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Temperature drives asymmetric competition between alien and indigenous freshwater snail species, Physa acuta and Physa fontinalis

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Abstract

Biological invasion represents one of the major threats to global biodiversity as alien species often displace indigenous species. Knowledge of the mechanisms behind such displacements and the driving factors of the competitive superiority of the alien species remain limited. We combined analysis of field data and laboratory experiments examining species interactions to investigate the impact of temperature in the case of the alien freshwater snail Physa acuta and the indigenous snail Physa fontinalis. From field data, we identified higher temperature as the most important difference between sites populated by P. acuta and P. fontinalis. Results of the species interaction experiment conducted at 15, 20, and 25 °C revealed that the competitive superiority of P. acuta over P. fontinalis increases at warmer temperatures. In single species treatments, increasing temperature stimulated growth rates in both species. Coexistence treatments revealed an asymmetric competitive interaction between the two snail species. In both species, the density of conspecifics did not affect growth rates; however, density of heterospecifics did. This effect of heterospecifics varied with temperature. At 15 °C, the presence of heterospecifics stimulated the growth rates of both species, while at higher temperatures the presence of heterospecifics stimulated the growth rate in P. acuta only, but inhibited the growth rate in P. fontinalis. Our study shows that temperature can be a powerful driver of competitive outcomes between alien and indigenous species and highlight that the environmental context influences species interactions and impacts of alien species.

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References

  • Appleton CC (2003) Alien and invasive fresh water Gastropoda in South Africa. Afr J Aquat Sci 28:69–81

    Article  Google Scholar 

  • Bacela-Spychalska K, Wattier RA, Genton C, Rigaud T (2012) Microsporidian disease of the invasive amphipod Dikerogammarus villosus and the potential for its transfer to local invertebrate fauna. Biol Invasions 14:1831–1842

    Article  Google Scholar 

  • Beran L, Juřičková L, Horsák M (2005) Mollusca. In: Farkač J, Král D, Škorpík M (eds) Red list of threatened species in the Czech Republic, invertebrates. AOPK ČR, Prague, pp 69–74

    Google Scholar 

  • Boland BB, Meerhoff M, Fosalba C, Mazzeo N, Barnes MA, Burks RL (2008) Juvenile snails, adult appetites: contrasting resource consumption between two species of applesnails (Pomacea). J Mollusc Stud 74:47–54

    Article  Google Scholar 

  • Brackenbury TD, Appleton CC (1991) Effect of controlled temperatures on gametogenesis in the gastropods Physa acuta (Physidae) and Bulinus tropicus (Planorbidae). J Mollusc Stud 57:461–469

    Article  Google Scholar 

  • Brackenbury TD, Appleton CC (1995) Recolonization of the Umsindusi River, Natal, South Africa, by the invasive gastropod, Physa acuta (Basommatophora, Physidae). J Medic Appl Malacol 5:39–44

    Google Scholar 

  • Brenneis VEF, Sih A, de Rivera CE (2010) Coexistence in the intertidal: interactions between the nonindigenous New Zealand mud snail Potamopyrgus antipodarum and the native estuarine isopod Gnorimosphaeroma insulare. Oikos 119:1755–1764

    Article  Google Scholar 

  • Brönmark C, Rundle SD, Erlandsson A (1991) Interaction between freshwater snails and tadpoles: competition and facilitation. Oecologia 87:8–18

    Article  Google Scholar 

  • Byers JE (2000a) Competition between two estuarine snails: implications for invasions of exotic species. Ecology 81:1225–1239

    Article  Google Scholar 

  • Byers JE (2000b) Differential susceptibility to hypoxia aids estuarine invasion. Mar Ecol-Prog Ser 203:123–132

    Article  CAS  Google Scholar 

  • Cope NJ, Winterbourn MJ (2004) Competitive interactions between two successful molluscan invaders of freshwaters: an experimental study. Aquat Ecol 38:83–91

    Article  Google Scholar 

  • Covich AP (2010) Winning the biodiversity arms race among freshwater gastropods: competition and coexistence through shell variability and predator avoidance. Hydrobiologia 653:191–215

    Article  CAS  Google Scholar 

  • Dextrase AJ, Mandrak NE (2006) Impacts of alien invasive species on freshwater fauna at risk in Canada. Biol Invasions 8:13–24

    Article  Google Scholar 

  • Dillon RT, Wethington AR, Rhett JM, Smith TP (2002) Populations of the European freshwater pulmonate Physa acuta are not reproductively isolated from American Physa heterostropha or Physa integra. Invertebr Biol 121:226–234

    Article  Google Scholar 

  • Domisch S, Jähnig SJ, Simaika JP, Kuemmerlen M, Stoll S (2015) Application of species distribution models in stream ecosystems: the challenge of spatial scale, environmental predictors and species occurrence data. Fund Appl Limnol 186:45–61

    Google Scholar 

  • Frank C, Reischütz PL (1994) Rote Liste gefährdeter Weichtiere Österreichs (Mollusca: Gastropoda und Bivalvia). In: Gepp J (ed) Rote Listen gefährdeter Tiere Österreichs. Grüne Reihe des Bundesministeriums für Umwelt, Jugend und Familie, Graz, pp 1–355

    Google Scholar 

  • Früh D, Stoll S, Haase P (2012a) Physicochemical and morphological degradation of stream and river habitats increases invasion risk. Biol Invasions 14:2243–2253

    Article  Google Scholar 

  • Früh D, Stoll S, Haase P (2012b) Physico-chemical variables determining the invasion risk of freshwater habitats by alien mollusks and crustaceans. Ecol Evol 2:2843–2853

    Article  PubMed  PubMed Central  Google Scholar 

  • Grabowski M, Bacela K, Konopacka A (2007) How to be an invasive gammarid (Amphipoda: Gammaroidea)—comparison of life history traits. Hydrobiologia 590:75–84

    Article  Google Scholar 

  • Grabowski M, Bacela K, Konopacka A, Jazdzewski K (2009) Salinity-related distribution of alien amphipods in rivers provides refugia for native species. Biol Invasions 11:2107–2117

    Article  Google Scholar 

  • Guo YH, Hwang CC, He HX (2009) Expansion of an invasive freshwater snail Physa acuta (Gastropoda: Physidae) in China. Molluscan Res 29:174–178

    Google Scholar 

  • Haase P, Lohse S, Pauls S, Schindehütte K, Sundermann A, Rolauffs P, Hering D (2004) Assessing streams in Germany with benthic invertebrates: development of a practical standardised protocol for macro invertebrate sampling and sorting. Limnologica 34:349–365

    Article  Google Scholar 

  • Havel JE, Lee CE, van der Zanden MJ (2005) Do reservoirs facilitate invasions into landscapes? Bioscience 55:518–525

    Article  Google Scholar 

  • Höckendorff S, Früh D, Hormel N, Haase P, Stoll S (2015) Biotic interactions under climate warming: temperature-dependent and species-specific effects of the oligochaete Chaetogaster limnaei on snails. Freshw Sci 34:1304–1311

    Article  Google Scholar 

  • Johnson PTJ, Olden JD, van der Zanden MJ (2008) Dam invaders: impoundments facilitate biological invasions into freshwaters. Front Ecol Environ 6:359–365

    Google Scholar 

  • Jungbluth JH, von Knorre D (2009) Rote Liste der Binnenmollusken [Schnecken (Gastropoda) und Muscheln (Bivalvia)] in Deutschland. 6. revidierte und erweiterte Fassung 2008. Mitteilung der Deutschen Malakozoologischen Gesellschaft 81:1–28

    Google Scholar 

  • Karatayev AY, Burlakova LE, Padilla DK, Mastitsky SE, Olenin S (2009) Invaders are not a random selection of species. Biol Invasions 11:2009–2019

    Article  Google Scholar 

  • Kawata M, Ishigami H (1992) The growth of juvenile snails in water conditioned by snails of a different species. Oecologia 91:245–248

    Article  Google Scholar 

  • Kiesecker JM, Blaustein AR (1998) Effects of introduced bullfrogs and smallmouth bass on microhabitat use, growth, and survival of native red-legged frogs (Rana aurora). Conserv Biol 12:776–787

    Article  Google Scholar 

  • Kinzelbach R (1995) Neozoans in european waters—exemplifying the worldwide process of invasion and species mixing. Experientia 51:526–538

    Article  CAS  Google Scholar 

  • Krist AC, Charles CC (2012) The invasive New Zealand mudsnail, Potamopyrgus antipodarum, is an effective grazer of algae and altered the assemblage of diatoms more than native grazers. Hydrobiologia 694:143–151

    Article  CAS  Google Scholar 

  • Lövei GL (1997) Biodiversity—global change through invasion. Nature 388:627–628

    Article  Google Scholar 

  • Mack RN, Simberloff D, Lonsdale WM, Evans H, Clout M, Bazzaz FA (2000) Biotic invasions: causes, epidemiology, global consequences, and control. Ecol Appl 10:689–710

    Article  Google Scholar 

  • MacNeil C, Dick JTA, Elwood RW (2000) Differential physico-chemical tolerances of amphipod species revealed by field transplantations. Oecologia 124:1–7

    Article  Google Scholar 

  • Manganelli G, Bodon M, Cianfanelli S, Favilli L, Giusti F (2000) Knowledge and conservation of Italian non-marine mollusks: the status of the research. Boll Malacol 36:5–42

    Google Scholar 

  • Morrison WE, Hay ME (2011) Feeding and growth of native, invasive and non-invasive alien apple snails (Ampullariidae) in the United States: invasives eat more and grow more. Biol Invasions 13:945–955

    Article  Google Scholar 

  • Mouthon J, Daufresne M (2010) Long-term changes in mollusc communities of the Ognon river (France) over a 30-year period. Fund Appl Limnol 178:67–79

    Article  CAS  Google Scholar 

  • Nunez V (2010) Differences on allocation of available resources, in growth, reproduction, and survival, in an exotic gastropod of Physidae compared to an endemic one. Iheringia Serie Zoologia 100:275–279

    Article  Google Scholar 

  • Oscoz J, Tomas P, Duran C (2010) Review and new records of non-indigenous freshwater invertebrates in the Ebro River basin (Northeast Spain). Aquat Invasions 5:263–284

    Article  Google Scholar 

  • Rahel FJ, Olden JD (2008) Assessing the effects of climate change on aquatic invasive species. Conserv Biol 22:521–533

    Article  PubMed  Google Scholar 

  • Riley LA, Dybdahl MF, Hall RO (2008) Invasive species impact: asymmetric interactions between invasive and endemic freshwater snails. J North Am Benthol Soc 27:509–520

    Article  Google Scholar 

  • Sakai AK, Allendorf FW, Holt JS, Lodge DM, Molofsky J, With KA, Baughman S, Cabin RJ, Cohen JE, Ellstrand NC, McCauley DE, O’Neil P, Parker IM, Thompson JN, Weller SG (2001) The population biology of invasive species. Annu Rev Ecol Syst 32:305–332

    Article  Google Scholar 

  • Sala OE, Chapin FS, Armesto JJ, Berlow E, Bloomfield J, Dirzo R, Huber-Sanwald E, Huenneke LF, Jackson RB, Kinzig A, Leemans R, Lodge DM, Mooney HA, Oesterheld M, Poff NL, Sykes MT, Walker BH, Walker M, Wall DH (2000) Biodiversity—global biodiversity scenarios for the year 2100. Science 287:1770–1774

    Article  CAS  PubMed  Google Scholar 

  • Sargent LW, Dolladay SW, Civich AP, Opsahl SP (2011) Physicochemical habitat association of a native and non-native crayfish in the Lower Flint river, Georgia: implications for invasion success. Biol Invasions 13:499–511

    Article  Google Scholar 

  • Schmidlin S, Schmera D, Baur B (2012) Alien molluscs affect the composition and diversity of native macroinvertebrates in a sandy flat of Lake Neuchâtel, Switzerland. Hydrobiologia 679:233–249

    Article  Google Scholar 

  • Shibata DM, Rollo DC (1988) Intraspecific variation in the growth rate of gastropods: five hypotheses. Memoirs Entomol Soc Can 120:199–213

    Article  Google Scholar 

  • Stoll S, Früh D, Westerwald B, Hormel N, Haase P (2013) Density-dependent relationship between Chaetogaster limnaei limnaei (Oligochaeta) and the freshwater snail Physa acuta (Pulmonata). Freshw Sci 32:642–649

    Article  Google Scholar 

  • Strayer DL (2010) Alien species in fresh waters: ecological effects, interactions with other stressors, and prospects for the future. Freshw Biol 55:152–174

    Article  Google Scholar 

  • Turner H, Wüthrich M, Rüetschi J (1994) Rote Liste der gefährdeten Weichtiere der Schweiz. In: Duelli P (ed) Rote Listen der gefährdeten Tierarten der Schweiz. Bundesamt für Umwelt, Wald und Landschaft, EDMZ, Bern, p 97

    Google Scholar 

  • van der Velde G, Leuven R, Platvoet D, Bacela K, Huijbregts MAJ, Hendriks HWM, Kruijt D (2009) Environmental and morphological factors influencing predatory behaviour by invasive non-indigenous gammaridean species. Biol Invasions 11:2043–2054

    Article  Google Scholar 

  • Verbrugge LNH, Schipper AM, Huijbregts MAJ, van der Velde G, Leuven R (2012) Sensitivity of native and non-native mollusc species to changing river water temperature and salinity. Biol Invasions 14:1187–1199

    Article  Google Scholar 

  • Vermonden K, Leuven R, van der Velde G (2010) Environmental factors determining invasibility of urban waters for exotic macroinvertebrates. Divers Distrib 16:1009–1021

    Article  Google Scholar 

  • Vitousek PM, Dantonio CM, Loope LL, Rejmanek M, Westbrooks R (1997) Introduced species: a significant component of human-caused global change. New Zeal J Ecol 21:1–16

    Google Scholar 

  • Walther G-R, Roques A, Hulme PE, Sykes MT, Pysek P, Kuhn I, Zobel M, Bacher S, Botta-Dukat Z, Bugmann H, Czucz B, Dauber J, Hickler T, Jarosik V, Kenis M, Klotz S, Minchin D, Moora M, Nentwig W, Ott J, Panov VE, Reineking B, Robinet C, Semenchenko V, Solarz W, Thuiller W, Vila M, Vohland K, Settele J (2009) Alien species in a warmer world: risks and opportunities. Trends Ecol Evol 24:686–693

    Article  PubMed  Google Scholar 

  • Weitere M, Vohmann A, Schulz N, Linn C, Dietrich D, Arndt H (2009) Linking environmental warming to the fitness of the invasive clam Corbicula fluminea. Glob Chang Biol 15:2838–2851

    Article  Google Scholar 

  • Werner S, Rothhaupt KO (2008) Mass mortality of the invasive bivalve Corbicula fluminea induced by a severe low-water event and associated low water temperatures. Hydrobiologia 613:143–150

    Article  Google Scholar 

  • Wijnhoven S, van Riel MC, van der Velde G (2003) Exotic and indigenous freshwater gammarid species: physiological tolerance to water temperature in relation to ionic content of the water. Aquat Ecol 37:151–158

    Article  Google Scholar 

  • Winterbourn MJ (1980) The distribution and biology of the fresh water gastropods Physa and Physastra in New-Zealand. J Malacol Soc Aust 4:233–234

    Google Scholar 

  • Zukowski S, Walker KF (2009) Freshwater snails in competition: alien Physa acuta (Physidae) and native Glyptophysa gibbosa (Planorbidae) in the River Murray, South Australia. Mar Freshw Res 60:999–1005

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We are grateful to State Agency for Nature, Environment and Consumer protection North Rhine Westphalia for kindly providing the species and physico-chemical data. The present study was funded by the research funding program “LOEWE-Landes-Offensive zur Entwicklung Wissenschaftlich-ökonomischer Exzellenz” of Hesse’s Ministry of Higher Education, Research, and the Arts.

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Authors and Affiliations

  1. Department of River Ecology and Conservation, Senckenberg Research Institute and Natural History Museum Frankfurt, Clamecystr. 12, 63571, Gelnhausen, Germany

    Denise Früh, Peter Haase & Stefan Stoll

  2. Department of River and Floodplain Ecology, Faculty of Biology, University of Duisburg-Essen, Essen, Germany

    Peter Haase

  3. Department of Ecotoxicology and Environment, University of Koblenz-Landau, 76829, Landau, Germany

    Stefan Stoll

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  1. Denise Früh
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  2. Peter Haase
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Correspondence to Stefan Stoll.

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Früh, D., Haase, P. & Stoll, S. Temperature drives asymmetric competition between alien and indigenous freshwater snail species, Physa acuta and Physa fontinalis . Aquat Sci 79, 187–195 (2017). https://doi.org/10.1007/s00027-016-0489-9

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