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Invader–invader mutualism influences land snail community composition and alters invasion success of alien species in tropical rainforest

Abstract

Mutualism between invaders may alter a key characteristic of the recipient community, leading to the entry or in situ release of other exotic species. We considered whether mutualism between invasive yellow crazy ant Anoplolepis gracilipes and exotic honeydew-producing scale insects indirectly facilitated land snails (exotic and native) via the removal of a native omnivore, the red land crab Gecarcoidea natalis. In plateau rainforest on Christmas Island, Indian Ocean, the land snail community was surveyed at 28 sites representing four forest states that differed in the density of red crabs, the abundance of yellow crazy ants and management history. One-way ANOVAs and multivariate analyses were used to determine differences in land snail species abundance and composition between forest states. Sample-based rarefaction was used to determine differences in species richness. The removal of the red land crab by supercolonies of yellow crazy ants was associated with a significant increase in the abundance of both invasive (14 species) and native (four species) land snails. Compositional differences in the land snail community were driven most strongly by the significantly greater abundance of a few common species in forest states devoid of red crabs. In forest where the crab population had recovered following management for ants, the land snail assemblage did not differ from intact, uninvaded forest. The land snail community was dominated by exotic species that can coexist alongside red crabs in rainforest uninvaded by exotic ants and scale insects. However, the ant–scale mutualism significantly increased land snail abundance and altered their composition indirectly though the alteration of the recipient community. We suggest these constitute ‘population-release’ secondary invasion in which the impacts of previously successful invaders facilitate a significant increase in abundance of other exotic species already established at low density within the community. Understanding facilitative interactions between invaders and indirect consequences of impacts will provide invaluable insights for conservation in heavily invaded ecosystems.

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References

  • Abbott KL (2006) Spatial dynamics of supercolonies of the invasive yellow crazy ant, Anoplolepis gracilipes, on Christmas Island, Indian Ocean. Divers Distrib 12:101–110

    Article  Google Scholar 

  • Abbott KL, Green PT (2007) Collapse of an ant-scale mutualism in a rainforest on Christmas Island. Oikos 116:1238–1246

    Article  Google Scholar 

  • Adams MJ, Pearl CA, Bury RB (2003) Indirect facilitation of an anuran invasion by non-native fishes. Ecol Lett 6:343–351

    Article  Google Scholar 

  • Aizen MA, Morales CL, Morales JM (2008) Invasive mutualists erode native pollination webs. PLoS Biol 6:e31

    Article  PubMed Central  PubMed  Google Scholar 

  • Aubry S, Magnin F, Bonnet V, Preece RC (2005) Multi-scale altitudinal patterns in species richness of land snail communities in south-eastern France. J Biogeogr 32:985–998

    Article  Google Scholar 

  • Barker GM, Mayhill PC (1999) Patterns of diversity and habitat relationships in terrestrial mollusc communities of the Pukeamaru Ecological District, northeastern New Zealand. J Biogeogr 26:215–238

    Article  Google Scholar 

  • Boland CRJ, Smith MJ, Retallick K et al (2011) Heli-baiting using low concentration fipronil to control invasive yellow crazy ant supercolonies on Christmas Island, Indian Ocean. In: Veitch CR, Clout MN, Towns DR (eds) Isl. invasives erad. manag. IUCN, Gland, pp 252–256

    Google Scholar 

  • Bourgeois K, Suehs CM, Vidal E, Medail F (2005) Invasional meltdown potential: facilitation between introduced plants and mammals on French Mediterranean islands. Ecoscience 12:248–256

    Article  Google Scholar 

  • Cameron RAD (1992) Land snail faunas of the Napier and Oscar Ranges, Western Australia; diversity, distribution and speciation. Biol J Linn Soc 45:271–286

    Article  Google Scholar 

  • Cameron RAD, Pokryszko BM (2005) Estimating the species richness and composition of land mollusc communities: problems, consequences and practical advice. J Conchol 38:529–547

    Google Scholar 

  • Cameron RAD, Mylonas M, Triantis K et al (2003) Land-snail diversity in a square kilometre of Cretan maquis: modest species richness, high density and local homogeneity. J Molluscan Stud 69:93–99

    Article  Google Scholar 

  • Catford JA, Jansson R, Nilsson C (2009) Reducing redundancy in invasion ecology by integrating hypotheses into a single theoretical framework. Divers Distrib 15:22–40

    Article  Google Scholar 

  • Clergeau P, Tapko N, Fontaine B (2011) A simplified method for conducting ecological studies of land snail communities in urban landscapes. Ecol Res 26:515–521

    Article  Google Scholar 

  • Colwell R (2013) EstimateS: statistical estimation of species richness and shared species from samples. Version 9 and earlier. User’s guide and application. http://purloclc.org/estimates

  • Cross JR (1981) The establishment of Rhododenron ponticum in the Killarney Oakwoods, SW Ireland. J Ecol 69:807–824

    Article  Google Scholar 

  • Davis NE, O’Dowd DJ, Green PT, Mac Nally R (2008) Effects of an alien ant invasion on abundance, behavior, and reproductive success of endemic island birds. Conserv Biol 22:1165–1176

    Article  PubMed  Google Scholar 

  • Davis NE, O’Dowd DJ, Mac Nally R, Green PT (2010) Invasive ants disrupt frugivory by endemic island birds. Biol Lett 6:85–88

    Article  PubMed Central  PubMed  Google Scholar 

  • de Chavez ERC, de Lara AV (2011) Diversity and spatial distribution patterns of macro land snails in Mount Makiling Forest Reserve, Philippines. Asia Life Sci 20:185–201

    Google Scholar 

  • de Winter AJ, Gittenberger E (1998) The land snail fauna of a square kilometer patch of rainforest in southwestern Cameroon, high species richness, low abundance and seasonal fluctuations. Malacologia 40:231–250

    Google Scholar 

  • Drescher J, Blüthgen N, Feldhaar H (2007) Population structure and intraspecific aggression in the invasive ant species Anoplolepis gracilipes in Malaysian Borneo. Mol Ecol 16:1453–1465

    Article  CAS  PubMed  Google Scholar 

  • Du Puy DJ (1993) Christmas Island. In: George AS, Orchard AE, Hewson HJ (eds) Flora of Australia, vol 50. Oceanic islands 2. Australian Government, Canberra, pp 1–30

    Google Scholar 

  • Elton CS (1958) The ecology of invasions by animals and plants. Methuen, London

    Book  Google Scholar 

  • Falkland AC (1986) Christmas Island (Indian Ocean) water resources development, study in relation to proposed waterfall. Unpublished report prepared by the Hydrology and Water Resources Unit, Transport Territories, and Works Division for the Department of Territories

  • Flory SL, Bauer JT (2014) Experimental evidence for indirect facilitation among invasive plants. J Ecol 102:12–18

    Article  Google Scholar 

  • Forys EA, Allen CR, Wojcik DP (2001) The likely cause of extinction of the tree snail Orthanlicus reses (Say). J Molluscan Stud 67:369–376

    Article  Google Scholar 

  • Giraud T, Pedersen J, Keller L (2002) Evolution of supercolonies: the Argentine ants of southern Europe. Proc Natl Acad Sci USA 99:6075–6079

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Gotelli NJ, Colwell RK (2001) Quantifying biodiversity: procedures and pitfalls in the measurement and comparison of species richness. Ecol Lett 4:379–391

    Article  Google Scholar 

  • Green PT (1997) Red crabs in rain forest on Christmas Island, Indian Ocean: activity patterns, density and biomass. J Trop Ecol 13:17–38

    Article  Google Scholar 

  • Green PT, O’Dowd DJ (2009) Management of invasive invertebrates: lessons from the management of an invasive alien ant. In: Clout MN, Williams PA (eds) Invasive species manag. a handb. princ. tech. Oxford University Press, Oxford, pp 153–172

    Google Scholar 

  • Green PT, Odowd DJ, Lake PS (1997) Control of seedling recruitment by land crabs in rain forest on a remote oceanic island. Ecology 78:2474–2486

    Article  Google Scholar 

  • Green PT, Lake PS, O’Dowd DJ (1999) Monopolization of litter processing by a dominant land crab on a tropical oceanic island. Oecologia 119:435–444

    Article  Google Scholar 

  • Green PT, O’Dowd DJ, Lake PS (2008) Recruitment dynamics in a rainforest seedling community: context-independent impact of a keystone consumer. Oecologia 156:373–385

    Article  PubMed  Google Scholar 

  • Green PT, O’Dowd DJ, Abbott KL et al (2011) Invasional meltdown: invader–invader mutualism facilitates a secondary invasion. Ecology 92:1758–1768

    Article  PubMed  Google Scholar 

  • Grinath JB, Inouye BD, Underwood N, Billick I (2012) The indirect consequences of a mutualism: comparing positive and negative components of the net interaction between honeydew-tending ants and host plants. J Anim Ecol 81:494–502

    Article  PubMed  Google Scholar 

  • Grosholz ED (2005) Recent biological invasion may hasten invasional meltdown by accelerating historical introductions. Proc Natl Acad Sci USA 102:1088–1091

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Grosholz ED, Ruiz GM, Dean CA et al (2000) The impacts of a nonindigenous marine predator in a California bay. Ecology 81:1206–1224

    Article  Google Scholar 

  • Helms KR, Hayden CP, Vinson SB (2011) Plant-based food resources, trophic interactions among alien species, and the abundance of an invasive ant. Biol Invasions 13:67–79

    Article  Google Scholar 

  • Holway DA, Suarez AV (2006) Homogenization of ant communities in mediterranean California: the effects of urbanization and invasion. Biol Conserv 127:319–326

    Article  Google Scholar 

  • Hylander K, Nilsson C, Gunnar Jonsson B, Göthner T (2005) Differences in habitat quality explain nestedness in a land snail meta-community. Oikos 108:351–361

    Article  Google Scholar 

  • Johnson PTJ, Olden JD, Solomon CT, Vander Zanden MJ (2009) Interactions among invaders: community and ecosystem effects of multiple invasive species in an experimental aquatic system. Oecologia 159:161–170

    Article  PubMed  Google Scholar 

  • Kessner V (2006) Report on the March 2006 survey of land snails (Mollusc: Pulmonata) of Christmas Island, Indian Ocean. Unpublished report to Parks Australia

  • Labaune C, Magnin F (2001) Land snail communities in Mediterranean upland grasslands: the relative importance of four sets of environmental and spatial variables. J Molluscan Stud 67:463–474

    Article  Google Scholar 

  • Lake PS, O’Dowd DJ (1991) Red crabs in rain forest, Christmas Island: biotic resistance to invasion by an exotic snail. Oikos 62:25–29

    Article  Google Scholar 

  • Liew TS, Schilthuizen M, bin Lakim M (2010) The determinants of land snail diversity along a tropical elevational gradient: insularity, geometry and niches. J Biogeogr 37:1071–1078

    Article  Google Scholar 

  • Lockwood JL, Cassey P, Blackburn TM (2009) The more you introduce the more you get: the role of colonization pressure and propagule pressure in invasion ecology. Divers Distrib 15:904–910

    Article  Google Scholar 

  • Meyer WM, Ostertag R, Cowie RH (2013) Influence of terrestrial molluscs on litter decomposition and nutrient release in a Hawaiian Rain Forest. Biotropica 45:719–727

    Article  Google Scholar 

  • Montgomery WI, Lundy MG, Reid N (2011) “Invasional meltdown”: evidence for unexpected consequences and cumulative impacts of multispecies invasions. Biol Invasions 14:1111–1125

    Article  Google Scholar 

  • O’Dowd DJ, Green PT, Lake PS (2003) Invasional “meltdown” on an oceanic island. Ecol Lett 6:812–817

    Article  Google Scholar 

  • Preston DL, Henderson JS, Johnson PTJ (2012) Community ecology of invasions: direct and indirect effects of multiple invasive species on aquatic communities. Ecology 93:1254–1261

    Article  PubMed  Google Scholar 

  • Relva MA, Nunez MA, Simberloff D (2010) Introduced deer reduce native plant cover and facilitate invasion of non-native tree species: evidence for invasional meltdown. Biol Invasions 12:303–311

    Article  Google Scholar 

  • Ricciardi A (2001) Facilitative interactions among aquatic invaders: is an “invasional meltdown” occurring in the Great Lakes? Can J Fish Aquat Sci 58:2513–2525

    Article  Google Scholar 

  • Rodriguez LF (2006) Can invasive species facilitate native species? Evidence of how, when, and why these impacts occur. Biol Invasions 8:927–939

    Article  Google Scholar 

  • Simberloff D (2006) Invasional meltdown 6 years later: important phenomenon, unfortunate metaphor, or both? Ecol Lett 9:912–919

    Article  PubMed  Google Scholar 

  • Simberloff D, Von Holle B (1999) Positive interactions on nonidigenous species: invasional meltdown? Biol Invasions 1:21–32

    Article  Google Scholar 

  • Styrsky JD, Eubanks MD (2007) Ecological consequences of interactions between ants and honeydew-producing insects. Proc Biol Sci 274:151–164

    Article  PubMed Central  PubMed  Google Scholar 

  • Suhr E, O’Dowd D, McKechnie S, Mackay D (2011) Genetic structure, behaviour and invasion history of the Argentine ant supercolony in Australia. Evol Appl 4:471–484

    Article  PubMed Central  PubMed  Google Scholar 

  • Sunamura E, Espadaler X, Sakamoto H et al (2009) Intercontinental union of Argentine ants: behavioral relationships among introduced populations in Europe, North America, and Asia. Insectes Soc 56:143–147

    Article  Google Scholar 

  • Tattersfield P, Warui CM, Seddon MB, Kiringe JW (2001) Land-snail faunas of afromontane forests of Mount Kenya, Kenya: ecology, diversity and distribution patterns. J Biogeogr 28:843–861

    Article  Google Scholar 

  • Thomas ML, Becker K, Abbott K, Feldhaar H (2010) Supercolony mosaics: two different invasions by the yellow crazy ant, Anoplolepis gracilipes, on Christmas Island, Indian Ocean. Biol Invasions 12:677–687

  • Vitousek PM, Walker LR (1989) Biological invasion by Myrica faya in Hawai’i: plant demography, nitrogen-fixation, eccosystem effects. Ecol Monogr 59:247–265

    Article  Google Scholar 

  • Wang B, Geng X-Z, Ma L-B et al (2014) A trophic cascade induced by predatory ants in a fig–fig wasp mutualism. J Anim Ecol 83:1149–1157

  • Wetterer JK (2005) Worldwide distribution and potential spread of the long-legged ant, Anoplolepis gracilipes (Hymenoptera: Formicidae). Sociobiology 45:77–97

    Google Scholar 

  • White EM, Wilson JC, Clarke AR (2006) Biotic indirect effects: a neglected concept in invasion biology. Divers Distrib 12:443–455

    Article  Google Scholar 

  • Wonham MJ, O’Connor M, Harley CDG (2005) Positive effects of a dominant invader on introduced and native mudflat species. Mar Ecol Ser 289:109–116

    Article  Google Scholar 

  • Yusa Y (2001) Predation of eggs of the apple snail Pomacea canaliculata (Gastropoda: Ampullariidae) by fire ant Solenopsis geminata. J Molluscan Stud 67:275–279

    Article  Google Scholar 

  • Zavaleta ES, Hobbs RJ, Mooney HA (2001) Viewing invasive species removal in a whole-ecosystem context. Trends Ecol Evol 16:454–459

    Article  Google Scholar 

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Acknowledgments

This project was undertaken with funding from the Hermon Slade Foundation and the Holsworth Wildlife Endowment. Fieldwork was conducted within the Christmas Island National Park under Permit AU-COM2011107. Thanks to all at Christmas Island National Parks for logistical support. Dion Maple and Dethklok provided invaluable insights into the Christmas Island ecosystem. Thea Shell and Max Cameron assisted with data collection. Vince Kessner provided his expertise in land snail identification. This manuscript benefitted from the helpful comments of three anonymous reviewers.

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Correspondence to Luke S. O’Loughlin.

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O’Loughlin, L.S., Green, P.T. Invader–invader mutualism influences land snail community composition and alters invasion success of alien species in tropical rainforest. Biol Invasions 17, 2659–2674 (2015). https://doi.org/10.1007/s10530-015-0903-6

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  • DOI: https://doi.org/10.1007/s10530-015-0903-6

Keywords

  • Anoplolepis gracilipes
  • Ant–scale insect interactions
  • Christmas Island
  • Facilitation
  • Giant African land snail (Achatina fulica)
  • Habitat complexity
  • Invasional meltdown
  • Secondary invasion