¹ SUNY Oneonta undergraduate student, Biology Department, SUNY Oneonta 2Assistant Professor of Invertebrate Zoology and Researcher, Biology Department and Biological Field Station, SUNY Oneonta

Cestodes of the fishes of Otsego Lake and nearby waters

Amanda Sendkewitz1, Illari Delgado1, and Florian Reyda2

INTRODUCTION This study of fish cestodes (i.e., tapeworms) is part of a survey of the intestinal parasites

of fishes of Otsego Lake and its tributaries (Cooperstown, New York) from 2008 to 2014. The survey included a total of 27 fish species, consisting of six centrarchid species, one ictalurid species, eleven cyprinid species, three percid species, three salmonid species, one catostomid species, one clupeid species, and one esocid species. This is really one of the first studies on cestodes in the area, although one of the first descriptions of cestodes was done on the Proteocephalus species Proteocephalus ambloplitis by Joseph Leidy in Lake George, NY in 1887; it was originally named Taenia ambloplitis.

Parasite diversity is a large component of biodiversity, and is often indicative of the

health and stature of a particular ecosystem. The presence of parasitic worms in fish of Otsego County, NY has been investigated over the course of a multi-year survey, with the intention of observing, identifying, and recording the diversity of cestode (tapeworm) species present in its many fish species. The majority of the fish species examined harbored cestodes, representing three different orders: Caryophyllidea, Proteocephalidea, and Bothriocephalidea.

METHODS

The fish utilized in this survey were collected through hook and line, gill net, electroshock, or seining methods throughout the year from 2008-2014. Cestodes were collected in sixteen sites throughout Otsego County. These sites included Beaver Pond at Rum Hill, the Big Pond at Thayer Farm, Canadarago Lake, a pond at College Camp, the Delaware River, Hayden Creek, LaPilusa Pond, Mike Schallart’s Pond in Schenevus, Moe Pond, a pond in Morris, NY, Oaks Creek, Paradise Pond, Shadow Brook, the Susquehanna River, the Wastewater Treatment Wetland (Cooperstown), and of course Otsego Lake. The specimens were then dissected and analyzed at the SUNY Oneonta Biological Field Station. The main organ examined was the intestine. However, other organs such as the stomach, pyloric cecae, heart, liver as well as the body cavity were also examined.

Cestode specimens collected were preserved either in 4% neutral-buffered formalin or in 100% ethanol. They were stained with Delafield’s Hematoxylin, dehydrated using a graded ethanol series, mounted in Canada balsam, and preserved as whole mount slides. The parasites were then studied with a light microscope and identified with the aid of a plethora of published scientific literature (i.e., all those listed in the References section). Representative specimens were also photographed with a digital camera. Electron microscopy was also used to aid in the identification of the cestodes. ____________________________

RESULTS

Among the fish examined, ~120 of the 400+ fish that were examined were infected with either adult or juvenile cestodes. To date, adult specimens of eight species, representing four genera and three orders of cestodes, were encountered in Otsego Lake or in nearby water bodies. The caryophyllid cestode Glaridacris catostomi (Figure 1) occurred in Catostomus commersoni and in Hypentelium nigricans. At least four species of Proteocephalus were also encountered. Proteocephalus cf ambloplitis (Figure 2) occurred in Micropterus dolomieu, Micropterus salmoides, and A. rupestris. Proteocephalus cf longicollis (Figure 3) occurred in Coregonus clupeaformis. Proteocephalus cf pinguis (Figure 4) occurred in Esox niger. Proteocephalus cf pearsei (Figure 5) occurred in Perca flavescens. Additional specimens of Proteocephalus that were encountered but not identified to species were found in the fish species Lepomis gibbosus, Catostomus commersonii, Coregonus clupeaformis, Salvelinus nemaycush, Cottus cognatus, and Noturus insignis. Each Proteocephalus species had distinctive scolex and bothrial features in combination with features of the strobila, but preliminary morphological examinations did not enable species-specific identification, owing to the lack of adequately mature specimens and the limitations in the reference taxonomic literature. Hence, the “cf” designation was given for each of the three Proteocephalus species encountered. The bothriocephalid cestode Bothriocephalus cuspidatus (Figure 6) occurred in Perca flavescens and in Sander vitreus. Another bothriocephalid cestode, Bothriocephalus acheilognathi (Figure 7), was found in Semotilus atromaculatus and in Notemigonus crysoleucas in a beaver pond at the base of Rum Hill. Additional specimens of Bothriocephalus that were not identified to species–i.e., they may or may not be conspecific with those mentioned above–were found in Micropterus salmoides, Lepomis gibbosus, Lepomis macrochirus, Ambloplites rupestris, Perca flavescens and Notropis heterodon. These specimens were limited in number and were generally not sexually mature, precluding specific identifications. Finally, a species of Eubothrium was found in Salvelinus nemaycush, but additional specimens of that taxon are needed to make a specific identification possible.

The juvenile cestodes encountered represented two genera of different cestode orders, Proteocephalus and Bothriocephalus. Unknown cestodes awaiting identification were also found in Ameiurus nebulosus, and Pimephales promelas.

DISCUSSION

Out of all the parasitic worms encountered during the survey, the cestodes were observed

the least frequently. Among those cestodes encountered, many were sexually immature. This is a problem because it limited our ability to make firm identifications. For example, our identifications of the species of Proteocephalus encountered in this survey were based on scolex morphology. Fully confirmed identifications would, however, require us to examine proglottid morphology in addition to scolex morphology. This was not an option owing to the generally lack of sexually mature specimens. In this study, species of Proteocephalus were therefore only tentatively identified to species, hence designated “cf”. This abbreviation is for the Latin word “confer”, meaning compare to the form in this taxonomic context. More work is needed to properly identify the species. Another limitation with identifying species of Proteocephalus is a lack of complete and useful reference in the taxonomic literature.

At least two species of Bothriocephalus were observed in this study, Bothriocephalus cuspidatus and Bothriocephalus achelognathi. The latter of the two is an invasive species of tapeworm, it was only found in one pond however, this finding is a first for New York state; B. cuspidatus has previously only been reported elsewhere in North America. Additional specimens of the species of Eubothrium that was encountered in Lake trout are needed to identify that tapeworm to species.

CONCLUSION

Furthering our understanding of the cestode species of Otsego Lake and nearby water

bodies will require the collection of additional specimens of Proteocephalus and Eubothrium that are sexually mature, to facilitate specific identifications.

ACKNOWLEDGMENTS

We would like to thank the students of Dr. Reyda’s Lab, the numerous summer interns from SUNY Oneonta, Steve Stowell, (SUNY Cobleskill) and Tim Pokorny (NYS DEC), for their help in fish and snail collections. We thank Anindo Choudhury (St. Norbert College) for his helpful comment on species identifications. Funding for this research was provided in part an NSF FSML grant to W. Harman (DBI 1034744). Also, special thanks to Dr. Bill Harman, Matt Albright, and Holly Waterfield of the Biological Field Station, and Dr. Janine Caira of the University of Connecticut. SUNY Biological Field Station provided the necessary equipment and work space to carry out this project. This work was done as an independent study by A.S. and I.D. over the course of three semesters.

REFERENCES

Andersen, K. 1979. Studies on the Scolex Morphology of Eubothrium spp. with emphasis on Characters Usable in the Species Discrimination and with Brief References on the Scolices of Bothriocephalus sp. And Triaenophorus spp. (Cestoda; Pseudophyllidea). Z. Parasitenkd. 60:147-156. Hanzelová, V., T. Scholz, D. Gerdeaux and R. Kuchta. 2002. A comparative study of Eubothrium salvelini and E. crassum (Cestoda: Pseudophyllidea) parasites of Artic char and brown trout in alpine lakes. Environmental Biology of Fishes. 64:245-256. Kuchta, R., T. Scholz, J. Brabec and R.A. Bray. 2008. Suppression of the tapeworm order Pseudophyllidea (Platyhelminthes: Eucestoda) and the proposal of two new orders, Bothriocephalidea and Diphyllobothriidea. International Journal for Parasitology. 38:49- 55. Mackiewicz, J.S. 1965. Redescription and Distribution of Glaridacris catostomi Cooper, 1920 (Cestoidea: Caryophyllaeidae)." Journal of Parasitology. 51(4): 554-560. Scholz, T. 1997. “A revision of the species of Bothriocephalus Rudolphi, 1808 (Cestoda: Pseudophyllidea) parasitic in American freshwater fishes. Systematic Parasitology. 36: 85-107. Scholz, T. and A. de Chambrier. 2003. “Taxonomy and biology of proteocephalidean cestodes: current state and perspectives.” Helmnithologia. 40(2): 65-77.