Dietary Flexibility of the Brown Howler Monkey Throughout Its Geographic Distribution

American Journal of Primatology

Volumn 75, Issue 1, 2013, Pages 16-29

  Chaves, Óscar M ^a   Bicca Marques, Júlio César ^a  

^a PONTIFICAL CATHOLIC UNIVERSITY OF RIO GRANDE DO SUL   (Brazil)

Author keywords

Alouatta guariba clamitans; Atlantic forest; Forest fragmentation; Generalist diet

Indexed keywords

ARBOREAL SPECIES; CONCENTRATION (COMPOSITION); DIETARY SHIFT; GEOGRAPHICAL DISTRIBUTION; HABITAT CONSERVATION; HABITAT FRAGMENTATION; HABITAT LOSS; INVASIVE SPECIES; LATITUDE; PLANT COMMUNITY; PRIMATE; WILD POPULATION;

ARGENTINA; ATLANTIC FOREST; BRAZIL;

ALOUATTA; ALOUATTA GUARIBA; ALOUATTA GUARIBA CLAMITANS; MAMMALIA; PRIMATES; ZANTHOXYLUM;

EID: 84871365524     PISSN: 02752565     EISSN: 10982345     Source Type: Journal    
DOI: 10.1002/ajp.22075     Document Type: Review

References (85)

1. Agostini I. 2009. Ecology and behavior of two howler monkey species (Alouatta guariba clamitans and Alouatta caraya) living in sympatry in Northeastern Argentina [PhD dissertation]. Rome: Università degli studi di Roma La "Sapienza." 202 p.
2. Agostini I, Holzmann I, Di Bitetti MS. 2010. Are howler monkey species ecologically equivalent? Trophic niche overlap in syntopic Alouatta guariba clamitans and Alouatta caraya. Am J Primatol 72:173-186.
3. Aguiar LM, Reis NR, Ludwig G, Rocha VJ. 2003. Dieta, área de vida, vocalizações e estimativas populacionais de Alouatta guariba em um remanescente florestal no Norte do estado do Paraná. Neotrop Primates 11:78-86.
4. Arroyo-Rodríguez V, Dias PAD. 2010. Effects of habitat fragmentation and disturbance on howler monkeys: a review. Am J Primatol 72:1-16.
5. Arroyo-Rodríguez V, Mandujano S. 2006. Forest fragmentation modifies habitat quality for Alouatta palliata. Int J Primatol 27:1079-1096.
6. Arroyo-Rodríguez V, Mujano S, Benitez-Malvido J, Cuende-Fanton C. 2007. The influence of large tree density on howler monkey (Alouatta palliata mexicana) presence in very small rain forest fragments. Biotropica 39:760-766.
7. Bicca-Marques JC. 2003 How do howler monkeys cope with habitat fragmentation. In: Marsh LK, editor. Primates in fragments: ecology and conservation. New York: Kluwer Academics/Plenum Publishers. p 283-303.
8. Bicca-Marques JC. 2009. Outbreak of yellow fever affects howler monkeys in southern Brazil. Oryx 43:173.
9. Bonilla-Sánchez YM, Serio-Silva JC, Pozo-Montuy G, Chapman CA. 2012. Howlers are able to survive in Eucalyptus plantations where remnant and regenerating vegetation is available. Int J Primatol 33:233-249.
10. Boyle SA. 2008. The effects of forest fragmentation on primates in the Brazilian Amazon [PhD dissertation]. Tempe, AZ: Arizona State University. 307 p.
11. Bravo SP, Sallenave A. 2003. Foraging behavior and activity patterns of Alouatta caraya in the northeastern Argentinean flooded forest. Int J Primatol 24:825-846.
12. Campbell-Smith G, Simanjorang HVP, Leader-Williams N, Linkie M. 2010. Local attitudes and perceptions toward crop-raiding by orangutans (Pongo abelii) and other nonhuman Primates in northern Sumatra, Indonesia. Am J Primatol 72:866-876.
13. Chapman CA, Peres CA. 2001. Primate conservation in the new millennium: the role of scientists. Evol Anthropol 10:16-33.
14. Chaves OM, Stoner KE, Arroyo-Rodríguez V. 2012. Differences in diet between spider monkey groups living in forest fragments and continuous forest in Lacandona, Mexico. Biotropica 44:105-113.
15. Chiarello AG. 1994. Diet of the brown howler monkey Alouatta fusca in a semi-deciduous forest fragment of southeastern Brazil. Primates 35:25-34.
16. Chiarello AG, Aguiar LM, Cerqueira R, Melo FR, Rodrigues FH, Silva VMF. 2008. Mamíferos ameaçados de extinção no Brasil. In: Hado ABM, Drummond GM, Paglia AP, editors. Livro Vermelho da fauna brasileira ameaçada de extinção. Brasília: Ministério do Meio Ambiente. p 681-879.
17. Coley PD, Barone JA. 1996. Herbivory and plant defenses in tropical forests. Ann Rev Ecol Syst 27:305-335.
18. Colwell RK. 2005. EstimateS: statistical estimation of species richness and shared species from samples. Version 7.5. User's guide and application. Storrs, CT: University of Connecticut. Available online at: http://purl.oclc.org/estimates [accessed March 24, 2012].
19. Colwell RK, Mao CX, Chang J. 2004. Interpolating, extrapolating, and comparing incidence-based species accumulation curves. Ecology 85:2717-2727.
20. Cortés-Ortiz L, Bermingham E, Rico C, Rodríguez-Luna E, Sampaio I, Ruiz-García M. 2003. Molecular systematics and biogeography of the Neotropical monkey genus, Alouatta. Mol Phylogenet Evol 26:64-81.
21. Cristóbal-Azkarate J, Arroyo-Rodríguez V. 2007. Diet and activity pattern of howler monkeys (Alouatta palliata) in Los Tuxtlas, Mexico: effects of habitat fragmentation and implications for conservation. Am J Primatol 69:1013-1029.
22. Cunha AS. 1994. Aspectos socio-ecologicos de um grupo de bugios (Alouatta fusca clamitans) do Parque Estadual de Itapuã [MSc dissertation]. Porto Alegre (RS): Universidade Federal do Rio Grande do Sul. 79 p.
23. Di Fiore A, Link A, Campbell CJ. 2010. The atelines: behavioral and socioecological diversity in a New World radiation. In: Campbell C, Fuentes A, Mackinnon KC, Panger M, Bearder SK, editors. Primates in perspective. Oxford: Oxford University Press. p 155-188.
24. Di Fiore A, Link A, Dew JL. 2008. Diets of wild spider monkeys. In: Campbell CJ, editor. Spider monkeys: behavior, ecology and evolution of the genus Ateles. New York: Cambridge University Press. p 81-137.
25. Dunn JC, Asensio N, Arroyo-Rodriguez V, Schnitzer S, Cristóbal-Azkarate J. 2012. The ranging costs of a fallback food: liana consumption supplements diet but increases foraging effort in howler monkeys. Biotropica. doi:10.1111/j.1744-7429.2012.00856.x.
26. Dunn JC, Cristóbal-Azkarate J, Vea JJ. 2009. Differences in diet and activity pattern between two groups of Alouatta palliata associated with the availability of big trees and fruit of top food taxa. Am J Primatol 71:654-662.
27. FAO. 2011. State of the world's forest 2011. Rome: Food and Agriculture Organization of the United Nations.
28. Fortes VB. 1999. Dieta, actividades e uso do espaço por Alouatta fusca clamitans (Cabrera, 1940) (Primates: Cebidade) na depressão central do Rio Grande do Sul [MSc dissertation]. Porto Alegre (RS): Universidade Federal do Rio Grande do Sul. 121 p.
29. Fortes VB. 2008. Ecologia e comportamento do bugio-ruivo (Alouatta guariba clamitans Cabrera, 1940) em fragmentos florestais na depressão central do Rio Grande do Sul, Brasil [PhD dissertation]. Porto Alegre (RS): Pontifícia Universidade Católica do Rio Grande do Sul. 130 p.
30. Freeland WJ, Janzen DH. 1974. Strategies of herbivory in mammals: the role of plant secondary compounds. Am Nat 108:269-289.
31. Galetti M, Pedroni F, Morellato LPC. 1994. Diet of the brown howler monkey Alouatta fusca in a forest fragment in southeastern Brazil. Mammalia 58:111-118.
32. Garcia AL. 2007. Forrageamento de Alouatta guariba clamitans cabrera, 1940 (Primates, Atelidae) em áreas fragmentadas da Mata Atlântica: influência de metabólitos secundários de plantas e da florística e estrutura das comunidades arbóreas [PhD dissertation]. Rio de Janeiro (RJ): Universidade Federal do Rio de Janeiro. 200 p.
33. Gaspar DA. 1997. Ecologia e comportamento do bugio ruivo, Alouatta fusca (Geoffroy, 1812, Primates: Cebidae), em fragmento de Mata de Campinas, SP [MSc dissertation]. Rio Claro (SP): Universidade Estadual Paulista Júlio de Mesquita Filho. 85 p.
34. Gentry AH. 1982. Patterns of neotropical plant species diversity. Evol Biol 15:1-84.
35. González-Zamora A, Arroyo-Rodríguez V, Chaves OM, Sánchez-López S, Stoner KE, Riba-Hernández P. 2009. Diet of spider monkeys (Ateles geoffroyi) in Mesoamerica: current knowledge and future directions. Am J Primatol 71:8-20.
36. Gotelli NJ, Colwell RK. 2001. Quantifying biodiversity: procedures and pitfalls in the measurement and comparison of species richness. Ecol Lett 4:79-391.
37. Gregorin R. 2006. Taxonomia e variação geográfica das espécies do gênero Alouatta Lacépède (Primates, Atelidae) no Brasil. Rev Bras Zool 23:64-144.
38. Guzzo GB. 2009. Ecologia e comportamento de Alouatta guariba clamitans Cabrera, 1940, em um fragmento de mata de araucária na Serra Gaúcha [Dissertation]. Porto Alegre (RS): Pontifícia Universidade Católica do Rio Grande do Sul. 53 p.
39. Hill RA, Barrett L, Gaynor D, Weingrill T, Dixon P, Payne H, Henzi SP. 2003. Day length, latitude and behavioural flexibility in baboons (Papio cynocephalus ursinus). Behav Ecol Sociobiol 53:278-286.
40. Jardim MMA, Oliveira LF. 2000. Aspectos ecológicos e do comportamento de Alouatta fusca (Geoffroyi, 1812) na Estação Ecológica de Aracuri, RS, Brasil. In: Alonso C, Langguth A, editors. A primatologia no Brasil, Vol. 7. João Pessoa (PB): Sociedade Brasileira de Primatologia. p 151-170.
41. Jones CB. 2005. Behavioral flexibility in primates: causes and consequences. New York: Springer.
42. Kikuzawa K, Lechowicz MJ. 2011. Ecology of leaf longevity. New York: Springer.
43. Kinzey WG. 1982. Distribution of primates and forest refuges. In: Prance GT, editor. Biological diversification in the tropics. New York: Columbia University Press. p 455-482.
44. Koch F. 2008. Dieta e comportamento de um grupo de Alouatta guariba clamitans Cabrera, 1940: uma relação de causa e efeito? [MSc dissertation]. Porto Alegre (RS): Pontifíca Universidade Católica do Rio Grande do Sul. 48 p.
45. Koch F, Bicca-Marques JC. 2007. Padrão de atividades e dieta de Alouatta guariba clamitans Cabrera, 1940: uma análise sexo-etária. In: Bicca-Marques JC, editor. A primatologia no Brasil, Vol. 10. Porto Alegre: Sociedade Brasileira de Primatologia. p 353-361.
46. Korstjens AH, Lehman J, Dunbar RIM. 2010. Resting time as an ecological constraint on primate biogeography. Anim Behav 79:361-374.
47. Kovach WL. 1998. MVSP: a multivariate statistical package for windows, version 3.0. Pentraeth, Wales: Kovach Computing Services.
48. Lansky EP, Paavilainen HM. 2011. Figs: the genus Ficus. New York: CRC Press.
49. Laurance WF, Nascimento HEM, Laurance SG, Andrade A, Ribeiro JELS, Giraldo JP, Lovejoy TE, Condit R, Chave J, Harms KE, D' Angelo S. 2006. Rapid decay of tree-community composition in Amazonian forest fragments. Proc Natl Acad Sci 103:19010-19014.
50. Lehman A, O'Rourke N, Hatcher L, Stepanski EJ. 2005. JMP® for basic univariate and multivariate statistics: a step-by-step guide. Cary, NC: SAS Institute.
51. Limeira VLA. 1996. Comportamento alimentar, padrão de atividades e uso do espaço por Alouatta fusca (Primates, Platyrrhini) em un fragmento degradado de floresta Atlântica no estado do Rio de Janeiro [MSc dissertation]. Rio de Janeiro (RJ): Universidade Federal do Rio de Janeiro. 135 p.
52. Ludwig G, Aguiar LM, Svoboda WK, Hilst CLS, Navarro IT, Vitule JRS, Passos FC. 2008. Comparison of the diet of Alouatta caraya (Primates: Atelidae) between a riparian island and mainland on the Upper Parana River, southern Brazil. Rev Bras Zool 25:419-426.
53. Lunardelli MC. 2000. Padrões de atividade e efeitos de compostos fenólicos na ecologia alimentar de um grupo de bugios-ruivos (Alouatta fusca) no sudeste brasileiro [MSc dissertation]. São Paulo (SP): Universidade de São Paulo. 70 p.
54. Marques AAB. 1996. O bugio ruivo Alouatta fusca clamitans (Cabrera, 1940) (Primates, Cebidae) na Estação Ecológica de Aracuri, RS: variações sazonais de forrageamento [MSc dissertation]. Porto Alegre (RS): Pontifícia Universidade Católica do Rio Grande do Sul. 129 p.
55. Marsh LK. 2003. The nature of fragmentation. In: Marsh LK, editor. Primates in fragments: ecology and conservation. New York: Kluwer Academic. p 1-10.
56. Martins CS. 1997. Uso de habitat pelo bugio, Alouatta fusca clamitans, em um fragmento florestal em Lençóis Paulista-SP [MSc dissertation]. Campinas (SP): Universidade Estadual de Campinas. 87 p.
57. Martins JN. 2008a. Flexibilidade alimentar e comportamental do bugio-ruivo Alouatta guariba clamitans Cabrera, 1940 (Primates, Atelidae) em relação ao uso de espécies vegetais alóctones em Caxias do Sul, RS [Monograph]. Caxias do Sul (RS): Universidade de Caxias do Sul. 109 p.
58. Martins MM. 2008b. Fruit diet of Alouatta guariba and Brachyteles arachnoides in southeastern Brazil: comparison of fruit type, color, and seed size. Primates 49:1-8.
59. Mendes SL. 1989. Estudo ecológico de Alouatta fusca (Primates: Cebidae) na Estação Biológica de Caratinga, MG. Rev Nordestina Biol 6:71-104.
60. Milton K. 1978. Cost-benefit-analysis of factors influencing leaf preferences of howler monkeys. Am J Phys Anthropol 48:420-420.
61. Milton K. 1979. Factors influencing leaf choice by howler monkeys: test of some hypotheses of food selection by generalist herbivores. Am Nat 114:362-78.
62. Milton K. 1981. Food choice and digestive strategies of two sympatric primate species. Am Nat 117:476-495.
63. Miranda JM. 2004. Ecologia e conservação de Alouatta guariba clamitans Cabrera, 1940 em Floresta Ombrófila Mista no estado do Paraná, Brasil [MSc dissertation]. Curitiba (PR): Universidade Federal do Paraná. 95 p.
64. Moles AT, Bonser SP, Poore AGB, Wallis IR, Foley WJ. 2011. Assessing the evidence for latitudinal gradients in plant defense and herbivory. Funct Ecol 25:380-388.
65. Myers N, Mittermeier RA, Mittermeier CG, Fonseca GAB, Kent J. 2000. Biodiversity hotspots for conservation priorities. Nature 403:853-858.
66. Ochoa-Gaona S, Gonzalez-Espinosa M, Meave JA, Bon VSD. 2004. Effect of forest fragmentation on the woody flora of the highlands of Chiapas, Mexico. Biodivers Conserv 13:867-884.
67. Oliveira EM. 2003. Ecologia de Alouatta guariba clamitans (Humboldt, 1812-Primates, Atelidae), em mata estacional semidecídua no Sudeste do Brasil [MSc dissertation]. Uberlandia (MG): Universidade Federal de Uberlândia. 81 p.
68. Oliveira-Filho AT, Fontes MAL. 2000. Patterns of floristic differentiation among Atlantic forest in southeastern Brazil and the influence of climate. Biotropica 32:793-810.
69. Onderdonk DA, Chapman CA. 2000. Coping with forest fragmentation: the primates of Kibale National Park, Uganda. Int J Primatol 21:587-611.
70. Pereira TS. 2008. Ecologia cognitiva e forrageamento de Alouatta guariba clamitans Cabrera, 1940: os bugios-ruivos possuem mapas mentais? [MSc dissertation]. Porto Alegre (RS): Pontifícia Universidade Católica do Rio Grande do Sul. 91 p.
71. Perez DM. 1998. Estudo ecológico do bugio-ruivo em uma floresta com araucária do sul do Brasil (Alouatta fusca, Ihering 1914 - Primates, Atelidae) [MSc dissertation]. São Paulo (SP): Universidade de São Paulo. 90 p.
72. Peter FP. 2007. Padrões de atividades e comportamento alimentar de um grupo de bugio-ruivos (Alouatta guariba clamitans) no limite austral da sua distribuição geográfica [Monograph]. Pelotas (RS): Universidade Católica de Pelotas. 51 p.
73. Piersma T, Drent J. 2003. Phenotypic plasticity and the evolution of organismal design. Trends Ecol Evol 18:228-233.
74. Pinto AC, Azevedo-Ramos C, de Carvalho Jr. O. 2003. Activity patterns and diet of the howler monkey Alouatta belzebul in areas of logged and unlogged forest in Eastern Amazonia. Anim Biodivers Conserv 26:39-49.
75. Pinto LP, Setz EZF. 2004. Diet of Alouatta belzebul discolor in an Amazonian Rain Forest of northern Mato Grosso State, Brazil. Int J Primatol 25:1197-1211.
76. Pozo-Montuy G, Serio-Silva JC. 2006. Comportamiento alimentario de monos aulladores negros (Alouatta pigra Lawrence, Cebidae) en hábitat fragmentado en Balancán, Tabasco, México. Acta Zool Mex 22:53-66.
77. Printes RC, Liesenfeld MVA, Jerusalinsky L. 2001. Alouatta guariba clamitans Cabrera, 1940: a new southern limit for the species and for Neotropical primates. Neotrop Primates 9:118-121.
78. Ribeiro MC, Metzger JP, Martensen AC, Ponzoni FJ, Hirota MM. 2009. The Brazilian Atlantic forest: how much is left, and how is the remaining forest distributed? Implications for conservation. Biol Conserv 142:1141-1153.
79. Rivera A, Calmé S. 2006. Forest fragmentation and its effects on the feeding ecology of black howlers (Alouatta pigra) from the Calakmul area in Mexico. In: Estrada A, Garber PA, Pavelka M, Luecke L, editors. New perspectives in the study of Mesoamerican primates: distribution, ecology, behavior, and conservation. New York: Springer. p 189-213.
80. Rylands AB, Mittermeier RA. 2009. The diversity of New World primates (Platyrrhini): an annotated taxonomy. In: Garber PA, Estrada A, Bicca-Marques JC, Heymann EW, Strier K, editors. South American primates: comparative perspectives in the study of behavior, ecology, and conservation. New York: Springer Press. p 23-54.
81. Santos GA. 2007. Dieta e dispersão de sementes pelo "bugio-ruivo" Alouatta clamitans Cabrera, 1940 (Primates, Atelidae) em um fragmento florestal no norte do Paraná, Brasil [MSc dissertation]. Londrina (PR): Universidade Estadual de Londrina. 85 p.
82. Shanahan M, So S, Compton SG, Corlett R. 2001. Fig-eating by vertebrate frugivores: a global review. Biol Rev 76:529-572.
83. Silver SC, Marsh LK. 2003. Dietary flexibility, behavioral plasticity, and survival in fragments: lessons from translocated howlers. In: Marsh LK, editor. Primates in fragments: ecology and conservation. New York: Kluwer Academics/Plenum Publishers. p 251-265.
84. Steinmetz S. 2000. Ecologia e comportamento do bugio (Alouatta fusca clamitans, Atelidae-Primates) no Parque Estadual Intervales-SP [MSc dissertation]. São Paulo (SP): Universidade de São Paulo. 101 p.
85. West-Eberhard MJ. 2003. Phenotypic accommodation: adaptive innovation due to developmental plasticity, with or without genetic change. Integr Comp Biol 43:970-970.