Hostname: page-component-cd9895bd7-hc48f Total loading time: 0 Render date: 2024-12-27T09:29:32.340Z Has data issue: false hasContentIssue false

Infection patterns of trematodes across size classes of an invasive snail species using field and laboratory studies

Published online by Cambridge University Press:  27 September 2018

Rebecca Z. Bachtel
Affiliation:
Department of Biology, University of Massachusetts Dartmouth, 285 Old Westport Road, Dartmouth, MA 02747, USA
Matthew Rittenhouse
Affiliation:
Department of Biology, University of Wisconsin La Crosse, La Crosse, WI, USA
Gregory J. Sandland
Affiliation:
Department of Biology, University of Wisconsin La Crosse, La Crosse, WI, USA
Jennifer A. H. Koop*
Affiliation:
Department of Biology, University of Massachusetts Dartmouth, 285 Old Westport Road, Dartmouth, MA 02747, USA
*
Author for correspondence: Jennifer A. H. Koop, E-mail: jkoop@umassd.edu

Abstract

In the Upper Mississippi River Region, invasive faucet snails (Bithynia tentaculata) and their trematode parasites have been implicated in more than 182 000 waterfowl deaths since 1996. Estimating transmission potential depends on accurate assessments of susceptible host population size. However, little is known about the mechanisms underlying snail–host susceptibility in this system. Prior field studies suggest that very small, likely young, faucet snails are less suitable secondary intermediate hosts. Here, we test whether the patterns observed in the field are because small snails (1) are refractory to infection by cercariae, (2) die from infection and are removed from sampled populations, and/or (3) are not preferred by cercariae. Our own field collections were consistent with the observation that smaller faucet snails exhibit lower metacercarial infection prevalence and abundance than larger snails. However, laboratory-based experiments show that smaller snails were actually more susceptible to infection than larger snails. Moreover, the smallest snail size class had significantly higher mortality than larger snails following infection, which may explain their reduced infection levels observed in the field. Our study demonstrates the importance of pairing field and laboratory studies to better understand mechanisms underlying patterns of infection.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2018 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Baker, FC (1898) The Mollusca of the Chicago Area: The Pelecypoda. Vol. Bulletin No. 3, Part 1. Chicago, Illinois: The Chicago Academy of Sciences, p. 328.Google Scholar
Beauchamp, WM (1880) Bythinia tentaculata Linn. American Naturalist 14, 518532.Google Scholar
Christensen, NO, Frandsen, F and Roushdy, MZ (1980) The influence of environmental conditions and parasite-intermediate host-related factors on the transmission of Echinostoma liei. Zeitschrift Fur Parasitenkunde (Berlin, Germany) 64, 4763.Google Scholar
Combes, C, Fournier, A, Mone, H and Theron, A (1994) Behaviours in trematode cercariae that enhance parasite transmission: patterns and processes. Parasitology 109(Suppl.), S3S13.Google Scholar
Fernandez, MV, Hamann, MI and Kehr, AI (2013) Biology of Kalipharynx sp. (Trematoda: Digenea) metacercariae in Biomphalaria (gasteropoda: Planorbidae) from Northeastern Argentina. International Journal of Tropical Biology and Conservation 61, 16471656.Google Scholar
Goedknegt, MA, Feis, ME, Wegner, KM, Luttikhuizen, PC, Buschbaum, C, Camphuysen, K, van der Meer, J and Thieltges, DW (2016) Parasites and marine invasions: ecological and evolutionary perspectives. Journal of Sea Research 113, 1127.Google Scholar
Graham, AL (2003) Effects of snail size and age on the prevalence and intensity of avian schistosome infection: relating laboratory to field studies. Journal of Parasitology 89, 458463.Google Scholar
Haas, W (1994) Physiological analyses of host-finding behaviour in trematode cercariae: adaptations for transmission success. Parasitology 109(Suppl.), S15S29.Google Scholar
Haas, W (2003) Parasitic worms: strategies of host finding, recognition and invasion. Zoology 106, 349364.Google Scholar
Haas, W, Haberl, B, Kalbe, M and Korner, M (1995) Snail-host finding by miracidia and cercariae: chemical host cues. Parasitology Today 11, 468472.Google Scholar
Henningsen, JP, Lance, SL, Jones, KL, Hagen, C, Laurila, J, Cole, RA and Perez, KE (2010) Development and characterization of 17 polymorphic microsatellite loci in the faucet snail, Bithynia tentaculata (Gastropoda: Caenogastropoda: Bithyniidae). Conservation Genetics Resources 2, 247250.Google Scholar
Herrmann, KK and Sorensen, RE (2009) Seasonal dynamics of two mortality-related trematodes using an introduced snail. Journal of Parasitology 95, 823828.Google Scholar
Herrmann, KK and Sorensen, RE (2011) Differences in natural infections of two mortality-related trematodes in Lesser scaup and American coot. Journal of Parasitology 97, 555558.Google Scholar
Hoeve, J and Scott, ME (1988) Ecological studies on Cyathocotyle bushiensis (Digenea) and Sphaeridiotrema globulus (Digenea), possible pathogens of dabbling ducks in southern Quebec. Journal of Wildlife Diseases 24, 407421.Google Scholar
Huffman, JE (1986) Structure and composition of the metacercarial cyst wall of Sphaeridiotrema globulus (Trematoda). International Journal for Parasitology 16, 647653.Google Scholar
Huffman, JE and Roscoe, DE (1989) Experimental infections of waterfowl with Sphaeridiotrema globulus (Digenea). Journal of Wildlife Diseases 25, 143146.Google Scholar
Huffman, JE, Fried, B, Roscoe, DE and Cali, A (1984) Comparative pathologic features and development of Sphaeridiotrema globulus (Trematoda) infections in the mute swan and domestic chicken and chicken chorioallantois. American Journal of Veterinary Research 45, 387391.Google Scholar
Huffman, JE, Stevens, P and Fried, B (2012) Light and scanning electron microscopic observations of the larval stages and adult of Sphaeridiotrema globulus (Trematoda: Psilostomidae). Journal of the Pennsylvania Academy of Science 86, 6168.Google Scholar
Khan, D. (1962) Studies on larval trematodes infecting freshwater snails in London (U.K.) and some adjoining areas. Part VI. The cercariae of the ‘vivax’ group and the life history of Cercaria bushiensis n.sp. (=Cyathocotyle bushiensis n.sp.)*. Journal of Helminthology 36, 6794.Google Scholar
Krist, AC and Lively, CM (1998) Experimental exposure of juvenile snails (Potamopyrgus antipodarum) to infection by trematode larvae (Microphallus sp.): infectivity, fecundity compensation and growth. Oecologia 116, 575582.Google Scholar
Kuris, AM and Warren, JM (1980) Echinostome cercarial penetration and metacercarial encystment as mortality factors for a second intermediate host, Biomphalaria glabrata. The Journal of Parasitology 66, 630635.Google Scholar
Lepitzki, DA (1993) Epizootiology and transmission of snail inhabiting metacercariae of the duck digeneans Cyathocotyle bushiensis and Sphaeridiotrema globulus. In Institute of Parasitology, McGill University, Montreal, Canada.Google Scholar
Lepitzki, DA and Bunn, BM (1994) A plug in the cyst wall of metacercariae of Sphaeridiotrema pseudoglobulus (Digenea: Psilostomidae) and a possible novel mode of transmission. International Journal for Parasitology 24, 273275.Google Scholar
Lepitzki, DAW, Scott, ME and McLaughlin, JD (1994) Assessing cercarial transmission of Cyathocotyle bushiensis and Sphaeridiotrema pseudoglobulus by use of sentinel snails. Canadian Journal of Zoology 72, 885891.Google Scholar
McCarthy, AM (1998) The influence of temperature on the survival and infectivity of the cercariae of Echinoparyphium recurvatum (Digenea: Echinostomatidae). Parasitology 118, 383388.Google Scholar
McKindsey, CW and McLaughlin, JD (1994) Hatching dynamics of eggs as further evidence for the existence of two separate species of Sphaeridiotrema (digenea) in Eastern North America. Journal of Helminthological Society of Washington 61, 126127.Google Scholar
McLaughlin, JD, Scott, ME and Huffman, JE (1993) Sphaeidiotrema globulus (Rudolphi, 1814) (Digenea): evidence for two species known under a single name and a description of Sphaeridiotrema pseudoglobulus n.sp. Canadian Journal of Zoology 71, 700707.Google Scholar
Menard, L and Scott, ME (1987) Seasonal occurrence of Cyathocotyle bushiensis Khan, 1962 (Digenea: Cyathocotylidae) metacercariae in the intermediate host Bithynia tentaculata L. (Gastropoda: Prosobranchia). Canadian Journal of Zoology 65, 29802992.Google Scholar
Pall-Gergely, B, Naggs, F and Asami, T (2016) Novel shell device for gas exchange in an operculate land snail. Biology Letters 12, 20160151. doi: 10.1098/rsbl.2016.0151.Google Scholar
Pan, CT (1965) Studies on the host-parasite relationship between Schistosoma mansoni and the snail Australorbis glabratus. American Journal of Tropical Medicine and Hygiene 14, 931976.Google Scholar
Richter, T (2001) Reproductive biology and life history strategy of Bithynia tentaculata (Linnaeus, 1758) and Bithynia leachii (Sheppard, 1823) (Dissertation). Hanover, Germany: University of Hannover.Google Scholar
Roy, C (2014) Investigation of Trematodes and Faucet Snails Responsible for Lesser Scaup Die-offs. Minnesota Department of Natural Resources, Division of Fish and Wildlife, Wildlife Populations and Research Unit, St. Paul, Minnesota.Google Scholar
Roy, CL and St-Louis, V (2017) Spatio-temporal variation in prevalence and intensity of trematodes responsible for waterfowl die-offs in faucet snail-infested waterbodies of Minnesota, USA. Interntational Journal for Parasitolology: Parasites and Wildlife 6, 162176.Google Scholar
Rozsa, L, Reiczigel, J and Majoros, G (2000) Quantifying parasites in samples of hosts. Journal of Parasitology 86, 228232.Google Scholar
Sandland, GJ and Minchella, DJ (2003) Effects of diet and Echinostoma revolutum infection on energy allocation patterns in juvenile Lymnaea elodes snails. Oecologia 134, 479486.Google Scholar
Sandland, GJ, Houk, S, Walker, B, Haro, RJ and Gillis, R (2013) Differential patterns of infection and life-history expression in native and invasive hosts exposed to a trematode parasite. Hydrobiologia 701, 8998.Google Scholar
Sauer, JS, Cole, RA and Nissen, JM (2007) Finding the Exotic Faucet Snail (Bithynia tentaculata): Investigation of Waterbird Die-offs on the Upper Mississipi River National Wildlife and Fish Refuge. U.S. Geological Survey Open-File Report 2007-1065. Reston, Virginia: U.S. Geological Survey.Google Scholar
Schmid-Hempel, P (2011) Evolutionary Parasitology: The Integrated Study of Infections, Immunology, Ecology, and Genetics. New York: Oxford University Press, Inc.Google Scholar
Sorensen, RE and Minchella, DJ (2001) Snail-trematode life history interactions: past trends and future directions. Parasitology 123, S3S18.Google Scholar
Toledo, R, Munoz-Antoli, MP and Esteban, JG (1999) Survival and infectivity of Hypoderaeum conoideum and Euparyhium albuferensis cercariae under laboratory conditions. Journal of Helminthology 73, 177182.Google Scholar
Vermeij, GJ and Williams, ST (2007) Predation and the geography of opercular thickness in turbinid gastropods. Journal of Molluscan Studies 73, 6773.Google Scholar
Walker, B (1893) The shell-bearing mollusca of Michigan. The Nautilus 6, 135140.Google Scholar
Wood, AM, Haro, CR, Haro, RJ and Sandland, GJ (2011) Effects of desiccation on two life stages of an invasive snail and its native cohabitant. Hydrobiologia 675, 167174.Google Scholar