Human-Induced Trophic Cascades along the Fecal Detritus Pathway

PLoS ONE

Volumn 8, Issue 10, 2013, Pages

  Nichols, Elizabeth ^a,b,i   Uriarte, María ^a   Peres, Carlos A ^c   Louzada, Julio ^d,e   Braga, Rodrigo Fagundes ^d   Schiffler, Gustavo ^f   Endo, Whaldener ^g   Spector, Sacha H ^h  

^a Och Spine at New York Presbyterian Hospitals   (United States)

^b DIVISION OF INVERTEBRATE ZOOLOGY   (United States)

^c UNIVERSITY OF EAST ANGLIA   (United Kingdom)

^d FEDERAL UNIVERSITY OF LAVRAS   (Brazil)

^e LANCASTER UNIVERSITY   (United Kingdom)

^f UNIVERSITY OF CAMPINAS   (Brazil)

^g NORWEGIAN UNIVERSITY OF LIFE SCIENCES   (Norway)

^h Department of Conservation Science Scenic Hudson ^*  (United States)

ⁱ UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; BEETLE; BIOLOGICAL TRAIT; BIOMASS; BODY SIZE; BRAZIL; COMMUNITY STRUCTURE; CONTROLLED STUDY; DETRITIVORE; DETRITUS; FECES; FOOD WEB; HUMAN; HUMAN ACTIVITIES; HUMAN IMPACT (ENVIRONMENT); LANDSCAPE; MAMMAL; NONHUMAN; SCARABAEINAE; SEED DISPERSAL; SPECIES DIVERSITY; SPECIES HABITAT; TROPHIC CASCADE; TROPICAL RAIN FOREST;

ANIMALS; BEETLES; BIODIVERSITY; BODY SIZE; BRAZIL; DEFECATION; ECOSYSTEM; FECES; FOOD CHAIN; HUMANS; MAMMALS; POPULATION DYNAMICS; TREES; TROPICAL CLIMATE;

EID: 84885811289     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0075819     Document Type: Article

References (97)

1. Schmitz OJ, Hamback PA, Beckerman AP, (2000) Trophic cascades in terrestrial systems: A review of the effects of carnivore removals on plants. American Naturalist 155: 141-153.
2. Schmitz OJ, (2006) Predators have large effects on ecosystem properties by changing plant diversity, not plant biomass. Ecology 87: 1432-1437.
3. Estes JA, Terborgh J, Brashares JS, Power ME, Berger J, et al. (2011) Trophic downgrading of planet Earth. Science 333: 301-306.
4. Terborgh J, Estes JA (2010) Trophic Cascades: Predators, Prey and the Changing Dynamics of Nature. Washington, DC: Island Press.
5. Wu X, Duffy JE, Reich PB, Sun S, (2011) A brown-world cascade in the dung decomposer food web of an alpine meadow: effects of predator interactions and warming. Ecological Monographs 81: 313-328.
6. Wardle DA, Bardgett RD, (2004) Human-induced changes in large herbivorous mammal density: the consequences for decomposers. Frontiers in Ecology and the Environment 2: 145-153.
7. Schmitz OJ, Hawlena D, Trussell GC, (2010) Predator control of ecosystem nutrient dynamics. Ecology Letters pp. 1199-1209.
8. Moore J, Berlow E, Coleman D, de Ruiter P, Dong Q, et al. (2004) Detritus, trophic dynamics and biodiversity. Ecology Letters 7: 584-600.
9. Nichols E, Gardner TA, Peres CA, Spector S, Scarabaeinae Res N, (2009) Co-declining mammals and dung beetles: an impending ecological cascade. Oikos 118: 481-487.
10. Zhao C, Griffin J, Wu X, Sun S, (2013) Predatory beetles facilitate plant growth by driving earthworms to lower soil layers. Journal of Animal Ecology.
11. Andresen E, Laurance SGW, (2007) Possible indirect effects of mammal hunting on dung beetle assemblages in Panama. Biotropica 39: 141-146.
12. Nichols E, Gardner TA, Peres CA, Spector S, (2009) Co-declining mammals and dung beetles: an impending ecological cascade. Oikos 118: 481-487.
13. Nichols E, Spector S, Louzada J, Larsen T, Amezquita S, et al. (2008) Ecological functions and ecosystem services of Scarabaeine dung beetles: a review. Biological Conservation 141: 1461-1474.
14. Terborgh J, Nuñez-Iturri G (2006) Disperser-free tropical forests await an unhappy fate. In: Laurance W, Peres CA, editors. Emerging Threats to Tropical Forests. Chicago & London: University of Chicago Press. pp. 241-252.
15. Stoner KE, Vulinec K, Wright SJ, Peres CA, (2007) Hunting and plant community dynamics in tropical forests: a synthesis and future directions. Biotropica 39: 385-392.
16. Andresen E, Feer F (2005) The role of dung beetles as secondary seed dispersers and their effect on plant regeneration in tropical rainforests. In: Forget PM, Lambert JE, Hulme PE, Vander Wall SB, editors. Seed fate: Predation, dispersal and seedling establishment Wallingford, Oxfordshire, UK: CABI International. pp. 331-349.
17. Polis GA, (1999) Why are parts of the world green? Multiple factors control productivity and the distribution of biomass. Oikos 86: 3-15.
18. Strong DR, (1992) Are trophic cascades all wet? Differentiation and donor-control in speciose ecosystems. Ecology 73: 747-754.
19. Persson L, (1999) Trophic cascades: abiding heterogeneity and the trophic level concept at the end of the road. Oikos 85: 385-397.
20. Polis GA, Strong DR, (1996) Food web complexity and community dynamics. American Naturalist 147: 813-846.
21. Otto SB, Berlow EL, Rank NE, Smiley J, Brose U, (2008) Predator diversity and identity drive interaction strength and trophic cascades in a food web. Ecology 89: 134-144.
22. Mooney KA, Halitschke R, Kessler A, Agrawal AA, (2010) Evolutionary trade-offs in plants mediate the strength of trophic cascades. Science 327: 1642-1644.
23. Werner EE, Peacor SD, (2003) A review of trait-mediated indirect interactions in ecological communities. Ecology 84: 1083-1100.
24. Vazquez DP, Chacoff NP, Cagnolo L, (2009) Evaluating multiple determinants of the structure of plant-animal mutualistic networks. Ecology 90: 2039-2046.
25. Bascompte J, Melian CJ, Sala E, (2005) Interaction strength combinations and the overfishing of a marine food web. Proceedings of the National Academy of Sciences of the United States Of America 102: 5443-5447.
26. Peres C, Palacios E, (2007) Basin-wide effects of game harvest on vertebrate population densities in Amazonian forests: implications for animal-mediated seed dispersal. Biotropica 39: 304-315.
27. Markl JS, Schleuning M, Forget PM, Jordano P, Lambert JE, et al. (2012) Meta-analysis of the effects of human disturbance on seed dispersal by animals. Conservation Biology 26: 1072-1081.
28. Bayley PN, Petrere M, (1989) Amazon fisheries: assessment methods, current status and management options. Special Publications of the Canadian Journal of Fisheries and Aquatic Sciences 106: 385-398.
29. Peres CA (2000) Evaluating the impact and sustainability of subsistence hunting at multiple Amazonian forest sites. In: Robinson JG, Bennett EL, editors. Hunting for Sustainability in Tropical Forests. New York: Columbia University Press. pp. 31-56.
30. Haugaasen T, Peres CA, (2005) Primate assemblage structure in Amazonian flooded and unflooded forests. American Journal of Primatology 67: 243-258.
31. Haugaasen T, Peres CA, (2005) Mammal assemblage structure in Amazonian flooded and unflooded forests. Journal Of Tropical Ecology 21: 133-145.
32. Newton P, Endo W, Peres CA, (2012) Determinants of livelihood strategy variation in two extractive reserves in Amazonian flooded and unflooded forests. Environmental Conservation 39: 97-110.
33. Puertas PE, Bodmer ER (2004) Hunting effort as a tool for community-based wildlife management in Amazonia. In: Silvius KM, Bodmer RE, Fragoso JMV, editors. People in Nature: Wildlife conservation in South and Central America. New York: Columbia University Press. pp. 122-135.
34. Hawes J, Peres C, Riley L, Hess L, (2012) Landscape-scale variation in structure and biomass of Amazonian seasonally flooded and unflooded forests. Forest Ecology and Management 281: 163-176.
35. Derickx J (1992) No Coração da Amazônia: Juruá- o Rio que Chora. Petropolis: Vozes.
36. Estercil N, Schweickardt K, (2010) Territórios amazônicos de reforma agrária e de conservação da natureza. Bol Mus Para Emílio Goeldi Cienc Hum 5: 59-77.
37. IBGE (2010) Censo Populacional 2010. Instituto Brasileiro de Geografia e Estatística (IBGE).
38. Jerozolimski A, Peres C, (2003) Bringing home the biggest bacon: a cross-site analysis of the structure of hunter-kill profiles in Neotropical forests. Biological Conservation pp. 111.
39. Urquiza-Haas T, Peres CA, Dolman PM, (2011) Large vertebrate responses to forest cover and hunting pressure in communal landholdings and protected areas of the Yucatan Peninsula, Mexico. Animal Conservation 14: 271-282.
40. Rist J, Rowcliffe M, Cowlishaw G, Milner-Gulland EJ, (2008) Evaluating measures of hunting effort in a bushmeat system. Biological Conservation 141: 2086-2099.
41. Naughton-Treves L, Mena JL, Treves A, Alvarez N, Radeloff VC, (2003) Wildlife survival beyond park boundaries: The impact of slash-and-burn agriculture and hunting on mammals in Tambopata, Peru. Conservation Biology 17: 1106-1117.
42. Fa JE, Ryan SF, Bell DJ, (2005) Hunting vulnerability, ecological characteristics and harvest rates of bushmeat species in afrotropical forests. Biological Conservation 121: 167-176.
43. Poulsen JR, Clark CJ, Bolker BM, (2011) Decoupling the effects of logging and hunting on an Afrotropical animal community. Ecological Applications 21: 1819-1836.
44. Fa J, Brown D, (2009) Impacts of hunting on mammals in African tropical moist forests: a review and synthesis. Mammal Review 39: 231-265.
45. Parry L, Barlow J, Peres CA, (2009) Allocation of hunting effort by Amazonian smallholders: Implications for conserving wildlife in mixed-use landscapes. Biological Conservation 142: 1777-1786.
46. Franzen M, (2006) Evaluating the sustainability of hunting: a comparison of harvest profiles across three Huaorani communities. Environmental Conservation 33: 36-45.
47. Wilkie DS, Carpenter JF, (1999) Bushmeat hunting in the Congo Basin: An assessment of impacts and options for mitigation. Biodiversity & Conservation 8: 927-955.
48. Refisch J, Kone I, (2005) Impact of commercial hunting on monkey populations in the Tai region, Cote d'Ivoire. BIOTROPICA 37: 136-144.
49. MEB (2003) Movimento Educação de Base Departamento de Carauari. Memorial Institucional do MEB. Amazonas Relatorio.
50. Peres CA, Cunha A (2011) Censo e monitoramento de vertebrados de médio e grandee porte por transecção linear em florestas tropicais. Brasília: Wildife Conservation Society, Ministério do Meio Ambiente e ICMBio, Brasil.
51. Peres CA (1999) Nonvolant mammal community structure in different Amazonian forest types. In: Eisenberg JF, Redford KH, editors. Mammals of the Neotropics: the Central Neotropics. Chicago: University of Chicago Press. pp. 564-581.
52. Nichols E, Gardner TA, (2011) Dung beetles as a model taxon for conservation science and management. Dung Beetle Ecology and Evolution.
53. Larsen TH, Lopera A, Forsyth A, (2006) Extreme trophic and habitat specialization by Peruvian dung beetles (Coleoptera: Scarabaeidae: Scarabaeinae). Coleopterists Bulletin 60: 315-324.
54. Howden HF, Nealis VG, (1975) Effects of clearing in a tropical rain forest on the composition of the coprophagous scarab beetle fauna (Coleoptera). Biotropica 7: 77-83.
55. Martin-Piera F, Lobo JM, (1996) A comparative discussion of trophic preferences in dung beetle communities. Miscellania Zoologica Barcelona 19: 13-31.
56. Vaz-de-Mello FZ, Edmonds WD, Ocampo FC, Schoolmeesters P, (2011) A multilingual key to the genera and subgenera of the subfamily Scarabaeinae of the New World (Coleoptera: Scarabaeidae). Zootaxa pp. 1-73.
57. Nichols E, Uriarte M, Bunker DE, Favila M, Slade EM, et al. (2013) Trait-dependent response of dung beetle populations to tropical forest conversion at local to global scales. Ecology 94: 180-189.
58. Slade EM, Mann DJ, Villanueva JF, Lewis OT, (2007) Experimental evidence for the effects of dung beetle functional group richness and composition on ecosystem function in a tropical forest. Journal of Animal Ecology 76: 1094-1104.
59. Halffter G, Edmonds WD (1982) The Nesting Behavior of Dung Beetles (Scarabaeinae): an Ecological and Evolutive Approach. México, D. F.: Institúto de Ecología.
60. Shipley B, (2009) Confirmatory path analysis in a generalized multilevel context. Ecology 90: 363-368.
61. Chame M, (2003) Terrestrial mammal feces: a morphometric summary and description. Memórias do Instituto Oswaldo Cruz 98: 71-94.
62. Bates D (2010) lme4: Mixed-effects modeling with R: Springer.
63. Shipley B (2002) Cause and Correlation in Biology: A User's Guide to Path Analysis, Structural Equations and Causal Inference. Cambridge: Cambridge University Press.
64. Pinheiro JC, Bates DM, DebRoy S (2010) nlme: Linear and Nonlinear Mixed Effects Models. Vienna, Austria.: The Comprehensive R Archive Network (CRAN).
65. R Development Core Team (2011) R: A Language and Environment for Statistical Computing. 2.10.01 ed. Vienna, Austria: R Foundation for Statistical Computing.
66. Robinson JG, Redford KH, (1986) Intrinsic rate of natural increase in Neotropical forest mammals- relationship to phylogeny and diet. Oecologia 68: 516-520.
67. Slade EM, Mann DJ, Lewis OT, (2011) Biodiversity and ecosystem function of tropical forest dung beetles under contrasting logging regimes. Biological Conservation 144: 166-174.
68. Vulinec K, (2002) Dung beetle communities and seed dispersal in primary forest and disturbed land in Amazonia. Biotropica 34: 297-309.
69. Gardner TA, Hernandez MIM, Barlow J, Peres CA, (2008) Understanding the biodiversity consequences of habitat change: the value of secondary and plantation forests for neotropical dung beetles. Journal of Applied Ecology 45: 883-893.
70. Silvius KM, (2002) Spatio-temporal patterns of palm endocarp use by three Amazonian forest mammals: granivory or 'grubivory'? Journal of Tropical Ecology 18: 707-723.
71. Culot L, Bovy E, Zagury Vaz-de-Mello F, Guevara R, Galetti M, (2013) Selective defaunation affects dung beetle communities in continuous Atlantic rainforest. Biological Conservation 163: 79-89.
72. Tribe GD, Burger BV (2011) Olfactory Ecology. In: Simmons LW, Ridsdill Smith TJ, editors. Ecology and Evolution of Dung Beetles. New York: Wiley-Blackwell. pp. 87-106.
73. Burger BV, Petersen WGB, (1991) Semiochemicals of the Scarabaeinae, III. Identification of an attractant for the dung beetle Pachyolomerus femoralis in the fruit of the spineless monkey orange tree Strychnos madagascariensis. Zeitschrift fur Naturforschung 46c: 1073-1079.
74. Horgan FG, (2005) Effects of deforestation on diversity, biomass and function of dung beetles on the eastern slope of the Peruvian Andes. Forest Ecology and Management 216: 117-133.
75. Wright JS, Zeballos H, Dominguez I, Gallardo MM, Moreno MC, et al. (2000) Poachers alter mammal abundance, seed dispersal and seed predation in a Neotropical forest. Conservation Biology 14: 227-239.
76. Nichols E, Larsen T, Spector S, Davis AL, Escobar F, et al. (2007) Global dung beetle response to tropical forest modification and fragmentation: A quantitative literature review and meta-analysis. Biological Conservation 137: 1-19.
77. Levi T, Shepard GH, Ohl-Schacherer J, Wilmers CC, Peres CA, et al. (2011) Spatial tools for modeling the sustainability of subsistence hunting in tropical forests. Ecological Applications 21: 1802-1818.
78. Sirén A, Hambäck P, Machoa J, (2004) Including spatial heterogeneity and animal dispersal when evaluation hunting a model analysis and an empircial assessment in an Amazonian community. Conservation Biology 18: 1315-1329.
79. Maron JL, Pearson DE, (2011) Vertebrate predators have minimal cascading effects on plant production or seed predation in an intact grassland ecosystem. Ecology Letters 14: 661-669.
80. Kauffman MJ, Brodie JF, Jules ES, (2010) Are wolves saving Yellowstone's aspen? A landscape-level test of a behaviorally mediated trophic cascade. Ecology 91: 2742-2755.
81. Braga RF, Korasaki V, Andresen E, Louzada J, (2013) Dung beetle community and functions along a habitat-disturbance gradient in the Amazon: a rapid assessment of ecological functions associated to biodiversity. Plos One 8.
82. Braga RF, Korasaki V, Audino LD, Louzada J, (2012) Are dung beetles driving dung-fly abundance in traditional agricultural areas in the Amazon? Ecosystems 15: 1173-1181.
83. Palacios E, Peres CA, (2005) Primate population densities in three nutrient-poor amazonian terra firme forests of south-eastern Colombia. Folia Primatologica 76: 135-145.
84. Peres CA, (1997) Effects of habitat quality and hunting pressure on arboreal folivore densities in neotropical forests: A case study of howler monkeys (Alouatta spp.). Folia Primatologica 68: 199-222.
85. Peres CA, Lake IR, (2003) Extent of nontimber resource extraction in tropical forests: Accessibility to game vertebrates by hunters in the Amazon basin. Conservation Biology 17: 521-535.
86. Clayton L, Keeling M, MilnerGulland EJ, (1997) Bringing home the bacon: A spatial model of wild pig hunting in Sulawesi, Indonesia. Ecological Applications 7: 642-652.
87. Newton P, Watkinson AR, Peres CA, (2011) Determinants of yield in a non-timber forest product: Copaifera oleoresin in Amazonian extractive reserves. Forest Ecology and Management 261: 255-264.
88. Newton P, Nichols ES, Endo W, Peres CA, (2012) Consequences of actor level livelihood heterogeneity for additionality in a tropical forest payment for environmental services programme with an undifferentiated reward structure. Global Environmental Change 22: 127-136.
89. Srivastava DS, Cardinale BJ, Downing AL, Duffy JE, Jouseau C, et al. (2009) Diversity has stronger top-down than bottom-up effects on decomposition. Ecology 90: 1073-1083.
90. Dyer LA, Letourneau D, (2003) Top-down and bottom-up diversity cascades in detrital vs. living food webs. Ecology Letters 6: 60-68.
91. Carpenter SR, DeFries R, Dietz T, Mooney H, Polasky S, et al. (2006) Millennium Ecosystem Assessment: Research Needs. Science 314: 257-258.
92. Loreau M, Mouquet N, Gonzalez A, (2003) Biodiversity as spatial insurance in heterogeneous landscapes. Proceedings Of The National Academy Of Sciences Of The United States Of America 100: 12765-12770.
93. Naranjo EJ, Bodmer RE, (2007) Source-sink systems and conservation of hunted ungulates in the Lacandon Forest, Mexico. Biological Conservation 138: 412-420.
94. Roslin T, Koivunen A, (2001) Distribution and abundance of dung beetles in fragmented landscapes. Oecologia 127: 69-77.
95. Beckerman AP, Uriarte M, Schmitz OJ, (1997) Experimental evidence for a behavior-mediated trophic cascade in a terrestrial food chain. Proceedings of the National Academy of Sciences of the United States of America 94: 10735-10738.
96. Hawlena D, Strickland MS, Bradford MA, Schmitz OJ, (2012) Fear of Predation Slows Plant-Litter Decomposition. Science 336: 1434-1438.
97. Matassa CM, Trussell GC, (2011) Landscape of fear influences the relative importance of consumptive and nonconsumptive predator effects. Ecology 92: 2258-2266.