwardt, 2004. Strongman, 2010.
Legeriomyces rarus Lichtwardt & Williams, 1993 (in Williams and Lichtwardt, 1993)
Trichospores long-obpyriform to almost ellipsoidal, (25-)27(-31) x 5.5-8 µm, collarless, with 2 long appendages. Zygospores (Type II) 42-51 x 6-9 µm.
Illustrations: Fig. 11.158.
Host: Tasmanocoenis sp. (Ephemeroptera, Caenidae); Caenis luctuosa Burmeister (in
Spain).
Distribution: Western Australia, Australia; Iberian Peninsula and
Balearic Islands, Spain. Ontario, Canada. Dominican Republic.
Reference: Williams and Lichtwardt, 1993; Valle and Santamaria,
2004b, Strongman and White, 2008. Valle and Cafaro, 2010.
Legeriosimilis
Williams, Lichtwardt, White & Misra, 1999
in Williams and Lichtwardt, 1999
Trichospores elongate-obpyriform, collarless, with 3 wide tapering appendages ending in a knob-like structure, with very fine appendages sometimes extending beyond the terminal knob. Zygospores biconical, submedian, attached at an oblique angle to the zygosporophore (Type II). Attached to hindgut cuticle of Ephemeroptera nymphs. Five species.
Type species: Legeriosimilis tricaudata
Williams,
Lichtwardt, White & Misra.
Legeriosimilis elegans
Strongman, Juan Wang & S.Q. Xu, 2010
Thallus sparse with 2-3 branches arising from a cup-shaped holdfast
that secretes material onto the hindgut lining. Trichospores (2-4) on
tips of short branches slightly obpyriform, 54-56 x 7-8 µm, with three
broad appendages, no collar. Zygospores unknown. Attached to hindgut of
mayfly nymphs.
Illustrations: Fig. 11-352.
Host: Baetidae, Ephemeroptera.
Distribution: Shaanxi Province, China.
Reference: Strongman, Wang, and Xu, 2010.
Legeriosimilis europaeus White & Lichtwardt, 2004
Trichospores long-obpyriform, 33-40 x 6-8 µm, with 3 wide appendages with a knob-like structure part way down each appendage. Zygospores (Type II) 70-83 x 11-13 µm, zygosporophores about 25-35 x 9 µm.
Illustration: Fig. 11.274.
Host: Ameletus inopinatus Easton nymph (Ephemeroptera, Siphlonuridae).
Distribution: Norway.
Reference: White and Lichtwardt, 2004.
Legeriosimilis
halifaxensis Strongman & M.M. White, 2011
Densely branched thallus with a thick (5-10 µm),
sometimes
bulbous elongated basal cell attached to the hindgut lining by a
disk-like
holdfast. Trichospores obpyriform, (12-)16.5-22 µm long, 3.5-5 µm wide
below
midline, tapering to 2-3.5 µm just behind the rounded apex, with three
thick
appendages tapering at the tips. Trichospores borne on terminal
branchlets, 2-8
per branchlet. Zygospores unknown.
Illustrations: Fig. 11.374.
Host: Eurylophella temporalis (Ephemerellidae,
Ephemeroptera),
Distribution: Nova Scotia, Canada.
Legeriosimilis leptocerci
M.M. White & Strongman, 2008.
Thallus composed of multiple thick branches, further dividing into thinner fertile branches. One to four generative cells on terminal branches. Trichospores 24-28 x 5,5-6 µm weakly obpyriform, with three thin basal appendages and no collar. Stout zygosporophores 24-31 x 9-11.5 µm, arise directly from conjugating hyphae Zygospores (Type II) 67-73 x 12-14 µm, attached to the zygosporophore obliquely and sub-medially.
Illustrations: Fig. 11.338.
Host: In hindgut of Siphlonurus sp. nymphs (Ephemeroptera, Siphlonuridae).
Distribution: Papineau Creek, Ontario,
Canada.
Reference: Strongman and White, 2008.
Legeriosimilis tricaudata Williams, Lichtwardt, White & Misra, 1999 (type species)
Trichospores up to 15 per fertile branch, elongate-obpyriform, (33-)47(-52) x (7-)9.5(-11) µm, collarless, with 3 wide tapering appendages ending in a knob-like structure, with very fine appendages sometimes extending beyond the terminal knob. Zygospores (Type II) 52-58 x 11-13 µm. Type species.
Illustrations: Fig. 11.51.
Host: Ameletus sp. (Ephemeroptera, Siphlonuridae).
Distribution: USA (Colorado, New York).
Reference: Williams and Lichtwardt, 1999.
Legeriosimilis
whitneyi Strongman & M.M. White,
2008.
Thallus usually with two successive swollen basal cells 20-30 x 7-9
µm, attached to the hindgut lining by cement secreted from the holdfast
cell. Branches from the basal cells further branch, bearing spores
distally. Trichospores slightly obpyriform, no collar, 20-26.5 x 4.5-6
µm, bearing three thick appendages equal in length. Six to eight
generative cells per fertile branch with each generative cell at least
half the length of the trichospore. Conjugation between adjacent hyphae
results in a swollen cell from which arises the zygosporophore (13-17 x
4.5-5
µm) arises. Zygospores (Type II) 46-54.5 x 7-8.5 µm, attached
obliquely to the zygosporophore and submedially near the spore tip,
with a short collar when released.
Illustration: Fig. 11.339.
Host: In hindgut of Ephemerella
temporalis McDunnough nymphs (Ephemeroptera, Ephemerellidae).
Distribution: Stream in Algonquin Provincial Park, Ontario, Canada.
Orphella
Léger & Gauthier, 1931
Sporulating branches in the form of a cyme. Generative cells subterminal, produced singly on separate branches, each generative cell giving rise to one curved trichospore. In hindgut of Plecoptera nymphs. Seven species.
Type species: Orphella coronata Léger & Gauthier.
Orphella was the first genus of Legeriomycetaceae described. It was again described as a "new genus" by Léger and Gauthier the following year (1932), along with six other new genera of Harpellales, at which time the family Genistellaceae (now Legeriomycetaceae) was established. A second but illegitimate species, Orphella culicis (nom. nud.) from mosquito larvae, was described by Tuzet and Manier (1947a); it was later renamed Smittium culicis by Manier (1969b).
At maturity, sporulating thalli of Orphella spp. typically
protrude
from the anus of the host, and their presence is evident before the
nymph is
dissected.
Orphella avalonensis White, Lichtwardt & Colbo
Thalli up to 900 µm long with a main axis bearing multiple short sterile branches at the base and apically producing several branches that terminate in clusters of basal cells, each producing several generative cells with terminal cells about 30-95 µm long. Trichospores about 6 µm wide, coiled, developing from generative cells 20-22 x ~6 µm. More rarely dissemination units much larger, with generative cells 28 x 11 µm, terminal cells 80 µm long, and trichospores 11 µm wide.
Illustration: Fig.
11.247
Host: Leuctra ferruginea (Walker) and Leuctra sp. (Plecoptera, Leuctridae).
Distribution: Newfoundland and Ontario, Canada; Great Smoky
Mountains National
Park.
Reference: Lichtwardt et al., 2001; White, Siri, and Lichtwardt,
2006. Strongman adn White, 2008.
Orphella catalaunica Santamaria & Girbal, 1998
Trichospores straight, 54-66 x 5.4-7.2 µm,
with parallel margins and a rounded apex (exceptionally the
trichospores may be
slightly bent, but never allantoid), without appendages, produced
singly from
clavate generative cells (22-29 x 4-7.2 µm,
including the supporting cell) that also bear apically a sterile,
usually
filiform terminal cell, which is, when fully developed, much longer
than the
trichospore [166(-252) µm,
or 11-18 mm when terminal
cells appear unusually
shortened] and 0.9(-3.6) µm diam. The
base of the generative cell possesses a small, inconspicuous,
supporting cell.
Thalli 500-800 µm long,
consisting of a
main axis of 3-5 cells [each (44-)72(-136) x 6-11 µm] with 4-12 lateral
subsidiary
branches at the somewhat
pointed base of the holdfast cell and 1-5 at lower septa along the main
axis.
These subsidiary branches are simple and unicellular. From the
unbranched main
axis arise 1-5 fertile simple or, rarely, once ramified branches, each
bearing
a sporulating head consisting of 3-4 clavate basal cells, each basal
cell
bearing 2-6 generative cells. Zygospores produced homothallically,
coiled 360 degrees at proximal end, distal end straight, 57-72 x 5.4-8
µm. May protrude from the
host's
anus. Zygospores discovered by Valle and Santamaria, 2005.
Illustrations: Fig.
11.162, Fig. 11.286.
Host: Leuctra sp. (Plecoptera, Leuctridae).
Distribution: Spain (Barcelona); Norway.
Reference: Santamaria and Girbal, 1998; White and Lichtwardt, 2004;
Valle and Santamaria, 2005.
Orphella coronata Léger & Gauthier, 1931
Thallus up to 1 mm long, attached to host cuticle by a cupulate swelling with short radiating branches. Fertile branch tips cymelike, commonly ending in three pairs of tapered branches, each of the six branches bearing one curved trichospore, 45-50 µm long, from a subapical generative cell. Zygospores helicoidal, 30-35 x 5.5-7 µm, heterothallic, associated with hyphal conjugations. Type species.
Illustrations: Fig.
11.7; Fig.
11.173, Fig. 11.287.
Host: In hindgut of Protonemura humeralis Pict. and possibly Nemura cinerea (Retz.) (= N. variegata Oliv.) nymphs (Plecoptera, Nemouridae).
Distribution: Streams of the Dauphiné French Alps, France; Norway,
Spain.
This unusual species has not been reported since Léger and Gauthier's descriptions were published. The cymose trichospore arrangement is unique, as is also the presence of a sterile terminal cell above the single generative cell of each fertile branch. Léger and Gauthier (1931) described the trichospores as detaching at maturity, but they observed no appendages. In fact, no appendages of trichospores were described until 1935(b), by Léger and Gauthier; in that publication their illustrations of trichospore appendages of several previously described genera of Harpellales did not include Orphella. Zygospores were found by Valle and Santamaria (2005).
References: Léger and Gauthier, 1931, 1932; White and Lichtwardt, 2004; Valle and Santamaria, 2005.
Orphella dalhousiensis Strongman & M.M. White, 2006
Thallus consisting of a central axial filament of 4-6 elongated cells, attached to the hindgut lining by a cup-shaped holdfast that bears small projections and is enveloped in mucilage. The central axis has at each septum a whorl of short, lateral branches and at its apex 1-3 long (>500 x 6-9 µm) fertile branches that are slightly clavate at the distal end. Each fertile branch bears at the clavate tip a complex arrangement of cells that produce and support the trichospores, 2-6 basal cells (28-40 x 6.5-9 µm), producing along one side 2-8 trichospores, each borne on a tripartite array of generative and accessory cells, consisting of a small supporting generative cell (4-5 x 1.5-2 µm) at the base of the generative cell (14.4-16 x 4-5.5 µm) and a terminal cell (5-8 x 2.5-4) µm on top of the generative cell. An allantoid trichospore (26-41 x 3-4.5 µm) emerges at the junction of the generative and terminal cells. The combined length and width of the generative and accessory cells is 19-26(-30) x 4-4.5 µm. The trichospore with its generative and accessory cells is shed from the basal cell, as a dissemination unit, when fully mature. Zygospores are homothallic or heterothallic. Lateral whorled branches on the central axial filament branch dichotomously to produce numerous fine branches at the tip. These conjugate and give rise to a long, often twisted conjugating hypha that swells at the tip to form the zygosporophore (25-32 x 5.5-7.5 µm) and one terminal cell that is very short (approx. 12-15 µm) after the zygospore forms, but at zygospore release can reach 100-200 µm. The zygospore is coiled, 63-82.5 x 4.5-6 µm (length x width) with a coil diameter of 18-25 µm. Zygospores produced sparsely within the gut but densely on hyphae associated with a protruding from the anus of the shed nymphal exuvium (after days to weeks of incubation at 4-5 C.
Illustrations: Fig. 11.311.
Host: Paracapnia angulata nymphs (Plecoptera, Capniidae).
Distribution: Nova Scotia and Prince Edward Island, Canada.
Reference: Strongman and White, 2006, Strongman,
2007.
Orphella haysii Lichtwardt & Williams, 1987
Thallus consisting of one principal axis, branched at the base, with apical branches producing 2-6 subsidiary cells in a cluster. Each subsidiary cell producing one or more branches that develop into a generative cell (20-)23(-24) x (6-)6.9(-7.2) µm with a sterile terminal cell generally shorter than the generative cell. Trichospores produced by the generative cell allantoid (more rarely coiled), (29-)34(-44) x (5.7-)6.5(-7.2) µm, released by dehiscence of the generative cell from the subsidiary cell, dispersing as a 3-celled unit without appendages. Zygospores unknown. May protrude from host's anus.
Illustrations: Fig. 11.78.
Host: Zapada haysi (Plecoptera, Nemouridae).
Distribution: Colorado, USA.
Reference: Williams and Lichtwardt, 1987.
Orphella helicospora Santamaria & Girbal, 1998
Trichospores spirally coiled, with a diameter of 11-16.2 µm, and a width of 3.6-4.5 µm, without appendages, produced from fusiform generative cells (16-19 x 2-4.5 µm, including the supporting cell) that also bear apically a sterile, clavate terminal cell (5.4-18 x 1.5-2 µm). The base of generative cell possesses a small, inconspicuous, supporting cell . Thalli 522-1008 µm long, consisting of a main axis of 2-3 very unequal cells (45-153 x 5.4-12.6 µm), the holdfast cell is shorter and bifurcate, with each branch bearing 5-12 subsidiary branches, simple and consisting of up to four cells, orientated in the opposite direction to that of the main axis. The main axis lacks lateral branches, and supports 2-5 simple or ramified fertile branches, each subtending a sporulating head of 4-6 clavate basal cells, each basal cell bearing 3-9 generative cells. Zygospores produced homothallically, helicoidal, 25-28 x 5.5-7.5 µm. May protrude from the host's anus.
Illustrations: Fig.
11.163, Fig. 11.288.
Host: Leuctra sp. (Plecoptera, Leuctridae).
Distribution: Spain (Barcelona); Norway.
Reference: Santamaria and Girbal, 1998; White and Lichtwardt, 2004;
Valle and Santamaria, 2005.
Orphella hiemalis Peterson, Lichtwardt & Huss, 1991
Trichospores allantoid, 65-120 x 6-7 µm, more rarely straight or slightly bent without appendages, produced from clavate generative cells [25-40 x (4-)6-8 µm] that also bear apically a sterile, filiform terminal cell, which is usually longer than the trichospore and 0.5-2 µm diam. Thalli up to 1 mm long, consisting of a main axis of cells (each 70-120 x 12-27 µm) with one or more lateral subsidiary branches at the somewhat pointed base of the holdfast cell and usually at each septum along the main axis. From the unbranched or branched apex of the main axis arise 1-7 fertile branches (100-330 x 7-15 µm) each bearing a sporulating head consisting of 3-6 clavate basal cells, each basal cell bearing 2-4 generative cells. Trichospores remain attached to their deciduous generative cells, forming a dissemination unit consisting of trichospore, generative cell, and terminal cell. Zygospores unknown. May protrude from host's anus.
Illustrations: Fig. 11.84.
Host: Allocapnia spp. (Plecoptera, Capniidae).
Distribution: USA (Arkansas, Oklahoma).
Reference: Peterson, Lichtwardt and Huss, 1991.
Pennella
Manier ex Manier, 1968
[= Pennella Manier, 1963b, nom. nud.]
Base of principal thallial cell simple, lobed or bifurcated, cemented to host cuticle by a mucilaginous secretion. Trichospores obpyriform to cylindrical, without a collar, bearing about 4-6 appendages. Biconical zygospores attached medially and oriented parallel to axis of zygosporophore. In hindgut of larval Simuliidae (Diptera). Eight species.
Type species: Pennella hovassi Manier ex Manier.
Pennella angustispora Lichtwardt, 1972
Thalli with little secondary branching, consisting of a main axis up to 1 mm long. Base of primary cell tapered to a rounded point, rarely slightly bifurcate, cemented to the hindgut lining by a mucilaginous substance. Trichospores cylindrical-clavate, almost filiform, straight to slightly curved or bent, (50-)80(-104) x (2.5-)4(-6) µm, without a collar, bearing 4-6(-7) fine appendages. Heterothallic. Biconical zygospores 82-92 x 15-17 µm, attached medially and oriented parallel to the zygosporophore axis, formed above the area of conjugation from the end of one of the conjugant cells. Zygosporophores 32-36 x 10-12 µm.
Illustrations: Fig. 11.169.
Hosts: In hindgut of many species of larval Simulium (Diptera, Simuliidae), including S. arcticum Mall., S. argus Will., S. virgatum Coq., and S. vittatum Zett.
Distribution: Montana, Wyoming, Colorado, Utah, Idaho, and
California, USA;
Aomori
Prefecture, Honshu, Japan, Spain, Armenia.
Pennella angustispora is relatively common in blackfly larvae in the montane regions of western USA. It often occurs along with other blackfly trichomycetes. The species has been found once in Japan, in 1967 (unpublished). Pennella simulii, a rarer species, has been found in some of the same blackfly species, but not in the same host specimens; it is readily distinguishable from P. angustispora by the long-ovoid shape of its trichospores. The fine structure of the holdfast cell of P. angustispora has been studied by Mayfield and Lichtwardt, 1980.
References: Lichtwardt, 1972; Dang, 1978; Mayfield and Lichtwardt,
1980; Lichtwardt et al., 1987, Sato, 2002, Valle, 2004, 2007, Nelder et
al., 2005. Beach and White, 2012.
Pennella arctica Lichtwardt & Williams, 1984 (in Lichtwardt, 1984a)
Mature thalli 500 mm or more in length, consisting of a large principal coenocytic cell whose base is simple to deeply and repeatedly bifurcate and embedded in a mucilaginous cementing substance. Trichospores long-obpyriform, (40-)48(-58) x (8-)9(-l 1) µm, with (2-)6(-7) fine appendages and no collar. Zygospores (65-)70(-72) x 15-18 µm, attached medially and parallel to the zygosporophores which measure 35-40 x 13-20 µm.
Illustrations: Fig. 7.10; Fig. 11.14.
Hosts: In hindgut of larval Prosimulium ferrugineus Wahlberg, P. exigens Dyar & Shannon, and Simulium arcticum Malloch (Diptera, Simuliidae).
Distribution: In river at Abisko, Sweden, Norway, and streams in northwestern Montana, USA.
The amount of bifurcation in the basal cell of mature thalli of Pennella arctica is quite variable, and in some cases it may resemble P. hovassi. However, the dimensions and shape of the trichospores alone are sufficient to distinguish P. arctica from all other described species.
Reference: Lichtwardt, 1984a; White and Lichtwardt, 2004.
Pennella
asymmetrica Williams &
Lichtwardt, 1990
Collarless trichospores ovoid, (35-)42(-52) x (12-)14(-17) µm, eccentrically attached at their base to a generative cell, each subterminal trichospore somewhat appressed to the generative cell above it, upon release bearing about four very fine appendages several times the length of the spore. Base of main thallial axis simple, with a mucilaginous secretion. Zygospores unknown.
Illustrations: Fig. 11.141.
Host: Austrosimulium tillyardianum (Diptera, Simuliidae).
Distribution: South Island, New Zealand.
<>Reference: William s and Lichtwardt, 1990.Pennella
grassei Manier, 1968
[ = Glotzia grassei Tuzet & Manier, 1955a, nom. nud.]
Thallus up to 1 mm long with a verrucous tapered basal cell which may be slightly digitate. Principal axis consisting of cells 7-9 µm diam and branches 5-7 µm diam. Trichospores cylindrical, 49-59 x 4.5-5.5 µm, with about 4 petaloid appendages that can subdivide at their extremity, and with no collar. Homothallic. Biconical zygospores about 90 x 15 µm, attached medially and oriented parallel to their zygosporophores which measure about 35 x 12 µm.
Illustrations: Fig. 11.167.
Host: In hindgut of Simulium equinum L. larvae (Diptera, Simuliidae).
Distribution: Streams of the Gorge d'Enfer, Les Eyzies, Dordogne, France.
The description of this apparently rare species was originally given under the name Glotzia grassei Tuzet & Manier, 1955a (nom. nud.). In 1963b Manier corrected the description and illegitimately transferred the fungus to the genus Pennella, which she established in that paper (she provided no Latin diagnosis nor did she cite a nomenclatural type for P. grassei). The name P. grassei was validly published by Manier in 1968, but was incorrectly cited as though it were a new combination (the "basionym" was not legitimate).
There is no mention of a mucilaginous secretion around the basal cell typically seen on most thalli of other Pennella spp. The trichospores of P. grassei have unusual appendages in that they are described and illustrated (in Manier, 1963b) as being petaloid and sometimes subdivided into finer filaments; appendages of other Pennella spp. are usually very fine throughout their length. Despite these features, P. grassei seems to be placed in the correct genus.
References: Tuzet and Manier, 1955a; Manier, 1963b, 1968.
Pennella
hovassi Manier ex Manier, 1968
[= Pennella hovassi Manier, 1963b, nom. nud.]
Mature thalli up to 1 mm long; basal cell of main axis 7-9 µm diam, simple or more often deeply and repeatedly bifurcated, with numerous branches 5-7 µm diam arising laterally; basal cell partially surrounded by a secreted mucilaginous cementing substance. Trichospores long-obpyriform, 22-33 x 4.5-7 µm, lacking a collar and with 6 appendages. Heterothallic. Zygospores 68-79 x 7.5-13 µm, attached medially and parallel to the zygosporophore, which measures about 25-30 X 8-12 µm. Type species.
Illustrations: Fig. 11.168.
Hosts: In hindgut of larval Simuliidae (Diptera), including Simulium monticola Fried, S. vittatum Zett., and Prosimulium sp.
Distribution: Department of Puy-de-Dôme, France; Newfoundland,
Canada, Armenia.
References: Manier, 1963b, 1968; Frost and Manier, 1971, Nelder et
al., 2005.
Pennella montana Lichtwardt, 1997
Bases of mature thalli dichotomously bifurcate one or more times, producing a mucilaginous secretion. Trichospores long-ovoid, (39-)60(-72) x 8-10 µm, with multiple very fine appendages. Zygospores 91-100 x 18-20 µm; zygosporophores 38-46 x 13-15 µm.
Illustrations: Fig. 11.132.
Hosts: Simulium spp. (Diptera, Simuliidae).
Distribution: Costa Rica. Thailand. Mexico.
Reference: Lichtwardt, 1997. Valle et al., 2011.
Pennella simulii Williams
&
Lichtwardt, 1971
Branched thalli up to 1 mm long, with a simple and tapered,
occasionally
digitate, basal cell surrounded by a mucilaginous cementing substance.
Trichospores long-ovoid, (30-)33(-41) x (6.5-)8(-10.5) µm, with about 6
fine appendages
and no collar. Biconical
zygospores (84-)90(-96) x (19-)22(-24) µm,
attached medially and oriented parallel to the zygosporophore, formed
above the
area of conjugation from the end of one of the conjugant cells.
Zygosporophore
(32-)36(-40) x (12-)14.5(-16) µm.
Illustrations: Fig. 11.171.
Host: In hindgut of larval Simulium spp. (Diptera, Simuliidae), including S. vittatum Zett. and S. venustum Say.
Distribution: Wyoming, Colorado, and Great Smoky Mountains Naitonal
Park, USA; Newfoundland and Ontario, Canada; Argentina.
The known distribution of Pennella simulii is limited to a few streams in the Rocky Mountains and in the vicinity of St. John's, Newfoundland. Infestation may be high in some populations of blackfly larvae. Distribution of the species is likely much greater than is currently known. Pennella simulii is distinguishable from the more widespread species, P. angustispora, by the long-ovoid shape of its trichospores, the often tapered basal cell, slightly greater branching of thalli, and its wider zygospores.
When conjugations occur in P. simulii between branches of two thalli, the zygosporophore and zygospore develop at the end of one of the conjugants, the receptor cell. Donor branches may conjugate with more than one receptor branch, and may terminate their development by producing a terminal trichospore.
Reference: Williams and Lichtwardt, 1971; Lichtwardt, White and
Colbo, 2001; White, Siri and Lichtwardt, 2006; López
Lastra et al.,
2005, Strongman and White, 2008.
Plecopteromyces
Lichtwardt, Ferrington & López Lastra, 1999
Trichospores long-ellipsoidal, without a collar, bearing one or two
broad
appendages. Zygospores (Type IV) turbinate, attached to zygosporophore
at
broader end. In Plecoptera nymphs. Two species.
Type species: Plecopteromyces patagoniensis Lichtwardt,
Ferrington
& López Lastra, 1999.
Plecopteromyces patagoniensis Lichtwardt, Ferrington & López Lastra, 1999
Thalli with few branches, producing up to 14 long-ellipsoidal trichospores per fertile branch, trichospores (25-)33(-42) x 5-7 µm, without a collar with two broad appendages that may remain fused into one; zygospores turbinate, 15-17 x 8-9 µm; zygosporophores 20-40 x 6-8 µm, arising from the conjugation tube.
Illustrations: Fig. 11.53.
Hosts: In nymphs of Limnoperla jaffueli (Navás) and Aubertoperla illiesi (Froehlich) (Plecoptera, Gripopterygidae).
Distribution: Patagonia, Argentina.
<>Reference: Lichtwardt et al., 1999.Plecopteromyces leptoperlarum M.C. Williams & Lichtwardt
Thalli sparsely branched, producing long series of small trichospores without a collar, 12-21 x 2-4 µm, with two short appendages that are sometimes partially curled. Zygospores unknown.
Illustration: Fig. 11.302.
Host: In hindgut of Leptoperla beroe Newman nymphs (Plecoptera, Grypopterygidae).
Distribution: Tasmania, Australia.
Reference: Ferrington, Lichtwardt, Hayford, and
Williams, 2005.
Thalli producing short or long series of trichospores without a collar, 2--30x 3-5 µm, with two short appendages that sometimes adhere together. Zygospores unknown.
Illustration: Fig. 11.303.
Host: In hindgut of Trinotoperla zwicki or T. hardyi Perkins (Plecoptera, Gryptopterygidae).
Distribution: Tasmania, Australia.
Reference: Ferrington, Lichtwardt, Hayford, and Williams, 2005.
Pseudoharpella
Ferrington, White & Lichtwardt - Aquatic Insects 25: 86, 2003
Branched thalli producing coiled trichospores with three appendages. Zygospores (Type II) with nearly median collar and a single appendage. Monotypic.
Etymology: From Gr. pseudos (false) and Harpella
Type species: Pseudoharpella arcolamylica Ferrington, White & Lichtwardt - Aquatic Insects 25: 86, 2003
Pseudoharpella arcolamylica Ferrington, White & Lichtwardt - Aquatic Insects 25: 88, 2003
Thalli branched, mature basal cell consisting of convoluted extensions forming a knot about 15 µm diameter. Trichospores coiled, up to 6 per fertile branch, 40-50 µm long by 3.6-3.8 µm diameter near the base, tapering to 1.3-2.0 µm diameter at the distal end, bearing 3 broad, short and tapered appendages. Zygospores (Type II) 47-62 x 6-7 µm, almost cylindrical, straight or slightly bent, pointed at each end, with a nearly median collar and a single appendage. In hindgut of Dixidae larvae.
Illustrations: Figs. 11.296; Figs. 11.297
Host: Dixa fluvica (Diptera, Dixidae)
Distribution: Minnesota, USA
Reference: Ferrington et al., 2003.
Pteromaktron
Whisler, 1963
Thallus consisting of an arbusculate coenocytic branched main cell with a compact cluster of short fertile branches at its distal end. Trichospores cylindrical, collarless, with a single appendage, each trichospore produced from a separate lateral generative (subsidiary) cell arranged in a unilateral series on a terminal fertile branch. In hindgut of Baetidae (Ephemeroptera) nymphs. Monotypic.
Type species: Pteromaktron protrudens Whisler.
Pteromaktron protrudens Whisler, 1963
Arbusculate, mature coenocytic thalli 942-1730 µm long with a main axis 7-47 µm diam and consisting of lateral and basal branches and a compact, brushlike terminal tuft of sporulating branches that project from the anus, attached to the host cuticle by a digitate to coralloid basal outgrowth. Each fertile branch with a unilateral series of oval to cylindrical generative (subsidiary) cells 21-31 x 4-6 µm, each producing terminally a cylindrical, collarless trichospore 85-97 x 4-6 µm bearing a single long (~1.8 µm) fine appendage with a knob near the trichospore base. Zygospores unknown. In Baetidae (Ephemeroptera) nymphs. Type species.
Illustrations: Fig. 11.7; Fig. 11.67.
Hosts: In hindgut of Callibaetis pacificus Seemann and Cloeon dipterum (L.) (Ephemeroptera, Baetidae).
Distribution: St. Helena Creek, Lake Co., California, and Vermont, USA; and Pierette Pond, near Saint-Gély-du-Fesc, Department of Hérault, France.
Pteromaktron protrudens, known only from two sites in the USA and one site in France (Manier, 1969b), is perhaps the most unusual species of Harpellales with respect to its thallus structure and sporulation. The thallus consists of essentially one large coenocytic arbusculate branching cell which, according to Whisler's description and drawings, is nonseptate except to delimit the generative cells and trichospores. Whereas most other Harpellales produce trichospores directly and basipetally from terminal branches divided into a row of end-to-end generative cells, the trichospores of Pteromaktron protrudens are produced from individual generative cells arranged unilaterally on terminal, nonseptate branches, and their maturation on each terminal branch is acropetalous. Apparently the brushlike fertile tip of the thallus matures entirely outside of the gut. Some thalli of Zygopolaris spp. (also in Ephemeroptera) may likewise sporulate only after protruding from the anus, but internal sporulation is generally more common. The trichospores of Pteromaktron protrudens are structurally similar to those of Spartiella barbata (in Baetidae), but the latter are produced from typical harpellid generative cells.
References: Whisler, 1961, 1963; Manier, 1969b (1970b).
Simuliomyces
Lichtwardt, 1972
Trichospores elongate-ellipsoidal, small, collarless, bearing 2-4 appendages that are usually no longer than the trichospore body. Zygospores attached perpendicularly and medially to the zygosporophore. In hindgut of Simuliidae (Diptera) or Capniidae (Plecoptera) larvae. Monotypic..
Type species: Simuliomyces microsporus Lichtwardt.
Simuliomyces microsporus Lichtwardt, 1972
Branched thalli without a main axis, basal cell sometimes swollen or lobed, producing usually 4-7 generative cells per fertile branch. Trichospores collarless, long-ellipsoidal, 20-30 x 4-6 µm, tip often appearing thick-walled, with 2-4 appendages approximately as long as the trichospore; appendages usually fine, but sometimes slightly broadened near the base and tapering toward the tip. Lateral trichospores arising from a short branchlike extension of the generative cell. Generative cells usually longer than trichospores. Zygospores biconical, somewhat flattened on side of attachment, 34-45 x 7-9 µm, attached medially and perpendicularly to zygosporophore. Zygosporophore about 12-17 x 7-11 µm, arising laterally from one of the conjugating cells. Type species.
Illustrations: Fig. 7.12; Fig. 11.15.
Hosts: In hindgut of many different species of Simuliidae (Diptera) larvae.
Distribution: Widespread in the USA: relatively common in the Rocky
Mountains of Colorado, Wyoming and Montana; and Idaho, and collections
include Kansas,
Utah,
and California. Also known from England, France, Sweden, Norway, and
Australia, Armenia. Ontario, Canada. Mexico.
Simuliomyces microsporus is most apt to be confused with species of Smittium, as apparently happened in two published reports of S. microsporus attached to thalli of Smittium sp. (Ingold, 1967; Moss, 1970) before S. microsporus was described as a new genus and species. What likely was also S. microsporus attached to a thallus of Paramoebidium sp. was identified by Manier (1955a) as Stipella vigilans. The released collarless trichospores with 2-4 short appendages and the Type I zygospores makes S. microsporus readily distinguishable. Attachment of a thallus to other trichomycetes coinhabiting blackfly hindguts in itself suggests that it may be S. microsporus. If thalli are sporulating, but released trichospores (or zygospores) are not available, one can tentatively identify this species on the basis of the size and shape of the trichospores, the usually long generative cells, and the small outgrowths from the generative cells subtending the lateral trichospores. The trichospore tips, especially those mounted in lactophenol-cotton blue, often have a characteristic thick-walled appearance.
References: Lichtwardt, 1972; Manier, 1955a, Ingold, 1967; Moss,
1970; White and Lichtwardt, 2004, Nelder et al., 2005 Strongman and
White, 2008. Valle et al., 2011. Beach and White, 2012.
Simuliomyces spica Peterson & Lichtwardt, 1983
See Ejectosporus spica Strongman.
Stachylina tianensis. Thallus 130–350 x 10–15 µm, with a lobulate,
bulbous base that penetrates the peritrophic matrix, producing 4–25
trichospores. Trichospores long-ellipsoidal, 55–90 x 7–10 µm, with a single
appendage and a short collar, produced on small lateral projections
from the
generative cell, near a septum. Zygospores not seen. On peritrophic matrix
of
chironomid larvae.
Smittium
Poisson, 1936
Trichospores ellipsoidal (or subellipsoidal) to almost cylindrical, with a short or long collar and a single appendage. Zygospores biconical to fusiform, attached to the zygosporophore obliquely and submedially, upon detachment having a collar and single appendage. In hindgut of larval Nematocera (Diptera). Seventy-eight species.
Type species: Smittium arvernense Poisson.
In 1932(b) Poisson named a fungus, Dixidium dixae, from Dixa
sp.
larvae (Dixidae, Diptera), which probably is a species of Smittium.
The
description was so incomplete, however, that it has to be rejected as
an
acceptable name (Manier and Lichtwardt, 1968). Several illegitimate
taxa, now
recognized as Smittium species, are to be found in the
literature. These
include species of the genera Orphella and Rubetella (see
Smittium
culicis), and Genistella and Typhella (see
Smittium
chironomi).
Smittium aciculare Lichtwardt, 1990 (in Lichtwardt and Williams, 1990)
Thalli small, 150-350 µm long, sparsely branched or unbranched, acicular, sometimes fascicled, tapered base without obvious mucilage. Trichospores long fusiform-ellipsoidal, 28-30 x 3.4 µm, without a visible collar. Zygospores unknown.
Illustrations: Fig. 11.102.
Host: Austrosimulium mirabile (Diptera, Simuliidae).
Chironomidae.
Distribution: Queensland, Australia. Mexico.
Reference: Lichtwardt and Williams, 1990. Valle et al.,, 2011.
Smittium acutum Lichtwardt & Grigg, 1998
Thalli well branched, with a tapered and pointed basal cell. Trichospores (21-)28-30 x 4-6 µm, with a collar 1-2 µm long slightly flared outward, and a very fine spiraled to tortuous appendage. Zygospores unknown.
Illustrations: Fig. 11.152.
Host: Chironomidae (Diptera).
Distribution: Oklahoma, USA.
Reference: Lichtwardt and Grigg, 1998.
Smittium alpinum Lichtwardt, 1984a
Thalli with 1-3 long generative cells per fertile branch. Trichospores oval to biconical, (23-)33(-44) x (10-)12(-14) µm, with a cylindrical collar (10-)14(-19) x (2-)3(-4) µm. Zygospores biconical, (63-)75(-83) x (14-)16(-18) µm with a single appendage and a collar (15-)22(-28) x (4-)5(-7) µm attached laterally near one end of the zygospore.
Illustrations: Fig. 11.80.
Hosts: In hindgut of larval Diamesa spp. (Diptera,
Chironomidae) and other Chironomidae.
Distribution: Small streams, near Continental Divide in Glacier National Park, Montana, Idaho, USA; Ontario, Canada, Abisko, Sweden; and Alps in France and Switzerland.
Reference: Lichtwardt, 1984a, Strongman and White, 2008. Beach and
White, 2012.
Smittium angustum Williams & Lichtwardt, 1992 (in Lichtwardt and Williams, 1992c)
Thalli growing in discrete radiating colonies, occasionally developing fusiform intercalary cells. Trichospores subcylindrical, 17-26 x 2.3-2.8 µm, cylindrical collar 3-4 µm long. Zygospores unknown.
Illustrations: Fig. 11.87.
Host: Cricotopus sp. (Diptera, Chironomidae).
Distribution: Western Australia, Australia.
Reference: Lichtwardt and Williams, 1992c.
Smittium annulatum Lichtwardt, 1997
Thalli small and compact, arising from a prominent basal structure consisting of about six cells arranged in a ring. Trichospores elongate-oval, 18-22(-33) x 4-6(-8) µm, collar 3-6 µm long. Up to 8 or more generative cells per fertile branch. Zygospores unknown.
Illustrations: Fig. 11.128.
Host: Simulium sp. (Diptera, Simuliidae).
Distribution: Costa Rica.
Reference: Lichtwardt 1997.
Smittium arcticum Y. Kobayasi, 1969 (in Kobayasi et al., 1969)
Thalli 300-400 µm or more long. Axial hyphae 6.5-12 mm diam near base, arising irregularly from a short cylindrical basal cell 8-10 mm diam and producing nondivergent monopodial branches 3.5-5 µm diam. Generative cells 1-5 per fertile branch, producing terminolateral outgrowths 6.5-12 x 2-2.5 µm bearing oval trichospores (15-)20(-24) x (7-)8(-9) µm; upon detachment trichospores have a short-campanulate or cylindrical collar 1.5-6.5 µm long and bear a single appendage. Zygospores unknown.
Illustrations: Fig. 11.177.
Hosts: In hindgut of Chironomidae (Diptera) larvae.
Distribution: Peters Lake, Alaska.
Reference: Kobayasi et al., 1969.
Smittium arvernense Poisson, 1936
Thalli up to 1.2 mm long, not highly branched, attached to host
cuticle by
means of a disklike holdfast. Trichospores ellipsoidal, 20-25 x 5 µm,
with a short collar and a
single short
fine appendage. Zygospores 30-35 x 8-10 µm,
with a small oblique submedian collar ~2 µm long. Type species. See Smittium mucronatum for
typification of Smittium.
Illustrations: Fig. 11.176.
Hosts: In hindgut of Smittia sp. (Diptera, Chironomidae) larvae.
Distribution: Flowing waters at Besse-en-Chandesse, Department of Puy-de-Dôme, France.
Smittium arvernense apparently has not been found since Poisson's 1936 publication. He referred to what we now call trichospores as "azygospores," and described and illustrated zygospores resulting from the fusion of two hyphae. His sole illustration of a zygospore, a drawing (erroneously called an azygospore in the legend), shows a small submedian collar attached at an angle. It appears that the angle of this collar is opposite to what it should be, on the basis of zygospores of other species subsequently placed in this genus as well as other genera with Type II zygospores. Nor did Poisson mention the single appendage now known to be attached to zygospores of some other Smittium species. Despite these differences, it seems clear that S. arvernense is the correct type for this, the largest, genus of Harpellales.
Reference: Poisson, 1936. Lichtwardt and White, 2011.
Smittium basiramosum Siri, 2010
Thalli up to 350 µm long, ramified only at the base from which a few
branches are produced; attached to the host hindgut by a disk-like
holdfast. Subcylindrical trichospores (30-)33(-35) x 5-6 µm, collar 1-2
µm long, bearing a single appendage. Zygospores unknown.
Illustration: Fig. 11.356.
Host: Polypedilum sp.
Distribution: Aregentina.
Reference: Siri and Lňpez Lastra, 2010.
Smittium biforme White & Lichtwardt, 2004
Thalli dimorphic, producing two trichospore forms: long ellipsoidal trichospores, 34-42 x 9-12 µm, with a campanulate collar; and oval trichospores, 13-15 x 6-7.5 µm, with a cylindrical collar. Zygospores biconical (Type II), 78-82 x 13-18 µm.
Illustration: Fig. 11.275.
Host: Diamesa aberrata Lundbeck larvae, possibly also D. bertrami Edwards larvae (Chironomidae, Diamesinae).
Distribution: Norway.
<>Reference: White and Lichtwardt, 2004.
Smittium bisporum Manier & Coste, 1971
Thalli 500-600 µm long, with a small holdfast and 2 or 3 main branches that rebranch in a bi- or trifurcate manner; branches about 5 µm diam. Trichospores (1-)2 per fertile branch, subcylindrical with a slight median swelling, 35-40 x 6-7 µm, collar 6-7 x 3-4 µm. Zygospores fusiform, 95-115 x 10-12 µm, with a collar 6-10 x 6 µm located on lower third of zygospore, and with a single long appendage.
Illustrations: Fig. 11.180.
Host: In hindgut of Psectrotanypus varius Fabr. (Diptera, Chironomidae) larvae.
Distribution: In still waters of the ancient quarries of Vendargues,
Department of Hérault, France. Possibly Mexico.
The trichospores of S. bisporum are most similar in size and shape to those of S. mucronatum, but lack the apical nipple of the latter species. Their respective zygospores make the two species quite distinct, however. In an unpublished dissertation, Coste (Coste-Mathiez, 1970) used the name S. megazygosporum for a new species, and illustrated it with four photomicrographs (her Figs. 54, 55, 57, 58); three of these photomicrographs were later published by Manier and Coste (1971) under the new name S. bisporum (their Figs. 3, 5, 6). Smittium megazygosporum was then used by Manier and Coste (1971) as the validly published name for another species of Smittium.
References: Manier and Coste, 1971; Coste-Mathiez,
1970. Valle et al., 2011.
Smittium brasiliense Alencar, Lichtwardt, Ríos-Velásquez & Hamada, 2003
Mature thalli often growing in large tufts or clumps, verticillate branching. Holdfast horseshoe shaped. Long-ellipsoidal trichospores (13-)18(-26) x1.6(-3) µm with a very short collar and one appendage. Biconical zygospores almost cylindrical (32-)40(-43) x 4-5 µm with a collar near one end and a single appendage.
Illustration: Fig. 11.257.
Host: Larvae or Simulium goeldii Cerqueira & Nunes, S.
ulyssesi Py-Daniel & Coscarón, S. rorotaense Flock
&
Abonnenc. Paratendipes sp., Polypodiilum sp. (Chironomidae).
Distribution: Amazonas, Brazil. Mexico.
Reference:
Alencar,
Ríos-Velásquez, Lichtwardt, and Hamada, 2003. Valle et al, 2011.
Smittium brevisporum Valle & Santamaria, 2004
Thalli profusely branched from the base, with an indeterminate pattern, tightly growing to form aggregates in which curved hyphae apexes can be observed. Basal cell with a simple disk-like holdfast. Trichospores long-ellipsoidal to ellipsoidal, (9-)12-14.5(-19) x 2-2.5 µm, each showing, after release from generative cells, a short and thick, longitudinally folded, appendage, and a nearly inconspicuous collar 0.5-1 x 1.5 µm, that becomes observable when the appendage unfolds. Each fertile branch with 4-8(-12) generative cells. Zygospores unknown.
Illustration: Fig. 11.259.
Hosts: Cricotopus spp. and other Chironomidae larvae.
Distribution: Spain. Ontario and Prince Edward Island, Canada
Reference: Valle and
Santamaria, 2004. Strongman and White, 2008. Strongman, 2007.
Smittium bulbosporophorus Valle & Santamaria, 2004
Thallus with a sparsely branched main axis, occasionally pinnate, and with secondary lateral branches arising from the base proximity. Basal cell often broadened in mature thalli, not differentiated in young individuals, secreting a disk-like holdfast. Trichospores obovate-ellipsoidal to broadly ellipsoidal, (9-)12-14.5(-18) x 3.5-5.5 µm, each showing, after release from the generative cells, a conspicuous, easily distinguishable appendage measuring about three times the trichospore length and a collar that is long, cylindrical or slightly narrowing toward the end, 1.5-3 x 2 µm. Each fertile branch with 2-6(-8) generative cells, 5-7.5 µm in length. Zygospores biconical, 35-40 x 7-8 µm; zygosporophore globose, nearly spherical, located at the last quarter of the zygospore length. Once released, the zygospore shows a globose collar 3.5-4 x 3.5 µm, and an easily observable appendage.
Illustration: Fig. 11.260.
Hosts: Diamesinae and Orthocladiinae (Chironomidae) larvae.
Distribution: Spain.
Reference: Valle and Santamaria, 2004.
Smittium bullatum Lichtwardt & Williams, 1992
Trichospores biconical, 20-24 x (5.5-)6(-7.2) µm, with a collar about 4 µm long. Young thalli consisting of an axis of wider cells from which narrower branches arise. Basal cell swollen, holdfast a small knoblike projection. Zygospores unknown.
Illustrations: Fig. 11.101.
Host: Naocladius forsythi (Diptera, Chironomidae)
Distribution: South Island, N.Z.
Reference: Lichtwardt and Williams, 1992d.
Smittium caribense L.G. Valle &
Cafaro, 2010
Thallus composed of a main axial hypha (5-6.8 µm diam) with secondary lateral opposite, rarely verticillate, branches (3.5-5.5 µm diam) arising from each node or septa, and a basal cell pinnately to verticillately branched, producing hypha usually shorter than the main axis. Basal cell slightly broadened in mature thalli (10-12 µm diam), not differentiated in young individuals (5-6.5 µm diam), secreting a conical or knobby holdfast, occasionally with short protuberances, or simply discoid in young specimens. Trichospores ellipsoidal to subcylindrical 22.5-27(-33) x 5-5.5(-6.5) µm, with a thin appendage and narrow collar, 3 µm long, with parallel or slightly divergent margins after release from the generative cells. Generative cells 1-4 per fertile branch, frequently longer than the trichospores. Zygospores not found.
Illustrations: Fig. 11.355.
Host:: Chironomidae larvae.
Distribution: Dominican Republic.
Reference: Valle and Cafaro, 2010.
Smittium caudatum Lichtwardt & Grigg, 1998
Trichospores oval to long-oval, (10-)16(-20) x (4-)-6(-9) µm, produced on long cylindrical extensions of their generative cells. Upon release, trichospore collars cylindrical, 5-20 µm long. Basal cells wide, sometimes up to 12-16 µm diam. Zygospores unknown.
Illustration: Fig. 11.150.
Hosts: Orthocladius (Orthocladius) sp., Cricotopus sp., Hydrobaenus sp. (Diptera, Chironomidae).
Distribution: USA (Kansas, Oklahoma).
Reference: Lichtwardt and Grigg, 1998.
Smittium cellaspora Williams, 1982
Thalli short, up to about 300 µm in length, sparsely branched, almost all cells becoming fertile. Trichospores ellipsoidal, (20-)29(-36) x (7-)8.5(-10) µm, single long appendage often coiled; collar (5-)9(-10) x 2.5 µm. Zygospores unknown.
Illustrations: Fig. 11.185.
Hosts: In hindgut of Sympotthastia sp. and possibly other Chironomidae (Diptera) larvae.
Distribution: USA (Missouri); Argentina.
The unusual feature of this small species is that virtually all cells can produce trichospores.
<>Reference: Williams, 1982; Lňpez Lastra et al., 2005Smittium chinliense Strongman & Xu, 2006
Thallus arising from a conspicuous foot-like holdfast, branching sparse, typically with 2-4 trichospores forming at the tips of fertile branches. Trichospores cylindrical to subcylindrical, 28.5-36 x 5-6 µm with a tubular collar 5-6 x 4 µm, often as wide as the spores, with a single appendages. Zygospores not found.
Illustration: Fig, 11.316.
Host: Crane fly larvae (Diptera, Tipulidae).
Distribution:
Smittium
chironomi Manier, 1970b (1969b)
[ = Typhella chironomi (Tuzet & Manier) Manier &
Mathiez, 1965, nom.
nud.]
[ = Genistella chironomi Tuzet & Manier, 1953, nom. nud.]
Mature thallus consisting of a main axis up to 800 µm long with branching along the upper part and producing numerous shorter basal branches radiating from above the disklike holdfast. Main axis and larger basal branches somewhat swollen at their base, 2.5-5 µm diam, tapering abruptly to 1.5-2 µm diam. Fertile upper branches of main axis each with 4-8 generative cells producing subcylindrical trichospores with a slight median swelling, 20-23 x 2.5-3 µm, collar 1-2 mm long x 1.5-2.5 µm wide. Zygospores unknown.
Illustrations: Fig. 11.184.
Hosts: In anterior hindgut of lotic Orthocladiinae larvae (Diptera, Chironomidae).
Distribution: Balaruc-le-Vieux and Sčte, Department of Hérault, France; possibly in England.
Smittium chironomi was incorrectly published by Manier (1969b) as a new combination based on an illegitimate basionym, Genistella chironomi Tuzet & Manier, 1953 (nom. nud.); her 1970b (1969b) publication of the name, however, is valid. Genistella chironomi was transferred improperly to another illegitimate genus Typhella (as T. chironomi), by Manier (1962a). Smittium chironomi is distinct from other Smittium spp. on the basis of the habit of the thallus and the dimensions of the trichospores as described, although no accurate illustrations are available for the latter.
Moss (1972) did an electron microscopic study of a Smittium sp., which he called S. chironomi, obtained from the hindgut of Tanytarsus sp.(Tanytarsini, Chironomidae) larvae collected in England, but there was no accompanying description or other indication to assure that it was correctly identified.
<>References: Manier, 1962a, 1969b (1970b); Tuzet and Manier, 1953; Moss, 1972.
Smittium colboi
Strongman, 2010
Thallus arising from an inconspicuous bulbous holdfast, branching
sparse, trichospores dimorphic with large trichospores 17.5-18 x 4-5.5
µm, ellipsoidal with a medial sselling, small spores 10.5-14 x 2.5-3.5
µm, narrow-ellipsoidal with a slight medial swelling, both large and
small trichospores with a short flared collar. Zygospores biconical,
cylindrical, 50-59.5 x 4-5.5 µm, typically bent slightly at the end
where the zygosporophore attaches, with a short collar after release
from the zygosporophore. The zygosporophore arises frm either a
communal basal aggregation of cells where a number of branches fuse or
can form directly from an undifferentiated branch.
Illustration: Fig.
11.370.
Host: Chironomidae larvae.
Distribution: Newfoundland, Canada.
<>Reference: Strongman, 2010.Smittium coloradense Lichtwardt & Williams, 1987 (in Williams and Lichtwardt, 1987b)
Trichospores up to 5 or more in a series per fertile branch, elongate-ellipsoidal (17-)26(-32) x (7-)8(-9.5) µm; collar (10-)12.5(-15) x ca. 3 µm tapering toward the distal end, with a single appendage that tends to curl and is greater than 6 times the spore length. Basal cell tapered toward the base, sometimes with small lateral projections. The first trichospore generally formed below the tip of the terminal generative cell. Zygospores Type II, 68-85 x 11-17 µm
Illustrations: Fig.
11.155, Fig. 11.321.
Hosts: Orthocladius (Orthocladius) sp., Eukiefferiella sp., Cricotopus sp., (Diptera, Chironomidae), possibly Prosimulium sp.(Simuliidae).
Distribution: USA (Colorado, South Carolina); Norway..
Zygospores were induced to form in the laboratory by placing the
specimens in ph10 KOH BHI medium by Beard and Adler.
Reference: Williams and Lichtwardt, 1987b. Beard and Adler, 2003;
White and Lichtwardt, 2004, Beard and Adler, 2003.
Smittium commune Lichtwardt & Grigg, 1998
Trichospores narrow-ellipsoidal with a slight median bulge, (10-)15(-30) x (2.5-)4(-6) µm, upon release having a short collar 1-3 µm long and a single short appendage. Thallus with some verticillate branching, branches not diverging, branchlets producing few to many trichospores. Zygospores unknown.
Illustrations: Fig. 11.151.
Hosts: Microtendipes sp., Cricotopus (Cricotopus) sp., Orthocladius (Orthocladius) sp., Phaenopsectra sp. (Diptera, Chironomidae).
Distribution: USA (Kansas, Oklahoma).
Reference: Lichtwardt and Grigg, 1998.
Smittium compactum Lichtwardt & Williams, 1992
Thalli aggregated into compact clusters, with little divergence of branches. Trichospores short-cylindrical with swollen midregion, 1-3 per fertile branch, 20-25 x 5-6.5 µm, collar 3-4 µm long. Zygospores unknown.
Illustrations: Fig. 11.90.
Host: Chironomidae (Diptera).
Distribution: Tasmania, Australia.
Reference: Lichtwardt and Williams, 1992b.
Smittium
culicis Manier, 1970b (1969b)
[= Orphella culicis Tuzet & Manier, 1947a, nom. nud.]
[= Rubetella culicis Tuzet, Rioux & Manier, 1961, nom.
nud.]
Thalli with divergent, often monopodial, branches attached to host cuticle by an inconspicuous holdfast; base sometimes pseudorhizoidal. Fertile terminal branches often arched, with 4-6 generative cells. Trichospores oval (15-)20(-32) x (4-)6(-8) µm, with a more or less campanulate collar (3-)5-9 µm long. Zygospores 47-55 x 11-12 µm, collar 4.5-8 x 3.5-5.5 µm
Illustration: Fig.
11.16A, Fig. 11.322.
Hosts: In hindgut of many genera and species of larval Culicidae (Diptera); rarely in Simuliidae, Chironomidae, Psychodidae, Stratiomyidae, and Thaumaleidae larvae.
Distribution: France, Norway, Spain, Tunisia, Canada, New Zealand,
Argentina, and USA
(California, Wyoming,
Nebraska, Kansas), Australia
In her 1969 monograph, Manier gave only average trichospore measurements of 16.5 x 4.8 mm, with a collar length of 4.7 mm. The description provided above shows a considerable range in trichospore sizes. These were determined from average measurements kindly provided by Manier in 1969 from sample collections from different mosquito larvae in France and Tunisia, and from measurements obtained by Lichtwardt from his own collections and from the many available axenic cultures. Because of the somewhat different, but overlapping, ranges of trichospore size from collection to collection, in addition to the size variation within single collections and cultures, it is possible that S. culicis consists of a species complex of several trichospore size variants. Nevertheless, the species is fairly easy to identify based on the oval shape and size of the trichospores, the relatively long and campanulate collar, and the mosquito host. Smittium culicis is readily distinguishable from the other common mosquito species, S. culisetae, on the basis of trichospore morphology alone. Sangar et al. (1972) found a distinct immunoelectrophoretic relationship among six isolates of S. culicis, four obtained from mosquito larvae and one each from a blackfly and a chironomid larva, thus adding serological confirmation to the morphological data.
Even though the mosquito is its usual host, S. culicis was
found and
isolated several times by Lichtwardt from Chironomus sp. larvae
(Chironomidae) in one site in southern France, and it was cultured
several
times from a population of Simulium vittatum Zett. larvae in
Leavenworth
Co., Kansas, USA by Lichtwardt and Peterson (unpublished). (This
blackfly
population was also infested with S. culisetae, which was also
isolated
axenically.) Whisler provided a culture (CAN-X-1) that he isolated from
a Simulium
sp. larva in Canada. In southern France S. culicis is common
and
widespread in many species of mosquito larvae, whereas it has been
found to
occur more sporadically in the USA. Its geographic distribution is
undoubtedly
much greater than present records indicate. It was found by Lichtwardt
in Culex
pervigilans Bergroth in New Zealand.
Zygospores of this common and widespread species were first discovered in Spain (Valle and Santamaria, 2004) in Eukiefferiella sp. larvae (Chironomidae, Orthocladiinae). Valle stated that thalli in which zygospores developed had trichospores that were smaller (14.5-19.5 x 5-6 µm) and fewer per branchlet.
Smittium culicis was one of the two species of Harpellales first cultured axenically (Clark et al., 1963). The species has been used in studies of host specificity (see Chapter 6) and a number of physiological experiments. The fine structure of its trichospore appendage, consisting of concentric electron-opaque rings in cross section (Moss and Lichtwardt, 1976), resembles that of S. mucronatum (Manier and Coste-Mathiez, 1968), a species to which S. culicis is serologically related (Sangar et al., 1972).
References: Manier, 1969b (1970b); Tuzet and Manier, 1947a; Tuzet et
al.,
1961; Manier et al., 1964; Clark et al., 1963; Chapman, 1966; Sangar,
1969;
Coste-Mathiez, 1970; Müller-Kögler, 1971; Williams and Lichtwardt,
1972;
Preisner, 1973; Moss and Lichtwardt, 1976; El-Buni and Lichtwardt,
1976a,
1976b; Cerniglia et al.]., 1978; Williams and Nagel, 1980; White and
Lichtwardt, 2004; Lňpez Lastra et al., 2005, Valle and Santamaria,
2004, Strongman and White, 2008. Strongman, 2010.
Smittium
culisetae Lichtwardt, 1964
= Smittium inopinatum Manier, 1970b (1969b)
[= Rubetella inopinata Manier, Rioux & Whisler, 1961, nom.
nud.]
Mature thalli large, attached to host cuticle by an inconspicuous holdfast, commonly verticillately branched, sporulating prolifically. Trichospores usually 4-10 per fertile branch, long-ovoid, (11-) 16(-30) x (3-)4(-7) µm, greatest width below midregion, with a short collar 1-2.5 µm long often flared outward; appendage fine and relatively short. Zygospores rare, biconical, (46-)52(-58) x (5.5-)6(-8) µm, with a collar (6-)7(-8) x (3.5-)4(-4.5) µm attached almost medially and perpendicularly to the zygospore body.
Illustrations: Fig. 7.14; Fig. 9.6; Fig. 9.12; Fig. 11.16.
Hosts: In hindgut of many species of Culicidae (Diptera) larvae; more rarely in larval Simuliidae, Chironomidae, Psychodidae, and Ceratopogonidae (Diptera) hindguts. Found once in an Ephemeroptera larva.
Distribution: Widespread in mosquito larvae in the USA (Colorado,
Nebraska,
Kansas, Wyoming, California, Hawaii, Great Smoky Mountains National
Park) and Japan; also in Australia, New
Zealand,
Brazil, Argentina, and France. Dominican Republic. Mexico.
Many axenic isolates of S. culisetae have been obtained. The type culture, COL-18-3, was isolated by Lichtwardt from a larva of Culiseta impatiens (Wlk.) in August of 1963, but the first isolate was obtained by Clark et al. (1963) from Culiseta incidens (Thompson), who named it Rubetella sp. (= Smittium sp.), later suggesting it was Smittium inopinatum. Smittium culisetae has been the most intensively studied trichomycete in the laboratory, as elaborated in Chapter 9. The unusual harpellid septum was first demonstrated in ultrastructural studies of this species (Farr, 1965; Farr and Lichtwardt, 1967).
Smittium culisetae occurs predominantly in mosquito larvae of several genera, including Culiseta, Aedes, Culex, and Anopheles. The smaller, long-ovoid trichospores with their short, flared collars readily distinguish S. culisetae from the other common inhabitant of mosquito hindguts, S. culicis. The latter species has been found most often in Europe. Some strains of S. culisetae produce trichospores not only from the usual terminal generative cells, but as well from normally vegetative cells that may spuriously become reproductive, such that all of the cells of entire sets of branches become fertile. In such cases the long vegetative cells may produce additional septa before trichospores commence to form. Although the range of trichospore lengths is great (11-30 mm), the size distribution is bimodal, with most spore sizes falling within the shorter end of the curve. The less common larger trichospores appear to develop from longer generative cells. Cultured colonies of S. culisetae tend to be more loose and floccose than those of other cultured Smittium spp. Colonies of some strains easily break apart on handling because of the weaknesses resulting from the spuriously reproducing thallial cells (generative cells, after sporulation, are devoid of cytoplasm and break readily).
Peterson and Lichtwardt in 1981 (unpublished) found a population of Simulium vittatum larvae (Simuliidae) along the dam spillway of Leavenworth County State Lake, Kansas, infested with both S. culisetae and S. culicis (some hindguts with both species intermixed), and were able to verify the identifications by axenically culturing both species. Other unusual hosts of S. culisetae include larvae of the ceratopogonid genus Dasyhelea (see next paragraph) and Chironomidae larvae. The latter hosts were populations of bloodworms (Chironomus sp.) studied by Lichtwardt in rock pools of the Georges River near Cambelltown, N.S.W., Australia. These same pools contained an unidentified mayfly (Ephemeroptera) nymph and larvae of Dasyhelea sp., both infested with S. culisetae.
Smittium inopinatum is considered to be a synonym of S. culisetae for the following reasons. Manier et al. (1961) described S. inopinatum (as Rubetella inopinata, nom. nud.)from the hindgut of Dasyhelea lithotelmatica larvae found in southern France. [This ceratopogonid species is also a host of Carouxella scalaris (Harpellaceae).] The single character that differentiates S. inopinatum from S. culisetae, other than the host, is the reported irregular, often dark, pseudorhizoidal branches at the base of thalli. This general form of growth, although not identical to that illustrated by Manier et al., may be present when dense clumps of S. culisetae grow in some hosts. More importantly, Lichtwardt has isolated S. culisetae from Dasyhelea sp. in southern France, and, in addition to morphological identity, this isolate (FRA-7-1) has been shown by Sangar et al. (1972) to have a strong serological affinity to other isolates of S. culisetae, including the type species. Lichtwardt also has found and cultured S. culisetae in a species of Dasyhelea (not D. lithotelmatica) taken from the same rock pools in Australia referred to in the preceding paragraph. Thus, it is clear that Dasyhelea spp. are occasionally hosts of S. culisetae, and neither host differences nor morphology can be the basis for maintaining the species S. inopinatum.
Smittium culisetae has trichospores that resemble the rarer mosquito pathogen, S. morbosum. Trichospores of S. morbosum tend to be more ellipsoidal than S. culisetae, but reference to other descriptive characters must be used to insure proper identification.
Zygospores of S. culisetae have been found in only two populations of mosquito larvae (Aedes vexans Meigen) collected by Williams (1983) and his assistant near Kearney, Nebraska in 1979. Williams was able to isolate the fungus, but no zygospores formed in vitro; nor was he able to find zygospores in larvae of Aedes aegypti (L.) infested in the laboratory, or when grown in vitro with two other S. culisetae isolates. The near median and perpendicular position of the collar on the zygospore body is not typical of other zygospore-producing Smittium spp., but is close to that described for the type species, S. arvernense.
References: Lichtwardt, 1964; Manier et al., 1961; Manier et al.,
1964;
Manier, 1969b (1970b); Clark et al., 1963; Farr, 1965; Farr and
Lichtwardt, 1967;
Chapman, 1966; Müller-Kögler, 1971; Williams and Lichtwardt, 1972;
Sangar et
al., 1972; Sangar and Dugan, 1973; Patrick et al., 1973; Preisner,
1973;
El-Buni and Lichtwardt, 1976a, 1976b; Moss and Young, 1978; Cerniglia
et al.,
1978; Starr et al., 1979; Sweeney, 1981; Williams, 1983; López Lastra,
1997; López Lastra et al., 2005; White, Siri and Lichtwardt, 2006,
Strongman and White, 2008. Valle and Cafaro, 2010. Valle et al., 2011.
Smittium culicisoides Lichtwardt, 1997
Mature thalli often 200-500 µm long. Bases tapered, occasionally with minute projections from the wall. Bases may occur in fascicles in well infected hosts. Trichospores oval, 20-25(-28) x 6-10 µm, collar 5-10 µm. Fertile branches with 1-4 generative cells. Zygospores unknown.
Illustrations: Fig. 11.137.
Hosts: Chironomidae and Simuliidae (Diptera), including Crozetia seguyi Beaucornu-Saguez & Vernon (Diptera, Simuliidae)
Distribution: Costa Rica; Crozet Islands (Indian Ocean)., possibly
Australia.
Smittium cylindrosporum Lichtwardt & Arenas, 1996
Thalli with densely branching uncontorted (essentially straight) basal cells. More terminal branches verticillate, growing at acute angles. Trichospores cylindrical, sometimes with a slight median bulge, (21-)26-33(-41) x 4-6 µm. Collar 4-6 µm long. Appendage not spiraled. Zygospores 51-52 x 10-11 µm
Illustrations: Fig. 11.138.
Hosts: Paraheptagyia cinerascens (Diptera, Diamesinae)m Paraheptagyia sp.; Cricotopus sp. (Orthocladiinae).
Distribution: Chile, Argentina.
Reference: Lichtwardt and Arenas, 1996.; Lichtwardt, Ferrington, and
Lopez Lastra, 1999.
Smittium delicatum Lichtwardt, 1990 (in Lichtwardt and Williams, 1990)
Thallus delicate, sparsely branched, occasionally branching verticillately, diameter of branches 6 µm near the base, tapering to about 3 µm near the tips, many main branches arising from a horseshoe-shaped holdfast cell. Fertile branches producing 2-8 generative cells. Trichospores subcylindrical, (18-)25-30 x 2.5 µm, with a very short collar, occasionally arising adventitiously from a cell along a main branch. Zygospores unknown.
Illustrations: Fig. 11.104.
Hosts: Chironomus (Chironomus) alternans, Cladopelma sp., and Phaenopsectra sp. (Diptera, Chironomidae).
Distribution: New South Wales, Australia; Great Smoky Mountains
National Park, USA.
Reference: Lichtwardt and Williams, 1990; White, Siri and
Lichtwardt, 2006.
Smittium dimorphum Lichtwardt & Williams, 1983a
Thalli producing two trichospore types: (1) long-ellipsoidal, 38-50 x 5.5-6.5 µm with a collar (2.5-)5 mm long, narrowed at the posterior end; (2) oval, 10-12 x 5.5-6.5 µm with a collar 2.5-4 µm long. Zygospores biconical, 71-96 x 13-14 µm, with an obliquely angled collar 12-17 µm diam connected to the zygospore wall one-third to one-quarter the length from one end, with a single appendage.
Illustration: Fig. 11.17.
Host: In hindgut of Boreoheptagyia lurida (Garrett) larvae (Diptera, Chironomidae).
Distribution: Several fast-flowing streams in and near Glacier National Park, Montana, USA.
This distinctive species and Stachylina pedifer (in the peritrophic membrane) are the only Harpellales known in larval Boreoheptagyiini. Both species often grow simultaneously in the same host specimens. Dimorphic trichospores also occur in S. alpinum, but the two species are easily distinguished by their zygospores and by the morphology of the larger trichospores, those of S. dimorphum being longer and somewhat narrower.
Reference: Lichtwardt and Williams, 1983a.
Smittium
dipterorum Lichtwardt, 1997
Thalli with a simple secreted holdfast, branches often verticillate with up to 8 or more generative cells per fertile branch. Trichospores long-ellipsoidal, almost cylindrical, (10-)12-18(-26) x 2-3(-4) µm, with a very fine appendage; collar 1-3 µm long. Zygospores 51-70 x 9-12 µm.
Illustrations: Fig. 11.133.
Hosts: Simuliidae and Chironomidae (Diptera).
Distribution: Costa Rica. Dominican Republic, Mexico.
Thalli profusely branched near base, wider hyphae often verticillately branched; holdfast inconspicuous. Fertile branches about 3 µm diam bearing long-ellipsoidal trichospores (20-)34(-44) x 3-6 µm, with a collar 2-4 µm long and a single, sometimes spiraled, appendage. Zygospores unknown.
Illustrations: Fig. 11.186.
Hosts: In hindgut of larval Diamesa near nivoriunda Fitch, and possibly also Cricotopus sp. (Diptera, Chironomidae).
Distribution: Stream draining Washington Gulch near Crested Butte,
Colorado, and Idaho,
USA. Australia.
Reference: Lichtwardt, 1972. Beach and White, 2012.
Smittium
esteparum Ferrington, Lichtwardt
& López Lastra, 1999
(in Lichtwardt, Ferrington, and López Lastra, 1999)
Thalli bearing both subcylindrical trichospores measuring 31-38 x 4.5-6.5 µm with a collar 4-6 mm long, and ellipsoidal trichospores with a median bulge, 12-14 x 4-5 µm with a collar 2 mm long. Zygospores about 50 x 10 µm; zygosporophores about 30 x 7-8 µm, attached about half way between mid region and lower end of zygospore.
Illustrations: Fig. 11.60.
Hosts: Cricotopus sp., Eukiefferiella sp. (Chironomidae).
Distribution: Patagonia, Argentina.
Reference: Lichtwardt et al., 1999.
Smittium fasciculatum Lichtwardt, 1994
Thalli aggregated into fascicled clumps up to 750 µm long, attached to anterior hindgut but growing in both directions. Branches extending into midgut tapering to produce fine sterile curved to circinate tips. Branches in hindgut terminating in series of 2-6 generative cells that produce subcylindrical trichospores 18-24(-29) x 2-3.5 µm with a very short (< 1 µm) collar and short appendage. Zygospores unknown.
Illustrations: Fig. 11.147.
Host: Chironomus sp. (Diptera, Chironomidae).
Distribution: Costa Rica.
Reference: Lichtwardt, 1994.
Smittium fastigatum Lichtwardt & Williams, 1992
Thalli up tµmo 500 µm long, consisting of a pointed basal cell and erect branches. Trichospores subcylindrical with a median swelling, 23-32 x 3.5-4 µm, with a short collar and single fine appendage. Zygospores unknown.
Illustrations: Fig. 11.88.
Host: Chironomidae (Diptera).
Distribution: Tasmania, Australia.
Reference: Lichtwardt and Williams, 1992b.
Smittium fecundum Lichtwardt & Williams, 1999
Thallus producing prolific short generative cells. Trichospores
ellipsoidal
with a slight median bulge, 17-20(-27) x 5-8 µm,
with a collar 5-10 µm long.
Basal
branches may produce small tuberculate projections from the wall.
Zygospores 70-85 x 18-19 µm, collar 9-12 µm.
Illustrations: Fig. 11.110.
Host: Psectrocladius sp. (Chironomidae).
Distribution: USA (Colorado). Spain.
Reference: Lichtwardt and Williams, 1999. Valle and Santamaria, 2004.
Smittium fruticosum Williams & Lichtwardt, 1992 (in Lichtwardt and Williams, 1992c)
Thalli forming bushy colonies up to 500 µm diam. Trichospores ellipsoidal with a median swelling, 21-28 x 4.5-5 µm, collar 3.2-4.8 µm long. Zygospores (Type II) 60-76 x 8-10 µm, attached to zygosporophore about 1/3 distance from one end.
Illustrations: Fig. 11.85.
Host: Cricotopus sp. (Diptera, Chironomidae).
Distribution: Western Australia, Australia.
<>Reference: Lichtwardt and Williams, 1992c.Smittium georgense Strongman, 2010
<>Thallus dense with many branches arising from the basal holdfast and branching prolifically. Holdfast basal cells initially knobby with several holdfasts ultimately forming a large mass with many radiating branches. Trichospores sub-cylindrical, 34-45 x 5-7 µm, with a collar 3-5 µm. Zygospores unknown.Smittium gigasporus Williams & Lichtwardt, 1984
Thallus base often branching prolifically with a number of lateral branches that rebranch once. Trichospores 1-2, rarely 3, per fertile branch, elongate-ellipsoidal to subcylindrical, 50-60 x 7-8.5 µm, collar 10-14 x 5 µm narrowing toward the end proximal to the generative cell, with a helical fine appendage up to 10 times the spore length. Zygospores unknown.
Illustrations: Fig. 11.187.
Host: In hindgut of larval Pagastia sp. (Diptera, Chironomidae).
Distribution: In algal growth on rocks and from wood in streams flowing into Hungry Horse Reservoir, Montana, USA.
Reference: Williams
and
Lichtwardt, 1984
.
Smittium gracilis Valle & Santamaria, 2004
Thalli with (2-)3-4(-6) branches arising directly from the basal cell, which is horseshoe-shaped and has lateral expansions. A small amount of secreted material of the holdfast can be seen in the concavity of the basal cell in its middle part. Secondary and tertiary branches verticillately arranged at the upper zone. Basal hyphae measuring 3-4 µm diam, to 2-3 µm in distal ones. Trichospores subcylindrical, (18-)20-26(-29) x 2-3.5 µm, each showing, after release from generative cells, a very thin appendage about twice or more as long as the trichospore length, and an inconspicuous collar of approximately 1 x 1 µm. Each fertile branch with 2-8 generative cells. Zygospores unknown.
Illustration: Fig. 11.261.
Hosts: Chironomus sp. and Diamesinae larvae (Chironomidae).
Distribution: Spain. Prince Edward Island, Canada.
Reference: Valle and Santamaria, 2004, Strongman, 2007.
Smittium gravimetallum Lichtwardt, Ferrington & Hayford
Mature thalli often verticillately branched, with a bulbous basal cell. Trichospores long-ellipsoidal, almost cylindrical, with a median bulge, (20-)27-30(-45) x 2.5-3.5(-4.5) µm, with a collar about 1-2 µm long and a very fine appendage. Zygospores unknown.
Illustration: Fig. 11.245.
Host: Dicrotendipes fumidus (Chironomidae).
Distribution: Kansas, USA.
Reference: Ferrington et al., 2000.
Smittium hecatei Valle & Santamaria, 2004.
Thalli branched from the basal cell, verticillate in the medial and upper areas. Basal cell not distinguished in young thalli, ramified and differentiated in a kind of broadened-leg ( 12 µm wide) coated with secreted holdfast material in mature thalli. Bulbous lateral protuberances often can arise in the hindgut lining. Trichospores subcylindrical to long-ellipsoidal, with two size ranges; type , 30-37(-49) x 3.5-5.5 µm, with a collar of 3.5-6 x 3.5 µm; type , 14.5-24 x 2.5-3.5 µm, with a collar of 1.5-2.5 x 2-2.5 µm, cylindrical or slightly narrowing to the end in both types. Each fertile branch with 8-14 or more generative cells, variable in size (longer when producing trichospores ), and narrowing to the distal ends (ca. 2.5-3.5 µm diam). Zygospores unknown.
Illustration: Fig. 11.262.
Hosts: Larvae of Cricotopus spp. and Diamesini (Chironomus).
Distribution: Spain.
Reference: Valle and Santamaria, 2004.
Smittium heterosporum Valle & Santamaria, 2004
Thalli branched, verticillate in the medial and upper areas. Some broadenings and constrictions are observed in the basal segment with hyphal cells highly variable diameter (6-14 µm or more). Basal cell with a simple, discoid or slightly campanulate holdfast. Trichospores dimorphic: type long-ellipsoidal, (36-)50-62(-74) x (7.5)9-13 µm, with a delicately granulated surface (more or less apparent depending on the individual), collar slightly narrowing toward the end, (10-)12.5-17(-20) x 3-4(-5.5) µm, filiform appendage (but ribbon-like under SEM), measuring up to eight times the trichospore length; type smaller, ovate-ellipsoidal or pyriform, 14-27 x 8.5-11 µm, with the surface slightly granulated or not, collar 8-9 x 1.5 µm, appendage identical to that of type . At the lowermost and medial areas of fertile branches, the generative cells may not arise directly from the main axis but from lateral peduncles, variable in size (18-50 µm). Zygospores fusiform, (160-)170-180(-190) x 15-18 µm; zygosporophore eccentric, located near one of the polar ends. Once released, the zygospore shows a collar of 17-20(-30) x 10-13 µm, and a large appendage. Specialized conjugation hyphae giving rise to angulous conjugation bridges, from which a peduncle develops, supporting both zygosporophore and zygospore.
Illustration: Fig. 11.263.
Hosts: Larvae of Diamesinae (Sympotthastia spp., Potthastia spp.) and Orthocladiinae (Cricotopus bicintus Meig.) (Chironomidae).
Distribution: Spain.
Reference: Valle and Santamaria, 2004.
Smittium imitatum Lichtwardt & Arenas, 1996
Mature thalli growing in dense clusters with compact branching. Holdfast region not horseshoe-shaped. Trichospores (16-)19(-21) x (3-)5(-6) µm, cylindrical but swollen in the middle; collar about 2 µm long. Zygospores unknown.
Illustrations: Fig. 11.89.
Hosts: Simulium spp. (Diptera, Simuliidae).
Distribution: Chile, Argentina.
Reference: Lichtwardt and Arenas, 1996; Lňpez Lastra et al., 2005.
Smittium incrassatum Y. Kobayasi, 1971 (in Kobayasi et al., 1971)
Thalli 100-130 µm long, prolifically branched near the base, branches 4-7 µm diam, often constricted at septa. Trichospores 1-2 per fertile branch, ellipsoidal, 12-14 x 7-9 µm with a thick and finely punctate wall, developing from a 7-10 x 3-4 µm outgrowth of the generative cell; upon detachment trichospores bearing a short collar and a single long appendage. Zygospores unknown.
Illustrations: Fig. 11.179.
Host: In hindgut of Chironomidae (Diptera) larvae.
Distribution: On surface of submerged pebbles in a cold stream, Angmagssalik, Greenland.
Reference: Kobayasi et al., 1971.
Smittium inexpectans Valle & Santamaria, 2004
Thalli pinnate to verticillately branched, with a main and other hyphal axes arising from the basal cell and tapering to the tips. The basal cell is slightly broadened with a simple, disk-like secreted holdfast located between the lateral basal branches. Trichospores subcylindrical, often with a median bulge, 23-27 x 2-2.5 µm, each showing, after release from generative cells, a cylindrical collar, 5.5-6 x 2 µm. Each fertile branch with 4-6 generative cells, variable in length. Zygospores unknown.
Illustration: Fig. 11.264.
Hosts: Orthocladiinae (Chironomidae) larvae.
Distribution: Spain.
Reference: Valle and Santamaria, 2004.
Smittium
insulare Strongman, 2007
Thallus long and sparsely branched. Holdfast inconspicuous and
undifferentiated from the thallus. Trichospores sparse, typically two
produced distally per fertile branch, small (15-20 x 3-4 µm), slightly
swollen medially
with a short (2.5-4 µm) collar and one appendage. Zygospores (Type II)
elongate, thin, 48-51 x 3.5-4 µm, nearly cylindrical, narrowing
abruptly at both ends. Zygospore attached obliquely to the
zygosporophore, near one end of the spore. In hindgut of midge larvae
(Chironomidae).
Illustrations: Fig. 11.324.
Hosts: Chironomidae, Culicidae larvae (Diptera)..
Distribution: Trout River near Tyne Valleu, Prince Edward Island,
Ontario,
Canada.
Reference: Strongman, 2007, Strongman and White, 2008.
Smittium kansense Lichtwardt & Grigg, 1998
Thalli sometimes branched verticillately, with a small secreted holdfast. Trichospores subcylindrical with a median bulge, (17-)23(-32) x (1.5-)2.7(-3.5) µm, with a collar about 2 µm long and a very fine appendage. Zygospores unknown.
Illustrations: Fig. 11.154.
Hosts: Hydrobaenus sp., Orthocladius (Orthocladius) sp. (Diptera, Chironomidae).
Distribution: USA (Kansas).
Reference: Lichtwardt and Grigg, 1998.
Smittium lentaquaticum Siri, White & Lichtwardt, 2006
Thalli up to 600 µm long, with verticillate branching and a horseshoe-shaped basal cell. Producing long-ellipsoidal trichospores with a slight median bulge, 12-19 x 3-5 µm, with a collar 1.5-3 µm long. Zygospores unknown.
Illustration: Fig. 11.249.
Host: Bloodworms, Chironomus sp. (Chironomidae)..
Distribution: Great Smoky Mountains National Park, USA.
The verticillate branching, horseshoe-shaped holdfast, and small trichospores distinguish this Smittium from others. Three axenic cultures have been obtained, TN-27-A3, TN-27-A4, and TN-27-A5.
Reference: White, Siri and Lichtwardt, 2006.
Smittium longisporum Williams, Lichtwardt & Peterson, 1982
Trichospores long fusiform-ellipsoidal, (40-)46(-55) x (6-)8(-10) µm, with a long, well-defined appendage that often has a zigzag appearance; collar (10-)13(-17) x 4 µm, slightly bulged centrally. Usually 1-2 trichospores per fertile branch, produced on long generative cells. Zygospores fusiform-biconical, (102-)110(-113) x (13-)15(-17) µm, collar 28-32 x 5 µm located near lower tip of the zygospore; single appendage several times longer than the zygospore.
Illustration: Fig. 11.18.
Hosts: In hindgut of Cricotopus sp. and other Chironomidae (Diptera) larvae.
Distribution: Flowing streams in Kansas, Missouri, and Nebraska, USA; small stream draining into north shore of Lake Torneträsk, Sweden.
The presently known, disjunct distribution of S. longisporum suggests that it remains to be found in other sites as well.
Reference: Williams et al., 1982.
Smittium macrosporum Y. Kobayasi, 1969 (in Kobayasi et al., 1969)
Axial hyphae several, 6.5-13 µm diam
at base, arising from a short-cylindrical basal cell 6.5-9 µm diam,
branching variously.
Fertile
branches 3-6.5 µm diam, with
1, rarely
2, long generative cells producing outgrowths 13-20 x 2.5-4 µm bearing
fusiform-ellipsoidal
trichospores
(26-)31(-42) x (6-)6.5(-7.5) µm with a
finely or coarsely verrucose surface; upon detachment trichospores have
a
cylindrical collar 10-18 mm
long and
bear a single appendage. Zygospores unknown.
Illustrations: Fig. 11.178.
Host: In hindgut of Chironomidae (Diptera) larvae.
Distribution: USA (Alaska).
Reference: Kobayasi et al., 1969.
Smittium megazygosporum Manier & Coste, 1971
Thalli in tufts, verticillately branched, branches 3-6 µm diam. Trichospores nearly cylindrical with a slight median swelling, 36-49 x 3.5-5 µm, and a prominent single appendage. Zygospores fusiform, 110-150 x 10-12 µm, with a collar 9-10 x 6 µm located on the lower fourth of the zygospore.
Illustrations: Fig. 11.183.
Host: Larval hindgut of Syncricotopus rufiventris Meig. (Diptera, Chironomidae).
Distribution: Ephemeral stream of Lirou near Roman bridge bordering route D 112, Department of Hérault, France; USA.
The name S. megazygosporum was first used by Coste in an unpublished dissertation (Coste-Mathiez, 1970). The description in that dissertation apparently included collections of both S. megazygosporum and S. bisporum; the two species were separated and validly published as two species by Manier and Coste in 1971.
References: Manier and Coste, 1971; Coste-Mathiez, 1970.
Thalli with a secreted holdfast. Trichospores long-ellipsoidal, 36-47 x 9-10 µm, with a campanulate collar 9-10 x 4-5 µm. Zygospores unknown.
<>Illustration: Fig. 11.305.Host: In hindgut of Thaumaleidae larvae (Diptera).
Smittium
microsporum Williams &
Lichtwardt, 1992
(in Lichtwardt and Williams, 1992c)
Trichospores ellipsoidal, 8-10 x 2.2-3 µm, with a short collar and inconspicuous appendage, produced in series of up to 15 on recurved fertile branches. Zygospores (Type II) cylindrical with pointed ends, 42-48(-55) x 4-4.5 µm from one end.
Illustrations: Fig. 11.86.
Hosts: Tanytarsus sp. and possibly Cricotopus sp. (Diptera, Chironomidae).
Distribution: Western Australia, Australia. Mexico.
Reference: Lichtwardt and Williams, 1992c. Valle et al., 2011.
Smittium minutisporum
Lichtwardt, Siri & White, 2006
Thallus not verticillately branched with a simple holdfast, producing elliptical trichospores with a slight median bulge, 10-15 x 2.5-3.5 µm, with a collar 1.5-2(-2.5) µm long. Zygospores unknown.
Illustration: Fig. 11.250.
Host: Larval Ochlarotatus japonicus (Theobold) (Culicidae).
Distribution: Great Smoky Mountains National Park, USA.
This is the fourth species of Smittium to be described from mosquito larvae. I somewhat resembles S. morbosum, a potential mosquito pathogen which S. minutisporum is not, and the latter has trichospores that are wider
Reference: White, Siri and Lichtwardt, 2006.
Smittium morbosum Sweeney, 1981a
Thalli forming a dense clump 0.5-2 µm diam, branches 2.5-4.5 µm diam. Generative cells 4-8 mm long, producing narrowly ellipsoidal trichospores (10-)15(-18) x (3.5)-4(-4.5) µm, collar slightly flared, 0.5-2.5 x 1-2 µm. Zygospores unknown.
Illustrations: Fig. 11.19.
Host: In anterior hindgut of larval Anopheles hilli, and possibly Anopheles annulipes (Diptera, Culicidae) in Australia. In Japan, Aedes albopictus and Culex pipiens. In Argentina, Aedes albifasciatus, A. crinifer, A. serratus, Anopheles annulipalpis, Culex dolosus, C. intricatus, C. maxi, Mansonia indubitansPsorophora ferox and Uranotaenia nataliae. Also see additional hosts below. Pathogenic to larvae, penetrating into anterior midgut and occasionally the Malpighian tubules. May occur in adults.
Distribution: Australia; Japan; Argentina, Italy, Russia, Armenia.
First reported in Italy by Coluzzi (1966), Dubitskii (1978) and Sweeney (1981) in laboratory-raised mosquito larvae, S. morbosum was first discovered in natural populations of mosquitoes by Sato et al. (1989) in Japan, and by López Lastra (1990) in Argentina (which she called Smittium morbosum var. rioplatensis). Subsequently, in Argentina it has been found in a wide variety of mosquito genera and species (García et al., 1994). Coluzzi (1966) reported this fungus as Rubetella culicis (nom. nud.) (= Smittium culicis) in Culex pipiens, C. hortensis, Culiseta longiareolata and Aedes vittatus, but the fungus was no doubt Smittium morbosum. Likewise, Dubitskii (1978) misidentified the fungus, not yet named S. morbosum, as S. culisetae; the fungus was infecting Aedes aegypti and Culex pipiens molestus, which he believed had become infested in the laboratory from an introduction of Aedes caspius larvae collected in a river floodplain. Sato et al. (1989) provided some electron micrographs of their specimens, and later Shimada et al. (1995) investigated in the laboratory the susceptibility of Aedes albopictus to the fungus.
The unusual pathogenicity of S. morbosum has been reviewed in Chapter 8. The fungus has been cultured axenically by Sweeney. Smittium morbosum is most likely to be confused with S. culisetae, for the morphological differences in the trichospores of these two mosquito-inhabiting species are subtle: those of S. culisetae have a wider range in size and are more consistently wider below the middle of the spore body. The branching of S. culisetae is more often verticillate, and colonies in culture tend to be more floccose than those of S. morbosum. Refer to the description of S. culisetae for other differences. Sweeney (1981a) also found S. culisetae in some of his mosquito cultures, and determined they were not pathogenic.
Reference: Coluzzi, 1966; Dubitskii, 1978; Sweeney, 1981a, 1981b;
Sato et
al., 1989; López Lastra, 1990; Shimada et al, 1995; García et al.,
1994, Nelder et al, 2005.
Smittium
mucronatum Manier & Mathiez
ex Manier, 1970b (1969b)
[= Smittium mucronatum Manier & Mathiez, 1965, nom. nud.]
Trichospores elongate-ellipsoidal, 33-37 x 6.5-7 µm, with a minute
apical nipple,
collar cylindrical to
campanulate, 7.5-9 x 3.3-4 µm;
single
appendage long and fine. Zygospores biconical, 44-60 x 11-13.5 µm,
collar 11-13.5 x 3.4-5.5 µm attached to lower third of
zygospore,
bearing a single fine appendage. See Lichtwardt and White, 2011, for
typification of Smittium
using S. mucronatum holotype.
Illustrations: Fig. 11.109.
Hosts: In hindgut of larval Psectrocladius sordidellus (Zett.)
Edw.
(Diptera, Chironomidae) (France), Psectrocladius sp. (USA), and
Psectrocladius limbellatus
(Norway).
Distribution: In waters of ancient quarries of Vendargues, and on rocks in large shallow pond north of St. Gély-du-Fesc, Department of Hérault, France, Norway. In a high altitude kettle pond in Colorado, USA, Ontario, Canada (Lichtwardt and Williams, 1999).
Smittium mucronatum was cultured axenically by Lichtwardt (in 1968) and Coste-Mathiez (1970). It was indistinguishable serologically from S. culicis (Sangar et al., 1972), a species common in mosquito larvae in the general region where S. mucronatum has been found. The trichospores of S. mucronatum are more elongate than those of S. culicis, and characteristically have a minute nipple at the tip of the trichospore, but that structure is not readily seen on all trichospores in cultured material. An electron microscopic study revealed that the nipple ("mucron") is a thickening of the outer trichospore wall, and that the long trichospore appendage is coiled and twisted within the region of the collar before spore release. In cross section, the appendage shows concentric electron-opaque rings (Manier and Coste-Mathiez, 1968; Coste-Mathiez, 1970), in this respect resembling S. culicis (Moss and Lichtwardt, 1976).
Smittium mucronatum is capable of infesting mosquito larvae under laboratory conditions (see Chapter 6), but the infestation is not persistent, and trichospores and zygospores formed within mosquito guts may be abnormal (Manier and Mathiez, 1965; Coste-Mathiez, 1970; Williams and Lichtwardt, 1972a). The presumption is that the fungus is not a natural commensal in the gut of mosquito larvae. No zygospores have been found or induced in axenic cultures. El-Buni (1975) and El-Buni and Lichtwardt (1976a, 1976b) have studied some facets of the physiology of this species in axenic culture (see Chapter 9). The sole sterol produced by S. mucronatum was desmosterol (Starr et al., 1979).
References: Manier and Mathiez, 1965; Manier and Coste-Mathiez,
1968;
Manier, 1969b (1970b); Coste-Mathiez, 1970; Williams and Lichtwardt,
1972a;
Sangar et al., 1972; Preisner, 1973; El-Buni, 1975; El-Buni and
Lichtwardt,
1976a, 1976b; Starr et al., 1979, Lichtwardt and Williams, 1999. White
and Lichtwardt, 2004, Strongman and White, 2008. Lichtwardt and White,
2011.
Smittium naiadis Strongman & Shengquan Xu, 2006
Thallus diffuse, primary branches arise from a simple cluster of
basal cells covered with mucilage, secondary branching strongly
verticillate along the length and at the end of the primary branches.
Trichospores cylidrical, long and narrow (30-36 x 2.5-3.5 µm) with a
conspicuous short (3 µm) collar that commonly appears to have 1 or 2
thickenings. Trichospores with a single, thin appendage. Zygospores not
found.
Illustrations: Fig. 11.314.
Host: In hindgut of a Chironomicae (Diptera) larva.
Distribution: Hao River, Shaanxi Province, China.
Strongman and Xu, 2006.
Smittium
nodifixum Strongman and Shengquan Xu, 2006
Thallus compact, primary branches arising from a conspicuous knobby
holdfast, secondary branching sparse. Trichospores subcylindrical
26-29.5 x 5-6 µm with a campanulate collar 5-6 µm long. Zygospores not
found. In hindgut of bloodworms and other midge species (Diptera:
Chironomidae).
Illustrations: Fig. 11-315.
Hosts: In hindgut of bloodworms and other midge species (Diptera:
Chironomidae).
Distribution: Hao River, Shaanxi Province, China.
Strongman and Xu. 2006.
Smittium orthocladii Manier, 1970b (1969b), emend. Lichtwardt, 1984a
Thalli compactly branched, with basal branches of smaller thalli often fascicled and sometimes enveloped in a brownish gelatinous sheath. Generative cells 2-10 per fertile branch. Trichospores either long-ellipsoidal, (25-)30(-40) x (6-)7(-8) µm with a cylindrical collar 5-10 µm long, or small and oval, 8-10 x 5-6 µm with a cylindrical collar 5-10 µm long. Zygospores biconical, subcylindrical in the middle, (81-)87(-98) x (9-) 1 0(-l 1) µm, with a collar 12-18 µm long attached close to one end of the zygospore, and bearing a single appendage.
Illustration: Fig. 11.20.
Hosts: In hindgut of larval Orthocladius spp., Diamesa sp., and other lotic Chironomidae (Diptera).
Distribution: Department of Hérault, France; northwestern Montana, USA.
Manier (1969b) validly published the name S. orthocladii, but erroneously as a new combination based on the illegitimate species, Rubetella orthocladii Manier & Mathiez, 1965 (nom. nud.). It was discovered in larvae of Orthocladius nr. rubicundus Meigen from an ephemeral stream. Lichtwardt's collections of this species were from a small alpine stream near Logan Pass, Glacier National Park (in 1975), and Doris Creek draining into Hungry Horse Reservoir (in 1977) in Montana, from midge larvae belonging to at least two subfamilies. The emended description provided information on zygospores and the small oval trichospores seen by Manier and Mathiez but interpreted as younger stages of development. The morphology of the regular larger trichospores are virtually identical in the European and North American collections. Like Smittium dimorphum, both trichospore types may occur on the same thallus. The fascicled appearance of the thallial base may be evident only in smaller thalli. Larger thalli form a dense, radiating growth such that the basal portion cannot be readily seen. Lichtwardt saw no brownish sheath around the basal branches in his specimens. The dimensions and shape of the longer trichospores with their long collar distinguish this Smittium species from others even in the absence of the distinctive zygospores.
References: Manier, 1969b (1970b); Manier and Mathiez, 1965; Coste
Mathiez,
1970; Lichtwardt, 1984a.
Smittium ouseli Williams & Lichtwardt, 1984
Thalli producing 1-2(-3) trichospores per fertile branch. Trichospores long-ellipsoidal, 21-25 x 6.5-7.5 µm with a collar 5-9 µm long. Zygospores biconical, 77-88 x 12-15 µm, with an obliquely angled collar connected to the zygospore wall one-third to one-fourth the length from one end, bearing a single appendage upon release.
Illustrations: Fig. 11.188.
Host: In hindgut of larval Eukiefferiella sp. (Diptera, Chironomidae).
Distribution: Mountain stream just south of Glacier National Park, Montana, USA.
Reference: Williams and Lichtwardt, 1984.
Smittium paludis Williams & Lichtwardt, 1990 (in Lichtwardt and Williams, 1990)
Main branches of thalli with mostly verticillate branchlets bearing series of trichospores 12-14 x 2.5-3.0 µm. Base of thallus with a swollen holdfast cell incurved at the point of attachment to the cuticle. Zygospores unknown.
Illustrations: Fig. 11.97.
Host: Tanytarsus near inextentus (Diptera, Chironomidae).
Distribution: Tasmania, Australia.
Reference: Lichtwardt and Williams, 1990.
Smittium parvum Lichtwardt, 1997
Branches closely arranged, with fertile branches bearing up to 6 or more generative cells. Trichospores oval, 9-14 x 3.5 µm, collar 2-6 µm long. Zygospores unknown.
Illustrations: Fig. 11.135.
Hosts: Cricotopus sp. (Diptera, Chironomidae).
Distribution: Costa Rica.
Reference: Lichtwardt, 1997.
Smittium pennelli Lichtwardt, 1984a
Thalli up to 300 µm long, sparsely branched, mucilaginous basal cell tapered to a point. Trichospores in series of 2-4, long fusiform-ellipsoidal, (31-)41(-55) x (6-)7(-8) µm, with a short rounded collar 3.4-4 µm long. Terminal trichospores often produced subapically. Zygospores unknown.
Illustration: Fig. 11.21.
Hosts: In hindgut of larval Prosimulium exigens Dyar & Shannon, P. onychodactylum Dyar & Shannon, Simulium defoliarti Stone & Peterson, and Simulium sp. (Diptera, Simuliidae).
Distribution: Lotic habitats in Rocky Mountain National Park, Colorado, and northwestern Montana, USA.
The thallus of Smittium pennelli somewhat resembles that of species of Pennella, which also grow in Simuliidae larvae, but the trichospores are clearly a Smittium. Thalli of S. pennelli sometimes are found growing together in bundles.
Reference: Lichtwardt, 1984a.
Smittium perforatum Williams & Lichtwardt, 1987
Trichospores commonly 1-2, occasionally more, per fertile branch, elongate-ellipsoidal to subcylindrical with a swollen midregion (33-)38(-45) X (7-)7.9(-8.2) µm; collar (6-)7(-8) X (3-)4.2(-4.6) µm with a single curling appendage several times to spore length. Basal cell commonly penetrating the hindgut lining forming bulbous swellings. Two basal (8-10 mm wide) cells often present before branching is initiated. Zygospores unknown.
Illustrations: Fig. 11.153.
Hosts: Orthocladius (Euorthocladius) sp. and Diamesa sp. (Diptera, Chironomidae).
Distribution: Colorado, USA.
Reference: Williams and Lichtwardt, 1987b.
Smittium phytotelmatum Lichtwardt 1994
Thalli sparsely branched, main branches bearing sets of single to often verticillate short branchlets with series of short generative cells. Trichospores subcylindrical, (14-)17-25(-30) x 2-3 µm, collar usually 2-3 µm long. Zygospores unknown.
Illustrations: Fig. 11.146.
Hosts: Chironomus sp., Polypedilum spp., Tanytarsus sp., and other Chironomini and Tanitarsini (Diptera, Chironomidae) inhabiting phytotelms (water in bromeliad leaf bases).
Distribution: Costa Rica, Argentina.
Reference:
Lichtwardt, 1994; Siri, Marti, and Lopez Lastra, 2008. Siri and Lopez
Lastra, 2010.
Smittium precipitiorum White & Lichtwardt, 2004.
Trichospores ellipsoidal, (13-)17-22 x 3.5-4.5 µm. Zygospores 66-75 x 10-13 µm.
Illustration: Fig. 11.276.
Host: Larvae of Orthocladius fuscimanus(Kieffer), and Diamesa sp. (Chironomidae, Orthocladiinae).
Distribution: Norway.
Reference: White and Lichtwardt, 2004.
Smittium prostratum Valle Santamaria, 2004.
Thalli prostrate on the hindgut lining, with lateral branches that form verticillate ramifications at the upper areas. Holdfast material secreted along the thallial surface keeping it in contact with the gut lining, functioning as glue. Basal cell variable, usually with lateral branched. Trichospores subcylindrical to elongate-ellipsoidal, 26-30 x 3.5-4.5 µm, with a campanulate collar, narrowing toward the end, 4.5-5.5 x 2.5-3.5 µm. Each fertile branch with 2-4(-6) generative cells. Zygospores unknown.
Illustration: Fig. 11.265.
Hosts: Orthocladiinae (Chironomidae) larvae.
Distribution: Spain.
Reference: Valle and Santamaria, 2004.
Smittium pseudodimorphum Valle & Santamaria, 2004
Thalli branched from the basal cell, verticillate at the medial and upper areas. Basal cell simple or bilobulate, with secreted holdfast material. Trichospores dimorphic: type alpha subcylindrical, (45-)50-55(-66) x (4-)5.5(-7) µm, with a thickened apex, collar cylindrical or with convergent margins, 9-11.5 x 3.5 µm; type beta broadly ellipsoidal, (12-)14-16.5 x 5.5-6 µm, collar cylindrical, 12.5-18 x 1.5-2 µm. Both trichospore types growing in the same thallus but on different branches, the trichospores of type beta being less common. Generative cells longer in branches producing the trichospores of type alpha, shorter and more numerous in fertile branches producing the trichospores of type beta. Zygospores biconical, 82-97 x (14-)16-18(-20) µm. Once released the zygospore shows a collar of 16.5-20 x 5-7 µm, and a visible appendage.
Illustration: Fig. 11.266.
Host: Diamesinae (Chironomidae) larvae.
Distribution: Spain.
Reference: Valle and Santamaria, 2004.
Smittium pusillum Manier & Coste, 1971
Thalli usually 200-300 µm long, attached to host cuticle by a pseudorhizal base; branches 4-6 µm diam. Trichospores 4-6 per fertile branch, ellipsoidal, 14-22 x 2.5-3 µm, collar 2-3.5 x 1.2-1.5 µm. zygospores fusiform, 50-60 x 6-7 µm, collar 5-6 x 2-3 µm.
Illustrations: Fig. 7.14; Fig. 11.181.
Host: In hindgut of Procladius sp. (Diptera, Chironomidae) larvae.
Distribution: In still waters of the ancient quarries of Vendargues, Department of Hérault, France.
References: Coste-Mathiez, 1970; Manier and Coste, 1971.
Smittium rarum Lichtwardt, 1990 (in Lichtwardt and Williams, 1990)
Trichospores subcylindrical, slightly swollen in the middle, with a single appendage, 20-26 x 3-4.5 µm, collar 0.5-1 µm long. Zygospores about 100 x 10 µm, with a collar attached about 25 µm from one end.
Illustrations: Fig. 11.142.
Hosts: Chironomidae (Diptera) and Austrothaumalea sp. (Diptera, Thaumaleidae).
Distribution: North Island, New Zealand.
Reference: Lichtwardt and Williams, 1990.
Smittium rupestre Lichtwardt, 1990 (in Lichtwardt and Williams, 1990)
Mature thalli with a dense, sometimes contorted, cluster of basal cells, fertile branches producing 2-4 generative cells. Trichospores subcylindrical with a median swelling, (34-)36(-39) x 4-6 µm, collar 4-6 µm long, with an appendage initially very spiraled. Zygospores fusiform, 90-128 x 9-12 µm, with a collar located about 1/4 the distance from one end; zygosporophore 1/2-1/3 the length of the zygospores.
Illustrations: Fig. 11.98.
Hosts: Orthocladiinae (Diptera, Chironomidae).
Distribution: New South Wales, Australia.
Reference: Lichtwardt and Williams, 1990.
Smittium shaanxiense Juan Wang, Strongman & S.Q. Xu, 2010
Thallus dense with prolific branching, attached to the hindgut lining by an inconspicuous holdfast. Trichospores dimorphic with large trichospores slightly swollen medially, 33.5-46 x 8.5-14 µm, possessing a long (11-18 µm) collar and one long, thin, appendage. Small trichospores, which can occur on the same branches as larger trichospores, oval, 9-12 x 4.5-7 µm, with a collar (11-14 µm) and a single appendage. Zygospores (Type II) biconical, 56.5-67 x 7.5-11.5 µm, borne on a zygosporophore arising directly from conjugated hyphae. Zygospores have a collar (15.5-19.5 x 3-4 µm and one long, thin appendages. Attached to hindgut of midge larvae.
Illustrations: Fig. 11-353.
Host: Chironomidae larvae.
Distribution: Shaanxi Province, China.
Reference: Strongman, Wang, and Xu, 2010.
Smittium simulatum Lichtwardt & Arenas, 1996
Trichospores ovoid, 19-23 x 6-8 µm; collar long-campanulate, about 5 µm long. Base of thallus consisting of cylindrical cells and not pseudorhizoidal, sometimes producing more than 6 generative cells per fertile branch. Zygospores unknown.
Illustrations: Fig. 11.106.
Hosts: Aphrophila bidentata (Diptera, Tipulidae).
Distribution: Chile.
Reference: Lichtwardt & Arenas, 1996.
Smittium
simulii Lichtwardt, 1964a
[= Rubetella simulii Manier, 1963b, nom. nud.]
Basal cell often swollen around a refractive holdfast and giving rise to several main branches usually without verticillate branching. Terminal fertile branches producing usually 4-6 generative cells. Trichospores cylindrical but swollen in the middle, (16-)23(-30) x (3-)5(-7) µm, collar cylindrical, (1.5-)3.5(-4.2) µm long; single appendage relatively short. Zygospores unknown.
Illustrations: Fig. 7.19; Fig. 9.7; Fig. 11.22.
Hosts: In hindgut of many species of larval Simuliidae and Chironomidae (Diptera); more rarely in Culicidae and Tipulidae larvae.
Distribution: Streams, ditches, and drainpipes with running water
for still
water with Culicidae larvae in many states of the USA, in Canada,
Japan,
Australia, New
Zealand, England, Sweden, Norway, Spain, and France. Mexico
Smittium simulii is relatively common in lotic midge and blackfly larvae in the USA. (California, Montana, Wyoming, Minnesota, Kansas). Manier in 1963(b) described Rubetella simulii (nom. nud.) from several species of Simulium larvae collected from sites north of Montpellier, France; her species appears to be S. simulii. Lichtwardt, Y. Kobayasi, and H. Indoh, collected S. simulii in several regions of Japan, the most unusual find coming from mosquito larvae. Williams and Lichtwardt in 1982 (unpublished) found what appeared to be S. simulii in larvae of Elliptera sp. (probably E. astigmatica Alexander) (Tipulidae) from Step Falls, part of a stream near route US 2 draining from Tranquil Basin, south of Glacier National Park, Montana, USA. A number of axenic isolates have been obtained from blackflies, midges, and (two) mosquitoes from the USA and Japan. Lichtwardt has found S. simulii in the endemic blackfly Austrosimulium australense (Shiner) in New Zealand; and in Australia in various endemic Simuliidae, in Chironomus sp., and in at least two genera of Culicidae. In Queensland, Australia, S. simulii was found in a predaceous mosquito, Culex halifaxii. An immunoelectrophoretic study by Sangar et al. (1972) using seven cultures representing three host families showed that they are serologically related, thus confirming the morphological basis for speciation. Williams and Lichtwardt (1972a) found that only one of four isolates obtained from blackfly and midge larvae would infest mosquito larvae (Aedes aegypti), whereas the other three infested 1st instars slightly and the infestation did not persist through moltings to the 4th instar. It would seem, therefore, that mosquitoes are infestable only by some strains. Smittium simulii cultures have been used in several physiological and experimental studies as well (see Chapter 9). The type culture is CAL-8-1, isolated from a larva of Simulium argus (Win.).
References: Lichtwardt, 1964a; Manier, 1963b, 1969b (1970b);
Chapman, 1966;
Williams and Lichtwardt, 1972a; Sangar et al., 1972; Preisner, 1973;
EI-Buni
and Lichtwardt, 1976a, 1976b; Cerniglia et al., 1978; Starr et al.,
1979; White and Lichtwardt, 2004, Strongman and White, 2008, Strongman,
2007. Valle et al., 2011. Beach and White, 2012.
Smittium tipulidarum Williams & Lichtwardt, 1987
Thalli with sparse divergent branching in the hindgut of larvae of Tipulidae. Trichospores up to 14 or more in a series on a fertile branch, elongate-ellipsoidal, (15-)17.5(-20) x (3.5-)4.5(-5) µm; collar 2-3.2 x ca. 2 µm, with a single appendage at least 3 times the spore length, appendages tending to curl. Holdfast simple. Zygospores unknown.
Illustrations: Fig. 11.156.
Host: Elliptera astigmatica (Diptera, Tipulidae).
Distribution: USA (Colorado).
Reference: Williams and Lichtwardt, 1987b.
Smittium tronadorium Lichtwardt, Ferrington & López Lastra, 1999
Thalli densely branched at acute angles. Trichospores long-ellipsoidal with a slight median bulge, (15-)23(-28) x 3-5 µm, collars 1-3 µm long. Zygospores unknown.
Illustrations: Fig. 11.61.
Hosts: Paraheptagyia sp., Cricotopus sp. (Chironomidae).
Distribution: Patagonia, Argentina, Armenia (?). Mexico.
Reference: Lichtwardt et al., 1999, Nelder et al., 2005. Valle et
al., 2011.
Smittium
tynense Strongman, 2007
Thallus short with a central axis and dense, profuse branching. Attached to the hindgut lining by a small disk-like holdfast and secreted material. Trichospores long-ellipsoidal, 31-37 x 3-3.5 µm, with a short, blunt collar (about 3 x 3 µm) and a single appendage. Zygospores unknown. In hindgut of Chironomidae larvae.
Illustrations: Fig. 11.325
Hosts: Chironomidae larvae.
Distribution: Trout River near Tyne Valley, Prince Edward Island, Canada.
Reference: Strongman, 2007.
.
Smittium typhellum Manier & Coste, 1971
Thalli up to 1.2 µm long, from the basal, region producing several main branches about 6 mm diam from which arise verticillate secondary branches about 4 mm diam. Generative cells short (7-10 µm), 5-6 per fertile branch; producing nearly cylindrical trichospores with a slight median swelling, 25-30 x 3-3.5 µm, with a narrow collar 3-3.5 x 1.5-2 µm. Zygospores unknown.
Illustrations: Fig. 11.182.
Host: Larval hindgut of Chironomus sp. (plumosus complex) (Diptera, Chironomidae).
Distribution: Small pond at junction of routes N 109 and D 5 E, Department of Hérault, France.
Manier and Mathiez (1965) Fig. 7, published under the name of Typhella choanifera Manier, 1962a (nom. nud.) [ = Genistella choanifera Tuzet & Manier, 1953 (nom. nud.)], is identical to Manier and Coste's (1971) Fig.14. Manier (1969, p. 622) stated that Typhella (Genistella) choanifera, which came from Chironomus plumosus L. larvae, was probably a Smittium sp., but she did not validate that species due to lack of a sufficient description.
References: Manier and Coste, 1971; Manier and Mathiez, 1965.
Smittium
urbanum López Lastra,
Mazzucchelli & Lichtwardt, 2000
(in Lichtwardt, López Lastra and Mazzucchelli, 2000)
Thallus compact, branching often verticillate. Trichospores long-ellipsoidal, 19-27 x 3-4 µm, with a short cylindrical collar, produced singly on terminal branches, more commonly 1-2 on short fertile branchlets. Zygospores unknown.
Illustrations: Fig. 11.55.
Host: Bloodworm (Chironomidae).
Distribution: Argentina.
Reference: Lichtwardt, López Lastra and Mazzucchelli, 2000.
Spartiella
Tuzet & Manier ex Manier, 1968
[= Spartiella Tuzet & Manier, 1950a, nom. nud.]
Trichospores obpyriform, without a collar, with a single appendage. Zygospores attached perpendicularly and medially to the zygosporophore, with a collar upon detachment. In hindgut of Baetidae (Ephemeroptera) nymphs. Two species.
Type species: Spartiella barbata Tuzet & Manier ex Manier.
The new genus and species were invalidly described by Tuzet and
Manier
(1950a), with further observations published by the two authors in
1953. Manier
(1962b) later provided a generic Latin diagnosis and a more accurate
description. The genus and species became validated by Manier only in
1968 upon
citing a nomenclatural type (Art. 37); she also provided a Latin
description of
the species in that paper, which was not necessary (Art. 42).
Spartiella animae Lichtwardt, 1997.
Thalli much branched, less than 500 µm long, with a slightly swollen or lobulate basal cell. Trichospores obpyriform, 13-20 x 4-7 µm, collarless, bearing a single long, fine appendage. Zygospores unknown.
Illustrations: Fig. 11.134.
Host: Baetis sp. (Ephemeroptera, Baetidae).
Distribution: Costa Rica.
Reference: Lichtwardt, 1997.
Spartiella
barbata Tuzet & Manier ex
Manier, 1968
[= Spartiella barbata Tuzet & Manier, 1950a, nom. nud.]
Thallus up to 1 mm long. Mature basal cell often branched, 10-12.5 µm diam with bulbous swellings around the zone of attachment to the host cuticle. Branches about 5 µm diam at terminal end. by 10-12.5 µm at their widest diam. Trichospores 22-27 x 7.5-10 µm, without a collar. Single trichospore appendage often with a small spherical knob near the trichospore base. Zygospores 25-30 x 6-7.5 µm, attached medially and perpendicularly to the zygosporophore, upon detachment retaining a collar 3-3.5 µm long by 2.5-3.5 µm wide. Type species.
Illustrations: Fig. 11.71.
Hosts: In hindgut of Baetis rhodani Pictet, B. gemellus Eaton, and other Baetidae nymphs (Ephemeroptera).
Distribution: Streams (le Lez, la Mosson), Department of Hérault,
France;
England; Wales., Spain; Newfoundland, Canada
Moss and Lichtwardt (unpublished) collected Spartiella barbata in Baetidae from the Lake District of England, (stream draining from Little Langdale Tarn and River Duddon), and in Wales (River Ystwyth). The appendage of this species characteristically has a small spherical knob just below the base of the spore. The appendage often does not unfurl completely after release of the trichospore, and may form a tangled clump at the base of the spore; however, when it unravels it can be seen to consist of a very fine and extremely long filament. Trichospores of Pteromaktron protrudens (also from Baetidae) have a knobbed, long single appendage somewhat resembling that of Spartiella barbata, but the two species are otherwise quite distinct.
References: Manier, 1950 (1951), 1962b, 1968; Tuzet and Manier,
1950a, 1953; Valle, 2007
, Strongman, 2010.
Stipella
Léger & Gauthier, 1932
Base of thallus attached to hindgut cuticle by mucilaginous
secretion.
Trichospores cylindrical, without a collar, bearing 3(-4) equal
appendages.
Biconical zygospores attached perpendicularly to the zygosporophore. In
hindgut
of larval Simuliidae (Diptera). Two species.
Type species: Stipella vigilans Léger & Gauthier.
The name Stipella is conceivably a homonym of Stypella Mö11er 1895 (Tremellales). However, the General Committee on Botanical Nomenclature, when asked for an opinion, was divided in its vote on this issue: 8 to 6 that the names should be treated as variants (Voss, 1973). As a consequence of this split opinion, we have elected to maintain the name Stipella for the trichomycete genus. Stipella
latispora Valle, 2007
Thallus pinnately ramified, with a central axis 8-9.5 µm wide. Basal cell lobulate or simple, coated with amorphous material. Small peg-like projections irregularly dispersed along the basal cell surface. Trichospores 60-70 x 8.5-9 µm, ovoid-ellipsoidal and slightly curved, eccentrically attached to the generative cell, without a collar, 6(-7) petalloid appendages present. Generative cells 3.5-4 µm diameter, arranged in series with 1-4 cells per fertile branch. Zygospores 89-92 x 13 µm, biconical, Type I, formed homothallically from cells near conjugation tubes. Zygosporophore 30 x 11 µm, partially carried as a collar in the zygospore once released. In hindgut of Simuliidae larvae.
Illustrations: Fig. 11.319.
Host: In hindgut of Simuliidae (Diptera) larvae.
Distribution: Spain.
Reference: Valle, 2007.
Stipella vigilans Léger & Gauthier, 1932
Thalli up to 1 mm long, consisting of a coenocytic principal cell 6-10 µm diam with a simple or forked verrucose base producing a mucilaginous adhesion substance, and branches 3-4 µm diam. Trichospores cylindrical, 37-80 x 3-5 µm, without a collar, bearing 3(-4) broad (petaloid) appendages, often produced from a long series of generative cells. Homothallic; zygospores 80-105 x 15-18 µm, attached perpendicularly to a zygosporophore ~27 µm long x 15 µm wide arising from one of the conjugated cells. Type species.
Illustrations: Fig. 11.7; Fig. 11.8; Fig. 11.72.
Hosts: In hindgut of various larval Simuliidae (Diptera), including Simulium equinum L., S. ornatum Meig., S. variegatum Meig., and S. bezzii Corti.
Distribution: Streams in several French Departments (Dauphiné,
Hérault,
Puy-de-Dôme), and in England (Bere stream, Dorset). Spain. Armenia.
Thailand..
Nonsporulating thalli of Stipella can be confused with the more common genus Pennella, because both are found in blackfly hindguts attached by a mucilaginous secretion surrounding the base of the principal cell. The genera are distinguishable by the larger number of trichospore appendages in Pennella spp., and especially by their different zygospore types, those of Stipella being Type I and those of Pennella Type III. The cylindrical trichospores of Stipella with 3 appendages somewhat resemble those of Glotzia (from mayfly nymphs), but one of the 3 appendages of Glotzia normally is much longer than the other two. The zygospore types of Glotzia and Stipella also are different. Manier (1955a) described Stipella vigilans as sometimes attaching to thalli of Paramoebidium sp., but the epiphytic fungus was no doubt a Simuliomyces, a genus not then described. Moss (1970) states that S. vigilans sometimes protrudes from the rectum of blackfly larvae.
References: Léger and Gauthier, 1932; Tuzet and Manier, 1950a;
Manier, 1950
(1951), 1955a, 1963b, 1969b (1970b); Moss, 1970; Valle, 2004, 2007,
Nelder et al., 2005.
Tectimyces
Valle & Santamaria, 2002b
Trichospores without appendages and bearing an inconspicuous collar upon release. Generative cells elongate and broadened distally. Biconical zygospores of Type II, submedially and obliquely attached to the zygosporophore. Upon release the zygospores bear a lateral collar and a single mucilaginous appendage-like structure. Thalli irregularly pinnate or umbellate. In hindgut of Leptophlebiidae (Plecoptera) nymphs. Two species..
Type species: Tectimyces leptophlebiidarum Valle & Santamaria.
Tectimyces leptophlebiidarum Valle & Santamaria, 2002b
Thalli pinnate (in young thalli) to irregularly branched (in old thalli), attached to the host gut cuticle by means of a broadened and sometimes lobulate basal cell, with a disk-like secreted holdfast. A variable number of lateral, rhizoid-like branches, arising from the main axis, probably functioning as 'subsidiary' holdfasts. Remaining branches projecting laterally from the main axis showing typically arcuate tips. Each fertile branch giving rise to 1-4 ovate-ellipsoidal unappendaged trichospores of 45-52 x l0.5-12.5 µm, with a rounded apex and a flattened base. Trichospores developing at the tips of up to110 µm long generative cells, or from a lateral outgrowth (3.5-)8-15(-25) µm of intermediate generative cells. Free trichospores bearing a very short collar, 1.5-2 µm, remainder of the upper part of the swollen generative cell. Biconical zygospores of Type II, measuring 41-47 x 6-8 µm, arising from the scalariform conjugation area, developing on long and thin specialized hyphae. Once released, zygospores show a lateral outwardly flared collar 3-4 x 3-4 µm. A single mucilaginous flame-shaped appendage-like structure, with a total length of 11-14(-80) µm, was found in most of the detached zygospores. Type species.
Illustration: Fig. 11.267.
Host: Habroleptoides confusa (Ephemeroptera, Leptophlebiidae).
Distribution: Spain.
Reference: Valle and Santamaria, 2002b.
Tectimyces robustus Valle & Santamaria, 2002.
Thalli umbellate, with distally broadened axes, with 3-7 branches arising per node, reaching up to a fifth order of ramification, attached to the host gut cuticle by a rounded basal cell with a disc-like holdfast (in young thalli), but later, when thalli mature, the holdfast is no longer observed and bidirectional growth occurs, giving rise to a napiform basal hypha, from which generative cells and trichospores can develop. Basal and medial cells broader than those of the apex, with a swollen zone at the apex, giving rise to multiple tapering branches with curled tips. Each fertile branch giving rise to 1-4 obovate-ellipsoidal unappendaged trichospores of (33-)38-40(-44) x 9-11 µm. Trichospores developing at the tips of generative cells that are abruptly constricted at the apex like a bottleneck. Free trichospores carrying a very short collar, 1.5-2 µm, consisting of the remainder of the upper part of the swollen generative cell. Terminal generative cells can reach up to 118 µm long. Intermediate generative cells very variable in size, with trichospores developing from lateral outgrowth of 15-90 µm. Zygospores unknown.
Illustration: Fig. 11.268.
Host: Habroleptoides confusa.
Distribution: Spain.
Reference: Valle and Santamaria, 2002b.
Trichozygospora
Lichtwardt, 1972
Trichospores ellipsoidal with a prominent collar from which emanate multiple fine appendages. Biconical zygospores with a prominent collar, attached obliquely to the zygosporophore, having numerous fine appendages upon release. In hindgut of larval Chironomidae (Diptera). Monotypic.
Type species: Trichozygospora chironomidarum Lichtwardt.
Trichozygospora chironomidarum Lichtwardt, 1972
Branched thalli attached to hindgut cuticle by an inconspicuous holdfast. Trichospores ellipsoidal, 17-29 x 4.5-11 µm, with a bulbous collar 2-13 µm long narrowing at the free end, bearing 5-7 very fine appendages. Zygospores biconical, (58-)65(-69) x (15-)16(-19) µm, bulbous collar 13-19 x 7-9 µm narrowing at the free end, bearing 10 or more fine appendages upon release. Collar attached obliquely 1/5 to 1/4 the distance from one end of the zygospore and connected to a zygosporophore that develops without septation from the free end of one of the conjugating branches. Type species.
Illustrations: Fig. 11.7; Fig. 11.8; Fig. 11.23.
Hosts: In larval hindgut of Orthocladius spp., Cricotopus sp., and Diamesa valkanovi Saether, and other unidentified midges (Diptera, Chironomidae).
Distribution: In fast-flowing streams in Wyoming, USA, northern Sweden, Switzerland, and possibly England.
Trichozygospora chironomidarum was first recorded from a stream in the Grand Teton National Park in the Rocky Mountains of Wyoming, and several years later was found at the mouth of Abiskojĺkka, a river draining into Lake Torneträsk located some 125 miles north of the Arctic Circle in Sweden. Such disjunct habitats suggest that it exists in other Holarctic sites as well. Moss and Lichtwardt, working in the Lake District of northern England in 1980, collected what appeared to be this species (based on trichospore-producing thalli only) in an unidentified species of midge larva. The Switzerland collection (from a stream draining Steingletscher, below Col de Susten) had zygospores as well as trichospores, so its identity was confirmed.
The midge larvae in Sweden, Orthocladius sp. and Diamesa valkanovi, were abundantly infested, and about a dozen axenic isolates of T. chironomidarum were obtained by Lichtwardt. However, they grew poorly, and the final isolate was lost some 18 months later despite attempts to satisfy its requirements for growth.
Moss and Lichtwardt (1976, 1977) studied the ultrastructure of the trichospores and zygospores of T. chironomidarum. The results are discussed in Chapter 7.
References: Lichtwardt, 1972; Moss and Lichtwardt, 1976, 1977.
Holdfast
basal cell 8-10 µm diam, cells of the central axis of the thallus 4-9
µm wide,
trichospore-bearing branchlets narrowing to 1.5-2.5 µm wide with 4-16
trichospores produced along one side of a branchlet. Trichospores
attached by a
short (< 1 µm) tapered base; young spores are ovoid but when mature,
before
release, they develop a protrusion on two sides giving a
trifoliate-leaf shape.
Trichospores have two, or more commonly, three thin appendages and no
collar.
Zygospores unknown.
Illustrations: Fig. 11.373.
Host: Eurylophella temporalis (Ephemerellidae,
Ephemeroptera),
Distribution: Nova Scotia, Canada.
Reference: Strongman and White, 2011.
Zygopolaris
Moss, Lichtwardt, & Manier, 1975
Trichospores elongate-obpyriform, with no collar or appendages. Modified biconical zygospores attached at one pole with axis in line with that of the zygosporophore. In hindgut of Ephemeroptera nymphs. Two species.
Type species: Zygopolaris ephemeridarum Moss, Lichtwardt,
&
Manier.
Zygopolaris borealis Lichtwardt & Williams, 1984
Branched thalli up to 1.5 mm long, rarely longer, attached to host cuticle by a well-defined basal holdfast, often showing dichotomous (or trichotomous) branching below the sporulating branchlets. Trichospores elongate-ovoid, (44-)50(-65) x 6-9 µm, borne on sporulating tufts of branchlets each consisting of 3-12 or more generative cells 10-20 µm long, sometimes projecting from the host's anus. Upon release, trichospores without a collar, or with a very short outwardly flared collar, and bearing no appendages. Modified biconical zygospores (74-)79(-84) x 18-22 µm, attached at one pole to a zygosporophore, 29-38 x 13-21 µm.
Illustrations: Fig. 11.189.
Host: In hindgut of larval Epeorus longimanus (Eaton) (Ephemeroptera, Heptageniidae).
Distribution: In streams, Montana, USA.
Reference: Lichtwardt and Williams, 1984.
Zygopolaris ephemeridarum Moss, Lichtwardt & Manier, 1975
Branched thalli up to 2 mm in length attached to hindgut cuticle by a short secreted holdfast formed laterally near the base of a slightly swollen basal cell. Main axis of the thallus producing infrequently septate branches 7-10 µm diam, which may project out of the host anus. Sporulating branchlets forming a more or less compact head, each branchlet composed of 3-15 generative cells 8-15 µm long. Trichospore elongate-obpyriform (25-)32(-38) x 5-8 µm, upon release having no collar or appendages (rarely 3 appendages). Modified biconical zygospores (40-)55(-86) x (13-)15(-26) µm, attached at one pole to a zygosporophore 17-31 µm in length. Type species.
Illustration: Fig. 11.24.
Hosts: In hindgut of lotic Ephemeroptera nymphs, especially in Baetidae such as Baetis bicaudatus Dodds, B. tricaudatus Dodds, B. parvus Dodds, and Acentrella trubida McDonnough; also in Ephemerellidae such as Ephemerella inermis Eaton and possibly other species of Ephemerella. In Mexico, in Baetidae nymphs.
Distribution: Mountain streams of Colorado, Wyoming, Idaho, and
Montana,
and stream
in Seattle, Washington, USA; Great Smoky Mountains National Park.
Veracruz, Mexico, Prince Edward Island and Newfoundland, Canada.
Zygopolaris ephemeridarum is relatively common in Rocky Mountain streams in mayfly nymphs of the Baetidae, less commonly in Ephemerellidae. The species is easily identified, but could be confused with the less common and geographically more restricted species, Z. borealis, if spore measurements are not made. However, Z. borealis lives in Heptageniidae. The two species of Zygopolaris have occasionally been found in the same stream but in different families of mayflies.
Both trichospores and zygospores are devoid of well-developed appendages. Trichospores rarely may have a small blob of material at their base upon release (Moss et al., 1975). Lichtwardt and Williams (1984) reported finding 3 short appendages on a released trichospore of Z. ephemeridarum and discrete appendages within the generative cells of unreleased spores. Zygospores have a fibrous substance at their base within the zygosporophore (Moss and Lichtwardt, 1977) which, upon release of the zygospore, may expand into a large, almost invisible skirt of clear material surrounding the base of the zygospore (Lichtwardt and Williams, 1984).
References: Moss et al., 1975; Moss and Lichtwardt, 1977; Lichtwardt
and
Williams, 1984; White, Siri and Lichtwardt, 2006; Valle, White, and
Cafaro, 2008, Strongman, 2007. Stribgman, 2010. Beach and White, 2012.
Manier ex Manier &
Lichtwardt,
1978 (in Lichtwardt and Manier, 1978
[= Asellariales Manier, , 1951 (1950), nom. nud.]
Thalli branched, septate, reproducing by fragmentation of the branches into uninucleate arthrospores. Sexual reproduction unknown. Attached by a specialized basal holdfast cell or holdfast apparatus to the hindgut cuticle of Isopoda or Insecta (Collembola).
Consisting of the single family Asellariaceae.
Characters same as those of the order. Three genera (including Baltomyces that might be a special case deserving a separate classification).
Type genus: Asellaria Poisson.
Formerly included in this family, the genus Trichoceridium
Poisson
(1932b), with the single species T. ramosum, is not recognized
by the
authors as a good taxon, and is consequently excluded from this
treatment.
Although recognizing it was incompletely described, the monotypic genus
was
placed in the Asellariaceae by Manier in 1951 (1950) (also see Manier,
1963a,
1969b, and Manier and Lichtwardt, 1968) solely on the basis of
Poisson's report
of some disarticulating cells in the branched thallus, a feature of
reproduction in the Asellariaceae. The "arthrospores" he described do
not appear to have the ontogeny and structure of typical Asellariaceae;
furthermore, on occasions the authors have seen similar cells of
Legeriomycetaceae that break away [e.g., Genistellospora
homothallica
(Lichtwardt, 1972, Fig. 12)]. Trichoceridium ramosum has the
type of
branching and holdfast structure found in many Legeriomycetaceae, and,
significantly, its larval host is a species of Trichocera
(Diptera,
Tipulidae). All other Asellariaceae occur in Isopoda or Collembola.
Lichtwardt
and Williams (unpublished) in 1982 found two species of Smittium
(Legeriomycetaceae) in cranefly larvae (Tipulidae) in the Rocky
Mountains of
Montana, USA. Possibly Poisson's fungus was, in fact, a species of Smittium
in a nonsporulating stage.
Asellaria
Poisson, 1932a
Branched thalli consisting of mostly coenocytic cells prior to development of uninucleate arthrospores. Basal cell morphologically distinct. Attached to hindgut cuticle of aquatic, marine and terrestrial Isopoda (Crustacea). Seven species.
Type species: Asellaria caulleryi Poisson.
Asellaria
armadillidii Tuzet & Mainer
ex Manier, 1968
[= Asellaria armadillidii Tuzet & Manier, 1953, nom.
nud.]
Thalli up to 1.1 mm long, consisting of a main axis with lateral branches 7-8 µm diam and secondary branches. Principal (basal) cell more or less cylindrical, 60-165 µm long by 8-17 µm diam, attached at its base to host cuticle by many short rhizoidal projections embedded in a mucilaginous substance. Principal cell producing a whorl of branches at its distal end, sometimes branching at its base above the rhizoidal outgrowths and at other parts of the side wall. Arthrospores 6-23 µm long.
Illustrations: Fig. 11.25; Fig. 11.201.
Hosts: In hindgut of Armadillidium simoni Dollfus, A.
vulgare (Latreille),
and A. nasatum Budde-Lund (Isopoda, Armadillidiidae). In
laboratory
experiments, infestation also established in the following Isopoda: Chaetophiloscia
elongata (Dollf.) (Oniscidae); Acaeroplastes melanurus B.-L.,
Porcellio
laevis (Latr.), Porcellio lamellatus Verh., Protracheoniscus
occidentalis Vand. (Porcellionidae).
Distribution: Terrestrial habitats in Department of Hérault, France, USA (Kansas, Missouri), and Argentina.
All of the naturally infested hosts of Asellaria armadillidii are species of Armadillidium, but Manier (1963a) was able in the laboratory to transmit the fungus successfully to five additional species that were uninfested in their natural habitats, by keeping them in containers with infested A. simoni (see Chapter 6). The other two naturally infested isopods, Armadillidium vulgare and A. nasatum, were collected several times in different sites in Kansas by the authors. Those two isopods are also hosts of Parataeniella armadillidii (Eccrinales). It is likely that Asellaria armadillidii is much more widely distributed than present records indicate.
References: Tuzet and Manier, 1953; Manier, 1963a, 1968, 1969b
(1970b);
Chapman, 1966.
Asellaria
aselli Scheer ex Moss &
Lichtwardt, 1984 (in Lichtwardt and Moss, 1984a)
[= Asellaria aselli (Sheer) Sheer, 1972a, nom. nud.]
[= Recticharella aselli Sheer 1944, nom. nud.]
Mature thalli up to 2.8 mm long. First cell of the main axis (above the holdfast cell) bearing a whorl of branches that may rebranch; other cells of the main axis often with one or more branches. Basal holdfast cell up to 170 µm long by 37 µm diam, major lower part divided into two appressed tapered prongs, each with pectinate rows of short to long (10 µm), sometimes branched, lateral outgrowths. Arthrospores usually (15-)50-93 x (6-)14-20 µm.
Illustrations: Fig. 7.10; Fig. 11.25; Fig. 11.195.
Host: In hindgut of Asellus aquaticus L. (Isopoda, Asellidae).
Distribution: Freshwater ponds, lakes, and streams in north-central Europe (Poland, Germany), and in England.
Scheer (1944) first described this species, under the new generic name Recticharella (nom. nud.), and later (1972a, 1972b) he reassigned it correctly, but invalidly, to the genus Asellaria. The species is widely distributed in north-central Europe and England, and one can assume it is also present in other, unreported localities because of the wide distribution of its host species.
Asellus aquaticus also harbors the morphologically similar (type) species, A. caulleryi. The most obvious way the two can be differentiated is by the structure of the basal holdfast cell, that of A. aselli being divided into two appressed prongs, each prong with one row of pectinate outgrowths; A. caulleryi's basal cell has no bifurcation, and has two series of pectinate outgrowths. Lichtwardt and Moss (1984) reported that some thalli of A. aselli, which they collected in England, had a mucilaginous secretion around the basal cell.
References: Lichtwardt and Moss, 1984a; Moss, 1979; Sheer, 1944,
1972a,1972b.
Asellaria caulleryi Poisson, 1932a
Thalli 200-1500 µm long, main axis (above the holdfast cell) ~10 µm diam, from whose basal region arise many branches without secondary branches. Basal holdfast cell coenocytic, 30-140 µm long, up to 20-25 µm diam, tapering basally and bearing on its incurved surface two parallel, pectinate rows of short outgrowths. Arthrospores 40-45 µm long. Type species.
Illustrations: Fig. 11.25; Fig. 11.204.
Hosts: In hindgut of Asellus aquaticus L. and A. meridianus Rac. (Isopoda, Asellidae).
Distribution: Ponds, and occasionally in streams, in Departments of Pas-de-Calais and Ille-et-Vilaine, France.
This freshwater species does not appear to have been collected by investigators other than Poisson. He provided a lengthy description of its morphology, cytology and development. The isopods were most highly infested when feeding on Volvox. When he fed them plant materials such as dead leaves, thalli broke loose and were voided with the excreta, presumably due to abrasive action of those materials. Thalli were not maintained in isopods fed a carnivorous diet such as earthworm fragments.
The holdfast cell of Asellaria caulleryi has some resemblance to that of A. aselli, which also lives in Asellus aquaticus, but the holdfast cell of the latter species is divided into two appressed prongs. Asellus meridianus, the other host of A. caulleryi, has been found infested also with A. gramenei, in southern France.
Reference: Poisson, 1932a.
Asellaria
dactylopus L.B. Valle & Cafaro, 2008
Thallus small, robust, 260-420 µm long, with main axis pinnately
branched. Basal cell 23-37 x 12-20 µm, broadly obpyriform to broadly
ellipsoid, with a slightly thick wall, with lobulate projections at the
proximal end, covered by a skirt of hyaline holdfast material, various
branches arising from the lower part of the basal cell, a single cell
arising directly above the upper septum of the basal cell, obpyriform,
typically smaller, giving rise to 2-4 verticillate branches that
disarticulate into arthrospores. Arthrospores not regularly cylindrical
but apically wider at the distal end, 12-20 µm long x 7-9.5 µm diam.
Illustrations: Fig. 11.328.
Host: In hindgut of Venezillo sp.
(Isopoda, Armadilliidae).
Distribution: Puerto Rico, Dominican Republic.
Reference: Valle and Cafaro, 2008.
Asellaria
gramenei Tuzet & Mainer ex
Manier, 1968
[= Asellaria gramenei Tuzet & Manier, 1950a, nom. nud.]
Thalli up to 1.8 mm long, main axis 15-23 µm diam, consisting of a row of several cells from whose bases arise one or more branches without secondary branches. Basal holdfast cell 40-50 µm long by 18-27 µm diam, campanulate, with the base invaginated to form a furrow. Arthrospores 40-65 µm long.
Illustration: Fig. 11.25; Fig. 11.193.
Host: In anterior hindgut of Asellus meridianus Rac. (Isopoda, Asellidae).
Distribution: In streams draining a salt marsh, Department of Hérault, France.
The original descriptions of Asellaria gramenei [Tuzet and Manier, 1950a; Manier, 1950 (1951)] identified the host as Asellus aquaticus, but subsequent publications called it A. meridianus. This isopod is a freshwater species, but was collected from streams with unspecified salinity draining the Salins de Gramenet near Montpellier.
Asellaria gramenei is very similar morphologically to A. ligiae from marine isopods (Ligia spp.), one species of which, L. italica, can be found infested with A. ligiae at Palavas on the Mediterranean coast not far from the single reported inland locality for A. gramenei. Asellaria ligiae, however, is considerably more dispersed geographically than A. gramenei. Other than their different host preferences, A. gramenei can be distinguished from A. ligiae by the shape and dimensions of the basal holdfast cell (it is campanulate and longer than wide), by lesser branching in mature thalli, and by having generally longer arthrospores.
References: Tuzet and Manier, 1950a; Manier, 1950 (1951), 1963a,
1968, 1969b
(1970b), 1978.
Asellaria
jatibonicua L.G. Valle & Cafaro, 2008.
Thallus 600-1000 x 11-15 µm, with main axis longer than lateral ramifications. Verticillate branches usually 2-4, arising from each of the axial cells next to the upper septum, those growing from the lower region being longer; mature specimens sometimes showing profuse verticillate branching up to fourth order. Basal cell elongate-fusiform, 70-120(-140) x 14-20 µm, tapering to a small bulbous or campanulate proximal end, secreting sticky material accommodating to the substrate, with 1-6 pairs of ramifications, 8-12.5 µm diam arising pinnately from the basal cell. Arthrospores 15-34 x 6.5-11 µm, the terminal ones longer, rounded at the apex, the intercalary ones shorter, truncate at both ends, disarticulating first from distal branches, although even the cells from the main axis finally may become disarticulated. Zygospores spherical, 14-16 µm diam, with prominently thick walls, slightly ellipsoid in young phases, arising not directly from conjugations tubes but on contiguous cells always next to a septum.
Illustrations: Fig. 11.329.
Host: Littorophiloscia
culebrae (Moore) (Isopoda, Oniscidae, Philosciidae).
Distribution: Puerto Rico.
Reference: Valle & Cafaro, 2008.
Asellaria
ligiae Tuzet & Manier ex
Manier, 1968
[= Asellaria ligiae Tuzet & Manier, 1950a, nom. nud.]
Mature thalli much branched, sometimes more than 1 mm long by almost 2 mm wide. Basal branches 13-25 µm diam. Basal holdfast cell 30-50 µm long by 40-50 µm diam, with a spherical, bulbous expansion invaginated at the base to form a furrow. Arthrospores 23-47(-70) µm long.
Illustrations: Fig. 7.11; Fig. 11.25; Fig. 11.26.
Hosts: In hindgut of Ligia italica Fab., L. exotica Roux, and other Ligia spp. (Isopoda, Ligiidae).
Distribution: Probably worldwide. On marine shorelines in Europe (France, Yugoslavia), USA (North Carolina, Florida, California, Hawaii), Japan, Puerto Rico, and Costa Rica. Also from an undescribed Ligia sp. living in a freshwater stream and pool in Hawaii.
Asellaria ligiae is the most widespread member of the Asellariales, and the only marine species. In the authors' experience, infestation of different populations varies from very low to very high. Infestation rates may depend upon the density of the isopods as well as the season and the molting frequencies. Ligia exotica is found in many oceans and seas, and this may account for the geographic dispersal of the fungus. These isopods, often called the rock louse, scamper about on rocks, pilings, seawalls, etc., near the water's edge, but can be considered marine in the sense that some species (e.g., L. exotica) can remain submerged in seawater for prolonged periods, if aerated. In Hawaii there exists an apparently undescribed and endemic species of Ligia that lives upstream in and near perfectly fresh water; this population was found to be highly infested with A. ligiae (see Chapter 4).
Manier (1973b) did an electron microscopic study of A. ligiae, and found the septal structure to resemble that found in the Harpellales. Manier (1963a) and Lichtwardt (1973a) germinated arthrospores of A. ligiae in vitro and found that they produced a limited exogenous growth that somewhat resembled a trichospore, but these did not detach. Such germinated arthrospores closely resemble the disarticulated generative cell-trichospore unit of Carouxella scalaris (Harpellaceae). Conjugating thallial branches and released arthrospores have been observed in A. ligiae, but there was no zygospore development (Lichtwardt, 1973a).
Lichtwardt has observed in heavily infested isopods on several occasions thalli of A. ligiae without the usual bulbous basal cell. Such thalli were held to the hindgut by a branching rhizoidal outgrowth that penetrated through the cuticle (Fig. 7.11C) and were interpreted as being branches that had broken away from other normal thalli in the gut and had attached by means of this unusual adventitious growth (see Chapter 7). Asellaria ligiae is capable of complete conversion of the thallus to arthrospores, leaving only the basal holdfast cell.
Asellaria ligiae morphologically is most similar to A. gramenei from the aquatic isopod Asellus meridianus. Asellaria ligiae has a basal cell that is more bulbous and usually at least as wide as it is long, and has a more developed branching system.
References: Tuzet and Manier, 1950a; Manier, 1950 (1951), 1963a,
1968,
1973b; Lichtwardt, 1973a, 1976.
Asellaria saezii L.G. Valle, 2006
Branched
thalli of
700-900 µm (x
= 832 µm)
long and main hyphal filaments of 5-5.5 µm (x = 5.3 µm)
wide, with verticillate projections and secondary. Basal cell 60-75 ×
17-20 µm
(x =
67.5 × 18.5 µm), elongated-pyriform, branched, with a broad invaginated
base. The
holdfast involves part of the hindgut lining in the central furrow.
Profuse
verticillate branches arise laterally from the basal cell. Upper thallial branches present broad cells at
the proximal zone, close to the main axis, making swollen and bulb-like
structures. All these branches become disarticulated at maturity to
produce
arthrospores. Arthrospores (17-)30-48 × (3.5-)5-7 µm (x
= 36.4 × 5.2 µm),
slightly
bent and with a truncate apex.
Illustration: Fig. 11.307, Fig. 11.25
Host: In hindgut or Trichoniscus
pusillus Brand (Isopoda, Oniscidae).
Distribution: Barcelona, Spain.
Reference: Valle, 2006.
Asellaria unguiformis Lichtwardt, 1984 (in Lichtwardt and Moss, 1984a)
Mature thalli highly branched. Basal holdfast cell consisting of two principal, curved talon-like cell extensions 70-120 µm long and tapered to a point, each with a pectinate series of short to long irregular projections and with accessory talon-like or bulbous outgrowths with irregular projections. Arthrospores usually 60-100 x 10-20 µm.
Illustrations: Fig. 11.25; Fig. 11.194.
Hosts: In hindgut of Lirceus hoppinae (Faxon) and Caecidotea laticauda (Williams) Caecidotea communis (Isopoda, Asellidae).
Distribution: Streams in Arkansas, Florida, Massachusetts, New
Hampshire,
USA.
.
All branches of A. unguiformis may disarticulate into
arthrospores,
leaving only the strikingly complex basal holdfast cell attached to the
host
cuticle as evidence of a former thallus.
Reference: Lichtwardt and Moss, 1984a; White, 1999.
Baltomyces
Cafaro, 1999
Thalli branched. Central main axis septate, attached lengthwise to the hindgut, bearing numerous free lateral fertile branches from each side. Long-fusiform sporangia produced in chains at terminal ends of branches, each bearing one cylindrical spore. In aquatic Isopoda. Monotypic.
Type species: Baltomyces styrax Cafaro
Baltomyces
styrax Cafaro, 1999, emend. Oman and M.M. White, 2012
Branched thalli 130-460(-500) µm, attached to the hindgut cuticle of
freshwater isopods. Thalli consists of a septate main axis, attached
lengthwise in the hindgut without a conspicuous holdfast but with
numerous free lateral branches, 100-420 x 1.3-3 µm. The main
(basal) axis derives from a more or less cylindrical nonseptate
sporangiospore, with 4-5 terminal appendages at each end, visible
occasionally upon release. The spore becomes fusiform while free, or in
rare cases before release, then develops multiple transverse septa and
a single sagittal septum when it attaches to the hindgut. Nonseptate
branches develop from the spore, presumably one per segment. Sporangia
(42-)52-70(-88) x 2.7-4 µm when nature, produced in chains at the
terminal ends of each branch. Branches are tapered at each end. Each
sporangium bears a cylindrical sporangiospore 20-25(-32) x 2-4 µm. The
spore released at maturity through a tear on the middle section of the
sporangium or simply by degradation of the sporangium wall The
free spore attaches to the gut, germinates and reproduces a new
thallus. No sexual reproduction was observed.
The species was studied from several new sites and redescribed by
Beach and and White (2012) who provided a series of new
illustrations based on the emended description.
Illustrations: Fig.
11.43. Fig. 11.382.
Hosts: Caecidotea obtusa and other Caecidotea spp.
including C. communis, C. intermedia.
Also Larcius sp. in Kansas.
Distribution: Louisiana, Illinois, Idaho, Kansas, Wisconsin, USA..
Reference: Cafaro, 1999. Oman and White, 2012.
Orchesellaria
Manier ex Manier & Lichtwardt, 1969 (1968)
[= Orchesellaria Manier, 1958, nom. nud.]
Branched thalli with a proliferation of cells or branches arising from the base of the original cell, attached to host cuticle by a holdfast structure secreted by one or more basal cells, or by basal rhizoidal cells. Arthrospores arising from disarticulated branches, or terminally. Attached to hindgut cuticle of Collembola (Insecta). Four species.
Type species: Orchesellaria lattesi Manier ex Manier & Lichtwardt.
The generic diagnosis provided above is emended so as to encompass
species
described subsequent to Manier and Lichtwardt's diagnosis.
Orchesellaria
lattesi Manier ex Manier
& Lichtwardt, 1969 (1968)
[= Orchesellaria lattesi Manier, 1958, nom. nud.]
Thalli 300-800 µm long by 150-400 µm wide, branches 2-5 µm diam. Basal holdfast complex consisting of a curved filamentous lateral growth from the initiating spore, this lateral growth secreting a holdfast substance and giving rise to a series of parallel short and long thallial branches more or less perpendicular to the initiating spore cell. Arthrospores 20-60 x 2-5 µm, bearing 3-4 serrations on the lateral wall near their apical end. Type species.
Illustrations: Fig. 11.27; Fig. 11.199.
Hosts: In hindgut of Orchesella villosa L. (Collembola, Entomobryidae).
Distribution: On water and damp vegetation by water's edge, Department of Hérault, France.
The fungus can be found throughout the hindgut, but in less infested individuals thalli may be present only in the posterior rectum. The unusual serrations that develop on the arthrospores even before they release later produce the characteristic lateral growth described above. This original cell (the arthrospore) may persist as part of the developing thallus, but in a degenerated form.
References: Manier, 1958, 1964c, 1979b; Manier and Lichtwardt, 1968
(1969).
Orchesellaria
mauguioi Manier ex Manier,
1970b (1969b)
[= Orchesellaria mauguioi Manier, 1964c, nom. nud.]
Thalli 200-400 µm long by 100-150 µm or more wide, attached to host cuticle by a somewhat bulbous basal region. Initiating spore remains persistent, producing at its base, directly and indirectly, a cluster of radiating branches that may in turn rebranch. Most thallial cells slightly wider at their distal ends, commonly 20-35 x 4-9 µm, disarticulating to form arthrospores.
Illustrations: Fig. 11.27; Fig. 11.28.
Hosts: In hindgut of Isotomurus palustris (Müller), Isotoma sp., and Agrenia bidenticulata (Tullberg) (Collembola, Isotomidae).
Distribution: On surface of lotic and lentic waters, and adjacent
vegetation
and other damp substrates, in Department of Hérault, France, and in USA
(Washington, Montana). Japan.
Orchesellaria mauguioi has been found in the widespread springtail species Isotomurus palustris in France and the USA. The fungus was reported by Lichtwardt and Moss (1984a) to be present in Montana in all three of the presently known hosts: Isotoma sp. and I. palustris from a cattail swamp, and Agrenia bidenticulata from rocks at the base of a waterfall.
Moss (1975) found the septal structure of O. mauguioi to be of the harpellid type, as it is also in O. podurae and Asellaria ligiae. Lichtwardt and Moss (1984a) reported finding numerous spherical intercalary, or more rarely terminal,
chlamydospores in one springtail.
References: Manier, 1964c, 1969b (1970b), 1979b; Moss, 1975, 1979;
Lichtwardt and Moss, 1984a. Degawa, 2009.
Orchesellaria pelta Lichtwardt, 1984 (in Lichtwardt and Moss, 1984a)
Branched thalli growing singly or in multiple tufts up to 200 µm long, attached to host cuticle by a flat shieldlike holdfast of irregular shape. Branches 2-6 µm diam, producing terminally single filiform deciduous cells 40-60 x 1.2-2.2 µm.
Illustrations: Fig. 11.27; Fig. 11.196.
Host: In hindgut of Hydroisotoma schaefferi (Krausbauer) (Collembola, Isotomidae).
Distribution: On water and marginal leaf packs in streams in Missouri and Arkansas, USA.
This species of Orchesellaria is unusual in two respects: It produces arthrospores that are filiform and develop singly at the ends of branches, and it is attached to the host's cuticle by a secreted holdfast structure that is flat and of irregular shape. Adjacent tufts of thalli may share a common shieldlike holdfast structure. Spherical chlamydospores have been found in some springtails.
Reference: Lichtwardt and Moss, 1984a.
Orchesellaria podurae Manier, 1979b
Thalli 120-170 µm long by 170-250 µm wide. Basal region attached to host cuticle by several small swollen cells with rhizoidal bases. Initiating spore persistent during thallus development. Thalli much branched, consisting of cells slightly wider at their apical ends, 23-25 x 4-5 µm, which disarticulate basipetally to form arthrospores.
Illustrations: Fig. 11.27; Fig. 11.197.
Host: In hindgut of Podura aquatica L. (Collembola, Poduridae).
Distribution: On bordering vegetation and water of two ephemeral streams, Department of Hérault, France.
Manier's 1979(b) description of O. podurae included an electron micrographic study that showed the septal structure to resemble the harpellid type, found also in O. mauguioi and Asellaria ligiae (Asellariales). The fungus has a thallus similar to O. mauguioi's, but has a distinctively different holdfast apparatus.
Léger
& Duboscq,
1929a
sensu Manier & Lichtwardt, 1969 (1968)
Thalli coenocytic, unbranched or (rarely) branched at the base. Producing basipetally one or more types of sporangiospores. Attached by a secreted holdfast to hindgut or foregut of Diplopoda, Crustacea, or Insecta.
Consisting of the families Eccrinaceae, Palavasciaceae, and Parataeniellaceae.
Léger and Duboscq's (1929a) concept of the order included the families Eccrinaceae, Arundinulaceae, and Taeniellaceae. The latter two were incorporated into the Eccrinaceae by Manier and Lichtwardt [1968 (1969)], at which time two new families, the Palavasciaceae and Parataeniellaceae, were established.
Terms: Primary infestation sporangiospores are released
from the gut
and germinate only after ingestion by a suitable host; they are usually
either
thin walled and uninucleate, or thick walled and 1- to 4-nucleate (Fig.
7.20A, B).
Secondary infestation sporangiospores germinate within the gut
where
they are produced, thus increase infestation endogenously; they are
typically
thin walled and 4- to 8-nucleate (Fig.
7.20C).
Spore mother-cells are the spores that give rise to a new
thallus by a
germination process; they may degenerate soon after germinating, or
they may
persist at the apex of maturing thalli as a distinct structure with or
without
a crosswall separating them from the thallus proper (Fig.
11.34D).
Léger
& Duboscq,
1929a
emend. Manier & Lichtwardt, 1969 (1968)
Thalli unbranched, or (in a few species) branched near the base. Two basic types of sporangiospores formed singly in basipetal series of terminal sporangia, usually on different thalli: (1) primary infestation spores that are uninucleate and thin walled, or (usually upon molting of the host) thick walled, with or without appendages, and 1- to 4-nucleate; and (2) secondary infestation spores that are multinucleate and thin walled. Other cell types may be produced. In hindgut or foregut of Diplopoda, Crustacea and Insecta. Fourteen genera.
Type genus: Enterobryus Leidy.
Alacrinella
Manier & Ormičres ex Manier, 1968
[= Alacrinella Manier & Orrničres, 1961b, nom. nud.]
Thalli dimorphic, with spore mother-cell persisting apically. Macrothalli lobed or inflated at the base, producing thick-walled, oval, 4-nucleate primary infestation sporangiospores, or multinucleate secondary infestation sporangiospores. Microthalli cleaving into a series of small cells. In hindgut of marine Isopoda (Limnoria spp.) (Crustacea). Two species.
Type species: Alacrinella limnoriae Manier & Ormičres ex Manier.
This genus is found only in the small marine wood-boring isopods
commonly
known as gribbles. Alacrinella morphologically is very similar
to the
genus Astreptonema from amphipods. Astreptonema species
do not
have lobed or inflated bases (see Fig.
11.29),
and the oval resistant spores in some species have two appendages, one
at each
pole. It should be noted that Hibbits [1978, p. 252 and Fig. 22 (d-l)]
found
limited material of a dimorphic fungus, which she called Astreptonema
sp.,
from the isopod Exosphaeroma amplicauda (Stimpson). The
macrothalli
of this unnamed species have a swollen base and produce oval spores
(20-22 x
6-7 mm) with a knob at each
end and
with a long (up to 50 mm)
appendage
attached to one of the knobs. Thus, her isopod eccrinid seems to have
characters of both genera.
Alacrinella
limnoriaeManier & Ormičres
ex Manier, 1968
[= Alacrinella limnoriae Manier & Ormičres, 1961b, nom.
nud.]
Macrothalli 450-600 µm long by 7-12 µm diam distally, basal region 50-75 mm wide consisting of several bulbous swellings and lobes just above a small flat holdfast. Primary infestation sporangiospores thick-walled, oval, 10-15 x 5-7 µm, becoming 4-nucleate. Microthalli up to 250 µm by ~4.5-5 µm diam basally to 2-3 µm diam. distally, distal part cleaving into more or less isodiametric uninucleate cells. Type species.
Illustrations: Fig. 11.65.
Host: In rectum of adult Limnoria tripunctata Menzies (Isopoda, Limnoidae).
Distribution: Marine, boring in old wood, in the Mediterranean Étang de Thau near Sčte, Hérault, France, and Woods Hole, Maine, USA.
Manier and Ormičres found about 80% of the adult gribbles infested. The number of thalli per isopod was not high, but usually both thallus types were present. The cells of the microthalli have no known function. The thick-walled primary infestation spores have 1, 2, or 4 nuclei, but all probably become 4-nucleate at full maturity. The secondary infestation spores may have up to 10 or 12 nuclei.
Reference: Manier, 1968, 1969b (1970b); Manier and Ormičres, 1961b.
Alacrinella sanjuanensis Hibbits, 1978
Macrothalli 750 µm long by 7-19 µm diam, basal region inflated unilaterally and bent at an angle, with a small holdfast at the interior angle of the bend. Primary infestation sporangiospores thick-walled, oval, 4-nucleate, 15-18 x 6-7 µm. Secondary infestation sporangiospores 4-nucleate (or more?), 40 x 10-25 µm. Microthalli 200 mm long by 3-5 µm diam, with a slightly inflated base, cleaving into cells 2 x 5 µm diam.
Illustrations: Fig. 11.120.
Host: In hindgut of Limnoria lignorum (Ratlike) (Isopoda, Limnoidae).
Distribution: Marine, in driftwood, near San Juan Island, Washington, USA.
Hibbits (1978) described the oval primary infestation spores as having a small knob at each end, but cautioned that these observations were made on preserved material and that the knobs could have been fixation artifacts. The macrothalli in some cases initially produced secondary infestation sporangia, and this was followed on the same thallus by production of the more numerous primary infestation spores.
References: Hibbits, 1978; Galt, 1971.
Arundinula
Léger & Duboscq, 1906
Thalli with spore mother-cell persisting apically, attached to foregut (stomach) and usually also to hindgut, of Decapoda (Crustacea). Secondary infestation sporangiospores usually nearly oval, not more than twice as long as broad, occasionally more elongate. Primary infestation sporangia often flat and disklike. Oval or ellipsoidal spores with appendages produced in some species. Seven species.
Type species: Arundinula capitata Léger & Duboscq.
The genus name first used by Léger and Duboscq (1905a, 1905b) was Arundinella, but it was changed to Arundinula in 1906 because the former name had priority as a genus of Gramineae: Arundinella Raddi 1823.
Most species of Arundinula are found in hermit crabs or
other marine
anomurids, the only exception being A. orconectis in
freshwater
crayfish. They inhabit the stomach of the crustaceans (like Enteromyces
callianassae) as well as the hindgut in most species. Sporulation
is
characteristically very prolific, possibly required to ensure
successful
transmission of spores among individuals of these types of hosts.
Arundinula abyssicola Van Dover & Lichtwardt, 1986.
Unbranched thalli usually not exceeding 2 mm in length, 24-27 µm diam, with sporulating tips occasionally up to 40 µm diam. Attached by a centric basal holdfast 10-20 µm long x 18-22 µm diam to the cardiac and pyloric stomach of Munidopsis subsquamosa. Primary infestation sporangia produced in very long series, their single sporangiospores ellipsoidal but flattened in side view, 12-17 µm long x 28-38 µm diam. Mature spores emerge successively through the end wall of the adjacent empty sporangium, becoming almost spherical after release, 22-27 µm diam and 4-8 nucleate. Secondary infestation sporangiospores 17-24 µm long x 22-27 µm diam, 4-8 nucleate. Spore mother-cells persistent and usually becoming fertile.
Illustrations: Fig. 11.117.
Host: Munidopsis subsquamosa (Decapoda, Anomura). Around hydrothermal vents at ~2600 m depth in Galapagos Rift and East Pacific Rise.
Reference: Van Dover and Lichtwardt 1986.
Arundinula
capitata Léger & Duboscq,
1906
[= Arundinella capitata Léger & Duboscq, 1905a, nom.
nud.]
Foregut thalli mostly thick-walled, 1-2(-3) µm long, spore mother-cell persisting at apex until sporulation commences; thalli 23-30 µm diam producing 5-30 4- to 6-nucleate secondary infestation sporangiospores 13-15(-30) µm long; thalli 17-22 µm diam producing series of (30-)70-80(-120) flat, disklike uninucleate primary infestation sporangiospores. Hindgut thalli 1 cm or more long, anterior ones 35-60 mm diam, posterior ones 9-17 µm, producing same kinds of spores as foregut thalli; upon molting of host larger thalli producing (rarely) numerous thickwalled, oval spores ~30 x 14 µm, becoming binucleate and bearing a spinelike appendage 18-25 µm long at each pole. Type species.
Illustrations: Fig. 11.108.
Hosts: In fore- and hindgut of Pagurus maculatus Hell. and Eupagurus cuanensis Thomps. (Decapoda, Paguridae), and possibly other hermit crabs.
Distribution: Marine, intertidal, Departments of Pyrénées-Orientales and Hérault, France.
The above description is based mostly on Manier's 1969(b) description. The original name used by Léger and Duboscq (1905a, 1905b) was Arundinella capitata (see note under generic description). The species was not illustrated until Duboscq, Léger, and Tuzet redescribed it in 1948. The oval resistant spores appear to be rare, for they found them in only 3 out of 150 molting hermit crabs. They considered these resistant spores to arise by a fusion of intrathallial "gametes," but this was not confirmed in Hibbit's (1978) study of similar spores in A. washingtoniensis, nor does such development conform to resistant spore production in other Eccrinales. Manier and Ormičres (1962) listed Pagurus spinimanus Luc as another host of A. capitata.
References: Léger and Duboscq, 1905a, 1905b, 1906; Duboscq et al.,
1948;
Manier, 1950 (1951), 1969b (1970b); Manier and Ormičres, 1962.
Arundinula
galatheae Manier & Ormičres
ex Manier, 1968
[= Arundinula galatheae Manier & Ormičres, 1962, nom.
nud.]
Thalli rigid and thick-walled, up to 3 mm long, 50-83 µm diam near the apex, narrowing to 27-47 µm diam near the base, with a spore mother-cell persisting apically until sporulation. Holdfasts narrow with a flared base, 25-30 µm long. Secondary infestation sporangiospores multinucleate, becoming oval, 45-65 x 30-45 µm. Upon molting of host, thalli completely converting to series of flat, multinucleate sporangia that release from the apex round (27-31 µm diam) or oval thick-walled primary infestation sporangiospores.
Illustrations: Fig. 11.214.
Host: In foregut of Galathea strigosa L. (Decapoda, Galatheidae).
Distribution: Marine, deep water off coast of Sčte, Department of Hérault, France.
Arundinula galatheae has several features that are unusual. The anomurid hosts were collected at depths of 15-25 m. The only other trichomycete collected from such depths is Enteromyces callianassae, but some of its hosts also live in the intertidal zone. The tapered thalli of A. galatheae have exceptionally heavy walls, up to 5-8 mm thick. Manier and Ormičres stated that occasionally some thalli would "molt" by slipping out of the end of the outer wall layer, and reattach to the gut cuticle; the old thallus wall remained in position attached by its original holdfast. The multinucleate thick-walled primary infestation spores of A. galatheae apparently have no appendages, as they do in A. capitata and A. washingtoniensis.
Other species of Arundinula can live in both the foregut and hindgut; at least it appears that the fungi in both locations belong to the same species. The host of A. galatheae, Galathea strigosa, also has an eccrinid that lives in the hindgut, but Manier and Ormičres came to the conclusion that those thalli were not an Arundinula, and assigned them to the genus Taeniella, as T. galatheae, considered here to be a synonym of T. carcini.
References: Manier, 1968; Manier and Ormičres, 1962.
Arundinula hapalogaster Hibbits, 1978
Foregut thalli thick-walled, spore mother-cell more or less persistent, of two types: (1) thalli slightly curved, 3 mm x 16-35 µm, producing 8-nucleate, doliiform secondary infestation sporangiospores 20-35 x 17-35 µm; (2) thalli usually straight, producing thin-walled uninucleate primary infestation sporangiospores 20-35(-43) x 5-7.5 µm; both thallus types may also occur in anterior part of hindgut. Hindgut thalli of four types (anterior to posterior): (1) undulate thalli 6 mm x 12-25 µm, producing 4-nucleate sporangiospores 60-95 x 10-12.5 µm, in exuviae dividing to form uninucleate spores 20 x 10 or 5-7 x 14 µm; (2) coarse thalli 15 mm long by 17-25 µm diam distally, 41-50 µm diam proximally, with holdfasts 40 mm long, producing 1-6 spores 26-70 x 17-30 µm; (4) thick-walled thalli 8 mm long by 55-105 µm diam near the base, tapering to 9 µm diam at the tip, sometimes internally cleaved into cells.
Illustrations: Fig. 11.121.
Host: In foregut and hindgut of Hapalogaster mertensii Brandt (Decapoda, Lithodidae).
Distribution: Marine, lowest tidal zone, rocky outcroppings of San Juan Island, San Juan Archipelago, Washington, USA.
The above description is adapted from Hibbits' (1978) paper, and exemplifies the complexities of growth found in this large anomurid. It also raises the question of spore functions and conspecificity of all thallus types, a matter that cannot be resolved satisfactorily without additional studies using experimental approaches.
References: Hibbits, 1978; Galt, 1971.
Arundinula opeongoensis M.M. White & Strongman, 2008
Thallus unbranched, swollen distally; spore mother cell 32-48.5 x
6.5-10.5 µm with 8 or more nuclei, persistent; cup-shaped, basal
holdfast 19-20 x 11.5-13 µm. Secondary sporangiospores rectangular,
30-17 x 7-7.5 µm, rounded at the ends when released. Primary
sporangiospores vaiable in length, 5.5-11 x 12-12.5 µm, both primary
and secondary sporangiospores produced at the distal end of the thallus.
Illustrations: Fig. 11.335.
Host: Hindgut of freshwater crayfish (Decapoda, Astacidae)
Distribution: Opeongo Lake, Algonquin Provincial Park, Ontario, Canada.
Reference: Strong and White, 2008.Arundinula orconectis Lichtwardt, 1962
Thalli up to 2 cm long by ~20 µm diam, thin-walled, spore mother-cell persistent, sporulating prolifically. Holdfast base slightly wider than thallus. Secondary infestation sporangiospores 8- or more nucleate, ~36 x 20 µm, slightly swollen at the proximal end, produced in series of up to more than 200 per thallus. Primary infestation sporangia variable in length, ~20 µm diam, producing spores that become spherical after release, 24-34 µm diam.
Illustrations: Fig. 11.213.
Host: In foregut and hindgut of Orconectis nais (Faxon) (Decapoda, Astacidae).
Distribution: In freshwater streams, Kansas, USA.
Arundinula orconectis is the only freshwater species of the genus. Although it occurs in a crayfish, rather than an anomurid, it appears to be, nevertheless, an Arundinula. The spherical spores described above were seen lying among thalli, and are only presumed to be matured primary infestation spores of this species.
Reference: Lichtwardt, 1962.
Arundinula washingtoniensis Hibbits, 1978
Foregut thalli thick-walled, spore mother-cell more or less persistent, of three types: (1) thalli 1.8 mm x 22-45 µm, holdfasts becoming variously lateral to the thallus base, producing up to 45 4-nucleate doliiform, secondary infestation sporangiospores 20-35 x 10-20 µm; (2) thalli 4.2 mm x 17-27 µm, holdfasts basal, producing series of more than 230 very flat sporangia 3-6 x 22-27 µm diam, releasing upon molting of the host uninucleate, thin-walled, ellipsoidal primary infestation sporangiospores with a long tapering appendage 120 µm long at each pole; (3) rare thalli 500-650 x 60-120 µm with basal holdfasts and very thick walls, sporulation unknown; thallus types (1) and (2) occasionally occur in anterior part of hindgut. Hindgut thalli thick-walled, of two types: (1) thalli 6.5 mm x 20-45 µm, producing 4-nucleate secondary infestation sporangiospores 40-80 x 14-19 µm; (2) thalli 13.5 mm x 11-30 mm, base with a lateral bulbous thickening in cell wall, producing 4- to 8-nucleate secondary infestation sporangiospores 135-390 x 11-20 µm, or rarely cleaving to produce many spherical uninucleate bodies.
Illustrations: Fig. 11.122.
Host: In foregut and hindgut of Paguristes turgidus (Stimpson) (Decapoda, Paguridae).
Distribution: Marine, subtidal, shores of Waldron Island, San Juan Archipelago, Washington, USA.
Arundinula washingtoniensis occurs in a large hermit crab and, like A. hapalogaster, constitutes one of the morphologically most complex species of trichomycetes, assuming all of the thallus types are conspecific. To complicate matters, Hibbits (1978) occasionally found what she considered to be Taeniella carcini in the rectum of this same species of hermit crab. Despite the careful study done by Hibbits, further investigations are needed to clarify the developmental interrelationships of the thallus and spore types. For instance, she presented only indirect evidence that the appendaged ellipsoidal spores found in molts have their origin in the foregut thalli. The appendaged spores of A. washingtoniensis differ from those of A. capitata in wall thickness and number of nuclei, as well as in other morphological features. In both species they occurred in exuviae, and their origin was not established with certainty. Nevertheless, they are of interest because only a few species of freshwater and marine Eccrinales produce appendaged spores (see Astreptonema and Taeniella). Alsoof interest is the report that some thalli in the hindgut (Type 2) rarely cleave internally to produce sporelike uninucleate cells. This is a feature found in the Parataeniellaceae, and if such cleavage is not artifactual, it could be a transitional character.
References: Hibbits, 1978; Galt, 1971.
Astreptonema
Hauptfleisch, 1895
Thalli dimorphic, spore mother-cell more or less persisting apically. Macrothalli typically curved at the base, which is not noticeably lobed or swollen, producing thick-walled, oval, usually 4-nucleate primary infestation sporangiospores, some with 1 appendage at each pole, or producing multinucleate secondary infestation sporangiospores. Microthalli cleaving into a series of small cells. In hindgut of marine or freshwater Amphipoda (Crustacea). Five species.
Type species: Astreptonema longispora Hauptfleisch.
The generic description above is an extension and reinterpretation of Hauptfleisch's, and is based on studies of subsequent species. See the discussion under the type species, A. longispora.
The spore mother-cell at the apex of thalli is the persistent cell
of the
spore from which the thallus evolved. In Astreptonema it is
usually
narrower than the macrothalli and wider than the microthalli (see Fig.
11. 29).
It disappears in the macrothalli after sporulation has commenced, but
often
remains at the tip of the less common microthalli even after these have
produced small, usually uninucleate, cells of unknown function. The
resistant
oval primary infestation spores have two appendages in A. gammari and
A.
typica. Further studies of the other species, preferably using
living
material, may show that appendages are a feature of all such oval
spores in
this genus. It should be noted that Hibbits (1978) described and
illustrated,
but did not name, an "Astreptonema sp." that she found in the
hindgut of an isopod, Exosphaeroma amplicauda. This fungus had
oval
spores with a knob at each end, and had an appendage projecting from
only one
of the knobs. Her Astreptonema sp. has some characters of the
genus Alacrinella.
Astreptonema
corophii (Manier) Manier ex
Manier, 1968
[= Astreptonema corophii (Manier) Manier, 1964b, nom. nud.]
[= Eccrinella corophii Manier, 1961b, nom. nud.]
Macrothalli up to 700 µm long by 7-12 µm diam near the curved base and 5-10 µm diam distally, spore mother-cell persisting. Primary infestation sporangiospores oval, 4-nucleate, 10-15 x 5-7 µm. Secondary infestation sporangiospores 1-8 per thallus, multinucleate, 14-30 µm long. Microthalli up to 200 µm long by 1.5-2.2 µm diam.
Illustrations: Fig. 11.124.
Host: In hindgut of Corophium volutator (Pall.) (Amphipoda, Corophiidae).
Distribution: Marine, littoral muddy sand, Department of Finistčre, France, and in Nova Scotia, Canada.
No appendages have been reported on the oval spores, possibly because they were not sought in living material (Manier, 1964b).
References: Manier, 1961b, 1964b, 1968.
Astreptonema
gammari (Léger & Duboscq)
Manier, 1964b
= Eccrinella gammari Léger & Duboscq, 1933
Macrothalli 1-2 mm long by 8-18 µm diam, curved at the base, spore mother-cell persisting. Primary infestation sporangiospores 4-nucleate, oval, thick-walled, bearing I long appendage at each pole, of two types: (1) more common, 25-30 x 7-10 µm , lying obliquely in series of up to 40-50 per thallus; (2) more rare, ~54-55 x 10 µm, lying longitudinally in series of 8-14 per thallus. Secondary infestation sporangiospores 2- to 8-nucleate, cylindrical with rounded ends, 25-50 x 8-10 µm. Microthalli uncommon, ~300 µm long by 2 µm diam, dividing into many small uninucleate cells.
Illustrations: Fig. 11.30.
Hosts: In hindgut of Gammarus pulex (L.), G. roeseld Gervais, and Echinogammarus berilloni (Catta) (Amphipoda, Gammaridae), and possibly other freshwater Gammaridae.
Distribution: Freshwater streams in the Dauphiné (French Alps) and Rhône valley, and Departments of Calvados and Hérault, France; in East Germany; in England; in USA (Minnesota).
The name of the basionym, Eccrinella gammari, was first used by Léger and Duboscq in 1906, but the species was not described by them until 1933. Poisson (1929) had also found this species, in southeastern France, but did not describe it. In 1964(b) Manier transferred all current species of Eccrinella to Astreptonema. The diagnosis above is based on these sources and some collections made by Lichtwardt in France and England, and including what may be this species in the USA. The amphipod host, G. roeseld, was recorded by Maessen (1955) in Germany. Scheer (1976a) made A. gammari a synonym of A. longispora, the type species, but there appears to be no justification for doing this on the basis of the oval spore measurements of A. longispora.
The peculiar, very long polar appendages of this species were apparently not observed until Manier described them in 1964(b). They are best seen in phase contrast after release from living thalli. Prior to this, the appendages are tightly folded within each end of the sporangium. Moss (1979) refers to them as mucilaginous, but in the authors' experience they appear to be ribbon-like and nonmucilaginous. Groups of spores released more or less simultaneously from a thallus may remain clumped by appendage entanglement. In the natural aquatic environment they perhaps function like the appendages of trichospores in the Harpellales. Whether the appendages of the two orders are at all homologous and have any similarities in their development have not been satisfactorily determined, and this knowledge would be of considerable interest in helping to understand the interrelationships of the two orders (Lichtwardt, 1973a). Moss (1972, 1975) has done an electron microscopic study of A. gammari, including the structure of the appendaged spores within their sporangia and the perforate septum of the sporangial crosswalls (see Chapter 7), and Grizel (1971) has also studied several aspects of the fine structure of this species. The present evidence is that the appendages of the Eccrinales form in a manner dissimilar to trichospore appendages.
References: Léger and Duboscq, 1906, 1933; Poisson, 1929; Manier,
1950
(1951), 1964b; Maessen, 1955; Moss, 1972, 1975, 1979; Grizel, 1971;
Lichtwardt,
1973a; Scheer, 1976a; Moss, 1998, 1999.
Astreptonema longispora Hauptfleisch, 1895
Thalli curved at the base, producing series of oval multinucleate (up to 8 nuclei) primary infestation sporangiospores 7-10 x 2-2.6 µm. Type species.
Illustrations: Fig. 11.206.
Host: In the posterior hindgut of Gammarus pulex (L.) (Amphipoda, Gammaridae). (See remarks below.)
Distribution: Freshwater habitats, Germany (Thüringen).
The diagnosis provided by Hauptfleisch (1895) was extremely brief, and was based upon limited fungal material. Nevertheless, it appears to correspond to other, more thoroughly studied related species that are now placed in this genus and which enable us to define better the generic characters. There were no appendages reported on the oval spores of this species [they were unknown until Manier (1964b) described them in the genus]. Hauptfleisch considered his fungus to belong to the Saprolegniaceae (Oomycetes), and believed the sporangia to be oogonia bearing single, multinucleate oospores. He apparently was not aware of the eccrinid literature of that time. Leidy (1920) was the first to recognize the similarity of Astreptonema and Enterobryus.
Hauptfleisch stated that the host of A. longispora was Gammarus locusta (L.). This is a seashore (marine) amphipod. Scheer (1976a) questioned the identification of the amphipod, and presented evidence that the locality where Hauptfleisch collected his specimens (Ichtershausen) is located some 350 km from any coastal areas, and that the misidentified host must have been the freshwater species, Gammarus pulex. We accept this identification. Gammarus pulex is also one of the hosts of Astreptonema gammari, and Scheer synonymized the two species. We, however, do not find the argument at all convincing. Astreptonema longispora was stated by Hauptfleisch to have oval spores measuring 7-10 x 2-2.6 mm, whereas the smaller of the two types of oval spores of A. gammari are considerably larger than that [25-30(-55) x 7-10 mm]. Scheer's argument is that the size of spores can vary with the diet of the host (an unsubstantiated statement), and that the ratio of length to width is more important than the actual dimensions. This would not conform to the general concepts of species identification in other trichomycetes. Nevertheless, that Hauptfleisch may have incorrectly measured the spore sizes cannot be definitively discounted.
Manier (1969, Figs. 8-11) provided photographs of an "Astreptonema sp. from Gammarus locusta", andaccording to the size scales in her Figs. 9 and 11, the (appendaged) oval spores are approximately 24 x 8 mm and 18 x 5.5 mm, respectively. Further studies of the fungi in these amphipods from their type localities are clearly needed.
References: Hauptfleisch, 1895; Scheer, 1976a.
Astreptonema pacificum Hibbits, 1978
Macrothalli up to 750 µm long by 17-38 µm diam near the curved base and 10-15 µm diam distally, attached to the cuticle by a long (15-45 µm) striated holdfast. Producing oval, thick-walled, uninucleate primary infestation sporangiospores 22-35 x 10-13 µm, or 4-nucleate secondary infestation sporangiospores 22-43 x 10-18 µm. Microthalli 60 x 5 µm, dividing into cells ~1 µm long.
Illustrations: Fig. 11.123.
Host: In hindgut of Orchestia traskiana Stimpson (Amphipoda, Talitridae).
Distribution: Marine, uppermost intertidal zone of sandy shores, San Juan Archipelago, Washington, USA, and British Columbia, Canada.
The amphipod host is commonly called a beach hopper or sandflea, and was found around decaying seaweed. No appendages were seen on the oval spores, and they were uninucleate (possibly immaturem).
References: Hibbits, 1978; Galt, 1971.
Astreptonema
typica Manier ex Manier, 1968
[= Astreptonema typica Manier, 1964b, nom. nud.]
Macrothalli up to 350 µm long, curved at the base, 10-13 µm diam. Primary infestation sporangiospores oval, thick-walled, 4-nucleate, 17-20 x 7-9 µm, with one long appendage at each pole. Secondary infestation sporangiospores 4-nucleate 15-25 long. Microthalli 100-150 x 2-2.5 µm, producing a terminal series of isodiametric cells.
Illustrations: Fig. 11.215.
Host: In hindgut of Gammarus duebeni Lilljeborg (Amphipoda, Gammaridae).
Distribution: Aquatic, in fresh and brackish water, Department of Hérault, France.
References: Manier, 1964b, 1968; Grizel, 1971.
Eccrinidus
Manier, 1970a (1969a)
Primary infestation sporangiospores cystlike, bilocular (rarely unilocular), each chamber producing and releasing a 4-nucleate cell. Attached to hindgut cuticle of Diplopoda. Monotypic.
Type species: Eccrinidus flexilis (Léger & Duboscq)
Manier.
Eccrinidus
flexilis (Léger & Duboscq)
Manier, 1970a (1969a)
= Eccrina flexilis Léger & Duboscq, 1906
Thalli up to 3 or 4 mm long by 5-30 µm diam, generally spiraled near the base. Holdfast columnar with a disklike basal expansion. Upon molting of the host producing oval cystlike primary infestation sporangiospores of two types: (1) bilocular, each chamber with a 4-nucleate cell 50-65 x 11-12 µm, or (2) unilocular, containing one 4-nucleate cell 25-50 x 5-12 µm. Secondary infestation sporangia variable in length and with perpendicular to oblique end walls. Type species.
Illustrations: Fig. 11.31.
Hosts: In hindgut of Glomeris marginata Villers, G. annulata Brandt, G. connexa Koch, G. conspersa Koch, and G. hexasticha Brandt (Diplopoda, Glomeridae).
Distribution: Terrestrial, widespread in France.
Eccrinidus flexilis is a variable yet distinct species known only in glomerid millipedes. Its morphology is basically similar to that of many Enterobryus spp., but E. flexilis is distinguished by the production of cystlike primary infestation spores when the host molts. The two-chambered ones are more common than those with one chamber, and they may be found in large numbers in the exuviae. The secondary infestation spores are short to long (up to 100 mm), but more or less consistent in length in any given thallus. The crosswalls that delimit the sporangia are sometimes very oblique. Other cell types of uncertain function have also been described in this species, including uninucleate and binucleate ones. Manier (1969b, p. 581) states that E. flexilis may also attach to the cuticle of intestinal nematodes, as do several species of Enterobryus. Manier and Grizel (1972) studied the fine structure of the holdfast in E. flexilis (see Table 7.3).
Duboscq et at. (1948) and Manier (1950) wrote extensively on E. flexilis, yet many of their observations on the variable spore forms need confirmation. Manier (1954) attempted to culture this species, but was able to get only limited stages of development in vitro. Duboscq et al. reported seeing some unusual developmental stages within the oval resistant spores involving nuclear divisions, aborting nuclei, plasmogamy, and karyogamy, suggesting a curious form of sexuality not found in other trichomycetes, or in other fungi for that matter. Manier (personal communication) has not confirmed such development, although she earlier (Manier, 1954, p. 268) claimed to have seen nuclear fusions. Nor has Lichtwardt seen such stages in his study of limited material collected near Montpellier, France. The diagnosis for the species provided above is adapted from Manier (1969b).
References: Manier, 1950 (1951), 1954, 1969a (1970a), 1969b (1970b); Léger and Duboscq, 1906, 1929a; Duboscq et al., 1948; Manier and Grizel, 1972; Lichtwardt, 1973a.
Eccrinoides
Léger & Duboscq, 1929a
Primary infestation sporangiospores oval, 4-nucleate, thick-walled, usually with a channel penetrating the endwalls at each pole. Attached to hindgut cuticle of Diplopoda and Isopoda. Four species.
Type species: Eccrinoides henneguyi Léger & Duboscq.
Eccrinoides broelemanni Léger & Duboscq, 1929a
Thalli up to 5 mm long by 11 µm diam, with 3-4 spirals at the base. Secondary infestation sporangiospores 4-nucleate, up to more than 100 µm long. Primary infestation sporangiospores of variable length. Thick-walled resistant spores more or less allantoid, ~30 µm long.
Illustrations: Fig. 11.207.
Host: In hindgut of Protoglomeris vasconica Bröl. (Diplopoda, Glomeridae).
Distribution: Terrestrial, in Pyrenees mountains, France.
The name of this species, but with a minimal description, was established by Léger and Duboscq (1929a) in the same paper describing the type species of the genus, E. henneguyi. The description of E. broelemanni was amplified by Duboscq et al. in 1948.
References: Léger and Duboscq, 1929a; Duboscq et al., 1948.
Eccrinoides
helleriae Manier ex
Lichtwardt, 1984c
[ = Eccrinoides helleriae (Léger & Duboscq) Manier, 1969, nom.
nud.]
[= Eccrinopsis helleriae Léger & Duboscq, 1906, nom.
nud.]
Thalli up to 4 mm long by 7-18 µm diam. Primary infestation sporangiospores uninucleate, variable in length. Secondary infestation sporangiospores 4-nucleate, 40-150 µm long. Upon molting of the host producing thick-walled, oval, 4-nucleate spores 47-50 x 12-18 µm or 36-40 x 12-13 µm.
Illustrations: Fig. 11.217.
Host: In hindgut of Helleria brevicornis Ebner (Isopoda, Tylidae).
Distribution: Terrestrial, oak forests, Mediterranean coast, and islands east of the Rhône delta, France.
Manier made a new combination for this species in 1969(b), but it was not valid because the basionym, Eccrinopsis helleriae, is a nomen nudum. The name Eccrinopsis helleriae was used by Léger and Duboscq in 1906 and 1916, but in neither publication was the fungus described. The first description appeared in Duboscq, Léger, and Tuzet's 1948 publication, at which time Art. 36 would apply, but no Latin diagnosis was provided. Furthermore, the type species of Eccrinopsis, E. hydrophilorum, has been transferred to the genus Enterobryus. The name Eccrinoides helleriae was validated by Lichtwardt (1984c).
Eccrinoides helleriae is said by Duboscq et al. (1948) to produce rarely a smaller, 2-nucleate type of resistant spore, which is somewhat allantoid and measures 18 x 8 mm. This species has developmental stages in the two larger resistant spores that need reinvestigation.
References: Lichtwardt, 1984b; Manier, 1963a, 1969b (1970b); Léger
and
Duboscq, 1906, 1916; Duboscq et al., 1948.
Eccrinoides henneguyi Léger & Duboscq, 1929a
Thalli up to 7 mm long by 10-13 µm diam, not spiraled. Secondary infestation sporangia with oblique endwalls, producing 4-nucleate sporangiospores ~75 µm long. Uninucleate primary infestation spores produced in repeating long series of sporangia alternating with nonsporulating coenocytic segments of the thallus. Upon molting of the host producing oval, 4-nucleate, thick-walled spores 30-34 µm long with a channel at each pole. Type species.
Illustrations: Fig. 11.66.
Hosts: In hindgut of Loboglomeris rugifera Verh. and L. pyrenaica Bröl. (Diplopoda, Glomeridae).
Distribution: Terrestrial, in Pyrenees mountains, France.
This species is similar in some respects to Eccrinidus flexilis, which also lives in glomerid millipedes, but the oval resistant spores of E. flexilis are usually bilocular and do not have the polar channels in the walls that distinguish the genus Eccrinoides.
References: Léger and Duboscq, 1929a; Manier, 1969b (1970b).
Eccrinoides
monticolae (Poisson) Manier,
1970b (1969b)
= Eccrinopsis monticolae Poisson, 1931a
Thalli up to 525 µm long by 11-14 µm diam, with a small holdfast. Primary infestation sporangiospores uninucleate, 30 x 10-12 µm. Secondary infestation sporangiospores up to 8-nucleate, 50-60 x 8-9 µm. Upon molting of the host producing thick-walled, oval, 4-nucleate spores 24-28 x 6-7 µm with a channel penetrating each pole.
Illustrations: Fig. 11.218.
Host: In hindgut of Porcellio monticola Lereboullet (Isopoda, Porcellionidae).
Distribution: Terrestrial, in Pyrenees mountains, France.
References: Manier, 1969b (1970b); Poisson, 1931a.
Enterobryus
Leidy, 1849a
Primary infestation sporangiospores uninucleate and thin walled, generally isodiametric, sometimes lacking. Secondary infestation spores cylindrical, usually 4- to 8-nucleate. Other cell types sometimes produced. Attached by a well-defined secreted holdfast to the hindgut cuticle of Diplopoda, less often Insecta (Coleoptera) or Crustacea (Decapoda). Twenty four species.
Type species: Enterobryus elegans Leidy.
Enterobryus (as Enterobrus) was the first genus of trichomycetes described. It is also the largest genus and, without question, the most difficult and taxonomically perplexing of all trichomycete genera. The basic difficulties lie in incomplete-sometimes misleading or erroneous-descriptions and the considerable morphological variation that exists in some of the species. In addition, a few species produce supplemental cell types whose function, if any, remains unknown. No species of Enterobryus has been cultured axenically in order to compare morphology under similar environments, nor have host specificity determinations been made. These problems have been outlined briefly in Chapter 10, with selected examples. Also see the note under Enterobryus isoporostrepti, and the description of E. tuzetae.
More than 20 species of Enterobryus have been illegitimately described, and are not included in this section. Other species have been effectively and validly published, but they are incompletely described and have not been accepted by the writer. All excluded taxa are listed at the end of this chapter.
Leidy himself did not describe the reproductive features of the type
species, E. elegans, but the species was restudied by
Lichtwardt
(1954b), and thus we have a reasonably good basis upon which to
determine the
characters of both the species and the genus. Nevertheless, the generic
characters are not as exclusive and clearly defined as would be
desirable,
certainly less so than many other genera of Eccrinales. The minimal
number of
diagnostic characters used for Enterobryus possibly has led to
the
inclusion in the genus of some unrelated species by virtue of their
exclusion
from other genera of Eccrinales.
Enterobryus adjanohouni Manier, Gasc & Bouix, 1975 (1974)
Thalli up to 4.5 mm long by, 8-16 µm diam, slightly swollen (10-20 µm diam) near the base, which may be recurved, often spiraled or sinuous. Holdfast flat or isodiametric, usually located laterally near the base. Producing 1-4 terminal sporangia 250-480 x 8-12 µm, within each a partially folded secondary infestation sporangiospore 260-520 µm by ~10 µm diam with a tapered, evenly thickened apical cap. Sporangia may collapse in a pleated fashion after spore release. Some thalli producing 1-3(-6) often clavate multinucleate terminal cells 65-290 x 9-18 µm that are packed with nuclei.
Illustrations: Fig. 11.239.
Host: In very anterior part of hindgut of Plethocrossus acutiformis Demange (Diplopoda, Odontopygidae).
Distribution: Terrestrial habitats, Dahomey, Africa.
According to the authors, the multinucleate cells may internally produce uninucleate cells measuring 10-15 mm diam.
See the note under Enterobryus isoporostrepti concerning the problem of identity of this and other species from Dahomey.
Reference: Manier et al., 1974 (1975).
Enterobryus ahlesi Lichtwardt, 1960
Thalli straight or curved near the base, 1 cm or more long by (7-)12-24 µm diam, tip bluntly pointed. Holdfast 6-60 µm long, longitudinally striated, usually without a basal disk. Secondary infestation sporangiospores 43-70 x 7-10 µm, or ~160 x 11-14 µm, with bulbous proximal ends. Primary infestation spores rare or absent.
Illustrations: Fig. 11.227.
Host: Throughout hindgut of Apheloria montana (Bollman) (Diplopoda, Xystodesmidae).
Distribution: Terrestrial habitats, Tennessee, USA.
Lichtwardt reported also finding in this host species two other larger spore types: one was fusiform; the other cylindrical, vacuolate, and with about 8 peripheral nuclei.
Reference: Lichtwardt, 1960.
Enterobryus apheloriae Lichtwardt, 1954b
Thalli up to 10 mm (or slightly more) long by 7-12 µm diam, long-fusiform, tip bluntly pointed, and the base tapering gradually to the holdfast. Holdfast long (often ~60 µm) with a basal disk or enlargement. Secondary infestation sporangiospores (68-)70-100(-265) x 7-12 µm with a bulbous basal end.
Illustrations: Fig. 11.32; Fig. 11.231.
Host: In hindgut of Apheloria iowa Chamberlin (Diplopoda, Xystodesmidae).
Distribution: Terrestrial habitats in Illinois, USA.
Lichtwardt (1954b) also reported that this fungus produces cells, packed with nuclei, that measure ~60 x 11 mm. He erroneously thought that some thalli with chains of binucleate cells that he described from the hindgut of this millipede were an unusual reproductive stage of E. apheloriae. However, it was undoubtedly an organism related to the non-trichomycete genus Mononema; see the last section of Chapter 12.
References: Lichtwardt, 1954a, 1954b.
Enterobryus bifurcatus Whisler, 1963
Thallus bifurcate, consisting of two divergent arms with a median lateral holdfast, often 1.2(-2.1) turn in overall length by 10(-14) µm diam. Primary infestation sporangiospores uninucleate, ~10 x 10 µm. Secondary infestation sporangiospores 4-nucleate, (43-)49(-56) x (7-)9 µm.
Illustrations: Fig. 11.235.
Host: In posterior hindgut of Californiobolus uncigerus Wood (Diplopoda, Spirobolidae).
Distribution: In decaying logs, California, USA.
This unusual thallus type develops due to the simultaneous growth of a lateral extension at the base of the thallus, while the more normal arm grows directly from the germinating spore. The terminal portions of both arms produce series of either primary or secondary infestation sporangiospores (Whisler, 1961), although the former are more common. In other respects, E. bifurcatus is a typical Enterobryus. Refer also to Enterobryus tuzetae, which produces a bifurcated thallus type, and to Ramacrinella raibauti, a member of the Eccrinaceae from amphipods, with multiple branching from the base of the thallus.
The anterior part of the hindgut of the same millipede species also contained another, unnamed Enterobryus sp., described by Whisler (1963) as having a large basal holdfast and averaging 7.2 mm in length by 21 mm diam, with multinucleate terminal cells measuring 91 x 21 mm. He considered such thalli likely to represent a different species.
References: Whisler, 1961, 1963.
Enterobryus borariae Lichtwardt, 1958
Thalli up to 5 mm long, (3.5-)8-18(-50) µm diam. Holdfasts up to 100 mm long, holdfast stalk usually 10-12 µm diam. with a prominent basal disk or swelling, longer stalks longitudinally striated. Primary infestation sporangiospores 9-16 µm long x 9-18 µm diam. Secondary infestation sporangiospores 45-170 x 8-32 µm, with a basal bulbous swelling. May produce other spore or cell types of unknown function or origin.
Illustrations: Fig. 7.11; Fig. 7.12; Fig. 11.234.
Host: In hindgut of Boraria carolina (Chamberlin) (Diplopoda, Xystodesmidae). Also attached to cuticle of oxyuroid nematodes in the hindgut, or to thalli of its own species.
Distribution: In leaf litter and under soil in North Carolina, USA.
Enterobryus borariae is one of the most variable species of the genus, which makes it difficult to delineate the characters of the species (Lichtwardt, 1978a). Although known only from one millipede species, it attaches not only to the hindgut cuticle, but to the cuticle of parasitic nematodes as well. In addition, Lichtwardt (1958) illustrated spores, germinating spores, and even sporulating thalli of E. borariae attached to other thalli and sporangia of its own species.
In a few instances thalli have been seen producing a series of terminal secondary infestation sporangiospores, followed by a series of primary infestation sporangiospores on the same thallus, or vice versa, suggesting that the type of sporangium produced on a given thallus is not due to some innate dimorphism factor. Combinations of both sporangial types have also been seen in single thalli of E. dixidesmi.
Enterobryus borariae produces several other kinds of cells or spores, some which have no known function or origin. One of unknown function is the type tightly packed with nuclei, which has been seen in a few other species of Enterobryus as well. Also, peculiar cystlike pyriform bodies have been found beneath the hindgut lining of some millipedes (Fig. 7.11 B). These were found in various stages of germination and penetration through the cuticle into the gut lumen, some having produced thalli with spores at their tips, indicating they were thalli of E. borariae. In the anterior region of some millipede hindguts were seen very narrow thalli producing overlapping bundles of sinuous, filiform sporangiospores, each in its own sporangium; these were intermixed with narrow thalli of E. borariae producing normal sporangiospores, and possibly were a stage of the same species. Finally, oval spores producing thalli as they germinated were observed in a few instances, but they were not associated with any stages of E. borariae producing such oval spores.
References: Lichtwardt, 1954a, 1958, 1978a.
Enterobryus centroboli Gorter, 1993
The fungus develops unbranched thalli which are attached to the anterior part of the hindgut, just below but occasionally also just inside the sphincter muscle. Hyphae also develop towards the posterior end of the hindgut. In both cases, the hyphae are fairly straight to undulating, 7.5-12.5(-15) µm wide, those at the front are up to 3800 mm long and those at the back up to 3000 mm. Most hyphae are hyaline but some of those in front tend to become wider towards the hyphal apex. The narrower hyaline hyphae produce at their apex short or longer type A sporangiospores. The short ones (15.0 x 7.5 µm) are uninucleate and the longer ones (40-60 x 7.5 µm) are quadrinucleate. The wider, more opaque hyphae produce 3-4 apical or sometimes intercalary spores, 90-125 x 10-20 µm, which appear to be multinucleate and of type E (see Fig. 11.230).
Illustrations: Fig. 11.164.
Host: Centroboli lawrencei (Diplopoda).
Distribution: South Africa.
Reference: Gorter, 1993.
Enterobryus chaleponci Gorter, 1993
The thalli are inside the sphincter muscle. The hyphae are hyaline, fairly straight but strongly hooped lower down, 2500 x (10-)12.5-15.0(-17.5) µm. The hoops are often wider than the straight parts of the hyphae, 15-20 µm. The latter are of variable width, widening by 2 mm and then narrowing again. A holdfast without a stalk or with a very short one, e.g. 2.5 µm, develops at the base of a hypha. The disc diameter varies from (12.5-)15-20 µm. The thicker hyphae and those that widen from bottom to top, have a dense granular cytoplasm and often become slightly brown Folded spores have been observed in the hooped as well as the straight part of hyphae. In the first, sporangia are 70-85 x 15 µm; in the latter, 105-150 x 12.5 µm. The spores are 125-230 x 10.0-12.5 µm and have a truncated basal end with a slight depression in the centre. After escaping from the sporangia, the folded spores straighten, germinate basal and soon attach themselves to the inside of the sphincter muscle. At the apex of a hypha with dense cytoplasm, a long cylindrical sporangium (up to 125 µm) is often formed. These sporangia are slightly swollen in comparison with the rest of the hyphae and each contains a multinucleate.
Illustrations: Fig. 11.166.
Host: Chaleponci polechanci (Diplopoda).
Distribution: South Africa.
Reference: Gorter, 1993
Enterobryus cherokiae Lichtwardt, 1960
Thalli straight or loosely spiraled, often 5-7 mm long by (8-)11-20(-26) µm diam. Mature holdfasts usually expanded into a broad disk up to 45 µm diam, without a holdfast stalk. Secondary infestation sporangiospores often with more than 8 nuclei, generally falling into one of three size ranges: (1) 100-240 x 8 µm; (2) 60-70 x 10-15 µm, with a distal bulbous end; and (3) 140-240 x 19-26 µm.
Illustrations: Fig. 11.229.
Host: In hindgut of Cherokia georgiana (Bollman) (Diplopoda, Xystodesmidae).
Distribution: In leaf litter, North Carolina, USA
In addition to primary infestation sporangiospores, E. cherokiae produces series of terminal cells tightly packed with nuclei, as found in some other species of Enterobryus. Those of E. cherokiae are usually large, measuring 60-83 x 15-30 mm.
References: Lichtwardt, 1954a, 1960.
Enterobryus cingaloboli Rajagopalan, 1967
Thalli up to 5 mm long, coiled or curved near the basal region, 15-22 µm diam. near the base, gradually narrowing to 8-14 µm distally. Holdfast up to 30 µm long, with a prominent basal disc up to 20 µm diam. Secondary infestation sporangiospores 4-nucleate, 60-100 x 6-8 mm, borne on slender thalli. Wider thalli bearing 1-10 multinucleate cells 50-120 x 15-21 µm. Primary infestation spores rare or absent.
Illustrations: Fig. 11.244.
Host: In hindgut of Cingalobolus carli Attems (Diplopoda, Pachybolidae).
Distribution: In plant debris, Kerala State, India.
Reference: Rajagopalan, 1967.
Enterobryus
cylindroiuli Manier, 1969
[= Enterobryus cylindroiuli Tuzet & Manier, 1949, nom
nud.]
[= Enterobryus cylindroiuli Tuzet & Manier in Manier,
1950
(1951), nom. nud.]
Thalli essentially straight, 600-800(-1200) µm long by 4-9.5 µm diam. Holdfasts 5-6 µm long, narrowing at the top. Narrower thalli (4-6 µm) producing 4-nucleate secondary infestation sporangiospores 40-60 x 4-6 µm. Wider thalli (7-9.5 µm) producing 2-20 uninucleate cells which are either (1) swollen and isodiametric (7 x 7 µm) or elongated (17-20 x 7-9 µm), or (2) cylindrical, elongated, and vacuolate (24 x 7 µm).
Illustrations: None available.
Host: In hindgut of Cylindroiulus londinensis Leach (Diplopoda, Julidae).
Distribution: Terrestrial habitats, Department of Hérault, France.
The name of this species was first used and designated as a new species by Tuzet and Manier in 1949, but no description was provided. The first description (without calling it a new species or validating the name) appeared in Manier's 1950 published dissertation. In 1969, Manier validly published the species name (but as though she were validating her 1950 species), and provided a concise description upon which this diagnosis is primarily based. There is no indication that either of the uninucleate cell types that Manier described function as sporangia for primary infestation sporangiospores; they may be merely cells of unknown function similar to others that are not uncommon in Enterobryus spp.
References: Manier, 1950 (1951), 1969; Tuzet and Manier, 1949.
Enterobryus dixidesmi Lichtwardt, 1960c
Thalli tightly coiled throughout their length, or curved predominantly near the base, up to 1.5 mm long (usually much shorter) by (5-)9-13(-17) µm diam. Holdfast stalk usually very short, with or without a basal disk. Secondary infestation sporangiospores 40-90 x 9-11 µm Primary infestation sporangiospores 8-11 x 9-13 µm.
Illustrations: Fig. 11.228.
Host: In hindgut of Dixidesmus tallulanus Chamberlin (Diplopoda, Polydesmidae).
Distribution: In leaf litter, North Carolina, USA.
The spiraled thalli of E. dixidesmi resemble those of E. moniliformis, but the two species differ in the sizes of their spores and holdfasts. Spiraling is most prevalent in well-infested guts. It should be noted that thalli in this species, and other spiraled species, can become straighter during dissection and preparation of slides. Sporangia producing primary infestation spores were found in series of up to 42 per thallus. Like E. borariae, single thalli of E. dixidesmi may occasionally produce in sequence both secondary and primary infestation sporangiospores. Small ellipsoid spores of unknown origin also were observed germinating in the gut of this millipede host, similar to those seen in some millipedes harboring E. borariae.
Reference: Lichtwardt, 1954a, 1960c.
Enterobryus elegans Leidy, 1849a, emend. Lichtwardt, 1954b
Thallus usually having a single loose coil near the base, up to 5 mm long, 19-23 µm diam, tapering to ~12 mm diam near the apex. Young thalli often apically clavate. Holdfast irregularly conical or campanulate, sometimes cylindrical above the flared base, usually large and prominent when fully formed but variable in size, commonly 30-85 µm long by 35-50 µm diam at the base. Secondary infestation sporangiospores typically 50-65 µm long by ~12 µm diam, and 8-nucleate. Primary infestation sporangiospores absent or rare. Some thalli producing slightly swollen terminal cells with numerous scattered nuclei, 50-100 x 15-22 µm. Type species.
Illustrations: Fig. 7.13; Fig. 11.32; Fig. 11.34.
Hosts: Narceus americanus (Beauvois), N. annularis (Rafinesque), and probably many other Narceus (Spirobolus)spp. (Diplopoda, Spirobolidae). Often attached to the cuticle of oxyuroid nematodes within the millipede hindgut.
Distribution: In and around decomposing leaves and logs in eastern North America, at least as far west as Kansas, USA.
Enterobryus elegans was the first species of trichomycetes to be described. The genus name was first spelled Enterobrus, but Leidy corrected the orthography in 1850(b). The fungus is present in many, if not most, species of Narceus in eastern USA. Lichtwardt has found it in millipedes in Kansas, Illinois, Michigan, New York, North Carolina, and Georgia. Leidy collected his material in Pennsylvania. Wright (1979) studied E. elegans in N. annularis from Ontario, Canada. The nomenclature of the original host species, N. americanus, has been in a state of flux, and its precise distribution remains uncertain. Leidy (1849a) called it Julus marginatus Say, whereas Hoffman (1951) established the name Spirobolus americanus (Beauvois). Dogma (1975) reported E. elegans from an unidentified millipede species in the Philippines, but provided no assurance that his identification was correct.
Leidy's descriptions of E. elegans (1849a, 1853) were very incomplete, but it was restudied by Lichtwardt (1951, 1954a, 1954b, and unpublished). This species does not appear to produce primary infestation sporangiospores, which leads to the interesting question of how it is transmitted so successfully from one millipede to another, since most spirobolid millipedes are infested. One possibility is that the secondary infestation sporangiospores, which normally serve to multiply the fungus endogenously, are the propagules that transmit the fungus to other individuals, and perhaps also can reinfest molting millipedes that eat part of their molt. The large multinucleate cells produced by some thalli could conceivably serve this function, but this has not been established. The multinucleate cells may break loose, according to Leidy (1853). Surprisingly, Leidy never found sporangiospores despite doing a large number of dissections over many seasons (Leidy, 1853). The slightly swollen multinucleate cells (which appear to be what Leidy described and illustrated) do not produce sporangiospores, and can be distinguished by their numerous nuclei scattered in the cytoplasm. In contrast, the sporangia are generally narrower and cylindrical, and, as they develop, a distinct wall is laid down by the sporangiospore, and the usual 8 nuclei at maturity are lined up more or less in a row.
The attachment of E. elegans to parasitic nematodes living in the hindgut is not unique to this species of Enterobryus, and has been observed by several persons (see Table 7.2). Lichtwardt (1954b) reported that, just before molting, a modified spore type that attached to nematodes was produced in some thalli, and that this attachment could be one means by which the fungus remained in the gut during ecdysis when other thalli attached to the hindgut cuticle were being expelled.
The holdfast of E. elegans has been studied with the electron microscope by several investigators (Dang, 1978; Wright, 1979; Mayfield and Lichtwardt, 1980), and its interesting ultrastructural features are discussed in Chapter 7 in the section on Holdfasts.
References: Leidy, 1849a, 1853; Lichtwardt, 1951, 1954a, 1954b;
Dogma, 1975;
Dang, 1978; Wright, 1979; Mayfield and Lichtwardt, 1980.
Enterobryus euryuri Lichtwardt, 1954b
Thalli with tips frequently curved, up to 4 mm long by (6-)10-13(-30) µm (rarely up to 90 µm) diam. Holdfasts unevenly cylindrical, (4-)15-25(-75) x (4-)6-8(-12) µm, with or without a basal disk. Secondary infestation sporangiospores (32-)50-100 x (6-)10-13(-16) µm, with a basal bulbous swelling. Primary infestation sporangiospores 5-15 x 10-13 µm diam.
Illustrations: Fig. 7.8; Fig. 7.20; Fig. 11.32; Fig. 11.230.
Host: In hindgut of Euryurus erythropygus (Brandt)
(Diplopoda,
Platyrhacidae). Apheloria
sp., Narceus sp.
Distribution: In rotting logs and leaf litter, Illinois, USA.
Ontario, Canada.
Enterobryus euryuri also produces two cell types of unknown function. One consists of series of swollen uninucleate cells often 11 mm long by 22 mm diam borne apically on wide thalli 23-30(-90) mm diam. The other cell type is filled with tightly packed nuclei, and measures ~35-60 x 11 mm diam. Although nematodes are often abundant in this millipede species, the fungus apparently is unable to attach to their cuticle, as do a few other species of Enterobryus.
References: Lichtwardt, 1954a, 1954b; Strongman and White, 2008.
Enterobryus halophilus Cronin & Johnson, 1958
Thalli sinuous and curved, 200-4500 µm long, 10-15 µm diam, usually with a wider basal part up to 25 µm diam, often with an apical cap. Holdfast 9-18 µm long, shaped like an inverted cup. Secondary infestation sporangiospores 35-58 x 8-14 µm. Primary infestation sporangiospores 8-14 x 11-17 µm diam.
Illustrations: Fig. 11.237.
Hosts: Attached to hindgut cuticle (sometimes on anal hairs and consequently exposed) of Emerita talpoida Say and E. analoga (Stimpson) (Crustacea, Decapoda, Hippidae), commonly called mole crabs.
Distribution: Wave-washed sandy beaches of intertidal zone, North Carolina and California, USA.
In addition to the two spore types cited above, Cronin and Johnson (1958) reported finding uninucleate endospores developing in short distal segments of some thalli. Such spore types have been occasionally reported by Manier and co-workers in a few species of Enterobryus, but in the writers' judgment these may be artifacts, or at least not a functional spore type. Almost certainly artifactual are the protoplasmic segments of various shapes that Cronin and Johnson observed emerging from the tips of some thalli; these are not uncommon in disintegrating, damaged thalli, or when the osmolality of the surrounding medium is not satisfactory. Lichtwardt has collected E. halophilus on the shores of North Carolina, but not in sufficient quantity to verify the observations of Cronin and Johnson.
An interesting point is that E. halophilus was found by Cronin and Johnson only in female specimens of the mole crab, Emerita talpoida, although males were also examined. If this proves to be constant, it would be the only recorded instance where infestation of an arthropod by a trichomycete is sex dependent. Emerita analoga is a mole crab found on the west coast of the USA, where Whisler (1963) reported finding in its hindgut a fungus that resembled E. halophilus.
Although a number of species of Eccrinales are marine, E. halophilus is the only published marine species of Enterobryus. Nevertheless, it appears to be classified in the correct genus based upon current (very broad) concepts of Enterobryus. Several mud-burrowing true crabs (Brachyura) have undescribed trichomycetes in their hindguts that also appear to be species of Enterobryus. These have been collected and partially studied by the writers in several burrowing crabs, including at least three species of fiddler crabs on the east coast of the USA (Uca pugilator, U. pugnax, U. minax), and another species of eccrinid in the west coast fiddler crab (U. crenulata). Wagner-Merner (1979) and Mattson and TeStrake (1983) have published their investigations of the Enterobryus sp. from Uca pugilator. The authors have seen Enterobryus-like fungi in Uca spp. from Puerto Rico (White et al., 2000) and the Pacific coast of Costa Rica (Lichtwardt, unpubl.). Wolf and Wolf (1947) reported that the mud crab, Panopeus herbsth, contains a gut fungus that they called Enterobryus sp. All of these, and several other crab fungi the we have collected, need further study to determine if Enterobryus spp. are common in some kinds of marine Decapods, and to ascertain if they indeed belong to the genus Enterobryus.
References: Cronin and Johnson, 1958; Johnson and Sparrow, 1961;
Whisler,
1961, 1963.
Enterobryus
hydrophilorum (Léger &
Duboscq) Manier, 1970b (1969b)
Eccrinopsis hydrophilorum Léger & Duboscq, 1916 (basionym)
[= Trichella hydrophilorum (Léger & Duboscq) Poisson,
1931a, nom.
nud.]
Thalli coiled near the base, 3-6 mm long by 9-20 µm diam, wider near the basal region. Holdfast near cylindrical to campanulate or funnel-shaped, often longitudinally striated. Secondary infestation sporangiospores 400-600 µm long by ~9-11 µm diam. Primary infestation sporangiospores sometimes in long series (up to 51), variable in size, 25-32 x 12-16 µm, but in wider thalli spores sometimes wider than long.
Illustrations: Fig. 11.208.
Hosts: In anterior hindgut of Hydrous piceus L., H. pistaceus Cost., and H. flavipes Steph. (Coleoptera, Hydrophilidae).
Distribution: Aquatic habitats in Departments of Hérault, Pyrénées Orientales, and Manche, France, and Germany.
The basionym of this species is Eccrinopsis hydrophilorum, the type species for the genus Eccrinopsis Léger & Duboscq, 1916, a genus no longer valid. [Eccrinopsis had been proposed but not validly published earlier by Léger and Duboscq (1906)]. Trichella hydrophilorum is the type species for Trichella Poisson 1931a, likewise no longer valid.
Enterobryus helocharei also occurs in a hydrophilid beetle. Both of these species of Enterobryus are reported to shed their shorter and wider primary infestation spores by a mechanism whereby the elastic sporangial wall acts as an elater (Léger and Duboscq, 1916; Poisson, 1931a).
References: Manier, 1969b (1970b), Léger and Duboscq, 1916; Poisson,
1931a;
Duboscq et al., 1948; Maessen, 1955.
Enterobryus isoporostrepti Manier, Gasc & Bouix, 1975 (1974)
Thalli sinuous, curved at the base, 1-1.5(-2. 1) mm long by 6-14 µm diam. Holdfast often wider than long, about as wide as the thallus. Producing two forms of secondary infestation sporangiospores: (1) long and folded within a sporangium 125-320 µm long, upon liberation being straight and tapered to a point apically, basal end rounded, 250-350 µm long, with 2-8 nuclei in a row; and (2) short, 20-30 x 15-18 µm, with 6-8 irregularly arranged nuclei.
Illustrations: Fig. 11.240.
Host: In very anterior part of hindgut of Isoporostreptus bouixi Demange (Diplopoda, Spirostreptidae).
Distribution: Terrestrial, Dahomey, Africa.
This species also produces terminal series of 1-5 cells packed with nuclei (or uninucleate cellsm) 60-110 x 8-16 mm.
Note: Manier et al. described in 1974 a number of species of Enterobryus living in millipedes from Dahomey, Africa. Four of these (Enterobryus isoporostrepti, E. adjanohouni, E. onychostrepti, and E. peridontopygei), from millipede hosts representing two families, have certain characteristics that make them very similar, if one excludes certain cell types of unknown function that are seen in many other Enterobryus spp., and if one accepts the considerable intraspecific variation of many Enterobryus spp. All of these four fungi live in the very anterior part of the hindgut just posteriad to the Malpighian tubes and were found in millipedes taken in the Porto-Novo botanic garden in Dahomey. Especially notable is a unique form of secondary infestation sporangiospore produced by all four species: It is very long (often several hundred micrometers) and folded within the somewhat shorter sporangium, and upon release the sporangium usually collapses in a pleated fashion, while the straightened released spore is seen to be tapered and pointed at its distal end. The question of proper specific identity arises. Two possibilities are suggested. One is that the four mentioned species are, in fact, conspecific and transmissible among the different millipedes, but differ morphologically because of their phenotypic plasticity. The other possibility is that more than one species of eccrinid lives in the millipedes' gut, and that the thalli with the long tapered spores belong to one fungal species and is shared by the other millipede species. Manier et al. (1974) recognized and discussed the difficulty of determining the species described in that paper. Since the problem presented here cannot be resolved at this time, we have chosen to maintain the four species as distinct until it can be demonstrated otherwise experimentally.
Reference: Manier et al., 1974 (1975).
Enterobryus leptoiuli Manier ex Manier, 1970b (1969b)
Thalli up to 2 mm long, curved at the base; basal region 9-15 µm diam, narrowing to 4.5-7 µm diam near the apex. Holdfast 9-19 µm long, irregularly campanulate, with only a slight basal enlargement. Secondary infestation sporangiospores 8-nucleate, 70-115 µm long, produced in series of 2-3 per thallus. Producing primary infestation sporangiospores in series of up to 65 per thallus, of three kinds: (1) 5-6 x 7 µm diam; (2) isodiametric, 7 x 7 µm; and (3) 8-11 x 4.5-6 µm diam.
Illustrations: Fig. 11.236.
Host: In hindgut of Leptoiulus belgicus Latzet (Diplopoda, Julidae).
Distribution: Terrestrial habitats, in Department of Hérault, France.
The original description of E. leptoiuli (Manier, 1950) included some peculiar thick-walled elongate to oval spores, which would proscribe placing this species in the genus Enterobryus. However, Manier restudied the fungus and believes those structures were artifacts (personal communication). Her 1969 description, the basis for the above diagnosis, differs from her earlier one in several other respects as well.
References: Manier, 1950 (1951), 1969b (1970b).
Enterobryus
moniliformis (Leidy)
Lichtwardt, 1957b
= Eccrina moniliformis Leidy, 1850b
Thalli up to 3 mm long by 6-12 µm diam, spiraled throughout their length, or curved or spiraled only at the base. Holdfasts 12-35 x ~10 µm, usually constricted near the attachment to the thallus, without a prominent basal disk; longer holdfasts usually striated longitudinally. Secondary infestation sporangiospores about 50-60 x 5-8 µm. Primary infestation sporangiospores about 8-15 x 6-10 µm, becoming spherical to oval upon release.
Illustrations: Fig. 7.20; Fig. 11.233.
Host: In hindgut of Scytonotus granulatus (Say) (Diplopoda, Polydesmidae).
Distribution: In leaf litter, Illinois and Pennsylvania, USA.
Leidy's (1850b) genus Eccrina cannot be differentiated from his first genus Enterobryus merely on the basis of the number of terminal cells (sporangia) produced, as Leidy had proposed (Lichtwardt, 1954b). Eccrina moniliformis, collected from the same millipede species as Leidy's (he called it Polydesmus granulatus) , was restudied by Lichtwardt (1957b) and transferred to the genus Enterobryus. Leidy (1850b) originally used the specific epithet moniliforma, but changed it to moniliformis in 1853. He never illustrated this species. Lichtwardt reported seeing ellipsoidal spores, 19 x 5 mm, germinating in the millipedes' gut, but the origin of the spores was not determined.
References: Leidy, 1850b, 1853; Lichtwardt, 1954a, 1957b.
Enterobryus onychostrepti Manier, Gasc, & Bouix, 1975 (1974)
Thalli up to 6 mm long by 6-28 µm diam, sinuous or looped. Holdfast basal, or formed on one side of an incurved base. Secondary infestation sporangiospores folded within sporangia 90-270 x 6-10 µm, upon release unfolding to 180-460 µm long, tapered and with a pointed distal end.
Illustrations: Fig. 11.241.
Hosts: In very anterior hindgut of Onychostreptus aoutii Demange and O. assiniensis Attems (Diplopoda, Spirostreptidae).
Distribution: Terrestrial, Dahomey, Africa.
The authors of this species also reported the production on some thalli of 1-3 terminal cells measuring 70-400 mm long; these were packed with nuclei (or round sporesm).
See the note under Enterobryus isoporostrepti concerning the problem of identity of this and other species from Dahomey.
Reference: Manier, Gasc, and Bouix, 1974 (1975).
Enterobryus oxidi Lichtwardt, 1960a
Thalli dimorphic. Larger thalli attached to cuticle by a large holdfast with a basal disk, located in most anterior region of the hindgut, with a prominently curved base, 15-21 µm diam, tapering to 6-9 µm diam distally, producing primary infestation sporangiospores 6-13 x 6-9 µm diam. Smaller thalli more scattered, straight or curved near the base, 5-7 µm diam, small holdfasts with variable shapes, producing either primary infestation sporangiospores 6-13 x 6-9 µm, or secondary ones up to 170 mm long by ~6 µm diam.
Illustrations: Fig. 11.232.
Host: In anterior hindgut of Oxidus gracilis (Koch) (Diplopoda, Paradoxosomatidae).
Distribution: In greenhouse in Illinois, USA, and forest humus in Madagascar.
Enterobryus flavus Maessen (1955), a species we do not recognize because of an insufficient description, was found by Maessen in the same millipede species in Germany (under the name Orthomorpha gracilis Koch). Lichtwardt did not believe her species resembled E. oxidi, although Tuzet and Manier (1967) thought the two might be conspecific.
Lichtwardt (1960a) reported finding some ellipsoidal spores of unknown origin measuring 18-20 x 4-5 mm and germinating in the millipede gut. He also found rare loose thalli bearing binucleate cells, which he erroneously thought were a different stage of E. oxidi. However, that organism is now clearly more closely related to the non-trichomycete genus Mononema (see last section-in Chapter 12).
Tuzet and Manier (1967) found an Enterobryus in Oxidus gracilis from Madagascar that they consider to be E. oxidi. Their study included observations on the fine structure of vegetative thalli. They also reported finding additional cell (spore?) types: Disklike uninucleate cells and longer binucleate cells on some wide (25-30 mm diam) thalli, as well as some multinucleate cells on narrower thalli.
Reeves (2000) in a study of fungal records from caves in Georgia, USA, reported E. oxidi in O. gracilis, which he states is a common troglophilic millipede in Howards Waterfall Cave. He also found several unidentified Enterobryus spp. in the hindguts of five cavernicolous millipedes. [See Manier (1964d) for description of E. gracilis (nom. dub.) from the millipede Perapolydesmus progressus (Bröl.), and Parataeniella scotonisci from the isopod Scotoniscus macromelos Racovitza, in French caves.]
References: Lichtwardt, 1954a, 1960a; Tuzet and Manier, 1967;
Maessen, 1955.
Enterobryus oxydesmi Manier, Gasc, & Bouix, 1975 (1974)
Thalli up to 6.5 µm long, either (1) cylindrical and 6-10 or 16-20 µm diam, or (2) wider at the base, 21-31 µm diam, and tapering to 8-20 µm diam distally. Holdfasts large and conical. Secondary infestation sporangiospores 90-220 x 6-14 µm. Primary infestation sporangiospores more or less isodiametric. Other uninucleate cells like stacked disks formed from multinucleate cells 80-130 µm long.
Illustrations: Fig.11.242.
Host: In hindgut of Oxydesmus ganulosus Palisot de Beauvois (Diplopoda, Polydesmidae).
Distribution: Terrestrial, Dahomey, Africa.
Reference: Manier et al., 1974 (1975).
Enterobryus peridontopygei Manier, Gasc, & Bouix, 1975 (1974)
Thalli curved to spiraled at the base, 1-2(-4.5) mm long by 14-28 µm diam. Holdfast as long as, or longer than, the diameter, with a slight basal enlargement. Secondary infestation sporangiospores 130-200 x 20-24 µm; or 170-370 x 14-20 µm, tapered to an apical point having a small bulbous wall thickening.
Illustrations: Fig. 11.243.
Host: In very anterior hindgut of Peridontopyge gasci Demange (Diplopoda, Odontopygidae).
Distribution: Terrestrial, Dahomey, Africa.
Manier et al. also reported that this species produces some multinucleate cells 70-260 x 14-28 mm that cleave internally into uninucleate (rarely 2- to 3-nucleate) round or oval (21-28 x 18-21 mm) cells. Such "sporangia" become swollen and deformed. See comments under Enterobryus tuzetae relating to such structures. Also see the note under Enterobryus isoporostrepti concerning the problem of identity of this and other species from Dahomey.
Reference: Manier et al., 1974 (1975).
Enterobryus tuzetae Manier, Gasc, & Bouix, 1972a
Four thallial types produced in four (anterior to posterior) zones of hindgut: (I) large thalli up to 6 mm long by 40 mm diam, with a holdfast 5-10 x 35-40 µm diam, producing (a) short multinucleate (up to 6 nuclei) secondary infestation sporangiospores with their bases curved back upon themselves, or (b) longer, 2- to 4-nucleate, secondary infestation sporangiospores 80-90 x 16-22 µm; (II) large thalli 1-5 µm long by 14-28 µm diam near the base and 11-26 µm diam distally, with a holdfast 15-40 x 10-14 µm diam with a basal disk, producing secondary infestation sporangiospores 70-110 µm long; (III) small thalli forked above the small (4-10 x 6-8 µm diam) holdfast so as to have two branches of unequal length (600-900 and 400-700 µm) and 5-8 µm diam, both branches producing 4-nucleate secondary infestation sporangiospores 40-50 µm long, or longer branch producing 1-2 uninucleate primary infestation sporangiospores; (IV) small thalli curved at their base, 1350 µm long by 5-10 µm diam, with a small holdfast, rarely producing primary or secondary infestation sporangiospores.
Illustrations: Fig. 11.238.
Host: In hindgut of the large millipede, Pachybolus ligulatus (Voges) (Diplopoda, Pachybolidae).
Distribution: In forests on litter or under surface of soil, Dahomey, Africa.
Thalli in zones I and II may also produce multinucleate spores, in the latter said to convert into uninucleate bodies. Upon molting of the host, some thalli of E. tuzetae are reported to produce throughout their length swollen and very irregularly shaped cells ("sporangia") that become filled with ovoid, thick-walled spores measuring ~2-26 x 1.5-16 mm. The bifurcated thalli in zone III are similar in their development to Enterobryus bifurcatus (see Fig. 11.235).
Enterobryus tuzetae is one of the most unusual and variable species of Enterobryus, but it is also one of the most thoroughly studied. The host is one of the large spirobolid millipedes such as occur in some tropical regions: Mature adults may be 13 cm long by 15 mm diam, and the hindgut alone measures 7-8 cm long (Manier et al., 1972a). The location of four thallial types producing morphologically different spores within four zones of the hindgut is reminiscent of the kind of partitioning described by Hibbits (1978) for Enteropogon sexuale in the hindgut of the marine anomurid Upogebia pugettensis. In instances such as these, where intermediate forms or developmental continuity are not clearly evident among the different thallial and spore types, one can rightly ask if they may not represent more than one species. Lichtwardt (1957a, 1978a) decided that in the hindgut of passalid beetles, which also have very long hindguts divided into at least four recognizable zones, the fungal flora consists of several different species of trichomycetes (see the discussion under Leidyomyces attenuatus). In the absence of experimental evidence to the contrary, we have tentatively accepted the conclusion of Manier et al. that the fungi in the millipede Pachybolus ligulatus represent one species, E. tuzetae.
Another problem presents itself, however. Are the unusual, completely segmented thalli with swollen and distorted cells containing masses of oval thick-walled spores found by Manier et al. in molts of these millipedes actually a reproductive stage of E. tuzetae?Terminal cells of Enterobryus spp. are sometimes densely packed with nuclei. These form in thalli that already contain more nuclei than other thalli normally contain, and the function of such cells is unknown (for examples, refer to E. apheloriae, E. borariae, E. cherokiae, and E. euryuri). In several other species of Enterobryus from Dahomey, Manier et al. (1974) have described similar cells, but sometimes containing fewer nuclei than the ones just described, and these are said to produce uninucleate (rarely 2- to 3-nucleate) sporelike bodies in E. isoporostrepti, E. onychostrepti, and E. peridontopygei. In E. peridontopygei the "sporangia" that produce such cells become swollen and distorted, as in E. tuzetae. The question here is whether such hypertrophied structures are indeed a reproductive phase of the trichomycete, or whether they might result from endoparasitism. For example, some water molds (Saprolegniales, Blastocladiales) parasitized by other fungi, such as the endoholocarpic genera O1pidiopsis (Lagenidiales), Rozella (Chytridiales), and Woronina (Plasmodiophorales), are stimulated by the parasite to produce crosswalls in their coenocytic thalli, and these cells frequently hypertrophy. The cells or cysts within the hypertrophied and distorted cells of E. tuzetae do not appear to be identical to the reproductive stages of the fungal parasites cited above, but given the rich flora and fauna of millipede guts, including many kinds of protozoans, the possibility of endoparasitism should be given some consideration. On the other hand, if the E. tuzetae cell types under discussion are in fact a functional form of reproduction as Manier et al. claim, E. tuzetae, and other species with such reproduction, would probably not belong to the genus Enterobryus, based upon the characters of the type species, E. elegans.
References: Manier et al., 1972a, 1974 (1975).
Enterobryus
viequensis Virella, Hern.-Roa & Cafaro, 2009
Illustrations: Fig. 11.348.
Host: Anadenobolus arboreus
DeSaussure (Diplopoda).
Distribution: Vieques Island, Puerto Rico.
Reference: Roa, Virella, and Cafaro, 2009.
Enterobryus zinophorae Gorter, 1993
The thalli are inside the sphincter muscle. The hyphae are hyaline, straight, bent or undulating towards their apex but occasionally hooped hear their base, 2000-3000 x (7.5)10.0-12.5(-15) µm. Hyphae have rounded ends and may widen slightly towards their base where they secrete a holdfast with a short stalk not longer than 6 mm and usually shorter than wide. Some hyphae produce a number of cells 175-300 µm long and usually 10 mm wide towards their apex. These are sporangia which, when mature, contain long, folded spores with a slightly swollen obtuse base and a pointed apex without a protecting cap. These spores are 250-350 x 7.5-10.0 µm. The sporangia from which they escape, contract to become empty cells with many folds. The escaped spores straighten out, immediately develop a hypha from the rounded base and attach themselves to the sphincter lining. The hypha keeps on growing after which the spore presumably degenerates. No other type of spore has been observed.
Illustrations: Fig. 11.165.
Hosts: Zinophorae spp. (Diplopoda).
Distribution: South Africa.
Reference: Gorter, 1993
Enteromyces
Lichtwardt, 1961a
Thalli dimorphic, growing mostly in tufts from a multiple holdfast system. Spore mother-cell persistent. Producing thick-walled uninucleate sporangiospores, or thin-walled uninucleate or multinucleate sporangiospores. Attached to foregut cuticle of Anomura and Branchyura (Crustacea). Monotypic.
Type species: Enteromyces callianassae Lichtwardt.
Enteromyces callianassae Lichtwardt, 1961a
Thalli dimorphic, up to 1.6 mm long by 25-46 or 10-14 µm diam, with a persistent spore mother-cell that may later function as a sporangium. Usually growing in tufts, holdfast of each thallus attached to a predominant holdfast that anchors the complex to the gut cuticle. Thick-walled (up to 7 µm thick) uninucleate sporangiospores subspherical, 25-35 x 30-45 µm. Small uninucleate primary infestation sporangiospores 4-7 x 7-13 µm. Multinucleate (-16 nuclei) secondary infestation sporangiospores 30-55 x 23-45 µm. Type species.
Illustrations: Fig. 11.35.
Hosts: In foregut (stomach) of many Crustacea: Callianassa uncinata H. Milne-Edwards, C. brachyophthalma H. Milne-Edwards, C. filholi H. Milne-Edwards, C. gigas Dana, C. californiensis Dana, Upogebia affinis (Say), U. pugettensis (Dana)(Anomura, Callianassidae); Uca pugilator (Bosc) (Ocypodidae), Hemigrapsus penicillatus (de Haan) (Grapsidae) (Brachyura).
Distribution: Marine, intertidal mud or sand flats, or deeper water, in Chile, Japan, New Zealand and USA (North Carolina, California, Washington, Massachusetts).
Enteromyces callianassae is not only widely distributed, but is known to infest both true crabs (Brachyura) and shrimplike crabs (Anomura) commonly called ghost or mud shrimps. Most of the known hosts are intertidal, but one, Callianassa brachyophthalma, was taken at a depth of 35-40 m. Arundinula galatheae is the only other marine trichomycete found in a host approaching this depth. It is probable that the fungus is more widely distributed than present records indicate. The record in Uca pugilator was from Buzzards Bay, Massachusetts, USA (Tuzet and Manier, 1962).
Enteromyces spp. appear to be restricted to the foregut of their hosts, in contrast to Arundinula spp., which occur also in the hindgut. The foregut in the anomurid Upogebia pugettensis may contain E. callianassae at the same time the hindgut is infested with Enteropogon sexuale (Hibbits, 1978).
The tufts of dimorphic thalli that readily identify E. callianassae arise when one or more curved thalli deposit their sporangiospores directly onto the first and predominant holdfast, where the spores attach and germinate (Fig. 11.35B). Dozens of thalli (up to 160, according to Hibbits) may constitute the mature cluster, but clusters may be found in all stages of development. Leidyomyces attenuatus in the hindgut of passalid beetles also form tufts of thalli.
References: Lichtwardt, 1961a; Tuzet and Manier, 1962; McCloskey and
Caldwell, 1965; Galt, 1971; Hibbits, 1978; Williams and Lichtwardt,
1990.
Enteropogon
Hibbits, 1978
Four thallus types, each producing thin-walled uninucleate and
multinucleate
cells. One thallus type producing scalariform fusions. In hindgut of
Anomura
(Crustacea).
Two species.
Type species: Enteropogon sexuale Hibbits.
The type species of Enteropogon is certainly distinct from all other Eccrinales. Whether the genus is distinct is less certain. In many respects it resembles Enterobryus, as that genus is currently conceived. The most unusual, but not unique, feature of Enteropogon is the fusion of thalli in a manner that could be interpreted as a sexual process; however, it has not yet been adequately demonstrated to involve karyogamy, nor has it been determined how it fits into the life cycle of the fungus. See the discussion in Chapter 7 under the section on sexual reproduction.
Enteropogon
formosensis Chien & Hsieh, 2001
(In Misra and Horn,
2001)
Four thallus types present. First thallus type 69-261 x 7-12 µm; terminal cell oar-shaped, 9-15 µm in diam; base of thalli evenly lobed or slightly asymmetrically expanded, 6-33 µm in diam; holdfast 2-6 x 4-9 µm. Spores differentiate within the oar-shaped cells, thin-walled, uninucleate, 6-12 x 6-8 µm; oval, binucleate spores 21 x 9 µm. Thalli attached to the cuticle of mid-region of the hindgut, especially in exuvia, fused in pairs to produce uninucleate spheres (zygotes) 9-18 µm in diam. Second thallus type rarely found in the middle regions of the hindgut of exuvia . Mature thalli 90-168 x 11-15 µm; base of thalli strongly expanded asymmetrically to 15-42 µm in diam; producing ellipsoidal, thick-walled spores, 18-21 x 9-15 µm; holdfast 7-15 x 3-7 µm. Third thallus type abundant near the rectum, mostly 800-2500 µm long, in exuvium up to 3.2 mm long, 6-15 µm in diam. Binucleate spores 11-38 x 6-15 µm; quadrinucleate spores 75-132 x 6-11 µm. Base of thallus predominantly inflated unilaterally, boot shaped or 'L' shaped and the protruding portion 6-36 x 9-21 µm. In exuvium proximal portions strongly expanded, measuring up to 24 µm, gradually narrowing, as wide as fourth thallus type but terminally wider, producing uninucleate spores 21-24 x 15-18 um, with the end spore slightly contracted. Fourth thallus type seen with third type of thalli, up to 3.5 mm long and 5-8 µm in diam, producing thick-walled, uninucleate spores 6-9 x 5-8 µm; the hyphal tip usually with the spore mother cell.
Illustration: Fig. 11.253.
Host: Upogebia edulis Ngoc-Ho & Cham (Crustacea, Thalassinidae, Upogebiidae).
Distribution: Taiwan.
Reference: Misra and Horn, 2001, Chapter 5.
Enteropogon
sexuale Hibbits, 1978
[= Paraenterobryus multiformis Galt, 1971, nom. provis.]
Four thallus types produced (from anterior to posterior region of hindgut): (1) Thalli 4 mm long by 11-19 µm diam, tightly coiled to slightly undulate, producing 4- or 8-nucleate secondary infestation sporangiospores 40-55 x 11-18 µm in coiled thalli or 70 x 9 µm in straighter thalli; or producing uninucleate cells 16-26 x 8-12 µm that fuse in pairs between adjacent thalli to form uninucleate spheres 32-40 µm diam. (2) Thalli 11 mm long by 7-20 µm diam with a bulbous base, producing 4-nucleate secondary infestation sporangiospores 7-15 x 8-9 µm; or uninucleate primary infestation sporangiospores 23-25 x 13-14 µm; or small uninucleate cytoplasmic segments 34-35 x 7-10 µm. (3) Thalli 8.5 µm long by 10 µm diam distally, base sigmoid and inflated to 65 µm diam, producing 4- or 8-nucleate secondary infestation sporangiospores 65-115 x 7.5-18 µm, or uninucleate primary infestation sporangiospores 35-45 x 27-29 µm (4) Thalli 3 mm long by 5-7 µm diam, producing small cytoplasmic segments. Type species.
Illustrations: Fig. 11.36.
Host: In hindgut of Upogebia pugettensis (Dana) (Crustacea, Callianassidae).
Distribution: Marine, mud flats, San Juan Archipelago, Washington, USA.
The foregut of the mud shrimp host of E. sexuale may also contain thalli of Enteromyces callianassae.
References: Hibbits, 1978; Galt, 1971.
Leidyomyces
Lichtwardt, White, Cafaro & Misra, 1999
Usually growing in whorled clusters of individual thalli attached to a fused holdfast system, less commonly thalli growing individually. Producing series of sporangia with either uninucleate sporangiospores or long multinucleate attenuated sporangiospores. In anterior hindgut of Passalidae (Coleoptera). Monotypic.
Type species: Leidyomyces attenuatus (Leidy) Lichtwardt,
White,
Cafaro & Misra.
Leidyomyces
attenuatus (Leidy) Lichtwardt,
White, Cafaro & Misra
Basionym: Enterobryus attenuatus Leidy, 1849b, emend. Lichtwardt,
1957a
= Eccrinopsis attenuatus (Leidy) Léger & Duboscq, 1916
[= Trichella attenuatus (Leidy) Poisson, 1931a, nom. nud.]
Thalli in anterior hindgut (ileum) growing singly but more often in whorled clusters with individual thalli attached to a common multiple holdfast system, up to 1.4 mm long by 8-16 µm diam, producing uninucleate primary infestation sporangia 10-22 x 9-15 µm, or multinucleate secondary infestation sporangiospores 240-250 x 5-10 µm diam. Thalli in midregion of hindgut (colon) up to ~2 µm long, sinuous and tapering toward the apex, growing singly or less commonly in small tufts, usually nonsporulating.
Illustrations: Fig. 11.33.
Host: In hindgut of adult and larval Odontotaenius disjunctus (Illiger) [= Popilius disjunctus (Illiger)] (= Passalus cornutus Fab.) and many other Passalidae (Insecta, Coleoptera).
Distribution: Terrestrial, usually in decaying logs, in USA, Brazil, Panama, Trinidad, Puerto Rico. Probably throughout North America and the Neotropics where Passalidae occur.
Leidy (1849b, 1853) described only the nonsporulating thalli of Leidyomyces attenuatus, which he named Enterobryus attenuatus, living in the colon of O. disjunctus, a large wood-inhabiting beetle that is sometimes called the bessbeetle, bessbug, or horned passalid. The fungus was more fully described by Lichtwardt (1957a). The authors have found L. attenuatus in most populations of passalid beetles examined in the USA and in the Neotropics. Manier and Théoridčs (1965) partly described and illustrated a fungus they called E. attenuatus growing in the gut of a passalid beetle (Leptaulax dentatus F.) from Laos, but the extremely long holdfasts of the thalli, although sometimes fused together, suggest that it may be another species. The fine structure of the multiple holdfast of L. attenuatus has been studied by Mayfield and Lichtwardt (1980), and is described in Chapter 7.
Passalid beetles also may have in their posterior rectum Passalomyces compressus) (= Enterobryus compressus, and, farther forward, an unnamed species of Enterobryus described by Heymons and Heymons (1934). Lichtwardt has collected specimens of both, and the latter appears to be a distinct species of Enterobryus. More anterior in the rectum, some of the tropical beetles have a small branched organism growing in the longitudinal fissures of the cuticle. In the USA White cultured a branched fungus that is not a trichomycete, Enteroramus dimorphus White, Lichtwardt, Misra & Cafaro (Lichtwardt et al., 1999); the fungus is dimorphic, being filamentous in the gut but converting to a yeastlike growth in culture.
References: Leidy, 1849b, 1853; Lichtwardt, 1954a, 1957a, 1968,
1978; Léger
and Duboscq, 1916; Manier and Théoridčs, 1965; Dang, 1978; Mayfield and
Lichtwardt, 1980, Lichtwardt et al., 1999.
Paramacrinella
Manier & Grizel, 1971
Thalli dimorphic. Macrothalli unbranched, spore mother-cell persisting at the base of the mature thallus, producing primary and secondary infestation sporangiospores. Microthalli cleaving into series of small uninucleate cells. In hindgut of Amphipoda. Monotypic.
Type species: Paramacrinella microdeutopi Manier & Grizel.
This genus closely resembles the eccrinid genus Ramacrinella whose
single species also lives in an amphipod, but whose macrothalli are
branched at
the base.
Paramacrinella microdeutopi Manier & Grizel, 1971
Macrothalli 1.2-l.5 mm long by 12-18 µm diam distally, 18-35 µm diam at the curved base. Spore mother-cell persisting at an angle on the thallus base just above the flat holdfast disk. Apex of macrothalli may have an ampulla 50 µm diam. Producing multinucleate secondary infestation sporangiospores 50-80 µm long; or numerous thin-walled uninucleate primary infestation sporangiospores 13-18 x 4.5-8.5 µm, upon liberation becoming globose and 10-12 µm diam. Microthalli 650-750 µm long by 12-14 µm diam, producing a long series of numerous uninucleate cells. Type species.
Illustrations: Fig. 11.29; Fig. 11.69.
Host: In hindgut of Microdeutopus anomalus (H. Rathke) (Amphipoda, Aoridae).
Distribution: Marine, in saltwater bay, Department of Hérault, France.
Single macrothalli of P. microdeutopi may produce successively both types of spores. The function of the microthallus cells is not known.
Reference: Manier and Grizel, 1971.
Passalomyces
Lichtwardt, White, Cafaro & Misra, 1999
Thalli with thick walls producing terminal series of thick-walled compressed sporangia each with a thin-walled uni- to multinucleate sporangiospore. In posterior hindgut of Passalidae (Coleoptera). Monotypic.
Type species: Passalomyces compressus (Thaxter) Lichtwardt,
White,
Cafaro & Misra.
Passalomyces
compressus (Thaxter)
Lichtwardt, White, Cafaro & Misra, 1999
Basionym: Enterobryus compressus Thaxter 1920.
[= Trichella compressus (Thaxter) Poisson, 1931a, nom. nud.]
Thalli 0.5-3.5 mm long by 20-35 µm diam, with walls 2-4 µm thick. Holdfast like an inverted cup. Apex of thallus becoming partially flattened upon producing a series of terminal sporangia 5-8 µm long by 20-35 µm wide, each containing a thin-walled, multinucleate, more or less allantoid sporangiospore slightly smaller than the sporangium.
Illustrations: Fig. 11.52.
Host: On anal plates of tropical Passalidae (Coleoptera).
Distribution: Terrestrial, usually in rotting logs, in Dominica, Costa Rica, Panama, and Amazon region of Brazil.
This is an unusual species of Eccrinalesin several respects. The flattened and sometimes slightly twisted ends of the thick-walled thalli produce series of short but wide sporangia, each containing a sausage-shaped multinucleate spore that lies at a right angle to the thallus axis. These spores are thin-walled, appear to be 4-nucleate at maturity, and emerge from the sidewall of the sporangium. They are morphologically secondary infestation spores. However, in this species the position of the thalli on the anal plates of the passalid beetle exposes the thalli and spores to the exterior of the gut; consequently, if such spores are functional they would function as primary infestation spores. Thaxter described thalli as "growing outside the anus," but in Lichtwardt's collections of P. compressus from Costa Rica, Panama and Brazil, very long sporulating thalli also occur within the gut, attached to the rectum. The spores produced by the long thalli often lie within the gut lumen and are identical to the more exposed spores; possibly they can function as secondary infestation spores. These same beetles often contain Leidyomyces attenuatus, a more common species, in the anterior hindgut.
References: Thaxter, 1920; Lichtwardt, 1978; Lichtwardt et al.,
1999.
Ramacrinella
Manier & Ormičres ex Manier, 1968
[= Ramacrinella Manier & Ormičres, 1961a, nom. nud.]
Thalli dimorphic. Macrothalli branched with several fertile axes, producing primary and secondary infestation sporangiospores. Spore mother-cell persisting at the base of the mature thallus. Microthalli unbranched, cleaving into series of small uninucleate cells. In hindgut of Amphipoda. Monotypic.
Type species: Ramacrinella raibauti Manier & Ormičres ex Manier.
The repeated branching of the coenocytic thalli of Ramacrinella is unusual among Eccrinales. Except for the branching, this genus resembles Paramacrinella, which also lives in an amphipod.
Ramacrinella
raibautiManier &
Ormičres; ex Manier, 1968
[ = Ramacrinella raibauti Manier & Ormičres, 1961 a, nom.
nud.]
Macrothalli with a principal fertile branch and several auxiliary fertile branches, up to 1.1 mm long by 12-13 µm diam. distally and 16-18 µm diam proximally, all axes rebranching repeatedly near their bases. Spore mother-cell persistent opposite the small holdfast. Producing multinucleate secondary infestation sporangiospores 26-30 x 6.5-12 µm, or numerous uninucleate oval primary infestation sporangiospores 15-20 x 4-7 µm that become somewhat globose after release. Microthalli unbranched, 150-275 µm long by 2.5-4 µm diam distally, 5-6 µm diam. proximally, producing long series of more or less globose cells 2.5-4 µm diam. Type species.
Illustrations: Fig. 11.29; Fig. 11.70.
Host: In hindgut of Microdeutopus gryllotalpa A. Costa (Amphipoda, Aoridae).
Distribution: Littoral, saltwater bay, under masses of vegetation, Department of Hérault, France.
The macrothalli of this unusual eccrinid are coenocytic and devoid of crosswalls except for those delimiting sporangia. The subsidiary basal branches are nonfertile. Except for its branched habit, Ramacrinella raibauti resembles Paramacrinella microdeutopi found in another species of Microdeutopus from the same saltwater bay, the Étang de Thau near Sčte. Two species of Enterobryus from millipede guts, E. bifurcatus and E. tuzetae, produce thalli with two divergent fertile axes, but they lack the repeated branching of R. raibauti.
References: Manier, 1968; Manier and Ormičres, 1961a; Grizel,
1971.
Taeniella
Léger & Duboscq, 1911
Thalli producing thick-walled resistant sporangiospores with 2 appendages at both poles, and thin-walled primary and secondary infestation sporangiospores. In hindgut of Decapoda (Brachyura and Anomura). Monotypic.
Type species: Taeniella carcini Léger & Duboscq.
The major character that distinguishes Taeniella is the
resistant
spore with its two polar appendages. These were not mentioned in the
original
description by Léger and Duboscq (1911), nor have they been described
from most
collections of Taeniella carcini. The appendages are usually
seen as a
gelatinous mass appressed to each end of the spore within the
sporangium, and
such structure may be taken as putative evidence of appendages if found
in
Decapods. When the resistant spores of T. carcini are
kept in seawater,
this gelatinous material unfolds, upon release of the spores from the
sporangia, to reveal the two long polar appendages at each pole (Moss,
1979).
It is possible that some of the resistant spores described in the
literature
have been immature. In most instances they have not been illustrated as
released spores, which is necessary for the unfurled appendages to be
seen,
preferably using phase-contrast microscopy. Hibbits (1978) reported
finding 2
appendages at only one pole. Further studies of Taeniella are
needed to
clarify the ontogeny of these appendages, and whether the number is
consistent.
Taeniella
carcini Léger & Duboscq,
1911
= Taeniella longa Léger & Duboscq, 1911
= Taeniella galatheae Manier & Ormičres ex Manier, 1968
[= T. galatheae Manier & Ormičres, 1962, nom. nud.]
= Taeniella grandis Hibbits, 1978
Thalli usually 2-4(-15) mm long by 2.5-12(-22) µm diam. Holdfast short and cylindrical. Thick-walled resistant sporangiospores oval to elongate oval, 1- to 4-nucleate, (15-)18-21(-32) x (6-)8-12(-18) µm, bearing two long appendages at each pole upon release from the sporangium. Uninucleate thin-walled sporangia in long series, 3-5 x 3-5 µm. Secondary infestation sporangiospores 4- to 8-nucleate, 30-150 x 5-12 µm. Type species.
Illustrations: Fig. 11.82.
Hosts: In hindgut of Decapoda: Carcinus maenas Penn., Portunus puber L., Cancer oregonensis (Dana), Pilumnus hirtellus L., Xantho pilipes M.-Edw., Hemigrapsus nudus (Dana), H. oregonensis (Dana), Gaetice depressus (de Haan), Sesarma hematocheir (de Haan), Helice crassa Dana (Brachyura); and Paguristes turgidus (Stimpson), Pagurus kennerlyi (Stimpson), P. beringanus (Benedict), P. ganosimanus (Stimpson), Eupagurus excavatus Herbst., Galathea strigosa L., Callianassa gigas Dana, C. californiensis Dana, C. filholi H. Milne-Edwards, Upogebia pugettensis (Dana), Oedignathus inermis (Stimpson) (Anomura).
Distribution: Marine, mostly on rocky shores and intertidal or subtidal, Mediterranean coast of France, Japan, and San Juan Archipelago, Washington, and Bodega Bay, California USA.
The original description by Léger and Duboscq (1911) was very brief, and the species was only illustrated (but poorly) in 1948 by Duboscq, Léger, and Tuzet. Nevertheless, additional studies by Manier (1961b, 1969), Johnson (1966), and Hibbits (1978) indicate that Taeniella carcini is widespread in many families of Decapoda, and is also quite variable. Given the wide host range, we believe that all species of Taeniella described so far are conspecific with T. carcini, for the morphological characters overlap considerably such that they cannot be used to differentiate the named species satisfactorily. The collections from Japan were made by Lichtwardt with Drs. Yosio Kobayasi and Hiroharu Indoh (unpublished). The distribution of T. carcini is undoubtedly much greater than present records indicate.
The resistant spores of T. carcini appear to form just prior to molting of the crabs. Their appendages have been clearly demonstrated only by Moss (1979), although other investigators have observed the gelatinous pads appressed to the ends of the spores while still within their sporangia. The number of nuclei in the resistant spores is difficult to determine, but it is possible they remain uninucleate even while the thick wall develops, but become 4-nucleate at full maturity.
Several reported features of T. carcini are worth noting. Manier (1961b) saw thalli producing both thin-walled and resistant spores simultaneously, the former ones located distally in sections of the thalli that were considerably narrower than the proximal end with developing resistant spores. Hibbits (1978) reported one instance of two thalli conjugating in a manner resembling this process in Enteropogon sexuale. She also saw "segments of thalli" attached to the walls of sporangia; one wonders if these might not be a spurious form of germination in situ, as commonly happens in Palavascia spp. On some thalli she also saw multicellular filaments of what appeared to be a large blue-green alga attached to the basal region of the thalli of T. carcini (T. grandis), and she suggested that these might be what Johnson (1966) saw attached to the apical region of thalli from the same kinds of crabs collected in the same general locality, and which led him to describe those thalli as "Palavascia sp."
References: Léger and Duboscq, 1911; Duboscq, et al., 1948; Manier,
1961b,
1968, 1969 (1970b); Manier and Ormičres, 1962; Johnson, 1966; Gait,
1971;
Hibbits, 1978; Moss, 1979; Whisler, 1979; Williams and Lichtwardt,
1990.
Taeniellopsis
Poisson, 1927
Thalli not dimorphic, upon molting of the host producing thick-walled, oval, uninucleate sporangiospores. Also producing thin-walled uninucleate primary infestation sporangiospores, and multinucleate secondary infestation sporangiospores. In hindgut of Amphipoda (Crustacea). Three species.
Type species: Taeniellopsis orchestiae Poisson.
Taeniellopsis flexilis Poisson, 1929
Thalli 700-1700 µm long by 3-10 µm diam. Holdfasts cylindrical, narrower than the thalli. Secondary infestation sporangiospores up to 10-nucleate and 65 µm long. Primary infestation sporangiospores variable in size, from 3 x 3 µm to 40-70 x 8-10 µm. Oval spores uninucleate 25-30 x 8-10 µm.
Illustrations: Fig. 11.73.
Host: In hindgut of Orchestia gammerella (Pallas) (Amphipoda, Talitridae).
Distribution: Terrestrial, near fresh, brackish or saltwater, Departments of Pyrénées-Orientales, Calvados and Finistčre, France.
Although the host has a wide distribution and infestation was found in several sites by Poisson, Taeniellopsis flexilis was not described as fully as the type species was, and the oval, presumably resistant, spores were not illustrated. Poisson stated that some thalli had "enigmatic protruberances" on their sidewalls. He also described some thalli consisting of 2- to 4-nucleate cells up to 70 mm. long that separated like arthrospores.
Reference: Poisson, 1929.
Taeniellopsis orchestiae Poisson, 1927
Thalli up to 1.2 mm long by 9-25 µm diam. Holdfasts short and disklike. Secondary infestation sporangiospores 4- to 10-nucleate, 40-110 x 20-25 µm. Primary infestation sporangiospores uninucleate, 2-4 x 5 µm or 8-12 x 16-20 µm. Upon molting of the host producing elongate-oval, uninucleate thick-walled resistant spores 30-38 x 9-12 µm in thalli that become spiraled. Type species.
Illustrations: Fig. 11.222.
Host: In posterior hindgut of Orchestia bottae M.-Edw. (Amphipoda, Talitridae).
Distribution: Terrestrial, border of a saline pond near Nancy, Department of Meurthe-et-Moselle, France.
Poisson illustrated and more fully described Taeniellopsis orchestiae in his second (1929) paper on this species. The resistant spores apparently have no appendage, as do some species of Astreptonema from amphipods, and they are uninucleate. Prior to their release, the sporangial crosswalls break down, and the resistant spores may emerge from an apical orifice in the spiraled thallus. Poisson (1929) claimed that the spore mother-cell may break off from the apex of a thallus, attach to the host cuticle, and develop into another thallus. He also stated that some sporangia were binucleate and became uninucleate after karyogamy, but it appears he did not actually see nuclear fusions.
Reference: Poisson, 1927, 1929.
Taeniellopsis
susplugasi Manier ex Manier,
1970b (1969b)
[= Taeniellopsis susplugasi Manier, 1950, nom. nud.]
Thalli 300-1200 µm long by 6-12 µm diam. Holdfast 3-4 mm. long, narrower than holdfast. Secondary infestation sporangiospores 20-55 µm long. Primary infestation sporangiospores flat and disklike or isodiametric. Thickwalled uninucleate oval spores 20-23 x 7-8 µm.
Illustrations: Fig. 11.226.
Host: In hindgut of Orchestia mediterranea Costa (Amphipoda, Talitridae).
Distribution: Terrestrial, near seashore of Mediterranean coast, Hérault, France.
Taeniellopsis susplugasi has smaller oval spores than the other species of the genus. Poisson (1929) dissected hindguts of Orchestia mediterranea, which he found in the Department of Finistčre, France, living among specimens of O. gammarella infested with T. flexilis, but found no fungi in their guts. Electronmicrographs of holdfasts and sporangia of T. susplugasi have been obtained by Grizel (1971), and some were published by Manier and Grizel (1972).
References: Manier, 1950 (1951), 1969b, (1970b); Grizel, 1971;
Manier and
Grizel, 1972.
Duboscq,
Léger &
Tuzet ex Manier & Lichtwardt 1969 (1968)
[= Palavasciaceae Duboscq, Léger & Tuzet 1948, nom. nud.]
Only multinucleate thick-walled primary infestation sporangiospores produced. Some sporangia capable of germination in situ instead of producing a sporangiospore. In hindgut of Isopoda (Crustaceae). One genus.
Type genus: Palavascia Tuzet & Manier ex Lichtwardt.
Palavascia
Tuzet & Manier ex Lichtwardt, 1964b
Palavascia Tuzet & Manier, 1947b, nom. nud.]
Series of terminal sporangia producing oval to ellipsoidal, thick-walled, multinucleate primary infestation sporangiospores; or, sporangia may germinate in situ to produce one or more narrow filaments that segment into uninucleate cells. Spore mother-cell persistent. In hindgut of halophilic or marine Isopoda. Three species.
Type species: Palavascia philosciae Tuzet & Manier ex
Manier
& Lichtwardt.
Palavascia patagonica Cafaro, 2000
Thalli unbranched, up to 1 cm long, uneven diam. Base of maturing thalli with U-shaped extension with a ring-shaped holdfast located on the outer part of the bend. Terminal end essentially straight, producing numerous irregularly stacked cylindrical to fusiform spores 17-18 x 54-67 µm, nuclear stage unknown. Immature thalli have a swollen persistent spore mother-cell.
Illustrations: Fig. 11.157.
Host: Exosphaeroma studeri (Isopoda: Sphaeromatidae).
Distribution: Patagonia, Argentina.
Reference: Cafaro, 2000.
Palavascia
philosciae Tuzet & Manier
ex Manier & Lichtwardt, 1969 (1968)
[ = Palavascia philosciae Tuzet & Manier in Lichtwardt,
1964b, nom. nud.]
[= Palavascia philosciae Tuzet & Manier, 1947b, nom.
nud.]
Thalli up to 1 mm long, 29-35 µm diam near the base, 18-26 µm diam distally. Tips straight, with a persistent narrow spore mother-cell. Primary infestation sporangiospores produced in series of up to 50 per thallus, oval or ellipsoidal, 4-nucleate, 19-25 x 7-12 µm. Sporangia may instead germinate in situ to produce a single filament 150-200 µm long by 4-6 µm diam that segments to form uninucleate cells containing small oval bodies 2 x 4-6 µm. Type species.
Illustrations: Fig. 11.221.
Host: In hindgut of Halophiloscia couchi Kin. (Isopoda, Oniscidae).
Distribution: In saline ponds near Palavas, Hérault, France.
The illegitimate original name was provided with a Latin diagnosis by Lichtwardt (1964b), but it was not validated until a nomenclatural type was cited by Manier and Lichtwardt in 1968 (1969).
The first specimens of Palavascia philosciae examined by Tuzet and Manier (1947b) did not have the ellipsoidal sporangiospores. These were described by them the following year (1948b). In that second publication they (and Manier, in 1950) suggested that the multinucleate spores of both P. philosciae and P. sphaeromae form subsequent to plasmogamy and karyogamy of adjacent uninucleate protoplasts in the thallus, but this has not been substantiated by Manier, nor by the authors, in subsequent studies of the more common species, P. sphaeromae. There is no known function for the small cells on the filaments that grow from germinated sporangia.
References: Tuzet and Manier, 1947b, 1948b; Manier and Lichtwardt, 1968 (1969); Lichtwardt, 1964b; Manier, 1950, 1963, 1969b (1970b).
Palavascia
sphaeromae
Tuzet & Manier ex Manier, 1968
[= Palavascia sphaeromae Tuzet & Manier, 1948b, nom.
nud.]
Palavascia beauforti Lichtwardt ex Lichtwardt, 1964b
[= Palavascia beauforti Lichtwardt, 1961b, nom. nud.]
Thalli 2-5 mm long, somewhat sinuate with uneven diam along their length, 30-60 µm diam near the base, 12-35 µm diam distally. Sporulating tips coiled, with a persistent spore mother-cell. Sporangia in long series in the coiled tips, producing oval or ellipsoidal uninucleate to 4-nucleate primary infestation sporangiospores 20-40 x 9-22 µm; or sporangia germinating in situ to produce one or more filaments ~170 µm long by 2-4 µm diam, up to 5-10 µm diam near the base, which segment to form small uninucleate cells. Sporulating tips may have sporangia with sporangiospores intermixed with germinating sporangia.
Illustrations: Fig. 7.10; Fig. 7.22; Fig. 11.37.
Hosts: In hindgut of Sphaeroma serratum F., S. quadridentatum Say, S. terebrans Bate Exosphaeroma oregonensis (Dana), Tecticeps japonicus Iwasa (Isopoda, Sphaeromidae).
Distribution: Marine, intertidal, in France (Hérault, Roscoff, Finistčre), Black Sea, USA (North Carolina, South Carolina, Florida), and Japan (Hokkaido). Sphaeroma terebrans in Florida was associated with roots of the red mangrove, Rhizophora mangle L.
Palavascia beauforti was described as a new species by Lichtwardt (1961b) in Sphaeroma quadridentatum from the coast of North Carolina on the basis of comparing it with the descriptions provided at that time for P. sphaeromae. However, subsequent and more accurate descriptions, and examination of fresh material by Lichtwardt from the type locality, make it apparent that the two species are synonyms. Naidenova and Mordvinova (1998) reported "P. beauforti" from S. serratum collected in the Black Sea, but the fungus was do doubt P. sphaeromae. The records of P. sphaeromae in Exosphaeroma oregonensis and Tecticeps japonicus from the northern Japanese island of Hokkaido were made by Lichtwardt et al. (1987) in June, 1964. It is probable that P. sphaeromae has a much wider distribution than present records indicate.
Tuzet and Manier (1948b) and Manier (1950) suggested that P. sphaeromae and P. philosciae produced the oval spores after fusion and karyogamy of adjacent uninucleate protoplasts in the thalli, but Manier (personal communication) does not now believe this interpretation is correct. In the writers' studies of this species, it appears that the thallus tips do not begin to coil and sporulate until they reach the anus. The coiled, sporulating tips are commonly seen protruding from the isopod's anus, and this may be one mechanism whereby younger isopods clinging to the pleopods of larger ones become infested (Lichtwardt, 1961b). The function of the small cells produced at the tips of filaments originating from germinated sporangia is unknown. Charmantier and Manier (1981) have done a study of the role of ecological parameters and population dynamics on infestation of Sphaeroma serratum by P. sphaeromae.
An interesting feature of P. sphaeromae is the germination of the spores after release from the sporangium. This has been described in some detail in Chapter 7 in the section on asexual reproduction in Eccrinales. Manier (1979a) has published an electron micrographic study of this species.
References: Tuzet and Manier, 1948b; Manier, 1950, 1961b, 1968,
1979a;
Lichtwardt, 1961b, 1964b, 1973a; Charmantier and Manier, 1981;
Naidenova and
Mordvinova, 1998.
Manier & Lichtwardt, 1969 (1968)
Thallus, or part of the thallus, developing into a sporangium containing many uninucleate primary infestation sporangiospores. Secondary infestation sporangiospores produced individually in sporangia, or absent. In hindgut of Isopoda or Insecta. Two genera.
Type genus: Parataeniella Poisson.
Lajasiella
Tuzet & Manier ex Manier, 1968
[= Lajasiella Tuzet & Manier, 1950b, nom. nud.]
Thalli short, with a persistent spore mother-cell. Producing a single large sporangium containing many uninucleate primary infestation sporangiospores, or series of terminal cells containing uninucleate bodies. In hindgut of larval Coleoptera (Insecta). Monotypic.
Type species: Lajasiella aphodii Tuzet & Manier ex
Manier.
Lajasiella
aphodii Tuzet & Manier ex
Manier, 1968
[= Lajasiella aphodii Tuzet & Manier, 1965, in Manier
and
Théoridčs, 1965, nom. nud.]
[= Lajasiella aphodii Tuzet & Manier, 1950b, nom. nud.]
Thalli usually 200-300 µm long, either 4-5 or 9-10 µm diam, with a narrowed apex consisting of the spore mother-cell. Primary infestation sporangiospores oval, uninucleate, 13-19 x 3.5-4.5 µm, formed in large numbers in a sporangium consisting of the entire thallus except for the basal region. Other thalli producing apical series of cells 13-35 µm long within which form many uninucleate spherical bodies 6-7 µm diam. Type species.
Illustrations: Fig. 11.68.
Host: In hindgut of larval Aphodius sp. (Coleoptera, Scarabaeidae).
Distribution: Terrestrial, near Lattes, Hérault, France.
In 1965 Manier and Théoridčs provided a Latin diagnosis for the illegitimate species, but the name was not validated until Manier (1968) cited a nomenclatural type.
The round uninucleate cells reported to form in terminal cells have no known function, and this species should be restudied to determine if they are possibly artifacts. There have been no secondary infestation sporangiospores reported in Lajasiella aphodii.
References: Manier, 1968; Tuzet and Manier, 1950b; Manier and
Théoridčs,
1965.
Parataeniella
Poisson, 1929
Thalli producing either a series of sporangia containing single, usually binucleate, secondary infestation sporangiospores, or entire thallus becoming one sporangium containing many uni- or binucleate primary infestation sporangiospores; or both types produced in one thallus. In hindgut of terrestrial Isopoda (Crustacea). Six species.
Type species: Parataeniella mercieri (Poisson) Poisson.
The crosswalls of the secondary infestation sporangia are
characteristically
somewhat oblique in most species.
Parataeniella armadillidii Lichtwardt & Chen, 1964
Thalli up to 385 µm long by 12-15 µm diam. Secondary infestation sporangiospores binucleate, ~ 12 x 10 µm. Primary infestation sporangiospores uninucleate, globose to angular in shape, ~11 µm diam, produced biseriately, rarely uniseriately, in a saccate (to cylindrical) thallus, emerging from thallus (sporangium) through a longitudinal slit. Thalli may produce series of secondary infestation sporangia terminally and a primary infestation sporangium basally in the same thallus.
Illustrations: Fig. 11.38.
Hosts: In hindgut of Armadillidium vulgare (Latr.) and A. nasatum Budde-Lund (Isopoda, Armadillidae).
Distribution: Terrestrial, Kansas, USA.
Reference: Lichtwardt and Chen, 1964.
Parataeniella
dilatata Poisson, 1929
= Parataeniella binucleata Poisson, 1929
= Parataeniella intermedia Poisson, 1929
Thalli of two types: (1) Thalli up to 300 µm long by (8-)12-14 µm diam, producing 2- (to 5-) nucleate secondary infestation sporangiospores (20-)45-50 µm long, or uninucleate sporangiospores 15-35 µm long; and (2) thalli 100-225 µm long by (12-)22-28 µm diam, producing uniseriate or biseriate thick-walled, oval to ellipsoidal, or uni- or binucleate primary infestation sporangiospores 16-22 x 9-11 µm, emerging from an apical orifice in the thallus (sporangium).
Illustrations: Fig. 11.223.
Hosts: In hindgut of Isopoda: Armadillo officinalis Dum. (Armadillidae); Androniscus dentiger Verh. (= Trichoniscus roseus Koch) (Trichoniscidae); Porcellio laevis (Latr.), P. lamellatus (Ulj.), Protracheoniscus occidentalis Vandel (Porcellionidae).
Distribution: Terrestrial, in France (Pyrénées-Orientales, Hérault, Calvados), Germany, and USA (South Carolina)..
Manier (1969b) considered Parataeniella intermedia to be a synonym of P. dilatata, based on her studies (1950, 1963a) of the latter species, and we are in agreement. We also consider P. binucleata to be conspecific with P. dilatata; although Manier did not go this far, she stated (1963a, p. 564) that the thick-walled primary infestation spores of the fungus in Porcellio laevis (host of P. binucleata) are identical with those in Armadillo officinalis (host of P. dilatata). The host of P. intermedia was reported by Poisson (1929) to be Androniscus dentiger. The other host records are those of Scheer (1976b), who collected extensively in Germany.
References: Poisson, 1929; Manier, 1950, 1963a, 1969b (1970b); Scheer, 1976b.
Parataeniella
flavospora Chien & Hsieh, 2001
(In Misra and Horn,
2001)
Mature thalli 210-690 x 6-16 µm, and primary reproductive thalli usually wider, up to 21 µm in diam. Holdfast disk-like, 6-15 µm in diam. Secondary infestation sporangiospores binucleate, thin-walled, (18-)22(-39) x 6-9 µm. Primary infestation sporangiospores binucleate, thick-walled, oval to ellipsoidal, uniseriate within sporangium. Mature spores consistently full of lipid bodies, yellowish, 15-24 x 7-12 µm.
Illustration: Fig. 11.254.
Host: Armadillidium vulgare Latreille and Porcellio scaber Latreille (Crustacea, Isopoda).
Distribution: Taiwan.
Reference: Misra and Horn, 2001, Chapter 5.
Parataeniella latrobi Williams & Lichtwardt, 1990 (in Lichtwardt and Williams, 1990)
Thalli short to more than 2 mm long. Producing within the thallus a uniseriate or biseriate row of uninucleate, oval to angular, primary infestation sporangiospores measuring (25-)31-35 x 15-18 µm; or the thallus dividing to form a row of sporangia, each producing one binucleate secondary infestation sporangiospore measuring 40-70 x 15-19 µm.
Illustrations: Fig. 11.79.
Host: Porcellio scaber (Isopoda, Porcellionidae).
Distribution: Victoria, Australia.
Reference: Lichtwardt and Williams, 1990.
Parataeniella
mercieri (Poisson) Poisson,
1929
= Eccrinopsis mercieri Poisson, 1928
Thalli 170-180(-300) µm long by 10-12(-15) µm diam. Secondary infestation sporangiospores 2- to 4-nucleate, 20-25(-35) µm long, or uninucleate and more or less isodiametric, 10-12 µm. Primary infestation sporangiospores uninucleate, ellipsoidal, uniseriate within the thallus (sporangium), 25-30 x 10-12 µm. Thalli may produce series of secondary infestation sporangia terminally and a primary infestation sporangium basally in the same thallus. Type species.
Illustrations: Fig. 11.224.
Hosts: In posterior hindgut of Oniscus asellus L. and Tracheoniscus rathkii (Brandt) (Isopoda, Oniscidae).
Distribution: Terrestrial, in France (Pyrénées-Orientales, Hérault, Calvados), and Germany.
This fungus was first discovered, but not named, by Mercier (1914). Scheer (1976b) reported Parataeniella mercieri to be common in Oniscus asellus in many sites in Germany, but less common in Tracheoniscus rathkii.
References: Poisson, 1928, 1929; Mercier, 1914; Scheer, 1976b.
Parataeniella
scotonisci Manier ex Manier,
1970b (1969b)
[= Parataeniella scotonisci Manier, 1964d, nom. nud.]
Thalli up to 80 µm long by 3.5-9 µm diam. Secondary infestation sporangiospores more or less biconical, uni- or binucleate. Primary infestation sporangiospores becoming binucleate, thick-walled, 11-14.5 x 2.5-4.5 µm, uniseriate or biseriate in the thallus (sporangium).
Illustrations: Fig. 11.225.
Host: In hindgut of Scotoniscus marcomelos Racovitza (Isopoda, Trichoniscidae).
Distribution: In caves, Pyrénées Mountains, France.
The cave-dwelling hosts of this small eccrinid, Parataeniella
scotonisci,
were collected in several different caves. Most of the adults, but
not
immature specimens, were infested. Manier (1964d) also reported Enterobryus
gracilis (nom. dub.) from a cavernicolous millipede. [For
other
cavernicolous millipede hosts with Enterobryus spp., see
Reeves, 2000.]
References: Manier, 1964d, 1969b (1970b).
Léger & Duboscq, 1929a
Thalli coenocytic and unbranched, entire protoplast producing
amoeboid cells
that encyst and form cystospores; or, in some, producing elongate
spores with
rigid walls. Attached by a secreted holdfast to the external cuticle
(exoskeleton) or hindgut cuticle of aquatic Crustacea or Insecta.
Consisting of the single family Amoebidiaceae.
Lichtenstein, 1917a
Characters same as those of the order. Two genera.
Type genus: Amoebidium Cienkowski.
Amoebidium
Cienkowski, 1861
Thalli on external cuticle (exoskeleton), more rarely in rectum, of fresh water Crustacea or Insecta. Producing uninucleate sporangiospores, or uninucleate, teardrop-shaped amoeboid cells that encyst and form elongate cystospores. Five species.
<>Type species: Amoebidium parasiticum Cienkowski.
Amoebidium appalachense Siri, White & Lichtwardt, 2006
Thalli cylindrical with a very short discoid holdfast, about 55-80 x 4-6(-8) µm at maturity, producing either (a) allantoid sporangiospores (15-)21(-25) x (1.5-)2.8(-4) µm, occasionally straight or almost lunate, or (b) motile teardrop-shaped amoebae about 20 µm long by 6-8 µm diameter near broader anterior end, forming spherical cysts initially about 6-8 µm diameter.
Illustrations: Fig. 11.280.
Hosts: Attached to anal tubules of Chironomus sp. larvae.
Distribution: Great Smoky Mountains National Park, USA.
Amoebidium appalachiense is most
similar to
A. colluviei, a species described by Lichtwardt (1997)
attached to the
anal tubules of Chironomus sp. larvae in a polluted stream in
Monteverde, Costa Rica. Thalli of A. appalachiense are
narrower, and
the sporangiospores are shorter and narrower. Two axenic cultures,
TN-27-A3 and
TN-46-A6, from two different sites were obtained.
References: White, Siri and Lichtwardt, 2006; Lichtwardt, 1997.
Amoebidium australiense Lichtwardt & Williams, 1992
Mature thalli cylindrical, up to 300 x 20 µm, rarely wider. Holdfast 7-13 µmlong x 20 µm diam. Released amoebae form an ellipsoidal walled cell that develops directly into a thallus.
Illustrations: Fig. 11.92.
Host: On external surfaces of Chironomus oppositus group (Diptera, Chironomidae).
Distribution: Western Australia, Australia.
Reference: Lichtwardt and Williams, 1992.
Amoebidium colluviei Lichtwardt, 1997
Thalli usually less than 80 mm long by about 10 µm diameter, producing allantoid sporangiospores 25-32 x 6-10 µm.
Illustration: Fig. 11.136.
Host: On external surfaces (primarily anal papillae) of Chironomidae and Simuliidae (Diptera).
Distribution: Costa Rica.
Reference: Lichtwardt, 1997.
Amoebidium
parasiticumCienkowski, 1861
= Amoebidium fasciculatum Lichtenstein, 1917a
[= Amoebidium poissoni Duboscq, Léger & Tuzet, 1948, nom.
nud.]
Thalli cylindrical to fusiform, variable in length and width, with a short holdfast. Sporangiospores typically lunate, or allantoid or fusiform, variable in number, 15-50 x 5-10 µm. Upon molting of the host producing amoebae that encyst. Cysts 6-32 µm diam, later forming one to many elongate cystospores 12-30 µm long. Type species.
Illustrations: Fig. 11.39.
Hosts: Widespread among Crustacea and Insecta, on external cuticle. Crustacea: Cladocera, Copepoda, Branchiopoda, Amphipoda (Gammaridae), and Isopoda (Asellidae), Insecta: larvae of Diptera (Chironomidae, Culicidae), Ephemeroptera, Trichoptera, and Odonata (in rectum).
Distribution: Probably worldwide, in freshwater, mostly lentic, habitats. Reported from Czech Republic, Denmark, England, France, Israel, Japan, Philippines, Poland, Puerto Rico, Singapore, Spain, Tunisia, and USA.
Amoebidium parasiticum, the only ectozoic trichomycete, shows little host specificity, and has even been reported to attach to inanimate objects (see Table 7.2), but not necessarily to grow to maturity on them. Although widespread geographically and abundant in given sites, it is not always easy to find this species in nature. In the authors' experience it is more likely to be found in pools or ditches that are polluted with organic matter. It was the first trichomycete to be cultured axenically (Whisler, 1960) (see Chapter 3 for methods), and as a consequence of its cultivation, the species has been used in many laboratory studies. These are discussed at length in Chapter 9. Of special interest are the factors that cause a developmental shift in thalli from sporangiospore to amoeba production (amoebagenesis) when hosts molt or are injured (also see Chapter 8).
Manier and Raibaut (1969) have produced a film on the life cycle of A. parasiticum (described in Chapter 7). Some aspects of the fine structure in this species have been studied (Whisler and Fuller, 1968; Coste-Mathiez, 1970; Dang, 1979). Poisson (1931b) claimed to have seen fusion of amoebae, but this has not been substantiated.
Cienkowski (1861) described and illustrated an interesting parasite of A. parasiticum, which he named Basidiolum fimbriatum. It somewhat resembles a Syncephalis van Tiegh. & Le Monnier (Zygomycetes), whose species, with one exception, are parasites of Mucorales. Despite abundant references to A. parasiticum, this parasite does not appear to have been collected and studied since that one report.
References: Cienkowski, 1861; Lichtenstein, 1917a, 1917b;
Lieberkühn, 1856;
Schenk, 1858; Moniez, 1887; Fritsch, 1895; Labbé, 1899; Chatton, 1906a,
1906b,
1908, 1920, 1925; Chatton and Roubaud, 1909; Raabe, 1911a, 1911b, 1912;
Lichtenstein, 1917a, 1917b; Debaisieux, 1920; Taylor, 1928; Taylor and
Colton,
1928; Poisson, 1931b; Margalef, 1946; Duboscq et al., 1948; Tuzet and
Manier,
1951b; Johnson, 1952, 1963; Whisler, 1960, 1961, 1962, 1966, 1968,
1978, 1979;
Whisler and Fuller, 1968; Borut, 1964; Trotter and Whisler, 1965;
Manier, Rioux
and Juminer, 1964; Coste-Mathiez, 1970; Sangar et al., 1972; Kuno,
1973;
Lichtwardt, 1976; Manier, 1962c, 1969b (1970b); Manier and Raibaut,
1969, 1970;
Coste-Mathiez, 1970; Grizel, 1971; Dogma, 1975; Cerniglia et al., 1978;
Dang,
1979; Moss, 1979; Porter and Smiley, 1979.
Amoebidium recticola Chatton, 1906b
Thalli curved, the basal region curved sharply inward, averaging 100 mm long by 15-18 µm diam. Holdfast 12 x 6 µmdiam. Producing short-cylindrical to oval sporangiospores 8-12 µm long, or amoeboid cells that encyst. Cysts 7-12 µm diam.
Illustrations: Fig. 11.205.
Host: Attached to rectal peritrophic membrane of Daphnia magna Straus and D. pulex (de Geer) (Crustacea, Cladocera).
Distribution: Aquatic, in reptile tanks at the Paris Museum, France.
Amoebidium recticola differs from the more commonly encountered ectozoic A. parasiticum in the morphology of the thalli and sporangiospores, as well as its location within the host. Although species of Paramoebidum, an endozoic genus, are attached to the hindgut cuticle of aquatic insect larvae, A. recticola is clearly not a Paramoebidium, because it produces sporangiospores. Furthermore, its location in the rectum of the host and mode of entry into the hindgut are different from Paramoebidium spp.
According to Chatton (I906b, 1920), A. recticola is attached to the inner surface of the "rectal peritrophic membrane" of daphnids. This rectal membrane is a loose tube attached only at the very anterior region of the hindgut, and apparently is formed by the hindgut epithelium, then peeled off (except for the anterior end) by a molting process as a new hindgut cuticle develops on the epithelium. Daphnids also have the type of midgut peritrophic membrane produced by many arthropods, which develops as a loose sleeve in the midgut but originates in the foregut. In Daphnia magna the anterior membrane continues to grow backward into the hindgut, inside the rectal membrane, and usually projects from the anus. Amoebidium recticola is located between the two membranes, and is not in direct contact with either the hindgut cuticle itself or the food bolus, as are thalli of Paramoebidium spp. Also, Paramoebidium spp. infest the hindgut after ingestion of cysts (or cystospores) by the host. In A. recticola spores enter through the anus and attach to the rectal membrane. This is accomplished, according to Chatton, as a result of the rhythmic dilations and contractions of the rectum, which is a respiratory process. As water is drawn into the rectum, so are spores of A. recticola. By placing minute granules of carmine near the anus of daphnids, Chatton was able to demonstrate that the granules were aspirated into the rectal lumen between the two membranes, as with A. recticola spores. It is interesting that the spores were never attached to the inner (anterior) peritrophic membrane.
Several developmental stages of A. recticola are of interest to compare with A. parasiticum. Thalli of A. recticola occasionally attached to the outside (new) integument of daphnids, but then degenerated. Amoeboid cells were produced either from thalli in the rectum of dead daphnids or from expelled sporangiospores settled on the bottom of a container. Such expelled spores were also observed to grow and produce a limited number of sporangiospores, Chatton never saw cystospores in A. recticola, but they are rarely seen in A. parasiticum either, whose cystospores usually form after a resting period.
References: Chatton, 1906b, 1920; Chatton and Roubaud, 1909; Le
Berre,
1967.
Paramoebidium
Léger & Duboscq, 1929c
Thalli attached to hindgut cuticle (or anal gills) of freshwater larvae of Insecta. Producing uninucleate, teardrop-shaped amoeboid cells that encyst and form elongate cystospores. No sporangiospores produced. Twelve species.
Type species: Paramoebidium inflexum Léger & Duboscq.
Paramoebidium species are very common in lotic populations of larval Plecoptera, Ephemeroptera, and Diptera (Simuliidae, rarely Chironomidae) throughout many parts of the world. They grow like weeds, and often can be found even when other trichomycetes (Harpellales) are not present in those kinds of insects.
Other species of Paramoebidium have been described, but the only valid species are those listed below. The illegitimate species names are listed in the next section of this Chapter. In many but not all cases, they differ from each other mostly on the basis of the hosts they were discovered in. Until such time as better criteria can be found to differentiate them, it seems advisable to let them remain as nomina nuda. A major problem in determining the range of variation in morphological characters and host specificity is that no Paramoebidum sp. has been cultured axenically. The authors have collected Paramoebidium extensively in many geographical areas, and have records of considerable morphological variation in thallus size and shape among theircollections, but these are not always consistent in given species or families of hosts. The reproductive phases (amoebae, cysts, cystospores), where they have been seen, do not appear to be useful characters to differentiate species of Paramoebidium. Given the wide distribution and abundance of Paramoebidium, it is probable that at least some of the species are not very host specific.
Occasionally one finds Paramoebidium thalli attached to
thalli of
Harpellales cohabiting the hindgut, or vice versa; or thalli of Paramoebidium
attached to thalli of its own species (see Table
7.2).
Paramoebidium
argentinense Mazzucchelli,
López Lastra & Lichtwardt, 2000
(in Lichtwardt, López Lastra and Mazzucchelli, 2000)
Thalli may be more than 600 x 30 mm, widest near the middle, bearing at the apex a small papillum 15-20 x 5-8 µm.
Illustrations: Fig. 11.57.
Host: Baetodes sp. (Ephemeroptera: Baetidae).
Distribution: Argentina.
Reference: Lichtwardt et al., 2000.
Paramoebidium bacillare Strongman, Juan Wang & S.Q. Xu, 2010
Thallus attached to the hindgut lining by a lateral bulbous holdfast
and fibrous secreted material. Thallus stonngly constricted at the
holdfast, developing unequally from the holdfast into a large anterior
arm tapered distally and a smaller posterior arm that develops after
the anterior arm has partially extended. Attached to hindgut of
stonefly nymphs.
Illustrations: Fig. 11-354.
Host: Leuctridae, Plecoptera.
Distribution: Shaanxi Province, China.
Reference: Strongman, Wang, and Xu, 2010.
Paramoebidium bibrachium Williams & Lichtwardt, 1990
Thalli up to 2300 µm in length, diam. up to 180 µm, decreasing slightly near the ends. Holdfast becoming cup shaped and located laterally at or near the middle of the mature thallus, the thallus often slightly bent in the holdfast region. One arm of the thallus often of greater diam.
Illustration: Fig. 11.94.
Host: Coloburiscus humeralis and Deleatidium sp. (Ephemeroptera, Leptophlebiidae).
Distribution: South Island, New Zealand.
Reference: Williams and Lichtwardt, 1990.
Paramoebidium cassidula Strongman & M.M. White, 2006
Thallus compact, bending tightly around a glued holdfast, giving the mature thallus a clamp-like appearance. Mature thalli typically 100-200 x 50-90 µm, releasing amoebae (approximately 21 x 8 µm) that encyst (12 µm diameter). Cystospores, 1-4 per cyst, kidney-shaped (10.5-16.5 x 6.5-7 µm) or spherical (~8 µm). Both forms of cystospores can occur in the same cyst.
Illustrations: Fig. 11.312.
Host: Paracapnia angulata nymphs (Plecoptera, Capniidae).
Distribution: Nova Scotia and Prince Edward Island, Canada.
Reference: Strongman and White, 2006, Strongman,
2007.
Paramoebidium
corpulentum Lichtwardt &
Williams, 1991
(in Lichtwardt, Peterson and Williams, 1991)
Thallus up to 300 µm long, more or less elongate-obpyriform at maturity and curved at the base, 30-90 µm diam. Holdfast usually located at the base of the mature thallus.
Illustrations: Fig. 11.159.
Host: Allocapnia spp. (Plecoptera, Capniidae).
Distribution: Several states in eastern USA, Idaho, and Great Smoky
Mountains National Park. Prince Edward Island, Canada.
Reference: Lichtwardt et al., 1991; White, Siri and Lichtwardt,
2006, Strongman, 2007. Beach and White, 2012.
Paramoebidium curvum Lichtwardt, 1979, in Dang and Lichtwardt, 1979
Thalli 140-280 x 20-60 µm, curved. Holdfast somewhat lateral on the incurved side of the thallus. Amoebae -20 x 8 µm Cysts spherical, enlarging to produce 1-14 fusiform to lunate cystospores 45-50 x 7-8 µm..
Illustrations: Fig. 7.24; Fig. 11.40.
Hosts: Attached to very posterior hindgut or to anal gills of larval stages of many species of Simuliidae (Diptera).
Distribution: Lotic habitats in USA (Arizona, Colorado, Kansas,
Montana,
Utah, Wyoming), Sweden, France, and England. Armenia. Ontario and
Prince Edward Island, Canada.
Simuliid (blackfly) larvae frequently have in their hindgut, but located more anteriad, another Paramoebidium sp. with larger thalli resembling P. inflexum. These two species may be found in the same gut, or either separately. When P. curvum thalli are attached to the retractable anal gills of blackfly larvae, they may be seen without dissecting the larva, provided the gills are extended. Paramoebidium curvum has a sausage-shaped thallus similar to Amoebidium recticola in the rectum of daphnids, and it was undoubtedly P. curvum that Chatton and Roubaud (1909) saw on the anal gills of two Simulium spp., but thought it might be A. recticola.
While conducting an electron microscopic study of P. curvum, Dang (1978) (Dang and Lichtwardt, 1979) discovered some virus-like particles in the cytoplasm. Previously, Manier et al. (1971) had found similar but smaller, virus-like particles in P. arcuatum (nom. nud.). See the last section in Chapter 7.
References: Dang and Lichtwardt, 1979; Lichtwardt, 1973a, 1976;
Chatton and
Roubaud, 1909; Dang, 1978, Nelder et al., 2005, Strongman and White,
2008, Strongman, 2007..
Paramoebidium
digitoideum Ferrington,
Lichtwardt & López Lastra, 1999
(in Lichtwardt, Ferrington and López Lastra, 1990)
Thalli essentially straight and cylindrical, up to 340 µm long by 10-22 µm diam., with an inconspicuous basal holdfast.
Illustration: Fig. 11.59.
Host: In Notonemouridae (Plecoptera) nymphs.
Distribution: Argentina.
Reference: Lichtwardt, Ferrington and López Lastra, 1990
Paramoebidium grande Lichtwardt & Arenas, 1996
Thalli curved to almost straight, up to 800 x 60 µm. Amoeboid cells 30-80 x 10-15 µm. Cysts enlarging to 35-60 µm diam., producing 2-10 usually allantoid cystospores 35-60 x 8-10 µm.
Illustrations: Fig. 11.83.
Hosts: Simulium spp. (Diptera, Simuliidae).
Distribution: Chile. Idaho, USA.
Reference: Lichtwardt and Arenas, 1996. Beach and White, 2012.
Paramoebidium
hamatum Bench & M.M. White.
Elongated thalli hooked basally, with one-eighth to one-third of the thallus length consisting of the curved portion Mature thalli variable, 150-800(-1120) x 10-60 µm long, producing amoebae that encyst after release; cysts 9-10 µm diam. Thalli with a secreted basal holdfast, attached to the hinguts of Chironomidae (midge) larvae as well as Ameletidae and Baetidae (mayfly) nymphs..
Illustratons Fig. 381.
H osts: Chironomidae and Ameletidae and Baetidae (Ephemeroptera).
Distribution: Idaho, USA.
Reference: Beach and White, 2012.
Paramoebidium inflexum Léger & Duboscq, 1929c
Thalli 1 mm x 21 mm, 700 x 7-8 µm, or 380 x 50-55 µm, the first two types sharply bent. Holdfast basal. Amoebae ~15 µm long. Cysts spherical, (12-)25-30(-50) µm diam. Cystospores 6-36 per cyst, elongate and slightly curved, averaging 15 x 6 µm. Type species.
Illustrations: Fig. 11.219.
Host: In hindgut of larval Nemoura variegata Oliv. (Plecoptera, Nemouridae).
Distribution: In alpine streams, France.
Duboscq et al. (1948) provided a fuller description of the developmental stages of Paramoebidium inflexum.
References: Léger and Duboscq, 1929c; Duboscq et al., 1948.
Paramoebidium papillatum Lichtwardt & Williams, 1992
Thalli up to 2300 mm long, diam up to 175 µm. Holdfast a depressed area located laterally about 1/5 to 1/3 from one end, the shorter arm bearing a small papilla 12-18(-25) x (5-)6-7 µm.
Illustration: Fig. 11.91.
Host: Nesameletus sp. (Ephemeroptera, Siphlonuridae).
Distribution: South Island, New Zealand.
Reference: Lichtwardt and Williams, 1992.
Paramoebidium stipula Strongman & M.M. White, 2006
Thalli variable in length and width, attached to hindgut membrane by a cemented holdfast. After a period of elongation, the thallus bends, and then growth occurs in both directions from that point, producing a stalk (30-80 x 20-45 µm) and two unequal branches. Mature thalli are about 650-700 µm in total length and typically 45 µm wide. Amoebae released from mature thalli encyst in the thallus or on the hindgut membrane and are about 18 µm in diameter. No cystospore observed.
Illustrations: Fig.
11.313.
Host: Nemouridae nymph (Plecoptera).
Distribution:
Reference: Strongman and White, 2006.
Paramoebidium
umbonatum Strongman & M.M. White, 2008.
Thallus unbranched 200-300 x 8-22 µm, attached to hindgut lining by a
conspicuous knob-like basal holdfast. Thallus recurved near the base,
with a protuberance on the outer side of the bend. The distal end of
the thallus swollen, with a small pipilla (6-12 µm).
Illustrations: Fig. 11.340.
Host: In hindgut of Haprophlebia
vibrans Needham nymphs (Ephemeroptera, Leptophlebiidae).
Distribution: Outflow from Costello Lake, Algonquin Provincial Park,
Ontario, Canada.
Reference: Strongman and White, 2008.
In this section are listed genera and species that are not
acceptable, and consequently are not included in the preceding
taxonomic treatment. Synonyms (both valid and illegitimate names) of
valid species will not be found in the list below, but rather are
placed under the accepted names.
The citation nomen nudum (nom. nud.) indicates that the taxon has not been validly published according to the International Code of Botanical Nomenclature, in most cases because no Latin diagnosis and nomenclatural type have been provided in accordance with Art. 36 and 37, or there is essentially no description that distinguishes it from other taxa (Art. 32). In these instances we have not validated the taxa, because they do not appear to warrant doing so without further study of the fungi. This is best done by obtaining fresh material. Unfortunately, type specimens of trichomycetes, usually consisting of prepared slides, would have limited value in resolving the taxonomic judgments in question.
The citation nomen dubium (nom. dub.) indicates that the taxon, although technically valid, in our opinion cannot be satisfactorily typified due to an insufficient description or questionable interpretation of the fungal material described.
The last section of Chapter 12 has brief accounts of several gut organisms that have similarities to the trichomycetes but are not related.
Amoebidium cienkowskianum Moniez, 1887, nom. nud. No description.
A. pauliani Manier, 1955c, nom. nud. Possibly an Enterobryus.Arundinula incurvata Léger & Duboscq, 1905a, nom. nud.
A. porcellanae Léger & Duboscq, 1911, nom. dub.Asellaria scutigerae Manier, 1950, nom. nud. May not be a trichomycete.
A. spirostrepti Tuzet, Manier & Jolivet, 1957, nom. nud.Astreptonema siphonoecetis Grizel, 1971, nom. provisorium.
Capillus Granata, 1908, nom. dub.
C. intestinalis Granata, 1908, nom. dub. Possibly an Enterobryus.Cestodella Tuzet, Manier, & Jolivet, 1957, nom. nud. Type species (C. straeleni) and other species probably are Enterobryus spp.
C. iuli Maessen, 1955, nom. dub.
C. allopori Tuzet & Manier, 1957a, nom. nud.Daloala Tuzet, Manier & Vogeli-Zuber, 1952, nom. nud.
C. attenuata Tuzet & Manier, 1957a, nom. nud.
C. glandulosa Tuzet, Manier, & Jolivet, 1957, nom. nud.
C. operculata Tuzet, Manier, & Jolivet, 1957, nom. nud.
C. pachyboli Tuzet & Manier, 1957a, nom. nud.
C. parva Tuzet & Manier, 1957a, nom. nud.
C. pseudonannolenis Tuzet & Manier, 1957a, nom. nud.
C. rhinocrici Tuzet & Manier, 1957a, nom. nud.
C. straeleni Tuzet, Manier, & Jolivet, 1957, nom. nud.
D. dixae Poisson, 1932b, nom. dub. Possibly a Smittium.Eccrina Leidy, 1850b. Genus indistinguishable from Enterobryus Leidy; refer to the valid species Enterobryus moniliformis (Leidy) Lichtwardt.
E. brevis Maessen, 1955, nom. dub.Eccrinella Léger & Duboscq, 1933. = Astreptonema Hauptfleisch, 1895; see valid species A. gammari (Léger & Duboscq) Manier, and A. corophii (Manier) Manier.
E. gigantea Tuzet & Manier, 1954b, nom. nud.
E. longa Leidy, 1850b, nom. dub. First of two species of Eccrina described by Leidy, but description insufficient.
E. longipes Maessen, 1955, nom. dub.
E. montana Maessen, 1955, nom. dub.
E. pseudoramosa Maessen, 1955, nom. dub.
E. uncigeri Maessen, 1955, nom. dub.
Eccrinoides stammeri Maessen, 1955, nom. dub.
Eccrinopsis Léger & Duboscq, 1916. Type species = Enterobryus hydrophilorum (Léger & Duboscq) Manier.
E. brachyspiroboli Tuzet, Manier & Jolivet, 1957, nom. nud.Genistella choanifera Tuzet & Manier, 1953, nom. nud. = Typhella choanifera (Tuzet & Manier) Manier & Mathiez, 1965, nom. nud. Probably a Smittium.
E. bresiliensis Tuzet & Manier, 1951a, nom. nud. = Pistillaria bresiliensis (Tuzet & Manier) Jeekel, Tuzet, Manier & Jolivet, 1959, nom. nud.
E. broelemanni Duboscq, Léger & Tuzet ex Manier, 1970b (1969b), nom. dub.
E. doscari Manier, 1950, nom. nud. May not be an Enterobryus.
E. duboscqui Tuzet & Manier ex Manier, 1968, nom. dub. Probably not an Enterobryus.
E. eurydesmi Tuzet & Manier, 1957a, nom. nud.
E. fertilis Tuzet & Manier, 1957a, nom. nud.
E. flavus Maessen, 1955, nom. dub. = Pistillaria flavus (Maessen) Jeekel, Tuzet, Manier, & Jolivet, 1959, nom. nud.
E. gracilis Duboscq, Léger & Tuzet ex Manier, 1970b (1969b), nom. dub. May not be an Enterobryus.
E. helocharei (Poisson) Manier, 1970b (1969b), nom. nud. Trichella helocharei Poisson, 1931a, nom. nud.
E. hyalinus Léger & Duboscq" nom. provisorium.
E. inflatus Duboscq, Léger & Tuzet, 1948, nom. nud.
E. iuli-terrestris Robin, 1853, nom. dub.
E. leptodesmi Tuzet & Manier, 1957a, nom. nud.
E. nudatus Tuzet, Manier & Jolivet, 1957, nom. nud.
E. orthomorphae Tuzet & Manier, 1957a, nom. nud.
E. pennatus Tuzet, Manier & Jolivet, 1957, nom. nud.
E. pentodoni (Manier) Manier, 1970b (1969b), nom. nud. Basionym illegitimate. = Paratrichella pentodona Manier, 1947, nom. nud.
E. philhydri (Poisson) Manier, 1970b (1969b), nom. nud. = Trichella philhydri Poisson, 1931, nom. nud. Probably not an Enterobryus.
E. pseudoeurydesmi Tuzet & Manier, 1957a, nom. nud.
E. rectus Duboscq, Léger & Tuzet ex Manier, 1970b (1969b) nom. dub.
E. robini Duboscq, Léger & Tuzet ex Manier, 1970b (1969b), nom. dub. May not be an Enterobryus.
E. sao-pauloi Tuzet & Manier, 1951 a, nom. nud.
E. schubarti Tuzet & Manier, 195 1 a, nom. nud.
E. seychelloboli Tuzet & Manier, 1957a, nom. nud.
E. spiralis Leidy, 1849b, nom. dub. Description insufficient.
E. spirostrepti Tuzet & Manier, 1957a, nom. nud.
E. strongy1osomae Duboscq, Léger & Tuzet, 1948, nom. nud.
E. tumidus, Duboscq, Léger & Tuzet, 1948, nom. nud.
E. vulgaris Tuzet, Manier, & Jolivet, 1957, nom. nud.
G. mailleti Tuzet & Manier, 1955, nom. nud. Probably = Legeriomyces ramosus Pouzar.Lactella Maessen, 1955, nom. dub. Generic characters similar to Enterobryus.
G. rhitrogenae Tuzet & Manier, 1955, nom. nud.
L. aphodii Maessen, 1955, nom. dub.
L. cercyonis Maessen, 1955, nom. dub.
L. chaetarthriae Maessen, 1955, nom. dub.
L. coelostomatis Maessen, 1955, nom. dub.
L. helocharidis Maessen, 1955, nom. dub.
L. laccobii Maessen, 1955, nom. dub.
L. philhydri Maessen, 1955, nom. dub.
L. platystethi Maessen, 1955, nom. dub.
Microasellaria Tuzet, Manier, & Jolivet, 1957, nom. nud.
M. funicularia Tuzet, Manier, & Jolivet, 1957, nom. nud.Microeccrina Maessen, 1955, nom. dub. Probably related to the prokaryotic genus Arthromitus (see last section of Chapter 12).
M. fertilis Maessen, 1955, nom. dub.Microtrichella Maessen, 1955, nom. dub. Probably related to the prokaryotic genus Arthromitus (see last section of Chapter 12).
M. glomeri Maessen, 1955, nom. dub.
M. iuli Maessen, 1955, nom. dub.
M. leptophylli Maessen, 1955, nom. dub.
M. ligidii Maessen, 1955, nom. dub.
M. orthomorphae Maessen, 1955, nom. dub.
M. parva Maessen, 1955, nom. dub.
M. siccophila Maessen, 1955, nom. dub.
M. hydrophilorum Maessen, 1955, nom. dub.Nodocrinella Scheer, 1977, nom. nud.
O. digitata, Léger & Gauthier, 1932, nom. nud. Probably a Stachylina.Paramoebidium arcuatum Léger & Duboscq ex Duboscq, Léger & Tuzet, 1948, nom. nud. = P. arcuatum Léger & Duboscq, 1929c, nom. nud.
Trichella Poisson, 1931a, nom. nud. Generic name used provisionally by Léger & Duboscq, 1929a; no description. First species assigned to genus by Poisson, 1931a, but without a generic description. Type species, T. hydrophilorum, now an Enterobryus.
T. choanifera (Tuzet & Manier) Manier & Mathiez, 1965, nom. nud. = Genistella choanifera Tuzet & Manier, 1953, nom. nud.