Biological Invasions

, Volume 17, Issue 2, pp 711–723 | Cite as

Coexistence of the endangered, endemic Chittenango ovate amber snail (Novisuccinea chittenangoensis) and a non-native competitor

  • Steven P. Campbell
  • Jacqueline L. Frair
  • James P. Gibbs
  • Rebecca J. Rundell
Original Paper


Distinguishing between non-native species that coexist with native species and those that threaten their persistence is critical for conservation and management. We investigated this distinction for a non-native terrestrial snail (Succinea sp.) (Sp. B) that occurs with the closely-related Chittenango ovate amber snail (Novisuccinea chittenangoensis) (COAS), an endangered species that is restricted to a single, known site. In 2008 and 2009, we performed ex situ competition experiments to examine the effects of density and body size of Sp. B on growth and mortality of COAS. We also conducted mark-recapture surveys from 2002 to 2009 to document trends of the in situ population of COAS and to identify spatio-temporal factors that may mitigate any competitive interactions between COAS and Sp. B. We observed lower growth rates and higher mortality rates of COAS at higher densities and larger sizes of Sp. B, indicating that the species compete. Nevertheless, population trends indicated that COAS population size was fluctuating but not in decline, and the spatial distribution, phenology, and size structure of each species indicated that there were enough mitigating factors to allow COAS to persist in the presence of Sp. B. Collectively, these results suggest that temporal niche partitioning resulting from a trade-off between growth and longevity of each species may enable their coexistence. Our results also suggest that control of Sp. B is unnecessary and, more generally, underscore the importance of conducting research aimed at understanding the effects of non-native species before instituting long-term, costly, and potentially unnecessary control measures.


Non-native species Competition Coexistence Succineid snails Endangered species Endemic species 



We would like to acknowledge Robyn Niver, Jeremy Coleman, Laury Zicari, and Alvin Breisch for guidance and oversight of the project, Joseph Brown and Jeffrey Wyatt for regularly helping with mark-recapture surveys, Stephanie Chapin for providing access to the park and on-site support, James Arrigoni and Kristian Whiteleather for conducting mark-recapture surveys prior to 2008, Robert Steidl for statistical advice, Timothy King for providing sequence data for Sp. B, and Brenden Holland and the Oregon Department of Agriculture for use of their Succineidae alignment. We are also grateful to Jacob Bengeyfield and Brian Stillwell for their help with all aspects of field work in 2008, Carolyn Miller and Ian Trewella for their help with field work in 2009, and the numerous volunteers who helped conduct mark-recapture surveys. Finally, we would like to thank two anonymous reviewers for their valuable comments on the manuscript. This study was funded by the United States Fish and Wildlife Service.

Supplementary material

10530_2014_763_MOESM1_ESM.doc (2.7 mb)
Supplementary material 1 (DOC 2765 kb)


  1. Abrams P (1984) Variability in resource consumption rates and the coexistence of competing species. Theor Popul Biol 25:106–124CrossRefGoogle Scholar
  2. Armstrong S (1995) Rare plants protect Cape’s water supplies. New Sci 145:8Google Scholar
  3. Baur B (1988) Population regulation in the land snail Arianta arbustorum: density effects on adult size, clutch size and incidence of egg cannibalism. Oecologia 77:390–394CrossRefGoogle Scholar
  4. Baur B, Baur A (1990) Experimental evidence for intra- and interspecific competition in two species of rock-dwelling land snails. J Anim Ecol 59:301–315CrossRefGoogle Scholar
  5. Baur A, Baur B (1992) Responses in growth, reproduction and life span to reduced competition pressure in the land snail Balea perversa. Oikos 63:298–304CrossRefGoogle Scholar
  6. Baur B, Raboud C (1988) Life history of the land snail Arianta arbustorum along an altitudinal gradient. J Anim Ecol 57:71–87CrossRefGoogle Scholar
  7. Byers JE, Reichard S, Randall JM, Parker IM, Smith CS, Lonsdale WM, Atkinson IAE, Seastedt TR, Williamson M, Chornesky E, Hayes D (2002) Directing research to reduce the impacts of non-indigenous species. Conserv Biol 16:630–640CrossRefGoogle Scholar
  8. 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 48:237–246CrossRefGoogle Scholar
  9. Campbell SP, Clark A, Crampton L, Guerry AD, Hatch L, Hosseini PR, Lawler JJ, O’Connor RJ (2002) An assessment of monitoring efforts in endangered species recovery plans. Ecol Appl 12:674–681CrossRefGoogle Scholar
  10. Carlsson NOL, Brönmark C (2006) Size-dependent effects of an invasive herbivorous snail (Pomacea canaliculata) on macrophytes and periphyton in Asian wetlands. Freshwater Biol 51:695–704CrossRefGoogle Scholar
  11. Carter MA, Ashdown M (1984) Experimental studies on the effects of density, size, and shell colour and banding phenotypes on the fecundity of Cepaea nemoralis. Malacologia 25:291–302Google Scholar
  12. Chesson P (1991) A need for niches? Trends Ecol Evol 6:26–28PubMedCrossRefGoogle Scholar
  13. Chesson P (2000a) Mechanisms of maintenance of species diversity. Annu Rev Ecol Syst 31:343–366CrossRefGoogle Scholar
  14. Chesson P (2000b) General theory of competitive coexistence in spatially varying environments. Theor Popul Biol 58:211–237PubMedCrossRefGoogle Scholar
  15. Chesson P, Huntly N (1997) The roles of harsh and fluctuating conditions in the dynamics of ecological communities. Am Nat 150:519–553PubMedCrossRefGoogle Scholar
  16. Choquenot D, Parkes J (2001) Setting thresholds for pest control: how does pest density affect resource viability? Biol Conserv 99:29–46CrossRefGoogle Scholar
  17. Cooch E, White G (2008) Goodness of fit testing. In: Cooch E, White G (eds) Program MARK: a gentle introduction, 7th edn. Fort Collins, Colorado, USA, pp 5.1–5.40Google Scholar
  18. Cross WF, Benke AC (2002) Intra- and interspecific competition among coexisting lotic snails. Oikos 96:251–264CrossRefGoogle Scholar
  19. 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 Moll Stud 48:257–265Google Scholar
  20. Đatkauskienë I (2005) Characteristic of lifespan and reproduction period of Succinea putris (L.) (Gastopoda: Styllomatophora). Ekologija 3:28–33Google Scholar
  21. Davison A, Blackie RL, Scothern GP (2009) DNA barcoding of stylommatophoran land snails: a test of existing sequences. Mol Ecol Resour 9:1092–1101PubMedCrossRefGoogle Scholar
  22. Drury WH (1980) Rare species of plants. Rhodora 82:3–48Google Scholar
  23. Gaston KJ, Kunin WE (1997) Rare-common differences: an overview. In: Kunin WE, Gaston KJ (eds) The biology of rarity: causes and consequences of rare-common differences. Chapmann and Hall, London, pp 11–29Google Scholar
  24. Grice T (2009) Principles of containment and control of invasive species. In: Clout MN, Williams PA (eds) Invasive species management: a handbook of principles and techniques. Oxford University Press Inc., New York, pp 61–76Google Scholar
  25. Grimm FW (1981) A review of the Chittenango ovate amber snail, Succinea chittenangoensis, Pisbry, 1908—a Pleistocene relict now greatly restricted in distribution. Contract report to the New York State Department of Environmental ConservationGoogle Scholar
  26. Grover JP (1997) Resource competition. Chapman and Hall, LondonCrossRefGoogle Scholar
  27. Hartley S, Shorrocks B (2002) A general framework for the aggregation model of coexistence. J Anim Ecol 71:651–662CrossRefGoogle Scholar
  28. Hoagland KE, Davis GM (1987) The succineid snail fauna of Chittenango Falls, New York: taxonomic status with comparisons to other relevant taxa. Proc Acad Nat Sci Phila 139:465–526Google Scholar
  29. Hubricht L (1985) The distributions of the native land mollusks of the Eastern United States. Fieldiana, Zoology, New Series, No. 24: 191 ppGoogle Scholar
  30. Ives AR (1988) Covariance, coexistence, and the population dynamics of two competitors using a patchy resource. J Theor Biol 133:345–361CrossRefGoogle Scholar
  31. Kimura K, Chiba S (2010) Interspecific interference competition alters habitat use patterns in two species of land snails. Evol Ecol 24:815–825CrossRefGoogle Scholar
  32. Kneitel JM, Chase JM (2004) Trade-offs in community ecology: linking spatial scales and species coexistence. Ecol Lett 7:69–80CrossRefGoogle Scholar
  33. Ledergerber S, Baminger H, Bisenberger A, Kleewein D, Sattmann H, Baur B (1997) Differences in resting-site preference in two coexisting land snails, Arianta arbustorum and Arianta chamaeleon (Helicidae), on alpine slopes. J Moll Stud 63:1–8CrossRefGoogle Scholar
  34. Leisnham PT, Juliano SA (2009) Spatial and temporal patterns of coexistence between competing Aedes mosquitoes in urban Florida. Oecologia 160:343–352PubMedCentralPubMedCrossRefGoogle Scholar
  35. Lloyd KM, Lee WG, Wilson JB (2002) Competitive abilities of rare and common plants: comparisons using Acaena (Rosaceae) and Chionochloa (Poaceae) from New Zealand. Conserv Biol 16:975–985CrossRefGoogle Scholar
  36. MacArthur R, Levins R (1967) The limiting similarity, convergence, and divergence of coexisting species. Am Nat 101:377–385CrossRefGoogle Scholar
  37. Maddison DR, Maddison WP (2001) MacClade 4: analysis of phylogeny and character evolution. Sinauer Associates, SunderlandGoogle Scholar
  38. Molloy AW, Norton RA (1993) Establishment of a captive colony of Chittenango ovate amber snails (Novisuccinea chittenangoensis). Interim technical report—Department of Environmental Conservation contract # C002743Google Scholar
  39. Moora M, Jõgar Ü (2006) Competitive responses of the rare Viola elatior and the common Viola mirabilis. Plant Ecol 184:105–110CrossRefGoogle Scholar
  40. Nature Conservancy (1996) America’s least wanted: alien species invasions of U.S. ecosystems. The Nature Conservancy, Arlington, VA, USAGoogle Scholar
  41. Oosterhoff LM (1977) Variation in growth rate as an ecological factor in the landsnail Cepaea nemoralis (L.). Neth J Zool 27:1–132CrossRefGoogle Scholar
  42. Osunkoya OO, Swanborough PW (2001) Reproductive and ecophysiological attributes of the rare Gardenia actinocarpa (Rubiaceae) compared with its common co-occurring congener, G. ovularis. Aust J Bot 49:471–478CrossRefGoogle Scholar
  43. Pearce TA (1997) Interference and resource competition in two land snails: adults inhibit conspecific juvenile growth in field and laboratory. J Moll Stud 63:389–399CrossRefGoogle Scholar
  44. Petraitis PS, Latham RE, Niesenbaum RA (1989) The maintenance of species diversity by disturbance. Q Rev Biol 64:393–418CrossRefGoogle Scholar
  45. Pimental D (ed) (2002) Biological invasions: economic and environmental costs of alien plant, animal, and microbe species. CRC Press, Boca RatonGoogle Scholar
  46. Rabinowitz D, Rapp JK, Dixon PM (1984) Competitive abilities of sparse grass species: means of persistence or cause of abundance. Ecology 65:1144–1154CrossRefGoogle Scholar
  47. Rundell RJ, Holland BS, Cowie RH (2004) Molecular phylogeny and biogeography of the endemic Hawaiian Succineidae (Gastropoda: Pulmonata). Mol Phylogenet Evol 31:246–255PubMedCrossRefGoogle Scholar
  48. 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 32:305–332CrossRefGoogle Scholar
  49. SAS Institute Inc. (2008) SAS 9.2 help and documentation. SAS Institute Inc., Cary, NCGoogle Scholar
  50. Schwarz CJ, Arnason AN (2008) Jolly–Seber models in MARK. In: Cooch E, White G (eds) Program MARK: a gentle introduction, 7th edn. Fort Collins, Colorado, USA, pp 13.1–13.53Google Scholar
  51. Shackelford N, Hobbs RJ, Heller NE, Hallett LM, Seastedt TR (2013) Finding a middle-ground: the native/non-native debate. Biol Conserv 158:55–62CrossRefGoogle Scholar
  52. Simberloff D (1981) Community effects of introduced species. In: Nitecki MH (ed) Biotic crises in ecological and evolutionary time. Academic Press, New York, pp 53–81CrossRefGoogle Scholar
  53. Simberloff D (2003) How much information on population biology is needed to manage introduced species? Conserv Biol 17:83–92CrossRefGoogle Scholar
  54. Smallridge MA, Kirby GC (1988) Competitive interactions between the land snails Theba pisana (Müller) and Cernuella virgata (da Costa) from south Australia. J Molluscan Stud 54:251–258CrossRefGoogle Scholar
  55. Snyder KM, Baskin JM, Baskin CC (1994) Comparative ecology of the narrow endemic Echinacea tennesseensis and two geographically widespread congeners: relative competitive ability and growth characteristics. Int J Plant Sci 155:57–65CrossRefGoogle Scholar
  56. Stearns SC (1989) Trade-offs in life history evolution. Funct Ecol 3:259–268CrossRefGoogle Scholar
  57. Strubbe D, Shwartz A, Chiron F (2011) Concerns regarding the scientific evidence informing impact risk assessment and management recommendations for invasive birds. Biol Conserv 144:2112–2118CrossRefGoogle Scholar
  58. Swofford DL (2001) PAUP*: phylogenetic analysis using parsimony (* and other methods), v. 4.0.b10. Sinauer Associates, SunderlandGoogle Scholar
  59. Tattersfield P (1981) Density and environmental effects on shell size in some sand dune snail populations. Biol J Linn Soc 16:71–81CrossRefGoogle Scholar
  60. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The ClustalX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 24:4876–4882CrossRefGoogle Scholar
  61. Tilman D (1982) Resource competition and community structure. Princeton University Press, PrincetonGoogle Scholar
  62. Tilman D (2000) Causes, consequences, and ethics of biodiversity. Nature 405:208–211PubMedCrossRefGoogle Scholar
  63. U.S. Fish and Wildlife Service (USFWS) (2006) Chittenango ovate amber snail (Novisuccinea chittenangoensis) recovery plan, 1st revision. Hadley, MAGoogle Scholar
  64. Walck JL, Baskin JM, Baskin CC (1999) Relative competitive abilities and growth characteristics of a narrowly endemic and a geographically widespread Solidago species (Asteraceae). Am J Bot 86:820–828PubMedCrossRefGoogle Scholar
  65. White GC, Burnham KP (1999) Program MARK: survival estimation from populations of marked animals. Bird Study 46:S120–S139CrossRefGoogle Scholar
  66. Wilcove DS, Rothstein D, Dubow J, Phillips A, Losos E (1998) Quantifying threats to imperiled species in the United States. Bioscience 48:607–615CrossRefGoogle Scholar
  67. Williamson MH (1996) Biological invasions. Chapman and Hall, New YorkGoogle Scholar
  68. Williamson P, Cameron RAD, Carter MA (1976) Population density affecting adult shell size of snail Cepaea nemoralis L. Nature 263:496–497PubMedCrossRefGoogle Scholar
  69. Zera AJ, Harshman LG (2001) The physiology of life history trade-offs in animals. Annu Rev Ecol Syst 32:95–126CrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2014

Authors and Affiliations

  • Steven P. Campbell
    • 1
    • 2
  • Jacqueline L. Frair
    • 1
  • James P. Gibbs
    • 1
  • Rebecca J. Rundell
    • 1
  1. 1.Department of Environmental and Forest BiologySUNY College of Environmental Science and ForestrySyracuseUSA
  2. 2.Albany Pine Bush Preserve CommissionAlbanyUSA

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