Herbivore diet breadth mediates the cascading effects of carnivores in food webs

Proceedings of the National Academy of Sciences of the United States of America

Volumn 111, Issue 26, 2014, Pages 9521-9526

  Singer, Michael S ^a   Lichter Marck, Isaac H ^a   Farkas, Timothy E ^a,b   Aaron, Eric ^c   Whitney, Kenneth D ^d   Mooney, Kailen A ^e  

^a WESLEYAN UNIVERSITY   (United States)

^b UNIVERSITY OF SHEFFIELD   (United Kingdom)

^c VASSAR COLLEGE   (United States)

^d UNIVERSITY OF NEW MEXICO   (United States)

^e UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Ecological specialization; Host specificity; Plant herbivore interactions; Tritrophic interactions; Trophic cascade

Indexed keywords

ARTICLE; BIODIVERSITY; BIRD; BODY SIZE; CARNIVORE; CATERPILLAR; DIET; FIELD EXPERIMENT; FOOD WEB; HERBIVORE; HOST; NONHUMAN; PHYLODIVERSITY; PLANT DAMAGE; PLANT LEAF; PREDATION; PREDATOR; PREDICTIVE VALUE; PRIORITY JOURNAL; STEREOTYPY; TREE;

ECOLOGICAL SPECIALIZATION; HOST SPECIFICITY; PLANT-HERBIVORE INTERACTIONS; TRITROPHIC INTERACTIONS; TROPHIC CASCADE;

ADAPTATION, BIOLOGICAL; ANALYSIS OF VARIANCE; ANIMALS; BIRDS; CARNIVORY; CONNECTICUT; DIET; FOOD CHAIN; HERBIVORY; HUMANS; LARVA; MODELS, BIOLOGICAL; MOTHS; PHYLOGENY; TIME FACTORS; TREES;

EID: 84903702462     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1401949111     Document Type: Article

References (55)

1. Schmitz OJ (2010) Resolving Ecosystem Complexity (Princeton Univ Press, Princeton) .
2. Mittelbach GG (2012) Community Ecology (Sinauer Associates, Sunderland, MA) .
3. Schmitz OJ, Krivan V, Ovadia O (2004) Trophic cascades: The primacy of trait-mediated indirect interactions. Ecol Lett 7(2):153-163.
4. Polis GA, Sears ALW, Huxel GR, Strong DR, Maron J (2000) When is a trophic cascade a trophic cascade? Trends Ecol Evol 15(11):473-475.
5. Schmitz OJ, Hambäck PA, Beckerman AP (2000) Trophic cascades in terrestrial systems: A review of the effects of carnivore removals on plants. Am Nat 155(2):141-153.
6. Terborgh J, Estes JA (2010) Trophic Cascades: Predators, Prey, and the Changing Dynamics of Nature (Island Press, Washington, DC) .
7. Beckerman AP, Uriarte M, Schmitz OJ (1997) Experimental evidence for a behaviormediated trophic cascade in a terrestrial food chain. Proc Natl Acad Sci USA 94(20): 10735-10738.
8. McIntosh AR, Townsend CR (1996) Interactions between fish, grazing invertebrates and algae in a New Zealand stream: A trophic cascade mediated by fish induced changes to grazer behaviour? Oecologia 108(1):174-181.
9. Wojdak JM, Luttbeg B (2005) Relative strengths of trait-mediated and densitymediated indirect effects of a predator vary with resource levels in a freshwater food chain. Oikos 111(3):592-598.
10. Stief P, Hölker F (2006) Trait-mediated indirect effects of predatory fish on microbial mineralization in aquatic sediments. Ecology 87(12):3152-3159.
11. Wootton JT, Parker MS, Power ME (1996) Effects of disturbance on river food webs. Science 273(5281):1558-1561.
12. Bridgeland WT, Beier P, Kolb T, Whitham TG (2010) A conditional trophic cascade: Birds benefit faster growing trees with strong links between predators and plants. Ecology 91(1):73-84.
13. Van der Stap I, Vos M, Verschoor AM, Helmsing NR, Mooij WM(2007) Induced defenses in herbivores and plants differentially modulate a trophic cascade. Ecology 88(10):2474-2481.
14. Schmitz OJ (1998) Direct and indirect effects of predation and predation risk in oldfield interaction webs. Am Nat 151(4):327-342.
15. Futuyma DJ, Gould F (1979) Associations of plants and insects in a deciduous forest. Ecol Monogr 49(1):33-50.
16. Strong DR, Lawton JH, Southwood R (1984) Insects on Plants: Community Patterns and Mechanisms (Harvard Univ Press, Cambridge, MA) .
17. Schoonhoven LM, Loon JJAv, Dicke M (2005) Insect-Plant Biology (Oxford Univ Press, New York) , 2nd Ed.
18. Dyer LA, et al. (2007) Host specificity of Lepidoptera in tropical and temperate forests. Nature 448(7154):696-699.
19. Bernays E, Graham M (1988) On the evolution of host specificity in phytophagous arthropods. Ecology 69(4):886-892.
20. Dyer LA (1995) Tasty generalists and nasty specialists: Antipredator mechanisms in tropical lepidopteran larvae. Ecology 76(5):1483-1496.
21. Vencl FV, Nogueira-de-Sá F, Allen BJ, Windsor DM, Futuyma DJ (2005) Dietary specialization influences the efficacy of larval tortoise beetle shield defenses. Oecologia 145(3):404-414.
22. Bernays EA (1989) Host range in phytophagous insects-the potential role of generalist predators. Evol Ecol 3(4):299-311.
23. Bernays EA, Cornelius ML (1989) Generalist caterpillar prey are more palatable than specialists for the generalist predator Iridomyrmex humilis. Oecologia 79(3):427-430.
24. Dyer LA (1997) Effectiveness of caterpillar defenses against three species of invertebrate predators. J Res Lepid 34:48-68.
25. Harvey PH, Pagel MD (1991) The Comparative Method in Evolutionary Biology (Oxford Univ Press, New York) .
26. Mooney KA, et al. (2010) Interactions among predators and the cascading effects of vertebrate insectivores on arthropod communities and plants. Proc Natl Acad Sci USA 107(16):7335-7340.
27. Boyles JG, Cryan PM, McCracken GF, Kunz TH (2011) Conservation. Economic importance of bats in agriculture. Science 332(6025):41-42.
28. Mäntylä E, Klemola T, Laaksonen T (2011) Birds help plants: A meta-analysis of topdown trophic cascades caused by avian predators. Oecologia 165(1):143-151.
29. Singer MS, Farkas TE, Skorik CM, Mooney KA (2012) Tritrophic interactions at a community level: Effects of host plant species quality on bird predation of caterpillars. Am Nat 179(3):363-374.
30. Hedges LV, Gurevitch J, Curtis PS (1999) The meta-analysis of response ratios in experimental ecology. Ecology 80(4):1150-1156.
31. Poulin R, Krasnov BR, Mouillot D (2011) Host specificity in phylogenetic and geographic space. Trends Parasitol 27(8):355-361.
32. Felsenstein J (1985) Phylogenies and the comparative method. Am Nat 125(1):1-15.
33. Davis RB, Õunap E, Javoiš J, Gerhold P, Tammaru T (2013) Degree of specialization is related to body size in herbivorous insects: A phylogenetic confirmation. Evolution 67(2):583-589.
34. Remmel T, Davison J, Tammaru T (2011) Quantifying predation on folivorous insect larvae: The perspective of life-history evolution. Biol J Linn Soc Lond 104(1):1-18.
35. Robinson GS, Ackery PR, Kitching IJ, Beccaloni GW, Hernandez LM (2012) HOSTS-A Database of the Hostplants of the World's Lepidoptera. Available at www.nhm.ac.uk/ research-curation/research/projects/hostplants/. Accessed April 30, 2012.
36. Ali JG, Agrawal AA (2012) Specialist versus generalist insect herbivores and plant defense. Trends Plant Sci 17(5):293-302.
37. Mooney KA, Halitschke R, Kessler A, Agrawal AA (2010) Evolutionary trade-offs in plants mediate the strength of trophic cascades. Science 327(5973):1642-1644.
38. Scoble MJ (1995) The Lepidoptera: Form, Function and Diversity (Oxford Univ Press, Oxford) .
39. Santos JC, Coloma LA, Cannatella DC (2003) Multiple, recurring origins of aposematism and diet specialization in poison frogs. Proc Natl Acad Sci USA 100(22):12792-12797.
40. Ruxton GD, Sherratt TN, Speed MP (2004) Avoiding Attack: The Evolutionary Ecology of Crypsis, Warning Signals, and Mimicry (Oxford Univ Press, New York) .
41. Van Bael SA, et al. (2008) Birds as predators in tropical agroforestry systems. Ecology 89(4):928-934.
42. Trussell GC, Schmitz OJ (2012) Species functional traits, trophic control and the ecosystem consequences of adaptive foraging in the middle of food chains. Trait-Mediated Indirect Interactions: Ecological and Evolutionary Perspectives, eds Ohgushi T, Schmitz OJ, Holt RD (Cambrige Univ Press, New York) , pp 324-338.
43. Hunter MD, Price PW (1992) Playing chutes and ladders-heterogeneity and the relative roles of bottom-up and top-down forces in natural communities. Ecology 73(3):724-732.
44. Rodríguez-Castañeda G (2013) The world and its shades of green: A meta-analysis on trophic cascades across temperature and precipitation gradients. Glob Ecol Biogeogr 22(1):1180130.
45. Shurin JB, Markel RW, Mathews B (2010) Comparing trophic cascades across ecosystems. Trophic Cascades: Predators, Prey, and the Changing Dynamics of Nature, eds Terborgh J, Estes JA (Island Press, Washington, DC) , pp 319-336.
46. Halaj J, Wise DH (2001) Terrestrial trophic cascades: How much do they trickle? Am Nat 157(3):262-281.
47. Hay ME, Steinberg PD (1992) The chemical ecology of plant-herbivore interactions in marine versus terrestrial communities. Herbivores: Their Interaction with Secondary Metabolites, Evolutionary and Ecological Processes, eds Rosenthal GA, Berenbaum M (Academic, San Diego) , pp 371-413.
48. Poore AGB, Hill NA, Sotka EE (2008) Phylogenetic and geographic variation in host breadth and composition by herbivorous amphipods in the family Ampithoidae. Evolution 62(1):21-38.
49. Mooney KA (2006) The disruption of an ant-aphid mutualism increases the effects of birds on pine herbivores. Ecology 87(7):1805-1815.
50. Wagner DL (2005) Caterpillars of Eastern North America: A Guide to Identification and Natural History (Princeton Univ Press, Princeton) .
51. Wagner DL (2011) Owlet Caterpillars of Eastern North America (Princeton Univ Press, Princeton) .
52. Wagner D, Ferguson D, McCabe T, Reardon R (2002) Geometroid caterpillars of Northeastern and Appalachian Forests. USFS Technology Transfer Bulletin (US Forest Service, Morgantown, WV) .
53. Karpestam E, Merilaita S, Forsman A (2013) Detection experiments with humans implicate visual predation as a driver of colour polymorphism dynamics in pygmy grasshoppers. BMC Ecol 13:17.
54. Endler JA, Mielke PW (2005) Comparing entire colour patterns as birds see them. Biol J Linn Soc Lond 86(4):405-431.
55. Garland T, Dickerman AW, Janis CM, Jones JA (1993) Phylogenetic analysis of covariance by computer-simulation. Syst Biol 42(3):265-292.