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Biological Invasions

, Volume 19, Issue 9, pp 2647–2661 | Cite as

Dispersal and local environment affect the spread of an invasive apple snail (Pomacea maculata) in Florida, USA

  • Steffan M. PierreEmail author
  • Pedro F. Quintana-Ascencio
  • Elizabeth H. Boughton
  • David G. Jenkins
Original Paper

Abstract

Dispersal and local environmental factors are major determinants of invasive species distribution. We examined how both dispersal-related geospatial characteristics and environmental factors influence an ongoing invasion of wetlands in a south-central Florida ranchland by non-native apple snails (Pomacea maculata, Ampullariidae). We found P. maculata in 73 (43%) of a random set of 171 wetlands in 2014. We used model selection to evaluate multiple hypotheses of predictors of P. maculata occurrence in 95 wetlands with standing water, including spatially-explicit distances in ditches from wetlands to the presumed entry point, Euclidean (overland) distances, presence/absence of ditches in wetlands, and environmental variables (e.g. pH). We also performed a 5-month field experiment in 20 wetlands to evaluate if snail absence was associated with conditions that limit survival and growth (i.e. unfavorable habitats). Snail occurrence was primarily associated with presence of ditches in wetlands and more neutral wetland pH. These variables more plausibly explained snail occurrence than did Euclidean (overland) distance and minimum ditch travel (rectilinear) distance from propagule sources (a major waterway). Wetland pH best explained survival and growth under the experimental conditions. We found no evidence that prior occupancy by conspecifics affected survival and growth, suggesting that dispersal limitation may contribute to lack of occupancy of wetlands, despite suitable pH. Our study supports man-made conduits as facilitators of dispersal by non-native species, where environmental characteristics (here pH) then also affect colonization within habitats. An understanding of both dispersal mechanisms and local environmental factors is necessary to better predict invasive species distribution.

Keywords

Invasion Pomacea maculata Dispersal Ditches Wetlands Colonization pH 

Notes

Acknowledgements

We are grateful to the staff at Buck Island Ranch and Archbold Biological Station for supporting our research and to the anonymous reviewers for comments that improved the manuscript. S. Pierre was supported by the Department of Biology, University of Central Florida (UCF) and the MacArthur Agro-ecology Research Center. Undergraduate and graduate students from the Department of Biology, UCF helped with field work, and Hilary Swain and Gene Lollis provided logistic support. This paper is contribution No. 174 from the MacArthur Agro-ecology Research Center.

References

  1. Bates D, Maechler M, Bolker B (2013) lme4: linear mixed-effects models using S4 classes. R Packag version 0999999-2 999999. citeulike article id: 1080437Google Scholar
  2. Bilton D, Freeland J, Okamura B (2001) Dispersal in freshwater invertebrates. Annu Rev Ecol Syst 32:159–181. doi: 10.1146/annurev.ecolsys.32.081501.114016 CrossRefGoogle Scholar
  3. Bissonette JA, Adair W (2008) Restoring habitat permeability to roaded landscapes with isometrically-scaled wildlife crossings. Biol Conserv 141:482–488. doi: 10.1016/j.biocon.2007.10.019 CrossRefGoogle Scholar
  4. Bliese PD (2012) Multilevel modeling in R (2.4): a brief introduction to R, the multilevel package, and the nlme package. 15:2006. http://cran.r-project.org/web/packages/multilevel/index.html
  5. Bohlen PJ, Lynch S, Shabman L et al (2009) Paying for environmental services from agricultural lands: an example from the northern Everglades. Front Ecol Environ 7:46–55. doi: 10.1890/080107 CrossRefGoogle Scholar
  6. Boughton EH, Quintana-Ascencio PF, Bohlen PJ et al (2010) Land-use and isolation interact to affect wetland plant assemblages. Ecography. doi: 10.1111/j.1600-0587.2009.06010.x Google Scholar
  7. Burks RL, Hensley SA, Kyle CH (2011) Quite the appetite: juvenile island apple snails (Pomacea insularum) survive consuming only exotic invasive plants. J Molluscan Stud 77:423–428. doi: 10.1093/mollus/eyr022 CrossRefGoogle Scholar
  8. Carlsson N (2004) Invading herbivory: the golden apple snail alters ecosystem functioning in Asian wetlands. Ecology 85:1575–1580. doi: 10.1890/03-3146 CrossRefGoogle Scholar
  9. Cattau CE, Fletcher RJ Jr, Reichert BE, Kitchens WM (2016) Counteracting effects of a non-native prey on the demography of a native predator culminate in positive population growth. Ecol Appl 26:1952–1968. doi: 10.1890/03-3146 CrossRefPubMedGoogle Scholar
  10. 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. doi: 10.1093/mollus/eyn024 CrossRefGoogle Scholar
  11. Cowie RH (2002) Apple snails (Ampullariidae) as agricultural pests: their biology, impacts and management. Molluscs Crop Pests. doi: 10.1079/9780851993201.0145 Google Scholar
  12. Diamond JM (1975) The island dilemma: lessons of modern biogeographic studies for the design of natural reserves. Biol Conserv 7:129–146. doi: 10.1016/0006-3207(75)90052-X CrossRefGoogle Scholar
  13. Figuerola J, Green AJ (2002) Dispersal of aquatic organisms by waterbirds: a review of past research and priorities for future studies. Freshw Biol 47:483–494. doi: 10.1046/j.1365-2427.2002.00829.x CrossRefGoogle Scholar
  14. Francis RA (2012) A handbook of global freshwater invasive species. Earthscan, London. doi: 10.4324/9780203127230 Google Scholar
  15. Glass NH, Darby PC (2008) The effect of calcium and pH on Florida apple snail, Pomacea paludosa (Gastropoda:Ampullariidae), shell growth and crush weight. Aquat Ecol 43:1085–1093. doi: 10.1007/s10452-008-9226-3 CrossRefGoogle Scholar
  16. Goodall DW (1968) Island biogeography. The theory of island biogeography Robert H. MacArthur Edward O. Wilson. BioScience 18:904–905. doi: 10.2307/1294167 CrossRefGoogle Scholar
  17. Gurevitch J, Fox GA, Wardle GM et al (2011) Emergent insights from the synthesis of conceptual frameworks for biological invasions. Ecol Lett 14:407–418. doi: 10.1111/j.1461-0248.2011.01594.x CrossRefPubMedGoogle Scholar
  18. Hanski I, Thomas CD (1994) Metapopulation dynamics and conservation: a spatially explicit model applied to butterflies. Biol Conserv 68:167. doi: 10.1016/0006-3207(94)90348-4 CrossRefGoogle Scholar
  19. Havel JE, Shurin JB, Jones JR (2002) Estimating dispersal from patterns of spread: spatial and local control of lake invasions. Ecology 83:3306–3318. doi: 10.1890/0012-9658(2002)083[3306:EDFPOS]2.0.CO;2 CrossRefGoogle Scholar
  20. Hayes KA, Joshi RC, Thiengo SC, Cowie RH (2008) Out of South America: multiple origins of non-native apple snails in Asia. Divers Distrib 14:701–712. doi: 10.1111/j.1472-4642.2008.00483.x CrossRefGoogle Scholar
  21. Hayes KA, Cowie RH, Thiengo SC, Strong EE (2012) Comparing apples with apples: clarifying the identities of two highly invasive Neotropical Ampullariidae (Caenogastropoda). Zool J Linn Soc 166:723–753. doi: 10.1111/j.1096-3642.2012.00867.x CrossRefGoogle Scholar
  22. Heger T, Pahl AT, Botta-Dukát Z et al (2013) Conceptual frameworks and methods for advancing invasion ecology. Ambio 42:527–540. doi: 10.1007/s13280-012-0379-x CrossRefPubMedPubMedCentralGoogle Scholar
  23. Herzon I, Helenius J (2008) Agricultural drainage ditches, their biological importance and functioning. Biol Conserv 141:1171–1183. doi: 10.1016/j.biocon.2008.03.005 CrossRefGoogle Scholar
  24. Hunter RD (1990) Effects of low pH and low calcium concentration on the pulmonate snail Planorbella trivolvis: a laboratory study. Can J Zool 68:1578–1583. doi: 10.1139/z90-233 CrossRefGoogle Scholar
  25. Kyle C, Kropf A, Burks R (2011) Prime waterfront real estate: apple snails choose wild taro for oviposition sites. Curr Zool 57:630–641. doi: 10.1093/czoolo/57.5.630 CrossRefGoogle Scholar
  26. 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), AucklandGoogle Scholar
  27. Mazerolle MJ (2005) Drainage ditches facilitate frog movements in a hostile landscape. Landsc Ecol 20:579–590. doi: 10.1007/s10980-004-3977-6 CrossRefGoogle Scholar
  28. Mazerolle MJ (2013) AICcmodavg: model selection and multimodel inference based on (Q)AIC(c). R package version 1.27. http://CRAN.R-project.org/package=AICcmodavg
  29. Medley KA (2010) Niche shifts during the global invasion of the Asian tiger mosquito, Aedes albopictus Skuse (Culicidae), revealed by reciprocal distribution models. Glob Ecol Biogeogr 19:122–133. doi: 10.1111/j.1466-8238.2009.00497.x CrossRefGoogle Scholar
  30. Medley KA, Boughton EH, Jenkins DG et al (2015) Intense ranchland management tips the balance of regional and local factors affecting wetland community structure. Agric Ecosyst Environ 212:207–244. doi: 10.1016/j.agee.2015.06.024 CrossRefGoogle Scholar
  31. Morrison WE, Hay ME (2010) 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. doi: 10.1007/s10530-010-9881-x CrossRefGoogle Scholar
  32. Nakagawa S, Schielzeth H (2013) A general and simple method for obtaining R2 from generalized linear mixed-effects models. Methods Ecol Evol 4:133–142. doi: 10.1111/j.2041-210x.2012.00261.x CrossRefGoogle Scholar
  33. Noss RF (2011) Between the devil and the deep blue sea: Florida’s unenviable position with respect to sea level rise. Clim Change 107:1–16. doi: 10.1007/s10584-011-0109-6 CrossRefGoogle Scholar
  34. Pimentel D, Lach L, Zuniga R, Morrison D (2000) Environmental and economic costs of nonindigenous species in the United States. Bioscience 50:53–65. doi: 10.1641/0006-3568(2000)050[0053:EAECON]2.3.CO;2 CrossRefGoogle Scholar
  35. 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. doi: 10.1093/mollus/eyt034 CrossRefGoogle Scholar
  36. Puth L, Post D (2005) Studying invasion: have we missed the boat? Ecol Lett. doi: 10.1111/j.1461-0248.2005.00774.x Google Scholar
  37. Rawlings T, Hayes K, Cowie R, Collins T (2007) The identity, distribution, and impacts of non-native apple snails in the continental United States. BMC Evol Biol 7:97. doi: 10.1186/1471-2148-7-97 CrossRefPubMedPubMedCentralGoogle Scholar
  38. Reiss KC (2006) Florida Wetland Condition Index for depressional forested wetlands. Ecol Indic 6:337–352. doi: 10.1016/j.ecolind.2005.03.013 CrossRefGoogle Scholar
  39. Ricklefs RE (1987) Community diversity: relative roles of local and regional processes. Science 235:167–171. doi: 10.1126/science.235.4785.167 CrossRefPubMedGoogle Scholar
  40. Ricklefs RE (2004) A comprehensive framework for global patterns in biodiversity. Ecol Lett 7:1–15. doi: 10.1046/j.1461-0248.2003.00554.x CrossRefGoogle Scholar
  41. R Core Team (2014) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/
  42. Sakai A, Allendorf FW, Holt J et al (2001) The population biology of invasive species. Annu Rev Ecol Evol Syst 32:305–332. doi: 10.1146/annurev.ecolsys.32.081501.114037 CrossRefGoogle Scholar
  43. Seuffert ME, Martín PR (2009) Dependence on aerial respiration and its influence on microdistribution in the invasive freshwater snail Pomacea canaliculata (Caenogastropoda, Ampullariidae). Biol Invasions 12:1695–1708. doi: 10.1007/s10530-009-9582-5 CrossRefGoogle Scholar
  44. Simberloff D (2003) Eradication—preventing invasions at the outset. Weed Sci 51:247–253. doi: 10.1614/0043-1745(2003)051 CrossRefGoogle Scholar
  45. Steinman AD, Conklin J, Bohlen PJ, Uzarski DG (2003) Influence of cattle grazing and pasture land use on macroinvertebrate communities in freshwater wetlands. Wetlands 23:877–889. doi: 10.1672/0277-5212(2003)023[0877:IOCGAP]2.0.CO;2 CrossRefGoogle Scholar
  46. Swain HM, Bohlen PJ, Campbell KL et al (2007) Integrated ecological and economic analysis of ranch management systems: an example from South Central Florida. Rangel Ecol Manag 60:1–11. doi: 10.2111/05-071R1.1 CrossRefGoogle Scholar
  47. Václavík T, Meentemeyer RK (2012) Equilibrium or not? Modelling potential distribution of invasive species in different stages of invasion. Divers Distrib 18:73–83. doi: 10.1111/j.1472-4642.2011.00854.x CrossRefGoogle Scholar
  48. Valéry L, Fritz H, Lefeuvre J-C, Simberloff D (2008) In search of a real definition of the biological invasion phenomenon itself. Biol Invasions 10:1345–1351. doi: 10.1007/s10530-007-9209-7 CrossRefGoogle Scholar
  49. Van Leeuwen C, Huig N, Van Der Velde G et al (2013) How did this snail get here? Several dispersal vectors inferred for an aquatic invasive species. Freshw Biol 58:88–99. doi: 10.1111/fwb.12041 CrossRefGoogle Scholar
  50. Wada T, Ichinose K, Yusa Y, Sugiura N (2004) Decrease in density of the apple snail Pomacea canaliculata (Lamarck) (Gastropoda:Ampullariidae) in paddy fields after crop rotation with soybean, and its population growth during the crop season. Appl Entomol Zool 39:367–372. doi: 10.1303/aez.2004.367 CrossRefGoogle Scholar
  51. Wickham H (2008) ggplot2: an implementation of the grammar of graphics. R package version 0.7Google Scholar
  52. Youens AK, Burks RL (2008) Comparing apple snails with oranges: the need to standardize measuring techniques when studying Pomacea. Aquat Ecol 42:679–684. doi: 10.1007/s10452-007-9140-0 CrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG Switzerland 2017

Authors and Affiliations

  • Steffan M. Pierre
    • 1
    • 2
    Email author
  • Pedro F. Quintana-Ascencio
    • 1
  • Elizabeth H. Boughton
    • 2
  • David G. Jenkins
    • 1
  1. 1.Department of BiologyUniversity of Central FloridaOrlandoUSA
  2. 2.MacArthur Agroecology Research Center, Archbold ExpeditionsLake PlacidUSA

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