Telogaster opisthorchis MacFarlane, 1945

Hechinger, Ryan F., 2012, Faunal survey and identification key for the trematodes (Platyhelminthes: Digenea) infecting Potamopyrgus antipodarum (Gastropoda: Hydrobiidae) as first intermediate host, Zootaxa 3418, pp. 1-27 : 15-17

Telogaster opisthorchis MacFarlane, 1945

(10. Teop; Figs. 1 , 19–20 )

Stages: rediae and cercariae

Host: Potamopyrgus antipodarum

Site in host: Rediae in gonad, digestive gland, basal visceral mass, and mantle.

Voucher locality: Waimakariri River, South Island (-43.4148o lat, 172.6517o long)

Prevalence: 5% (n = 100)

Specimens deposited: USNPC #: 105683

Diagnosis: Redia translucent, elongate (~5:1 to 9:1 length:width), gradually tapering anterior to posterior. Length up to ~2000. Cercaria embryos number up to over 50, typically tightly packed and exhibit very pronounced posterior to anterior developmental gradient. Pharynx appears to be relatively small compared to S. anguillae or Lepocreadiid sp. II, <1/3 width of anterior redia body width.

Cercaria oculate, with dorso-ventral tail fin, no ventral sucker, with penetration glands. Main excretory collecting ducts frequently pronounced, sinusoidal, empty into small squarish bladder. Body length ~220–400. Tail length greater than 1.3 times body length. Tail fin originates dorsally ~1/5 into tail from base, continues around posterior tip to insert ~1/3 into tail from tip.

Descriptive notes: Redia pharynx <1/3 width of anterior redia. Cercaria tail fin originates dorsally ~1/5 into tail, continues around posterior tip, inserts ~1/3 into tail from tip.

Remarks: MacFarlane (1945) described T. opisthorchis and its life cycle. Cercariae encyst as metacercariae in fishes (particularly in muscles of small eleotrids) and infect eels ( Anguilla spp.) as final hosts. Cribb (1986) reported adults from eels in SE Australia, where P. antipodarum is introduced, and describes aspects of adult morphology.

MacFarlane (1952) contributed a forward-thinking ecological consideration of how host behavioral ontogeny interacts with parasite encounter rates to dictate patterns of infections in second intermediate hosts and final hosts for both T. opisthorchis and Stegodexamine anguillae (sp. 8). Kelly et al. (2010b) showed that infection of a threatened galaxiid fish second intermediate host results in deformities in juvenile fish, potentially with strong effects on recruitment to fish populations. Further, the widely used herbicide, glyphosate, can influence cercarial output by infected snails under laboratory conditions, and infection by metacercaria appears more likely to kill fish that are also exposed to the herbicide ( Kelly et al. 2010a).

Coitocaecum spp. ( C . parvum Crowcroft, 1945; and C . zealandicum Hine, 1977) (11, 12. Coit; Figs. 1 , 21–23 )

[It is almost certain that both of these congeners infect P. antipodarum , but are currently indistinguishable.]

Stages: sporocysts (daughter) and cercariae

Host: Potamopyrgus antipodarum

Site in host: Sporocysts in gonad, digestive gland, basal visceral mass, and mantle Voucher localities: Ngaruroro River, North Island (-39.3803o lat, 176.3326o long); Taieri River, South Island

(-45.2572o lat, 170.2716o long); Mataura River, South Island (-46.3894o lat, 168.7968o long) Prevalence: 6% at Ngaruroro River (n = 100); 8% at Taieri River (n = 100); 3% (n = 100) at Mataura River Specimens deposited: USNPC #s: 105684-105686

Diagnosis: Sporocysts sometimes active, translucent, elongate (~5:1 to 9:1 length:width), bluntly tapered at each both ends. Length up to ~2000. Cercaria number from ~10 to over 45, in various developmental stages lacking pronounced antero-posterior developmental gradient.

Cercaria non-oculate, with short glandular sucker-like tail, oral and ventral suckers, a two-pointed oral stylet ("a cotylocercous xiphidiocercaria"). Body length up to ~300. Tail length ~1/6 body length, not more than two times tail width. Stylet ~15 long.

Remarks: At least two species likely infect P. antipodarum : Coitocaecum parvum and C. zealandicum . MacFarlane (1939) described the life cycle of C. parvum and documented that it uses P. antipodarum as first intermediate host in New Zealand. However, he misidentified it as C. anaspidis Hickman 1934 , and this name has been widely promulgated in the literature (see Holton 1983; Holton 1984b). Adults of both C. parvum and C. zealandicum have been found in freshwater fishes on both North and South Islands ( Hine 1978; Hine et al. 2000; Holton 1983; Holton 1984b). It appears almost certain that C. zealandicum also infects P. antipodarum as first intermediate host as there is no obvious alternative first intermediate host for C. zealandicum to use. I list it here to foster its recognition in future surveys.

Coitocaecum parvum infects small crustaceans (e.g., mysidaceans, amphipods, copepods) as second intermediate hosts, where it can become progenetic (mature and produce eggs) while encysted ( Holton 1984a; Lefebvre & Poulin 2005; MacFarlane 1939). Coitocaecum zealandicum likely also used crustaceans as second intermediate hosts. However, this cannot be certain as opecoelids can infect a wide range of other invertebrates or even fishes ( Cribb 2005). As typical final hosts, C. parvum uses a range of fishes ( Crowcroft 1945; Holton 1983; Holton 1984b; MacFarlane 1939). Coitocaecum zealandicum has been reported from eels, torrent fish ( Cheimarrichthyidae ), and Gobiomorphus spp. ( Eleotridae ) ( Hine et al. 2000).

Coitocaecum parvum infection is associated with smaller and narrower snails compared to uninfected snails ( Lagrue et al. 2007a). This appears to be adaptive for the parasite by permitting an increased mass of reproductive tissues (sporocysts) for a given shell size ( Lagrue et al. 2007a). Lagrue et al. (2007b) developed markers for nine microsatellite (=short tandem repeat) loci, and Lagrue et al. (2007a) used this tool to show that multi-clone infections can occur in C. parvum first intermediate host infections.

A substantial amount of research has examined aspects of the biology, ecology, and evolution of C. parvum at other life stages, beyond the above citations. Interested readers can consult the literature for this work, most of which has been undertaken by Dr. Robert Poulin’s Evolutionary and Ecological Research Group at Otago University in Dunedin, South Island.

Coitocaecum parvum was originally described from Tasmanian adult stages ( Crowcroft 1945). If the Tasmanian and New Zealand C. parvum are actually the same species, it is possible that the parasite was introduced to Tasmania with P. antipodarum , which has been invasive in Tasmania since at least the 1800s ( Ponder 1988). Determining the first intermediate host used by C. parvum in Tasmania would clarify this matter.

Citing ICZN Cord Art. 33.3.1, Yoshida and Urabe (2005) argued that the original spelling of this genus (Coitocoecum Nicoll 1915) should be adopted. This may be due to a misunderstanding of what is meant by “prevailing use.” It is clear that prevailing use is of Coitocaecum , including attribution to Nicoll 1915, justifying maintaining the “incorrect” spelling as is done here.

Figures

FIGURE 1. General characteristics of the parthenitae and cercariae of the trematodes infecting Potamopyrgus antipodarum as first intermediate host. Microphallus sp. “ livelyi ” (sp. 13), whose embryos develop directly to metacercariae, is not figured. Species numbers and codes follow Table 1 and species accounts. Cercariae are all to scale, with additional magnified views of three small cercariae (indicated by dashed lines). Parthenitae are not to scale. Scale bars consistently indicate 100 µm.

FIGURES 19 – 20. Telogaster opisthorchis. 19, Redia, live, with embryonic cercaria being pressed out of birth pore. Scale bar = 100. Numerical scale division = 25. 20, Cercaria, live. Scale bar = 100. Numerical scale division = 10.

FIGURES 21 – 23. Coitocaecum spp. 21, Sporocyst, live (Taieri River Voucher). Scale bar = 100. Numerical scale division = 10. 22, Cercaria, live (photo of a Mataura River specimen different than voucher). Scale bar = 100. Numerical scale division = 10. 23, Close up of cercaria oral sucker showing two-pointed oral stylet, live (Ngaruroro River voucher). Scale bar = 15.