Choosing exotic over the familiar taste: habitat-specific preferences of a malacophagous leech for freshwater snails as prey gastropod establishment?

Authors

  • Pranesh Paul University of Calcutta
  • Rupsha Karmakar University of Calcutta
  • Gautam Aditya University of Calcutta

DOI:

https://doi.org/10.17161/eurojecol.v6i1.13693

Keywords:

Invasive species, Planorbarius corneus, Indoplanorbis exustus, Glossiphonia weberi, habitat complexity, prey preference

Abstract

The spread of freshwater invasive species through aquarium trade poses a threat to the ecosystem, economy and human health. The availability of the exotic freshwater gastropod mollusc, Planorbarius corneus (Linnaeus, 1758) (Gastropoda: Planorbidae), in pet shops in Kolkata, West Bengal, India, raises concern for its potential establishment as an invasive species. Assuming the role of the native predators as a potential biotic barrier for invasion, observations on the predation pattern of the malacophagous leech, Glossiphonia weberi (Blanchard, 1897) (Clitellata: Glossiphoniidae) against P. corneus was made in single as well as in combination with the native snail Indoplanorbis exustus (Deshayes, 1834) (Gastropoda: Planorbidae). Using varying size classes and densities of P. corneus, the predation potential of G. weberi was estimated after a 24 hour period. In another set of experiments, the predation of G. weberi against the snail P. corneus was observed in the presence of I. exustus under four different habitat conditions. The purpose was to justify - (1) the effect of conspecific and heterospecific conditions of the prey availability and (2) the effect of habitat complexity on the predatory efficacy of G. weberi. The results indicated that G. weberi consumed varied numbers of P. corneus, depending on the size and the densities of the prey and predator. Although the prey heterogeneity and complex habitats caused significant reduction of predation on both of the prey species, G. weberi significantly preferred P. corneus over I. exustus in open (P < 0.0001), macrophyte (P = 0.002) and pebbles and macrophyte containing habitats (P < 0.0001). Apparently, G. weberi preferred the exotic snail P. corneus in presence of alternative prey snail I. exustus, under different habitat conditions. Therefore, G. weberi may act as a significant biotic resistance against the colonization and establishment of P. corneus in the Indian context. However, further studies including the multiple prey and predators are required to ascertain the food web level impact of the exotic snail P. corneus in invaded freshwater ecosystems.

Author Biographies

  • Pranesh Paul, University of Calcutta

    Working as a Junior Research Fellow (CSIR-JRF), Government of India fellowship in the University of Calcutta, on the ecology of freshwater and terrestrial snails.

  • Rupsha Karmakar, University of Calcutta

    Rupsha is working as a Research Fellow (UGC) in the Department of Zoology, University of Calcutta. She is working on the ecology of the freshwater snails and the biological regulation of vector mosquitoes.

References

Addinsoft SARL. (2010) XLSTAT softwere, version 9.0. Paris: Addinsoft.
Aditya, G. & Raut, S.K. (2002a) Potential of the leech Glossiphonia weberi (Blanchard) in controlling the sewage snails Physa acuta Draparnaud. Current Science, 83(11), 1317–1319.
Aditya, G. & Raut, S.K. (2002b) Predation potential of the water bugs Sphaerodema rusticum on the sewage snails Physa acuta. Memórias do Instituto Oswaldo Cruz, 97(4), 531–534.
Aditya, G. & Raut, S.K. (2005) Feeding of the leech Glossiphonia weberi on the introduced snail Pomacea bridgesii in India. Aquatic ecology, 39, 465–471.
Baltz, D.M. & Moyle, P.B. (1993) Invasion resistance to introduced species by a native assemblage of California stream fishes. Ecological Applications, 3(2), 246–255.
Berrie, A.D. (1963) Life-cycle of Planorbarius corneus (L.). Nature, 198, 805–806.
Beukers, J.S. & Jones, G.P. (1997) Habitat complexity modifies the impact of piscivores on a coral reef fish population. Oecologia, 114, 50–59.
Biswas, G. (1991) Snail borne diseases and their role in veterinary public health. In: Director, Zoological Survey of India (Eds.), Snails, Flukes and Man (pp. 73–78). Zoological Survey of India.
Boukal, D.S. (2014) Trait and size-based descriptions of trophic links in freshwater food webs: current status and perspectives. Journal of Limnology, 73, 171–185.
Brönmark, C. & Malmqvist, B. (1986) Interactions between the leech Glossiphonia complanata and its gastropod prey. Oecologia, 69, 268–276.
Carlsson, N.O.L & Lacoursiére, J.O. (2005) Herbivory on aquatic vascular plants by the introduced golden apple snail (Pomacea canaliculata) in Lao PDR. Biological Invasions, 7, 233–241.
Carlsson, N.O.L. & Brönmark, C. (2006) Size‐dependent effects of an invasive herbivorous snail (Pomacea canaliculata) on macrophytes and periphyton in Asian wetlands. Freshwater Biology, 51, 695–704.
Carlton, J.T. (2003) Community assemblage and historical biogeography in the North Atlantic Ocean: the potential role of human-mediated dispersal vectors. Hydrobiologia, 503, 1–8.
Chakraborty, S. & Chattopadhyay, J. (2011) Effect of cannibalism on a predator-prey system with nutritional value: a model based study. Dynamical Systems, 26(1), 13–22.
Chang, A.L., Grossman, J.D., Spezio, T.S., Weiskel, H.W., Blum, J.C., et al. (2009) Tackling aquatic invasions: risks and opportunities for the aquarium fish industry. Biological Invasions, 11, 773–785
Chesson, J. (1978) Measuring Preference in Selective Predation. Ecology, 59(2), 211–215.
Cobbaert, D., Bayley, S.E. & Greter, J. (2010) Effects of a top invertebrate predator (Dytiscus alaskanus; Coleoptera: Dytiscidae) on fishless pond ecosystems. Hydrobiologia, 644, 103–114.
Cooper, W.E. & Anderson, R. (2006) Adjusting prey handling times and methods affect profitability in the broad-headed skink (Eumeces laticeps). Herpetologica, 62(4), 356–365.
Costil, K. & Daguzan, J. (1995a) Comparative lifecycle and growth of two freshwater gastropod species, Planorbarius corneus (L.) and Planorbis planorbis (L.). Malacologia, 37(1), 53–68.
Costil, K. & Daguzan, J. (1995b) Effect of temperature on reproduction in Planorbarius corneus (L.) and Planorbis planorbis (L.) throughout the life span. Malacologia, 36(1–2), 79–89.
Cowie, R.H. & Robinson, D.G. (2003) Pathways of introduction of nonindigenous land and freshwater snails and slugs. In: Ruiz, G.M. & Carlton, J.T. (Eds.), Invasive species: vectors and management strategies (pp. 93–122). Island Press.
Cowie, R.H. (2002) Apple snails as agricultural pests: their biology, impacts, and management. In: Baker GM (Ed.) Molluscs as crop pests (pp. 145–192). CABI Publishing, Wallingford.
Crowl, T.A., Crist, T.O., Parmenter, R.R., Belovsky, G. & Lugo, A.E. (2008) The spread of invasive species and infectious disease as drivers of ecosystem change. Frontiers in Ecology and the Environment, 6, 238–246.
Dobson, M. (2004) Replacement of the native freshwater snail by the exotic Physa acuta (Gastropoda: Physidae) in southern Mozambique; a possible control mechanism for schistosomiasis. Annals of Tropical Medicine and Parasitology, 98(5), 543–548.
Doherty, T.S., Glen, A.S., Nimmo, D.G., Ritchie, E.G. & Dickman, C.R. (2016) Invasive predators and global biodiversity loss. Proceedings of the National Academy of Sciences, 113(40), 11261–11265.
Duggan, I.C. (2010) The freshwater aquarium trade as a vector for incidental invertebrate fauna. Biological Invasions, 12, 3757–3770.
Emlen, J.M. (1975) Optimal choice in diet: test of a hypothesis. The American Naturalist, 109, 427-435.
Estebenet, A.L. (1995) Food and feeding in Pomacea canaliculata (Gastropoda, Ampullariidae). Veliger, 38, 277e283.
Gathman, J.P. (2020) Do Predators Structure Wetland Macroinvertebrate Assemblages? Different Effects of Mudminnows and Dragonfly Nymphs in Field Experiments. Wetlands, 40, 143–152.
Giller, P.S. & McNeill, S. (1981) Predation strategies, resource partitioning and habitat selection in Notonecta (Hemiptera/Heteroptera). Journal of Animal Ecology, 50, 789–808.
Gillis, C. & Chalifour, M. (2010) Changes in the macrobenthic community structure following the introduction of the invasive algae Didymosphenia geminata in the Matapedia River (Québec, Canada). Hydrobiologia, 647, 63–70.
Grabowski, J.H. 2004. Habitat complexity disrupts predator-prey interactions but not the trophic cascade on oyster reefs. Ecology, 85(4), 995–1004.
Greenlees, M., Phillips, B.L. & Shine, R. (2010) Adjusting to a toxic invader: native Australian frog learns not to prey on cane toads. Behavioral Ecology, 21, 966e971.
Grosholz, E. (2002) Ecological and evolutionary consequences of coastal invasions. Trends in Ecology and Evolution, 17(1), 22–27.
Harris, L.A., Buckley, B., Nixon, S.W. & Allen, B.T. (2004) Experimental studies of predation by bluefish Pomatomus saltatrix in varying densities of seagrass and macroalgae. Marine Ecology Progress Series, 281, 233–239.
Hellmair, M., Goldsmith, G. & Kinziger, A.P. (2011) Preying on invasives: the exotic New Zealand mudsnail in the diet of the endangered tidewater goby. Biological Invasions, 13, 2197.
Hosokawa, T., Nikoh, N. & Fukatsu, T. (2014) Fine-scale geographical origin of an insect pest invading Nort h America. PLoS ONE, 9(2), e89107.
Human, K.G. & Gordon, D.M. (1996) Exploitation and interference competition between the invasive Argentine ant, Linepithema humile and native ant species. Oecologia, 105, 405–412.
Kratina, P., Vos, M., Bateman, A. & Anholt, B.R. 2009. Functional responses modified by predator density. Oecologia, 159, 425–433.
Kreps, T.A., Baldridge, A.K. & Lodge, D.M. (2012) The impact of an invasive predator (Orconectes rusticus) on freshwater snail communities: Insights on habitat-specific effects from a multilake long-term study. Canadian Journal of Fisheries and Aquatic Sciences, 69, 1164–1173.
Kwong, K.L., Wong, P.K., Lau, S.S.S. & Qiu, J.W. (2008) Determination of the distribution of apple snails in Hong Kong two decades after their initial invasion. Malacologia, 50, 293–302.
Lieb, B., Dimitrova, K., Kang, H., Braun, S., Gebauer, W., Martin, A., et al. (2006) Red blood with blue-blood ancestry: Intriguing structure of a snail haemoglobin. Proceedings of the National Academy of Sciences, 103(32), 12011–12016.
MacArthur, R. & Pianka, E. (1966) On Optimal Use of a Patchy Environment. American Naturalist, 100, 603–609.
Mack, R.N., Simberloff, D., Lonsdale, W.M., Evans, H., Clout, M. & Bazzaz, F.A. (2000) Biotic invasions: causes, epidemiology, global consequences, and control. Ecological Applications, 10(3), 689–710.
Malek, E.A. & Cheng, T.C. (1974) Medical and Economic Malacology. (Academic Press: New York.) Marine Ecology Progress Series 329, 225–238.
Mayntz, D., Raubenheimer D., Salomon, M., Toft, S., & Simpson, S. (2005) Nutrient-Specific Foraging in Invertebrate Predators. Science, 307(5706), 111–113.
Miranda, N.A.F. & Perissinotto, R. (2014a) Benthic assemblages of wetlands invaded by Tarebia granifera (Lamarck, 1822) (Caenogastropoda: Thiaridae) in the iSimangaliso Wetland Park, South Africa. Molluscan Research, 34, 40–48.
Miranda, N.A.F. & Perissinotto, R. (2014b). Effects of an alien invasive gastropod on native benthic assemblages in coastal lakes of the iSimangaliso Wetland Park, South Africa. African Invertebrates, 55, 209–228.
Miranda, N.A.F., Perissinotto, R. & Appleton C.C. (2011) Population structure of an invasive parthenogenetic gastropod in coastal lakes and estuaries of Northern KwaZulu-Natal, South Africa. PLoS ONE, 6, e24337.
Ng, T.H., Tan, S.K., Wong, W.H., Meier, R., Chan, S-Y., Tan, H.H. & Yeo, D.C.J. (2016) Molluscs for Sale: Assessment of Freshwater Gastropods and Bivalves in the Ornamental Pet Trade. PLoS ONE, 11(8), e0161130.
Nyström, P. & Pérez, J.R. (1998) Crayfish predation on the common pond snail (Lymnaea stagnalis): the effect of habitat complexity and snail size on foraging efficiency. Hydrobiologia, 368, 201–208.
O’Donnell, S., Webb, J.K. & Shine, R. (2010) Conditioned taste aversion enhances the survival of an endangered predator imperilled by a toxic invader. Journal of Applied Ecology, 47, 558e565.
Paini, D.R., Sheppard, A.W., Cook, D.C., De Barro, P.J., Worner, S.P. & Thomas, M.B. (2016) Global threat to agriculture from invasive species. Proceedings of the National Academy of Sciences, 113(27), 7575–7579.
Parveen. S., Karmakar, R., Paul, P., Banerjee, S., Barman, H. & Aditya, G. (2020) Shell morphometry and fecundity of the exotic snail Planorbarius corneus (Linnaeus, 1758) (Gastropoda: Planorbidae) In Kolkata, India. Uttar Pradesh Journal of Zoology, 40(4), 236–244.
Pointier, J.P. (1999) Invading freshwater gastropods: some conflicting aspects for public health. Malacologia, 41, 403–411.
Rall, B.C., Guill, C. & Brose, U. 2008. Food-web connectance and predator interference dampen the paradox of enrichment. Oikos, 117, 202–213.
Raut, S.K. & Nandi, R. (1984) Experimental studies on effectiveness of the predatory leech, Glossiphonia weberi in the biological control of vector snail Lymnaea luteola. Bulletin of Zoological Survey of India, 6(1–3), 5–19.
Raut, S.K. (1981) Population interactions among freshwater snails. Proceedings of the Symposium of Ecology and Animal Population, Zoological Survey of India, 2, 163–173.
Rehage, J.S., Barnetti, B.K. & Sih, A. (2005) Foraging behavior and invasiveness: do invasive Gambusia exhibit higher feeding rates and broader diets than their noninvasive relatives? Ecology of Freshwater Fish, 14, 352–360.
Rilov, G., Figueira, W.F., Lyman, S.J. & Crowder, L.B. (2007) Complex habitats may not always benefit prey: linking visual field with reef fish behavior and distribution. Marine Ecology Progress Series, 325, 225–238.
Rilov, G., Gasith, A. & Benayahu, Y. (2002) Effect of an exotic prey on the feeding pattern of a predatory snail. Marine Environmental Research, 54(1), 85–98.
Rixon, C.A.M., Duggan, I.C., Bergeron, N.M.N., Ricciardi, A. & Mac-Isaac, H.J. (2005) Invasion risks posed by the aquarium trade and live fish markets to the Laurentian Great Lakes. Biodiversity and Conservation, 14, 1365–1381.
Sanders, N.J., Gotelli, N.J., Heller, N.E. & Gordon, D.M. (2003) Community disassembly by an invasive species. Proceedings of the National Academy of Sciences, 100(5), 2474–2477.
Sawyer, R.T. (1986) Leech Biology and Behaviour. Oxford University Press.
Schoener, T.W. (1971) Theory of feeding strategies. Annual Review Ecology, Evolution, and Systematics, 11, 369–404.
Seddon, M.B. & Van Damme, D. (2011) Planorbarius corneus. The IUCN Red List of Threatened Species, e.T156083A4889234.
Skalski, G.T. & Gilliam, J.F. (2001) Functional responses with predator interference: viable alternatives to the Holling type II mode. Ecology, 82, 3083–3092.
Somaweera, R., Webb, J.K., Brown, G.P. & Shine, R. (2011) Hatchling Australian freshwater crocodiles rapidly learn to avoid toxic invasive cane toads. Behaviour, 148, 501e 517.
Stoner, A.W. (1982) The influence of benthic macrophytes on the foraging behaviour of pinfish, Lagodon rhomboids (Linnaeus). Journal of Experimental Marine Biology and Ecology, 58, 271–284.
Su, S., Cassey, P. & Blackburn, T.M. (2016) The wildlife pet trade as a driver of introduction and establishment in alien birds in Taiwan. Biological Invasions, 18, 215–229.
Tully, T., Cassey, P. & Ferrière, R. (2005) Functional response: rigorous estimation and sensitivity to genetic variation in prey. Oikos, 111, 479-487.
Turner, A.M. & Chislock, M.F. (2007) Dragonfly predators influence biomass and density of pond snails. Oecologia, 153, 407–415.
Van Voorn, G.A.K., Stiefs, D., Gross, T., Kooi, B.W., Feudel, U. & Kooijman, S.A.L.M. (2008) Stabilization due to predator interference: Comparison of different analysis approaches. Mathematical Biosciences and Engineering, 5, 567–583.
Warner, G.F., Wood, J.C. & Orr-Erwing, R.H. (1995) Signal crayfish (Pacifastacus leniusculus) feeding on pond snails: Optimal foraging? Freshwater Crayfish, 8, 352–359.
Wesselingh, F.P., Cadeé GC & Renema, W. (1999) Flying high: On the airborne dispersal of aquatic organisms as illustrated by the distribution histories of the gastropod genera Tryonia and Planorbarius. Geologie en Mijnbouw, 78, 165–174.
Wilcove, D.S., Rothstein, D., Dubow, J., Phillips, A. & Losos, E. (1998) Quantifying threats to imperilled species in the United States. BioScience, 48(8), 607–615.
Wilken, G.B. & Appleton, C.C. (1991) Avoidance responses of some indigenous and exotic freshwaler pulmonate snails to leech predation in South Africa. South African Journal of Zoology, 26, 6–10.
Wong, M.C. & Barbeau, M.A. (2006) Rock crab predation of juvenile sea scallops: the functional response and its implications for bottom culture. Aquaculture International. 14, 355–376.
Young, J.O. & Ironmonger, J.W. (1980) A laboratory study of the food of three species of leeches occurring in British lakes. Hydrobiologia, 68, 209–215.
Zar, J,H. (1999) Biostatistical analysis. Pearson Education India Singapore Pvt. Ltd., Indian branch.
Zhao, W. (2013) The great ramshorn (Planorbarius corneus): a new favorite in aquarium. Aquarium, 128–133. (In chinese).
Zotin, A.A. (2018) Individual growth of Planorbarius corneus (Planorbidae, Gastropoda) in postlarval entogenesis. Russian Journal of Developmental Biology, 49(6), 381–387.

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2020-08-21

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Paul, P., Karmakar, R., & Aditya, G. (2020). Choosing exotic over the familiar taste: habitat-specific preferences of a malacophagous leech for freshwater snails as prey gastropod establishment?. European Journal of Ecology, 6(1), 121-136. https://doi.org/10.17161/eurojecol.v6i1.13693