Abstract
The mechanisms causing native species displacement by invasive species can be challenging to identify. We used survey data to demonstrate a local extinction of a native gastropod (Pomacea paludosa) from a Florida wetland coincident with invasion of a non-native gastropod (Pomacea maculata). We then examined the potential for P. maculata to displace P. paludosa. Two field experiments examined effects of densities and heterospecific interactions on juvenile P. paludosa growth in situ and lab and mesocosm experiments explored chemically-mediated interactions between the species. Field experiments produced variable results; evidence for reduced P. paludosa growth in the presence of P. maculata was found under higher nutrient conditions with fast snail growth rates, but growth inhibition disappeared under oligotrophic conditions. Resource reduction was not seen in the field experiments. Juvenile P. paludosa did not avoid mucus of P. maculata and did not reduce feeding in response to chemical cues. Nevertheless, exposure to mucus and waterborne cues of P. maculata reduced P. paludosa growth by 53% relative to conspecific cue exposure. In mesocosms juvenile P. paludosa growth was significantly negatively correlated with exposure to adult P. maculata waterborne cues. Stronger effects were evident when waterborne cues were combined with mucus at low exposure (20%). We documented the first apparent local extinction of P. paludosa by P. maculata. We found no evidence for competition, but the results collectively pointed to an effect of direct chemical inhibition that could be important at field scales and at low invasive densities.
Similar content being viewed by others
Availability of data and material
The data that support the findings of this study are available on request from the corresponding author, DKD.
References
Barnes MA, Fordham RK, Burks RL (2008) Fecundity of the exotic applesnail, Pomacea insularum. Freshw Sci 27:738–745
Bates D, Mächler M, Bolker B, Walker S (2014) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48
Bellard C, Cassey P, Blackburn TM (2016) Alien species as a driver of recent extinctions. Biol Let 12:20150623
Berrie AD, Visser SA (1963) Investigations of a growth-inhibiting substance affecting a natural population of freshwater snails. Physiol Zool 36:167–173
Brönmark C, Hansson LA (2000) Chemical communication in aquatic systems: an introduction. Oikos 88:103–109
Brönmark C, Pettersson LB (1994) Chemical cues from piscivores induce a change in morphology in crucian carp. Oikos 70:396–402
Brown KM (1982) Resource overlap and competition in pond snails: an experimental analysis. Ecology 63:412–422
Bull CM, Baker GH, Lawson LM, Steed MA (1992) Investigations of the role of mucus and faeces in interspecific interactions of two land snails. J Molluscan Stud 58:433–441
Bullock M, Legault G, Melbourne BA (2020) Interspecific chemical competition between Tribolium castaneum and Tribolium confusum (Coleoptera: Tenebrionidae) reduces fecundity and hastens development time. Ann Entomol Soc Am 113:216–222
Burks RL, Lodge DM (2002), Cued in: advances and opportunities in freshwater chemical ecology. J Chem Ecol, 28: 1901–1917
Byers JE (2000) Competition between two estuarine snails: implications for invasions of exotic species. Ecology 81:1225–1239
Cameron RAD, Carter MA (1979) Intra- and interspecific effects of population density on growth and activity in some helicid land snails (Gastropoda: Pulmonata). J Anim Ecol 48:237–246
Cattau CE, Martín J, Kitchens WM (2010) Effects of an exotic prey species on a native specialist: example of the snail kite. Biol Cons 143:513–520
Cattau CE, Darby PC, Fletcher RJ, Kitchens WM (2014) Reproductive responses of the endangered snail kite to variations in prey density. J Wildl Manag 78:620–631
Conner SL, Pomory CM, Darby PC (2008) Density effects of native and exotic snails on growth in juvenile apple snails Pomacea paludosa (Gastropoda: Ampullariidae): a laboratory experiment. J Molluscan Stud 74:355–362
Croll RP (1983) Gastropod chemoreception. Biol Rev 58:293–319
Cross WF, Benke AC (2002) Intra-and interspecific competition among coexisting lotic snails. Oikos 96:251–264
Crowl TA, Covich AP (1990) Predator-induced life-history shifts in a freshwater snail. Science 247:949–951
Dan N, Bailey SER (1982) Growth, mortality, and feeding rates of the snail Helix aspersa at different population densities in the laboratory, and the depression of activity of helicid snails by other individuals, or their mucus. J Molluscan Stud 48:257–265
Darby PC, Bennetts RE, Percival HF (2008) Dry down impacts on apple snail (Pomacea paludosa) demography: implications for wetland water management. Wetlands 28:204–214
Davidson AT, Dorn NJ (2018) System productivity alters predator sorting of a size-structured mixed prey community. Oecologia 186:1101–1111
Davies M, Blackwell J (2007) Energy saving through trail following in a marine snail. Proc R Soc Lond B 274:1233–1236
Davis MA (2003) Biotic globalization: does competition from introduced species threaten biodiversity? Bioscience 53:481–489
Didham RK, Tylianakis JM, Hutchison MA, Ewers RM, Gemmell NJ (2005) Are invasive species the drivers of ecological change? Trends Ecol Evol 20:470–474
Doherty TS, Glen AS, Nimmo DG, Ritchie EG, Dickman CR (2016) Invasive predators and global biodiversity loss. Proc Natl Acad Sci 113:11261–11265
Dorn NJ (2013) Consumptive effects of crayfish limit snail populations. Freshw Sci 32:1298–1308
Dorn NJ, Cook MI (2015) Hydrological disturbance diminishes predator control in wetlands. Ecology 96:2984–2993
Dorn NJ, Hafsadi M (2016) Native crayfish consume more non-native than native apple snails. Biol Invasions 18:159–167
Dorn NJ, Urgelles R, Trexler JC (2005) Evaluating active and passive sampling methods to quantify crayfish density in a freshwater marsh. J N Am Benthol Soc 24:346–356
Drumheller DK (2020) Population limitations of the Florida apple snail (Pomacea paludosa). Florida Atlantic University, Boca Raton, USA, Thesis
Fogarty MJ, Albury JD (1967) Late summer foods of young alligators in Florida. Proc Southeastern Assoc Game Fish Comm 21:220–222
Gaiser EE, Scinto LJ, Richards JH, Jayachandran K, Childers DL, Trexler JC, Jones RD (2004) Phosphorus in periphyton mats provides the best metric for detecting low-level P enrichment in an oligotrophic wetland. Water Res 38:507–516
Gaiser EE, Trexler JC, Wetzel PR (2012) The Florida everglades. In: Batzer DP, Baldwin AH (eds) Wetland habitats of North America: ecology and conservation concerns. University of California Press, Berkely, pp 231–252
Gurevitch J, Padilla DK (2004) Are invasive species a major cause of extinctions? Trends Ecol Evol 19:470–474
Gurevitch J, Morrow LL, Wallace A, Walsh JS (1992) A meta-analysis of competition in field experiments. Am Nat 140:539–572
Gutierre SM, Darby PC, Valentine-Darby PL, Mellow DJ, Therrien M, Watford M (2019) Contrasting patterns of Pomacea maculata establishment and dispersal in an everglades wetland unit and a central Florida lake. Diversity 11:183
Hanning GW (1979) Aspects of reproduction in Pomacea paludosa (Mesogastropoda: Pilidae). M.S. Thesis, Florida State University, Tallahassee, FL
Hierro JL, Callaway RM (2003) Allelopathy and exotic plant invasion. Plant Soil 256:29–39
Horgan FG, Stuart AM, Kudavidanage EP (2014) Impact of invasive apple snails on the functioning and services of natural and managed wetlands. Acta Oecologica 54:90–100
Jobin WR, Ferguson FF, Berrios-Duran LA (1973) Effect of Marisa cornuarietis on populations of Biomphalaria glabrata in farm ponds of Puerto Rico. Am J Trop Med Hyg 22:278–284
Joshi RC, Cowie RH, Sebastian LS (2017) Biology and management of invasive apple snails. Philippine Rice Research Institute, Nueva Ecija, 406 pp
Kawata M, Ishigami H (1992) The growth of juvenile snails in water conditioned by snails of a different species. Oecologia 91:245–248
Kiesecker JM, Blaustein AR, Miller CL (2001) Potential mechanisms underlying the displacement of native red-legged frogs by introduced bullfrogs. Ecology 82:1964–1970
Kyle CH, Plantz AL, Shelton T, Burks RL (2014) Count your eggs before they invade: identifying and quantifying egg clutches of two invasive apple snail species (Pomacea). PLoS ONE 9:e99149
Levy MG, Tunis M, Isseroff H (1973) Population control in snails by natural inhibitors. Nature 241:65–66
Lowe S, Browne M, Boudjelas S, De Poorter M (2000) 100 of the World’s worst invasive alien species. A selection from the global invasive species database. The invasive species specialist group (ISSG) a specialist group of the species survival commission (SSC) of the World Conservation Union (IUCN)
Maida M, Sammarco PW, Coll JC (1995) Effects of soft corals on scleractinian coral recruitment. I: Directional allelopathy and inhibition of settlement. Mar Ecol Prog Ser 121:191–202
Marzolf N, Golladay S, McCormick P, Covich A, Wilde S (2018) Inter- and intra-annual apple snail egg mass dynamics in a large southeastern US reservoir. Hydrobiologia 811:155–171
Mooney HA, Cleland EE (2001) The evolutionary impact of invasive species. Proc Natl Acad Sci 98:5446–5451
Nguma JFM, McCullough FS, Masha E (1982) Elimination of Biomphalaria pfeifferi, Bulinus tropicus and Lymnaea natalensis by the ampullarid snail, Marisa cornuarietis, in a man-made dam in northern Tanzania. Acta Trop 39:85–90
O’Hare NK (2010) Pomacea paludosa (Florida Apple Snail) reproduction in restored and natural seasonal wetlands in the Everglades. Wetlands 30:1045–1052
Osenberg CW (1989) Resource limitation, competition and the influence of life history in a freshwater snail community. Oecologia 79:512–519
Pointier JP, David P (2004) Biological control of Biomphalaria glabrata, the intermediate host of schistosomes, by Marisa cornuarietis in ponds of Guadeloupe: long-term impact on the local snail fauna and aquatic flora. Biol Control 29:81–89
Pointier JP, Théron A, Imbert-Establet D, Borel G (1991) Eradication of a sylvatic focus of Schistosoma mansoni using biological control by competitor snails. Biol Control 1:244–247
Posch H, Garr AL, Reynolds E (2013) The presence of an exotic snail, Pomacea maculata, inhibits growth of juvenile Florida apple snails, Pomacea paludosa. J Molluscan Stud 79:383–385
Putnam AB, Peckol P (2018) Asymmetric interference competition between herbivorous gastropods, introduced Littorina littorea and indigenous L. obtusata. Mar Ecol Prog Ser 594:135–147
Raw JL, Miranda NA, Perissinotto R (2013) Chemical cues released by an alien invasive aquatic gastropod drive its invasion success. PLoS ONE 8:e64071
Rawlings TA, Hayes KA, Cowie RH, Collins TM (2007) The identity, distribution, and impacts of non-native apple snails in the continental United States. BMC Evol Biol 7:97
Reitz SR, Trumble JT (2002) Competitive displacement among insects and arachnids. Annu Rev Entomol 47:435–465
Relyea RA (2002) Competitor-induced plasticity in tadpoles: consequences, cues, and connections to predator-induced plasticity. Ecol Monogr 72:523–540
Riley LA, Dybdahl MF, Hall RO Jr (2008) Invasive species impact: asymmetric interactions between invasive and endemic freshwater snails. J N Am Benthol Soc 27:509–520
Rundle SD, Brönmark C (2001) Inter–and intraspecific trait compensation of defence mechanisms in freshwater snails. Proceedings of the royal society of london. Series B: biological sciences 268:1463–1468
Shuford RBE III, McCormick PV, Magson J (2005) Habitat related growth of juvenile Florida apple snails (Pomacea paludosa). Florida Sci 68:11–19
Snyder NF, Snyder HA (1969) A comparative study of mollusc predation by limpkins, Everglade kites, and boat-tailed grackles. Living Bird 8:177–223
Snyder NF, Snyder HA (1971) Defenses of the Florida apple snail Pomacea paludosa. Behaviour 40:175–214
Sykes PW, Rodgers JA, Bennetts RE (1995) Snail Kite (Rostrhamus sociabilis). In: Poole A, Gills F (eds) The birds of North America, No. 171, The academy of natural sciences, Philadelphia and the American ornithologists’ Union, Washington, DC
Thomas JD, Lough AS, Lodge RW (1975) The chemical ecology of Biomphalaria glabrata (Say), the snail host of Schistosoma mansoni Sambon: the search for factors in media conditioned by snails which inhibit their growth and reproduction. J Appl Ecol, 421–436
Turner RL (1996) Use of stems of emergent plants for oviposition by the Florida apple snail, Pomacea paludosa, and implications for marsh management. Florida Scientist 59:34–49
Turner AM, Fetterolf SA, Bernot RJ (1999) Predator identity and consumer behavior: differential effects of fish and crayfish on the habitat use of a freshwater snail. Oecologia 118:242–247
Turner AM, Turner RR, Ray SR (2007) Competition and intraguild egg predation among freshwater snails: re-examining the mechanism of interspecific interactions. Oikos 116:1895–1903
Wight BR, Darby PC, Fujisaki I (2017) Quantifying edge effects on apple snails (Pomacea paludosa) and their eggs at the junction of two wetland habitat types. J Molluscan Stud 83:351–359
Acknowledgements
We especially thank E. Cline for his management of the study wetlands and J. Sommer for his tireless help collecting data in the field and setting up experiments. T. Cocoves, A. LaGala, and B. McKenna also provided help with the experiments in the field. All experimental P. maculata were destroyed or remained captive at FAU upon termination of the study. Two anonymous reviewers provided helpful comments on an earlier version of the manuscript. The work was supported by a contract between South Florida Water Management District and FAU (#9500007911 to NJD). Metaphyton samples were processed for phosphorus at the Freshwater Resources Division at Florida International University (Miami, FL). This is contribution #1374 of the Freshwater Resources Division of the Institute of Environment at Florida International University.
Funding
This work was supported by the South Florida Water Management District.
Author information
Authors and Affiliations
Contributions
DKD, NJD and MIC conceived the studies. DKD carried out the experiments and analyzed the data with guidance from NJD. DKD and NJD wrote the manuscript with editorial feedback from MIC.
Corresponding author
Ethics declarations
Conflicts of interest
The authors have no competing interests.
Code availability
No custom code was used in this study. Code is available on request from the corresponding author, DKD.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Drumheller, D.K., Cook, M.I. & Dorn, N.J. The role of direct chemical inhibition in the displacement of a native herbivore by an invasive congener. Biol Invasions 24, 1739–1753 (2022). https://doi.org/10.1007/s10530-022-02752-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10530-022-02752-3