Exotic Slugs Pose a Previously Unrecognized Threat to the Herbaceous Layer in a Midwestern Woodland

Restoration Ecology

Volumn 19, Issue 6, 2011, Pages 786-794

  Hahn, Philip G ^a   Draney, Michael L ^a   Dornbush, Mathew E ^a  

^a UNIVERSITY OF WISCONSIN GREEN BAY   (United States)

Author keywords

Deroceras reticulatum; Exotic plants; Forest restoration; Garlic mustard; Herbivory; Invasive species; Slugs; Woodland understory

Indexed keywords

ECOLOGICAL IMPACT; EXPERIMENTAL STUDY; HERB; HERBIVORY; INTRODUCED SPECIES; INVASIVE SPECIES; LABORATORY METHOD; NATIVE SPECIES; PLANT; RESTORATION ECOLOGY; SLUG; UNDERSTORY; WOODLAND;

EUROPE;

ALLIARIA PETIOLATA; ALLIUM SATIVUM; DEROCERAS RETICULATUM; ELYMUS; ELYMUS VIRGINICUS; GASTROPODA;

EID: 81355160848     PISSN: 10612971     EISSN: 1526100X     Source Type: Journal    
DOI: 10.1111/j.1526-100X.2010.00710.x     Document Type: Article

References (66)

1. Albrectsen, B. R., H. Gardfjell, C. M. Orians, B. Murray, and R. S. Fritz 2004. Slugs, willow seedlings and nutrient fertilization: intrinsic vigor inversely affects palatability. Oikos 105:268-278.
2. Blossey, B., V. Nuzzo, H. Hinz, and E. Gerber 2001. Developing biological control of Alliaria petiolata (M. Bieb.) Cavara and Grende (Garlic Mustard). Natural Areas Journal 21:357-367.
3. Bossdorf, O., S. Schroder, D. Prati, and H. Auge 2004. Palatability and tolerance to simulated herbivory in native and introduced populations of Alliaria petiolata (Brassicaceae). American Journal of Botany 91:856-862.
4. Briner, T., and T. Frank 1998. The palatability of 78 wildflower strip plants to the slug Arion lusitanicus. Annals of Applied Biology 133:123-133.
5. Bruelheide, H., and U. Scheidel 1999. Slug herbivory as a limiting factor for the geographical range of Arnica montana. Journal of Ecology 87:839-848.
6. Burlakova, L. E., A. Y. Karatayev, D. K. Padilla, L. D. Cartwright, and D. N. Hollas 2009. Wetland restoration and invasive species: apple snail (Pomacea insularum) feeding on native and invasive aquatic plants. Restoration Ecology 17:433-440.
7. Buschmann, H., P. J. Edwards, and H. Dietz 2005. Variation in growth pattern and response to slug damage among native and invasive provenances of four perennial Brassicaceae species. Journal of Ecology 93:322-334.
8. Cates, R. G., and G. J. Orians 1975. Successional status and the palatability of plants to generalized herbivores. Ecology 56:410-418.
9. Chichester, L. F., and L. L. Getz 1973. The terrestrial slugs of northeastern North America. Sterkiana 51:11-42.
10. Cipollini, D. 2002. Variation in the expression of chemical defenses in Alliaria petiolata (Brassicaceae) in the field and common garden. American Journal of Botany 89:1422-1430.
11. Cipollini, D., and B. Gruner 2007. Cyanide in the chemical arsenal of garlic mustard, Alliaria petiolata. Journal of Chemical Ecology 33:85-91.
12. Cipollini, D., J. Mbagwu, K. Barto, C. Hillstrom, and S. Enright 2005. Expression of constitutive and inducible chemical defenses in native and invasive populations of Alliaria petiolata. Journal of Chemical Ecology 31:1255-1267.
13. Costanza, R., R. d'Arge, R. de Groot, S. Farber, M. Grasso, B. Hannon, et al. 1997. The value of the world's ecosystem services and natural capital. Nature 387:253-260.
14. Côté, S. D., T. P. Rooney, J. Tremblay, C. Dussault, and D. M. Waller 2004. Ecological impacts of deer overabundance. Annual Review in Ecology, Evolution, and Systematics 35:113-147.
15. Cottam, D. A. 1986. The effects of slug-grazing on Trifolium repens and Dactylis glomerata in monoculture and mixed sward. Oikos 47:275-279.
16. Dirzo, R. 1980. Experimental studies on slug-plant interactions: I. The acceptability of thirty plant species to the slug Agrioloimax caruaneae. Journal of Ecology 68:981-998.
17. Dirzo, R., and J. L. Harper 1980. Experimental studies on slug-plant interactions: II. The effect of grazing by slugs on high density monocultures of Capsella bursa-pastoris and Poa annua. Journal of Ecology 68:999-1011.
18. Dirzo, R., and J. L. Harper 1982. Experimental studies on slug-plant interactions: IV. The performance of cyanogenic and acyanogenic morphs of Trifolium repens in the field. Journal of Ecology 70:119-138.
19. Ehrlén, J. 1995a. Demography of the perennial herb Lathrus vernus. I. Herbivory and individual performance. Journal of Ecology 83:287-295.
20. Ehrlén, J. 1995b. Demography of the perennial herb Lathrus vernus. II. Herbivory and population dynamics. Journal of Ecology 83:297-308.
21. Ehrlén, J. 2003. Fitness components versus total demographic effects: evaluating herbivore impacts on a perennial herb. American Naturalist 162:796-810.
22. Fenner, M. 1987. Seedlings. New Phytologist 106:35-47.
23. Fenner, M., M. E. Hanley, and R. Lawrence 1999. Comparison of seedling and adult palatability in annual and perennial plants. Functional Ecology 13:546-551.
24. Flinn, K. M., and M. Vellend 2005. Recovery of forest plant communities in post-agricultural landscapes. Frontiers in Ecology and the Environment 3:243-250.
25. Getz, L. L. 1959. Notes on the ecology of slugs: Arion circumscriptus, Deroceras reticulatum, and D. leave. American Midland Naturalist 61:485-498.
26. Gilliam, F. S. 2006. The ecological significance of the herbaceous layer in temperate forest ecosystems. Bioscience 57:845-858.
27. Givnish, T. J. 1987. Comparative studies of leaf form: assessing the relative roles of selective pressures and phylogentic constraints. New Phytologists 106:131-160.
28. Gleason, H. A., and A. Cronquist 1991. Manual of vascular plants of northeastern United and adjacent Canada. New York Botanical Garden, New York.
29. Hanley, M. E. 2004. Seedling herbivory and the influence of plant species richness in seedlings neighborhoods. Plant Ecology 170:35-41.
30. Hanley, M. E., M. Fenner, P. J. Edwards 1995a. The effects of seedling age on the likelihood of herbivory by the slug D. reticulatum. Functional Ecology 9:754-759.
31. Hanley, M. E., and O. C. May 2006. Cotyledon damage at the seedling stage affects growth and flowering potential in mature plants. New Phytologist 169:243-250.
32. Hanley, M. E., M. Fenner, and P. J. Edwards 1995b. An experimental field study of the effects of mollusc grazing on seedling recruitment and survival in grassland. Journal of Ecology 83:621-627.
33. Harris, J. G., and M. W. Harris 2001. Plant identification terminology: an illustrated guide. Spring Lake Publishing, Spring Lake, Utah.
34. Harper, J. L. 1977. Population biology of plants. Academic Press, London, England.
35. Hitchmough, J. D. 2003. Effects of sward height, gap size, and slug grazing on emergence and establishment of Trollius europaeus (Globeflower). Restoration Ecology 11:20-28.
36. Hobbs, R. J., and J. A. Harris 2001. Restoration ecology: repairing the Earth's ecosystems in the new millennium. Restoration Ecology 9:239-246.
37. Jennings, T. J., and J. P. Barkham 1975. Food of slugs in mixed deciduous woodland. Oikos 26:211-221.
38. Joe, S. M., and C. C. Daehler 2008. Invasive slugs as under-appreciated obstacles to rare plant restoration: evidence from the Hawaiian Islands. Biological Invasions 10:245-255.
39. Jolls, C. L. 2003. Populations and threats to rare plants of the herb layer: more challenges and opportunities for conservations biology. Pages 105-159 in F. S. Gilliam, and M. R. Roberts, editors. The herbaceous layer of forests of eastern North America. Oxford University Press, New York.
40. Keddy, P. A., and C. G. Drummond 1996. Ecological properties for the evaluation, management, and restoration of temperate deciduous forest ecosystems. Ecological Applications 6:748-762.
41. Lankau, R. A., and S. Y. Strauss 2008. Community complexity drives patterns of natural selection on a chemical defense of Brassica nigra. The American Naturalist 171:150-161.
42. nd edition. SAS Institute Inc., Cary, North Carolina.
43. Mack, R. N., D. Simberloff, W. M. Lonsdale, H. Evans, M. Clout, and F. A. Bazzaz 2000. Biotic invasions: causes, epidemiology, global consequences, and control. Ecological Applications 10:689-710.
44. McCracken, G. F., and R. K. Selander 1980. Self-fertilization and monogenic strains in natural populations of terrestrial slugs. Proceedings of the National Academy of Sciences of the United States of America 77:684-688.
45. McLachlan, S. M., and D. R. Bazely 2001. Recovery patterns of understory herbs and their use as indicators of deciduous forest regeneration. Conservation Biology 18:1-15.
46. Muller, R. 2003. Nutrient relations of the herbaceous layer in deciduous forest ecosystems. Pages 15-37 in F. Gilliam, and M. Roberts, editors. The herbaceous layer in forests of eastern North America. Oxford University Press, Oxford, United Kingdom.
47. Muller, R., and F. Bormann 1976. Role of Erythronium americanum Ker. in energy flow and nutrient dynamics of a northern hardwood forest system. Science 193:1126-1128.
48. Nekola, J. C. 2003. Large-scale terrestrial gastropod community composition patterns in the Great Lakes region of North America. Diversity and Distributions 9:55-71.
49. Neufeld, H. S., and D. R. Young 2003. Ecophysiology of the herbaceous layer in temperate deciduous forests. Pages 38-90 in F. S. Gilliam, and M. R. Roberts, editors. The herbaceous layer of forests of eastern North America. Oxford University Press, New York.
50. Pallant, D. 1969. The food of the grey field slug (Agriolimax reticulates (Muller)) in woodland. Journal of Animal Ecology 38:391-397.
51. Pearce, D. W. 2001. The economic value of forest ecosystems. Ecosystem Health 7:284-296.
52. Price, P. W. 1991. The plant vigor hypothesis and herbivore attack. Oikos 62:244-251.
53. Rathcke, B. 1985. Slugs as generalist herbivores: tests of three hypotheses on plant choice. Ecology 66:828-836.
54. Rawlings, T. A., K. A. Hayes, R. H. Cowie, and T. M. Collins 2007. The identity, distribution, and impacts of non-native apple snails in the continental United States. BMC Evolution Biology 7:97.
55. Robinson, D. G. 1999. Alien invasions: the effects of global economy on non-marine gastropod introductions into the United States. Malacologia 41:413-438.
56. Rodgers, D. A., T. P. Rooney, T. J. Hawbaker, V. C. Radeloff, and D. M. Waller 2009. Paying the extinction debt in southern Wisconsin forest understories. Conservation Biology 23:1497-1506.
57. Scheidel, U., and H. Bruelheide 1999. Selective slug grazing on montane meadow plants. Journal of Ecology 87:828-838.
58. Sessions, L., and D. Kelly 2002. Predator-mediated apparent competition between an introduced grass, Agrostis capillaris, and a native fern, Botrychium australe (Ophioglossaceae), in New Zealand. Oikos 96:102-109.
59. South, A. 1992. Terrestrial slugs: biology, ecology, and control. Chapman & Hall, London, United Kingdom.
60. Speiser, B. 2001. Food and feeding behavior. Pages 259-288 in G. M. Baker, editor. The biology of terrestrial molluscs. CABI Publishing, New York.
61. Strauss, S. Y., M. L. Stanton, N. C. Emery, C. A. Bradley, A. Carleton, D. R. Dittrich-Reed, et al. 2009. Cryptic seedling herbivory by nocturnal introduced generalists impacts survival, performance of native and exotic plants. Ecology 90:419-429.
62. Vellend, M. 2003. Habitat loss inhibits recovery of plant diversity as forests regrow. Ecology 84:1158-1164.
63. Vidra, R. L., T. H. Shear, and J. M. Stucky 2007. Effects of vegetation removal on native understory recovery in an exotic-rich urban forest. Journal of the Torrey Botanical Society 134:410-419.
64. Whigham, D. F. 2004. Ecology of woodland herbs in temperate deciduous forests. Annual Review of Ecology, Evolution and Systematics. 35:585-621.
65. Wiegmann, S. M., and D. M. Waller 2006. Fifty years of change in northern upland forest understories: identity and traits of "winner" and "loser" plant species. Biological Conservation 129:109-123.
66. Wilcove, D. S., D. Rothstein, J. Dubow, A. Phillips, and E. Losos 1998. Quantifying threats to imperiled species in the United States. Bioscience 48:607-615.