Forest fragmentation reduces parasitism via species loss at multiple trophic levels

Ecology

Volumn 93, Issue 11, 2012, Pages 2407-2420

  Fenoglio, María Silvina ^a   Srivastava, Diane ^b   Valladares, Graciela ^a   Cagnolo, Luciano ^a   Salvo, Adriana ^a  

^a UNIVERSIDAD NACIONAL DE CÓRDOBA   (Argentina)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

Biodiversity; Chaco Serrano forest, Argentina; Ecosystem functioning; Habitat loss; Leaf miners; Parasitoids; Species traits

Indexed keywords

BIODIVERSITY; ECOSYSTEM FUNCTION; ENERGY FLOW; HABITAT FRAGMENTATION; HABITAT LOSS; INSECT; PARASITOID; RELATIVE ABUNDANCE; SPECIES RICHNESS; TROPHIC LEVEL;

ANIMAL; ARTICLE; BIODIVERSITY; FEEDING BEHAVIOR; FOOD CHAIN; INSECT; PHYSIOLOGY; SPECIES EXTINCTION; TREE;

ANIMALS; BIODIVERSITY; EXTINCTION, BIOLOGICAL; FEEDING BEHAVIOR; FOOD CHAIN; INSECTS; TREES;

ARGENTINA; CHACO [ARGENTINA];

AGROMYZIDAE; HEXAPODA;

EID: 84869169223     PISSN: 00129658     EISSN: None     Source Type: Journal    
DOI: 10.1890/11-2043.1     Document Type: Article

References (67)

1. Aguilar, R., L. Ashworth, L. Galetto, and M. A. Aizen. 2006. Plant reproductive susceptibility to habitat fragmentation: review and synthesis through a meta-analysis. Ecology Letters 9:968-980.
2. Andow, D. A. 1991. Vegetational diversity and arthropod population response. Annual Review of Entomology 36:561-586.
3. Arbuckle, J. L. 2003. Amos 5.0 update to the Amos user's guide. Smallwaters, Chicago, Illinois, USA.
4. Balvanera, P., A. B. Pfisterer, N. Buchmann, J. S. He, T. Nakashizuka, D. Raffaelli, and B. Schmid. 2006. Quantifying the evidence for biodiversity effects on ecosystem functioning and services. Ecology Letters 9:1146-1156.
5. Cabido, M., M. L. Carranza, A. Acosta, and S. Paez. 1991. Contribucion al conocimiento fitosociologico del Bosque Chaqueño Serrano en la provincia de Cordoba, Argentina. Phytocoenologia 19:547-566.
6. Cagnolo, L., M. Cabido, and G. Valladares. 2006. Plant species richness in the Chaco Serrano Woodland from central Argentina: ecological traits and habitat fragmentation effects. Biological Conservation 132:510-519.
7. Cagnolo, L., A. Salvo, and G. Valladares. 2011. Network topology: patterns and mechanisms in plant-herbivore and host-parasitoid food webs. Journal of Animal Ecology 80:342-351.
8. Cagnolo, L., G. R. Valladares, A. Salvo, M. Cabido, and M. Zak. 2009. Habitat fragmentation and species loss across three interacting trophic levels: effects of life-history and food-web traits. Biological Conservation 23:1167-1175.
9. Cardinale, B. J., E. Duffy, D. Srivastava, M. Loreau, M. Thomas, and M. Emmerson. 2009. Towards a food-web perspective on biodiversity and ecosystem functioning. Pages 105-120 in S. Naeem, D. E. Bunker, A. Hector, M. Loreau, and C. Perrings, editors. Biodiversity, ecosystem functioning, and human wellbeing: an ecological and economic perspective. Oxford University Press, Oxford, UK.
10. Cardinale, B. J., D. S. Srivastava, J. E. Duffy, J. P. Wright, A. L. Downing, M. Sankaran, and C. Jouseau. 2006. Effects of biodiversity on the functioning of trophic groups and ecosystems. Nature 443:989-992.
11. Diaz, S., and M. Cabido. 2001. Vive la difference: plant functional diversity matters to ecosystem processes. Trends in Ecology and Evolution 16:464-655.
12. Diaz, S., A. J. Symstad, F. S. Chapin, III, D. A. Wardle, and L. Huenneke. 2003. Functional diversity revealed by removal experiments. Trends in Ecology and Evolution 18:140-146.
13. Dobson, A., et al. 2006. Habitat loss, trophic collapse, and the decline of ecosystem services. Ecology 87:1915-1924.
14. Duffy, J. E. 2009. Why biodiversity is important to the functioning of real-world ecosystems. Frontiers in Ecology and Environment 7:437-444.
15. Duffy, J. E., B. J. Cardinale, K. E. France, P. B. McIntyre, E. Thebault, and M. Loreau. 2007. The functional role of biodiversity in ecosystems: incorporating trophic complexity. Ecology Letters 10:522-538.
16. Duffy, J. E., D. S. Srivastava, J. McLaren, M. Sankaran, J. Griffin, M. Emmerson, M. Solan, and K. E. Jones. 2009. Forecasting decline in ecosystem services under realistic scenarios of extinction. Pages 60-77 in S. Naeem, D. E. Bunker, and A. Hector, editors. Biodiversity, ecosystem functioning, and human wellbeing: an ecological and economic perspective. Oxford University Press, Oxford, UK.
17. Dunne, J. A., and R. Williams. 2009. Cascading extinctions and community collapse in model food webs. Philosophical Transactions of the Royal Society B 364:1711-1723.
18. Finke, D. L., and W. E. Snyder. 2008. Niche partitioning increases resource exploitation by diverse communities. Science 321:1488-1490.
19. Fox, J. W. 2005. Interpreting the 'selection effect' of biodiversity on ecosystem function. Ecology Letters 8:846-856.
20. Godefroid, S., and N. Koedam. 2003. How important are large vs. small forest remnants for the conservation of the woodland flora in an urban context? Global Ecology and Biogeography 12:287-298.
21. Godfray, H. C. J. 1994. Parasitoids: behavioural and evolutionary ecology. Princeton University Press, Princeton, New Jersey, USA.
22. Gonzalez, A., and E. J. Chaneton. 2002. Heterotroph species extinction, abundance and biomass dynamics in an experimentally fragmented microecosystem. Journal of Animal Ecology 71:594-602.
23. Gross, K., and B. J. Cardinale. 2005. The functional consequences of random vs. ordered species extinctions. Ecology Letters 8:409-418.
24. Hawkins, B. A. 1994. Pattern and process in host-parasitoid interactions. Cambridge University Press, Cambridge, UK.
25. Hill, J. L., and P. J. Curran. 2003. Area, shape and isolation of tropical forest fragments: effects on tree species diversity and implications for conservation. Journal of Biogeography 30:1391-1403.
26. Hillebrand, H., and B. Matthiessen. 2009. Biodiversity in a complex world: consolidation and progress in functional biodiversity research. Ecology Letters 12:1405-1419.
27. Holt, R. D., J. H. Lawton, G. A. Polis, and N. D. Martinez. 1999. Trophic rank and the species-area relationship. Ecology 80:1495-1504.
28. Hunter, M. D., and P. W. Price. 1992. Playing chutes and ladders: heterogeneity and the relative roles of bottom-up and top-down forces in natural communities. Ecology 73:724-732.
29. Hutchinson, G. E. 1959. Homage to Santa Rosalia or why are there so many kinds of animals. American Naturalist 93:145-159.
30. Ives, A. R., and B. J. Cardinale. 2004. Food-web interactions govern the resistance of communities following non-random extinctions. Nature 429:174-177.
31. Ives, A. R., B. J. Cardinale, and W. E. Snyder. 2005. A synthesis of subdisciplines: predator prey interactions, and biodiversity and ecosystem functioning. Ecology Letters 8:102-116.
32. Knops, J. M. H., D. Tilman, N. M. Haddad, S. Naeem, C. E. Mitchell, J. Haarstad, M. E. Ritchie, K. M. Howe, P. B. Reich, E. Siemann, and J. Groth. 1999. Effects of plant species richness on invasion dynamics, disease outbreaks, insect abundances and diversity. Ecology Letters 2:286-293.
33. Krauss, J., A. Klein, I. Steffan-Dewenter, and T. Tscharntke. 2004. Effects of habitat area, isolation, and landscape diversity on plant species richness of calcareous grasslands. Biodiversity and Conservation 13:1427-1439.
34. Laurance, W. F., T. E. Lovejoy, H. L. Vasconcelos, E. M. Bruna, R. K. Didham, P. C. Stouffer, C. Gascon, R. O. Bierregaard, S. G. Laurance, and E. Sampaio. 2001. Ecosystem decay of Amazonian forest fragments: a 22-year investigation. Conservation Biology 16:605-618.
35. Lewis, O. T., J. Memmott, J. La Salle, C. H. C. Lyal, C. Whitefoord, and H. C. J. Godfray. 2002. Structure of a diverse tropical forest insect-parasitoid community. Journal of Animal Ecology 71:855-873.
36. Loreau, M., and A. Hector. 2001. Partitioning selection and complementarity in biodiversity experiments. Nature 412:72-76.
37. McKinney, M. L. 1997. Extinction vulnerability and selectivity: combining ecological and paleontological views. Annual Review of Ecology and Systematics 28:495-516.
38. Moglia, G., and A. M. Gimenez. 1998. Rasgos anatomicos caracteristicos del hidrosistema de las principales especies arboreas de la region Chaqueña Argentina. Investigacion Agraria: Sistemas y Recursos Forestales 7:53-71.
39. Montoya, J. M., M. A. Rodriguez, and B. A. Hawkins. 2003. Food web complexity and higher-level ecosystem services. Ecology Letters 6:587-593.
40. Naeem, S., and J. P. Wright. 2003. Disentangling biodiversity effects on ecosystem functioning: deriving solutions to a seemingly insurmountable problem. Ecology Letters 6:567-579.
41. Northfield, T. D., G. B. Snyder, A. R. Ives, and W. E. Snyder. 2010. Niche saturation reveals resource partitioning among consumers. Ecology Letters 13:338-348.
42. Petermann, J. S., C. B. Muller, A. Weigelt, W. W. Weisser, and B. Schmid. 2010. Effect of plant species loss on aphid-parasitoid communities. Journal of Animal Ecology 79:709-720.
43. R Development Core Team. 2010. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.
44. Reiss, J., J. R. Bridle, J. M. Montoya, and G. Woodward. 2009. Emerging horizons in biodiversity and ecosystem functioning research. Trends in Ecology and Evolution 24:505-514.
45. Rodríguez, M. A., and B. A. Hawkins. 2000. Diversity, function and stability in parasitoid communities. Ecology Letters 3:35-40.
46. Sala, O. E., et al. 2000. Global biodiversity scenarios for the year 2100. Science 287:1770-1774.
47. Salvo, A., and G. Valladares. 2004. Looks are important: parasitic assemblages of agromyzid leafminers (Diptera) in relation to mine shape and contrast. Journal of Animal Ecology 73:494-505.
48. Salvo, A., G. Valladares, and L. Cagnolo. 2011. Parasitic assemblages on leafminers: a comparison of structure and function among host orders. Studies on Neotropical Fauna and Environment 64:11-22.
49. Sheehan, W. 1986. Response by specialist and generalist natural enemies to agroecosystem diversification: a selective review. Environmental Entomology 15:456-461.
50. Shipley, B. 2000. Cause and correlation in biology: a user's guide to path analysis, structural equations and causal inference. Cambridge University Press, Cambridge, UK.
51. Siemann, E., D. Tilman, J. Haarstad, and M. Ritchie. 1998. Experimental tests of the dependence of arthropod diversity on plant diversity. American Naturalist 152:738-749.
52. Srivastava, D. S., and T. Bell. 2009. Reducing horizontal and vertical diversity in a foodweb triggers extinctions and impacts functions. Ecology Letters 12:1016-1028.
53. Srivastava, D. S., and M. Vellend. 2005. Biodiversity-ecosystem function research: Is it relevant to conservation? Annual Review of Ecology, Evolution, and Systematics 36:267-294.
54. Terborgh, J. L., L. Lopez, P. Nuñez, M. Rao, G. Shahabuddin, G. Orihuela, M. Riveros, R. Ascanio, G. H. Adler, T. D. Lambert, and L. Balbas. 2001. Ecological meltdown in predator-free forest fragments. Science 294:1923-1926.
55. Thebault, E., V. Huber, and M. Loreau. 2007. Cascading extinctions and ecosystem functioning: contrasting effects of diversity depending on food web structure. Oikos 116:163-173.
56. Tylianakis, J. M., E. Laliberte, A. Nielsen, and J. Bascompte. 2010. Conservation of species interaction networks. Biological Conservation 143:2270-2279.
57. Tylianakis, J. M., T. A. Rand, A. Kahmen, A. M. Klein, N. Buchmann, J. Perner, and T. Tscharnkte. 2008. Resource heterogeneity moderates the biodiversity-function relationship in real world ecosystems. PLoS Biology 6:947-956.
58. Tylianakis, J. M., and C. M. Romo. 2010. Natural enemy diversity and biological control: making sense of the context-dependency. Basic and Applied Ecology 11:657-668.
59. Tylianakis, J. M., T. Tscharntke, and A. M. Klein. 2006. Diversity, ecosystem function, and stability of parasitoid-host interactions across a tropical habitat gradient. Ecology 87:3047-3057.
60. Valladares, G., L. Cagnolo, and A. Salvo. 2012. Forest fragmentation leads to food web contraction. Oikos 121:299-305.
61. Valladares, G., A. Salvo, and L. Cagnolo. 2006. Habitat fragmentation effects on trophic processes of insect-plant food webs. Conservation Biology 20:212-217.
62. Valladares, G., A. Salvo, and H. C. J. Godfray. 2001. Quantitative food webs of dipteran leafminers and their parasitoids in Argentina. Ecological Research 16:925-939.
63. Vet, L. E. M., and M. Dicke. 1992. Ecology of infochemical use by natural enemies in a tritrophic context. Annual Review of Entomology 37:141-172.
64. Vet, L. E. M., M. B. Sokolowski, D. E. MacDonald, and H. Snellen. 1993. Responses of a generalist and a specialist parasitoid (Hymenoptera: Eucoilidae) to drosophilid larval kairomones. Journal of Insect Behavior 6:615-624.
65. Wang, X. G., and M. A. Keller. 2002. A comparison of the host-searching efficiency of two larval parasitoids of Plutella xylostella. Ecological Entomology 27:105-114.
66. Zak, M. R., M. Cabido, and J. G. Hodgson. 2004. Do subtropical seasonal forests in the Gran Chaco, Argentina, have a future? Biological Conservation 120:589-598.
67. Zar, J. H. 1999. Biostatistical analysis. Fourth edition. Prentice-Hall, Upper Saddle River, New Jersey, USA.