Biological Invasions

, Volume 10, Issue 2, pp 245–255 | Cite as

Invasive slugs as under-appreciated obstacles to rare plant restoration: evidence from the Hawaiian Islands

  • Stephanie M. Joe
  • Curtis C. Daehler
Original Paper


Introduced slugs have invaded many parts of the world where they were recognized as important pests of gardens and agriculture, but we know little about the effects of introduced slugs on rare plants in natural areas. The Hawaiian Islands have no native slugs, but over a dozen introduced slug species are now established. We reviewed Rare Plant Recovery Plans produced by the U.S. Fish and Wildlife Service for Hawaii and found that introduced slugs were specifically mentioned as threats or potential threats to 59 rare plant species (22% of all endangered and threatened plants), based mainly on anecdotal observations by field biologists. We then initiated an experimental field study to assess the impact of slug herbivory on the growth and survival of two endangered plant species (Cyanea superba, and Schidea obovata), one non-endangered native species (Nestegis sandwicensis) and two co-occurring invasive plant species (Psidium cattleianum and Clidemia hirta). In mesic forest on the Island of Oahu, we tracked the fate of outplanted seedlings in replicated 1 m2 plots, with and without slug control. Slugs decreased seedling survival of the endangered species by 51%, on average. Slugs did not significantly affect survival of the non-endangered or invasive plant species. Introduced slugs seem to be under-appreciated as a direct cause of plant endangerment. Invasive slugs may also facilitate the success of some invasive plant species by reducing competition with more palatable, native plant competitors. Slug control measures are relatively inexpensive and could facilitate rare plant establishment and population recovery.


Invasive slugs Endangered plants Herbivory Mollusk Pacific Islands Seedling predation 



This research received funding from Sigma Xi Grants in Aid of Research, the Beatrice Krauss Fellowship in Botany, the Pacific Cooperative Studies Unit, and the University of Hawaii at Manoa Ecology, Evolution and Conservation Biology Program. Seedling material, as well as access to the research site, was provided by the Oahu Army Natural Resource Program. The following people have supported this research and we appreciate their unique contributions of time, materials and/or advice: N. Arcand, J. Beachy, K. Brimacombe, M.D. Burt, S. Cato, C.G. Chimera, S.N. Ching, V. Cizankas, V. Costello, R.H. Cowie, D. Drake, D.C. Duffy, D. Foreman, H. Fraiola, B. Joe, W. Garnett, J. Gustine, W. Haines, H.K. Kawelo, M.J. Keir, P.D. Krushelnycky, K.K. Koza, T. Menard, D. Palumbo, J.L. Rohrer, R. Romualdo, D. Sailer, L. Salbosa, S. Seaphan, D. Souza, A.D. Taylor, W. Weaver, L. Weisenberger, K. Winger, B.K. Wong, M. Yorkston, and A. Yoshinaga.


  1. Akau G, Beachy J, Burt MD, Ching S, Costello V, Foreman D, Gustine J, Joe SM, Kawelo HK, Keir MJ, Masnker M, Morgan L, Mosher S, Palumbo D, Rohrer JL, Romualdo R, Sailer D, Salbosa L, Souza D, Trafton A, Walker M, Weaver W, Weisenberger L, Winger K, Wong BK (2006) Status Reports for the Makua Implementation Plan and the Draft Oahu Implementation Plan. The Pacific Cooperative Park Studies Unit, Honolulu, HawaiiGoogle Scholar
  2. Armstrong S (1995) Rare plants protect Cape’s water supplies. New Sci 11:8Google Scholar
  3. Beck MJ, Cardina TM, Alicata JE (1980) Eosinophilic meningitis due to Angiostrongyliasis cantonensis in American Samoa. Hawaii Med J 39:254–257PubMedGoogle Scholar
  4. Barker GM (1999) Naturalised terrestrial stylommatophora: (Mollusca: Gastropoda). Fauna of New Zeal 38:1–253Google Scholar
  5. Bowen L, VanVuren D (1997) Insular endemic plants lack defenses against herbivores. Cons Biol 11:1249–1254CrossRefGoogle Scholar
  6. Breadmore KN, Kirk WDJ (1998) Factors affecting floral herbivory in a limestone grassland. Acta Oecologica 19:501–506CrossRefGoogle Scholar
  7. Briner T, Frank T (1998) The palatability of 78 wildflower strip plants to the slug Arion lusitanicus. Ann Appl Biol 133:123–133CrossRefGoogle Scholar
  8. Bruegmann MM, Caraway V, Maunder M (2002) A safety net for Hawai’i’s rarest plants. Endang Species Bull 27:8–10Google Scholar
  9. Buschmann H, Keller M, Porret N, Dietz H, Edwards PJ (2005) The effect of slug grazing on vegetation development and plant species diversity in an experimental grassland. Func Ecol 19:291–298CrossRefGoogle Scholar
  10. Buschmann H, Edwards PJ, Dietz H (2006) Responses of native and invasive Brassicaceae species to slug herbivory. Acta Oecologica 30: 126–135CrossRefGoogle Scholar
  11. Carlsson NOL, Broenmark C, Hansson LA (2004) Invading herbivory: The golden apple snail alters ecosystem functioning in Asian wetlands. Ecology 85:1575–1580CrossRefGoogle Scholar
  12. Cates RG, Orians GH (1975) Successional status and the palatability of plants to generalized herbivores. Ecology 56:410–418CrossRefGoogle Scholar
  13. Christel G, Johan E, Ove E (2002) Recruitment in Dentaria bulbifera: the roles of dispersal, habitat quality and mollusc herbivory. J Veg Sci 13:719–724CrossRefGoogle Scholar
  14. Coomes DA, Allen RB, Forsyth DM, Lee WG (2003) Factors preventing the recovery of New Zealand forests following control of invasive deer. Cons Biol 17:450–459CrossRefGoogle Scholar
  15. Cowie RH (1995) Variation in species diversity and shell shape in Hawaiian land snails: In situ speciation and ecological relationships. Evolution 49:1191–1202CrossRefGoogle Scholar
  16. Cowie RH (1997) Catalog and bibliography of the nonindigenous nonmarine snails and slugs of the Hawaiian Islands. Bishop Mus Occas Papers 50, pp. 66Google Scholar
  17. Cowie RH (1999) New records of alien nonmarine mollusks in the Hawaiian Islands. Bishop Mus Occas Papers 59:48–50Google Scholar
  18. Cowie RH (2002) Invertebrate invasions on Pacific islands and the replacement of unique native faunas: A synthesis of the land and freshwater snails. Biol Invasions 3:119–136CrossRefGoogle Scholar
  19. Cowie RH (2005) Alien non-marine molluscs in the islands of the tropical and subtropical Pacific: A review. Am Malacol Bull 20:95–103Google Scholar
  20. Dirzo R (1980) Experimental studies on slug-plant interactions. I. The acceptability of thirty plant species to the slug Agriolimax caruuanae. J Ecol 68:981–998CrossRefGoogle Scholar
  21. Drake DR (1998) Relationships among seed rain, seed bank, and vegetation of a Hawaiian forest. J Veg Sci 9:103–112CrossRefGoogle Scholar
  22. Feeny P (1992) Evolution of plant chemical defense against herbivores. In: Rosenthal GA, Berenbaum MR (eds) Herbivores: their interactions with secondary plant metabolites, Vol. 2: ecological and evolutionary processes. Academic Press, New York, pp 1–35Google Scholar
  23. Gagné WC, Christenson CC (1985) Conservation status of native terrestrial invertebrates in Hawai’i. In: Stone CP, Scott MK (eds) Hawaii’s terrestrial ecosystems: Preservation and management. University of Hawaii Press, Honolulu, Hawai’i, pp 105–126Google Scholar
  24. Gagné WC, Cuddihy LW (1999) Classification of Hawaiian plant communities. In: Wagner WL, Herbst DR, Sohmer SH (eds) Manual of the flowering plants of Hawaii revised edition. Bishop Museum Press, Honolulu, Hawai’i, pp 45–85Google Scholar
  25. Hadfield MS, Mountain BS (1980) A field study of a vanishing species, Achatinella mustelina (Gastropoda, Pulmonata), in the Waianae Mountains of Oahu. Pac Sci 34:345–358Google Scholar
  26. Hanley ME, Fenner M, Edwards PJ (1996) The effect of mollusk grazing on seedling recruitment in artificially created grassland gaps. Oecologia 106:240–246CrossRefGoogle Scholar
  27. Hanley ME, Fenner M, Edwards PJ (1995) The effect of seedling age on the likelihood of herbivory by the slug Deroceras reticulatum. Func Ecol 9:754–759CrossRefGoogle Scholar
  28. Harper JL (1977) Population biology of plants. Academic Press, LondonGoogle Scholar
  29. Hata TY, Hara AH, Hu BK-S (1997) Molluscicides and mechanical barriers against slugs, Vaginula plebeia Fischer and Veronicells cubensis (Pfeiffer) (Stylommatophora: Veronicellidae). Crop Protect 16:501–506CrossRefGoogle Scholar
  30. Hawkins JW, Lankester MW, Nelson RRA (1998) Sampling terrestrial gastropods using cardboard sheets. Malacologia 39:1–9Google Scholar
  31. Hulme PE (1994) Seedling herbivory in grassland: relative impact of vertebrate and invertebrate herbivores. J Ecol 82:873–880CrossRefGoogle Scholar
  32. Kaneshiro KY (1988) The uniqueness of Hawai’i’s biota. In: Stone CP, Stone DB (eds) Conservation biology in Hawai’i. University of Hawai’i Press, Honolulu, Hawai’i, pp 7–10Google Scholar
  33. Loope LL (1992) An overview of problems with introduced plant species in national parks and biosphere reserves of the United States. In: Stone CP, Smith CW, Tunison JT (eds) Alien plant invasions in native ecosystems of Hawai’i: Management and research. University of Hawai’i Press, Honolulu, Hawai’i, pp 3–28Google Scholar
  34. McCoy KD (1999) Sampling terrestrial gastropod communities: using estimates of species richness and diversity to compare two methods. Malacologia 41:271–281Google Scholar
  35. Moles AT, Drake DR (1999) Potential contributions of the seed rain and seed bank to regeneration of native forest under plantation pine in New Zealand. New Zeal J Bot 37:83–93Google Scholar
  36. Nystrand O, Granström A (1997) Forest floor moisture control predator activity on juvenile seedlings of Pinus sylvestris. Can J Forest Res 27:1746–1752CrossRefGoogle Scholar
  37. Pimentel D, Zuniga R, Morrison D (2005) Update on the environmental and economic costs associated with alien-invasive species in the United States. Ecol Econ 52:273–288CrossRefGoogle Scholar
  38. Rai JPN, Tripathi RS (1985) Effect of herbivory by the slug, Mariaella dussumieri, and certain insects on growth and competitive success of two sympatric annual weeds. Agric Ecosyst Environ 13:125–137CrossRefGoogle Scholar
  39. Rathke B (1985) Slugs as generalist herbivores: Tests of three hypotheses on plant choice. Ecology 66:828–836CrossRefGoogle Scholar
  40. Ryan B, Joiner B, Cryer J (2005) Minitab handbook, 5th Edn. Thomson Brooks/Cole, Belmont, CaliforniaGoogle Scholar
  41. Scherber C, Crawley MJ, Porembski S (2003) The effects of herbivory and competition on the invasive alien plant Senecio inaequidens (Asteraceae). Divers Distribut 9:415–426CrossRefGoogle Scholar
  42. Schreiner IH (1997) Demography and recruitment of selected trees in the limestone forest of Guam in relation to introduced ungulates. Micronesica 30:169–181Google Scholar
  43. Severns RM (1981) Growth rate determinations of Achatinella lila, a Hawaiian tree snail. Nautilus 95:140–144Google Scholar
  44. Stone CP (1985) Alien animals in Hawai’i’s native ecosystems: toward controlling the adverse effects of introduced vertebrates. In: Stone CP, Scott MK (eds) Hawai’i’s Terrestrial Ecosystems: Preservation and Management. University of Hawai’i Press, Honolulu, Hawai’i, pp 251–297Google Scholar
  45. USFWS (U.S. Fish and Wildlife Service) (1994) Lanai plant cluster recovery plan. U.S. Fish and Wildlife Service, Portland, OregonGoogle Scholar
  46. USFWS (U.S. Fish and Wildlife Service) (1995) Waianae Plant Cluster Recovery Plan. U.S. Fish and Wildlife Service, Portland, OregonGoogle Scholar
  47. USFWS (U.S. Fish and Wildlife Service) (1997) Recovery plan for the Maui plant cluster. U.S. Fish and Wildlife Service, Portland, OregonGoogle Scholar
  48. USFWS (U.S. Fish and Wildlife Service) (1998) Recovery plan for Oahu plants. U.S. Fish and Wildlife Service, Portland, OregonGoogle Scholar
  49. USFWS (U.S. Fish, Wildlife Service) (2005) Endangered and threatened wildlife and plants; Review of native species that are candidates or proposed for listing as endangered or threatened; Annual notice of findings on resubmitted petitions; Annual description of progress on listing actions; proposed rule. Federal Register 70:24869–24934Google Scholar
  50. USGS (U.S. Geological Survey) (2004) Rainfall records for Poamoho rain gage no. 2 near Wahiawa, Oahu. Hawaii, Island of Oahu, pp. 2 Google Scholar
  51. Westerbergh A, Nyberg AB (1995) Selective grazing of hairless Silene dioica plants by land gastropods. Oikos 73:289–298CrossRefGoogle Scholar
  52. Wagner WL, Herbst DR, Sohmer SH (1999) Manual of the flowering plants of Hawaii revised edition. Bishop Museum Press, Honolulu, Hawai’iGoogle Scholar
  53. Wilby A, Brown VK (2001) Herbivory, litter and soil disturbance as determinants of vegetation dynamics during early old-field succession under set-aside. Oecologia 127:259–265CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2007

Authors and Affiliations

  1. 1.Department of BotanyUniversity of HawaiiHonoluluUSA

Personalised recommendations