Fruit as a key factor in howler monkey population density: Conservation implications

Howler Monkeys: Behavior, Ecology, and Conservation

Volumn , Issue , 2015, Pages 357-382

  Behie, Alison M ^a   Pavelka, Mary S M ^b  

^a AUSTRALIAN NATIONAL UNIVERSITY   (Australia)

^b UNIVERSITY OF CALGARY   (Canada)

Author keywords

Fruit consumption; Population density; Reproduction

Indexed keywords

EID: 84939979197     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1007/978-1-4939-1960-4_13     Document Type: Book

References (108)

1. Abbott DH (1987) Behaviorally mediated suppression of reproduction in female primates. J Zool 213:455-470.
2. Agostini I, Holzmann I, Di Bitetti S (2010) Are howler monkey species ecologically equivalent? Tropic niche overlap in syntopic Alouatta guariba clamitans and Alouatta caraya. Am J Primatol 72:173-186.
3. Aldana AM, Beltran M, Torres-Neira J, Stevenson PR (2008) Habitat characteristics and population density of brown spider monkeys (Ateles hybridus) in Megdalena Valley, Columbia. Neotrop Primates 15:46-50.
4. Altmann J (1974) Observational study of behaviour: Sampling methods. Behaviour 49:227-267.
5. Asensio N, Cristobal-Azkarate J, Dias PAD, Vea JJ, Rodriguez-Luna E (2007) Foraging habits of Alouatta palliata mexicana in three forest fragments. Folia Primatol 78:141-153.
6. Avitsur R, Stark JL, Sheridan JF (2001) Social stress induces glucocorticoid resistance in subordinate animals. Horm Behav 39:247-257.
7. Behie AM, Pavelka MSM (2005) The effect of a hurricane on the food supply of black howlers (Alouatta pigra) in Southern Belize. Biotropica 37:102-108.
8. Behie AM, Pavelka MSM (2012) Food selection in the black howler monkey following habitat disturbance: Implications for the importance of mature leaves. J Trop Ecol 28:153-160.
9. Behie AM, Pavelka MSM, Chapman CA (2010) Ecological sources of variation in fecal cortisol levels in howler monkeys in Belize. Am J Primatol 72:600-606.
10. Bercovitch FB, Ziegler TE (2002) Current topics in primate socioendocrinology. Annu Rev Anthropol 31:45-67.
11. Bicca-Marques JC (2003) How do howler monkeys cope with habitat fragmentation? In: Marsh LK (ed) Primates in fragments: Ecology and conservation. Kluwer, New York.
12. Bicca-Marques JC, Calegaro-Marques C (1994) Exotic plant species can serve as staple food sources for wild howler populations. Folia Primatol 63:209-211.
13. Blouch RA (1997) Distribution and abundance of orangutans (Pongo pygmaeus) in the Lanjak Entimau Wildlife Sanctuary, Sarawak, Malaysia. Trop Biodivers 4:259-274.
14. Boose ER, Foster DR, Fluet M (1994) Hurricanes impacts to tropical and temperate forest landscapes. Ecol Monogr 64:369-400.
15. Boutin S (1990) Food supplementation experiments with terrestrial vertebrates: Patterns, problems and the future. Can J Zool 68:203-220.
16. Bravo SA, Sallenave A (2003) Foraging behavior and activity patterns of Alouatta caraya in northeastern Argentinean flooded forest. Int J Primatol 24:8525-8846.
17. Brockett RC, Horwich RH, Jones CB (2000) Reproductive seasonality in the Belizean black howling monkey (Alouatta pigra). Neotrop Primates 8:136-138.
18. Chapman CA (1987) Flexibility in diets of three Costa Rican primates. Folia Primatol 49:90-105.
19. Chapman CA (1988) Patterns of foraging and range use by three species of Neotropical primates. Primates 29:177-194.
20. Chapman CA, Balcomb SR (1998) Population characteristics of howlers: Ecological conditions or group history. Int J Primatol 19:385-403.
21. Chapman CA, Chapman LJ (1999) Implications of small scale variation in ecological conditions for the diet and density of red colobus monkeys. Primates 40:215-231.
22. Chapman CA, Chapman LJ, Bjorndal K, Onderdonk DA (2002) Application of protein-to-fiber ratios to predict colobine abundance on different spatial scales. Int J Primatol 23:283-310.
23. Chapman CA, Chapman LJ, Naughton-Treves L, Lawes MJ, McDowell LR (2004) Predicting folivore abundances: Black-and-white colobus and other primates in forest fragments of Western Uganda. Am J Primatol 62:55-69.
24. Chapman CA, Wasserman MD, Gillespie TR, Speirs ML, Lawes MJ, Saj TL, Ziegler TE (2006) Do food availability, parasitism and stress have synergistic effects on red colobus populations living in forest fragments. Am J Phys Anthropol 131:525-534.
25. Chiarello AG (1994) Diet of the brown howler monkey Alouatta fusca in a semi-deciduous forest fragment of southeastern Brazil. Primates 35:25-34.
26. Clarke M (1983) Infant-killing and infant disappearance following male takeovers in a group of free-ranging howling monkeys (Alouatta palliata) in Costa Rica. Am J Primatol 5:241-247.
27. Clarke MR, Glander KE (1984) Female reproductive success in a group of free-ranging howling monkeys (Alouatta palliata) in Costa Rica. In: Small MF (ed) Female primates: Studies by women primatologists. Alan R. Liss, New York.
28. Creel S, Fox JE, Hardy A, Sands J, Garrott B, Peterson RO (2002) Snowmobile activity and glucocorticoid stress responses in wolves and elk. Conserv Biol 16:809-814.
29. Cristobal-Azkarate J, Arroyo-Rodriguez V (2007) Diet and activity of howler monkeys (Alouatta palliata) in Los Tuxlas, Mexico: Effects of habitat fragmentation and implications for conservations. Am J Primatol 69:1013-1029.
30. Crockett CM (1987) Diet, dimorphism and demography: Perspectives from howlers to hominids. In: Kinzey WG (ed) The evolution of human behaviour: Primate models. State University of New York Press, Albany.
31. Crockett CM, Rudran R (1987) Red howler monkey birth data I: Seasonal variation. Am J Primatol 13:347-368.
32. DaSilva GL (1992) The western black-and-white colobus as a low energy strategist: Activity budgets, energy expenditure and energy intake. J Anim Ecol 61:79-91.
33. Davies AG (1994) Colobine populations. In: Davies AG, Oates JF (eds) Colobine monkeys: Their ecology, evolution and behaviour. Cambridge University Press, Cambridge.
34. de Souza LL, Ferrari SF, da Costa ML, Kern DC (2002) Geophagy as a correlate of folivory in red-handed howler monkeys (Alouatta belzebul) from Eastern Brazilian Amazonia. J Chem Ecol 28:1613-1621.
35. Degama-Blanchet HN, Fedigan LM (2006) The effects of forest fragment age, isolation, size, habitat type and water availability on monkey density in a tropical dry forest. In: Estrada A, Garber PA, Pavelka MSM, Luecke L (eds) New perspectives in the study of Mesoamerican primates. Developments in primatology: Progress and prospects. Springer, New York.
36. Dias PAD, Rangel-Negrin A, Canales-Espinosa D (2011) Effects of lactation on the time-budgets and foraging patterns of female black howlers (Alouatta pigra). Am J Phys Anthropol 145:137-146.
37. DiBitetti MS, Janson CH (2000) When will the stork arrive? Patterns of birth seasonality in neo-tropical primates. Am J Primatol 50:109-130.
38. Dunn JC, Asensio N, Arroyo-Rodriguez V, Schnitzer S, Cristobal-Azkarate J (2009) The ranging costs of a fallback food: Liana consumption supplements diet but increases foraging effort in howler monkeys. Biotropica 43:612-618.
39. Dunn JC, Cristobal-Azkarate J, Vea JJ (2010) Seasonal variations in the diet and feeding effort of two groups of howlers in different sized forest fragments. Int J Primatol 31:887-903.
40. Estrada AR (1982) Survey and census of howler monkeys (Alouatta palliata) in the rainforest "Lox Tuxlas" Veracruz, Mexico. Am J Primatol 2:363-372.
41. Estrada A (1984) Resource use by howler monkeys (Alouatta palliata) in the rain forest of Los Tuxlas, Veracruz, Mexico. Int J Primatol 5:105-131.
42. Estrada A, Coates-Estrada R (1993) Aspects of ecological impact of howling monkeys (Alouatta palliata) on their habitat: A review. In: Estrada A, Rodriguez-Luna E, Lopez-Wilchis R, Coates-Estrada R (eds) Avances en studio primatologicos en Mexico. Patronatto Pro-Universitdad Veracruzana, Veracruz.
43. Estrada A, Anzures A, Coates-Estrada R (1999) Tropical rain forest fragmentation, howler monkeys (Alouatta palliata), and dung beetles at Los Tuxlas, Mexico. Am J Primatol 48:253-262.
44. Fashing PJ, Diernfeld ES, Mowry CB (2007) Influence of plant and soil chemistry on food selection, ranging patterns, and biomass of Colobus guereza in Kakamega Forest, Kenya. Int J Primatol 28:673-703.
45. Fedigan LM, Rose LM (1995) Interbirth interval variation in three sympatric species of neotropical primates. Am J Primatol 37:9-24.
46. Felton AM, Felton A, Raubenheimer D, Foley WJ (2009) Nutritional goals of wild primates. Funct Ecol 23:70-78.
47. Filipovic D, Gavrilovic L, Dronjak S, Radojcic MB (2007) The effect of repeated physical exercise on hippocampus and brain cortex in stressed rats. Ann NY Acad Sci 1096:207-219.
48. 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.
49. Ganas J, Ortmann S, Robbins MM (2009) Food choices of the mountain gorilla in Bwindi Impenetrable National Park, Uganda: The influence of nutrients, phenolics and availability. J Trop Ecol 25:125-134.
50. Garber PA, Righini R, Kowalewski MM (2014) Evidence of alternative dietary syndromes and nutritional goals in the Genus Alouatta. In: Kowalewski M, Garber P, Cortés-Ortiz L, Urbani B, Youlatos D (eds) Howler monkeys: Behavior, ecology and conservation. Springer, New York.
51. Gaulin S, Gaulin CK (1982) Behavioral ecology of Alouatta seniculus in Andean Cloud Forest. Int J Primatol 3:1-32.
52. Gesquiere LR, Onyango PO, Alberts SC, Altmann J (2011) Endocrinology of year-round reproduction in a highly seasonal habitat: Environmental variability in testosterone and glucocorticoids in baboon males. Am J Phys Anthropol 144:169-176.
53. Glander K (1980) Reproduction and population growth in free-ranging mantled howling monkeys. Am J Phys Anthropol 53:25-36.
54. Glander K (1981) Feeding patterns in mantled howler monkeys. In: Kamil AC, Sargent TD (eds) Foraging behavior. Garland Press, New York.
55. Glander K (1982) The impact of plant secondary compounds on primate feeding behavior. Am J Phys Anth 25:1-18.
56. Grant GS, Craig P, Trail P (1997) Cyclone-induced shift in foraging behavior in flying foxes in American Samoa. Biotropica 29:224-228.
57. Hack M, Flannery D, Schluchter M, Cartar L, Borawski E, Klein N (2002) Outcomes in young adulthood for very low birth weight infants. New Engl J Med 346:149-157.
58. Hau M (2001) Timing of breeding in variable environments: Tropical birds as model systems. Horm Behav 40:281-290.
59. Homan RN, Regosin JV, Rodrigues DM, Reed JM, Windmiller BS, Romero LM (2003) Impacts of varying habitat quality on the physiological stress of spotted salamanders (Ambystoma maculatum). Anim Conserv 6:11-18.
60. Juan S, Estrada A, Coates-Estrada R (2000) Contrastes y similitudes en el uso de recursos y patron general de actividades en tropas de monos aulladores (Alouatta palliata) en fragmentos de selva de Los Tuxlas, Mexico. Neotrop Primates 8:131-135.
61. Julliot C (1996) Fruit choice by red howler monkeys (Alouatta seniculus) in a tropical rain forest. Am J Primatol 40:261-282.
62. Julliot C, Sabatier D (1993) Diet of the red howler monkey (Alouatta seniculus) in French Guiana. Int J Primatol 14:527-550.
63. Kowalewski M, Zunino GE (2004) Birth seasonality in Alouatta caraya in northern Argentina. Int J Primatol 25:383-400.
64. Kramer MS, Platt R, Yang H, Joseph KS, Wen SW, Morin L, Usher R (1998) Secular trends in pre-term birth: A hospital based cohort study. JAMA 280:1849-1857.
65. Krebs CJ (1978) A review of the chitty hypothesis of population regulation. Can J Zool 56:2463-2480.
66. Lopez GO, Terborgh J, Ceballos N (2005) Food selection by a hyperdense population of red howler monkeys (Alouatta seniculus). J Trop Ecol 21:445-450.
67. Lynn SE, Breuner CW, Wingfield JC (2003) Short-term fasting affects locomotor activity, corticosterone, and corticosterone binding globulin in a migratory songbird. Horm Behav 43:150-157.
68. Martinez-Mota R, Valdespino C, Sanchez-Ramos MA, Serio-Silva JC (2007) Effects of forest fragmentation on the physiological stress response of black howler monkeys. Anim Conserv 10:374-379.
69. Martins MM (2009) Lianas as a food resource for brown howlers (Alouatta guariba) and southern muriquis (Brachyteles arachnoides) in a forest fragment. Anim Biodivers Conserv 32:51-58.
70. Milton K (1979) Factors influencing leaf choice by howler monkeys: A test of some hypotheses of food selection by generalist herbivores. Am Nat 114:362-378.
71. Milton K (1980) The foraging strategy of howler monkeys: A study in primate economics. Columbia University Press, New York.
72. Milton K (1981) Food choices and digestive strategies of two sympatric species. Am Nat 117:496-505.
73. Milton K (1982) Dietary quality and demographic regulation in a howler monkey population. In: Leigh EG, Rand AS, Windsor DM (eds) The ecology of a tropical forest. Smithsonian Institution Press, Washington, DC.
74. Milton K (1998) Physiological ecology of howlers (Alouatta): Energetic and digestive considerations and comparison with the Colobinae. Int J Primatol 19:513-548.
75. Milton K, McBee RH (1983) Rates of fermentative digestion in the howler monkey, Alouatta palliata (Primates, Ceboidea). Comp Biochem Physiol 74:29-31.
76. Moscovice LR, Issa MH, Petrzelkoca KJ, Keuler NS, Snowdon CT, Huffman MA (2007) Fruit availability, chimpanzee diet, and grouping patterns on Rubondo Island, Tanzania. Am J Primatol 69:487-502.
77. Nicholson AJ (1933) The balance of animal populations. J Anim Ecol 2:132-178.
78. Oates JF, Whitesides GH, Davies AG, Waterman PG, Green SM, Dasilva GL, Mole S (1990) Determinants of variation in tropical forest biomass: New evidence from West Africa. Ecology 71:328-343.
79. Palacios E, Rodriguez A (2001) Ranging pattern and use of space in a group of red howler monkeys (Alouatta seniculus) in a southeastern Colombian rainforest. Am J Primatol 55:233-251.
80. Pave R, Kowalewski MM, Garber PA, Zunino GE, Fernandez VA, Peker SM (2012) Infant mortality in black-and-gold howlers (Alouatta caraya) living in a flooded forest in Northeastern Argentina. Int J Primatol 33:937-957.
81. Pavelka MSM, Behie AM (2005) The effect of a hurricane on the food supply of black howlers (Alouatta pigra) in Southern Belize. Biotropica 37:102-108.
82. Pavelka MSM, Knopff KH (2004) Diet and activity in black howler monkeys (Alouatta pigra) in southern Belize: Does degree of frugivory influence activity level. Primates 45:105-111.
83. Pavelka MSM, Brusselers OT, Nowak D, Behie A (2003) Population reduction and social disorganization in Alouatta pigra following a hurricane. Int J Primatol 24:1037-1055.
84. Pavelka MSM, McGoogan KC, Steffens TS (2007) Population size and characteristics of Alouatta pigra before and after a major hurricane. Int J Primatol 28:919-929.
85. Pinto LP, Setz EZF (2004) Diet of Alouatta belzebul discolor in an Amazonian rainforest of northern Mato Grosso State, Brazil. Int J Primatol 25:1197-1211.
86. Pinto ACB, Azevedo-Ramos C, de Carvalho O Jr (2003) Activity patterns and diet of the howler monkey Alouatta belzebul in areas of logged and unlogged forest in Eastern Amazonia. Anim Biodiv Conserv 26:39-49.
87. Poppit SD, Speakman JR, Racey PA (1994) Energetics of reproduction in the lesser hedgehod Tenrec, Echinops telfairi (Martin). Physiol Zool 67:967-994.
88. Prates HM, Bicca-Marques JC (2008) Age-sex analysis of activity budget, diet and positional behavior in Alouatta caraya in an Orchard Forest. Int J Primatol 29:703-715.
89. Roberts NS, Copel JA, Bhutani V, Otis C, Gluckman S (1985) Intestinal parasites and other infections during pregnancy in Southeast Asian refugees. J Reprod Med 30:720-725.
90. Rodriguez-Luna E, Dominguez-Dominguez LE, Morales MJ, Martinez-Morales M (2003) Foraging strategy changes in Alouatta palliata mexicana troop released on an island. In: Marsh LK (ed) Primates in fragments: Ecology and conservation. Kluwer, New York.
91. Saltzman W, Schultz-Darken NJ, Wegner FH, Wittwer DJ, Abbott DH (1998) Suppression of cortisol levels in sub-ordinate female marmosets: Reproductive and social contributions. Horm Behav 33:58-74.
92. Sapolsky RM (1986) Endocrine and behavioral correlates of drought in wild olive baboons (Papio anubis). Am J Primatol 11:217-227.
93. Sapolsky RM (1992) Neuroendocrinology of the stress-response. In: Becker JB, Breedlove SM, Crews D (eds) Behavioural endocrinology. MIT Press, Cambridge.
94. Serio-Silva JC, Rico-Gray V, Hernandez-Salazar LT, Espinosa-Gomez R (2002) The role of Ficus (Moraceae) in the diet and nutrition of a troop of Mexican howler monkeys, Alouatta palliata mexicana, released on an island in southern Veracruz, Mexico. J Trop Ecol 18:913-928.
95. Shedden-Gonzalez A, Rodriguez-Luna E (2010) Responses of a translocated howler monkey Alouatta palliata group to new environmental conditions. Endanger Species Res 12:25-30.
96. Silanikove N, Shamay A, Sinder D, Moran A (2000) Stress down regulates milk yield in cows by plasmin induced ß-casein production that blocks K + channels on the apical membranes. Life Sci 67:2201-2212.
97. Silver SC, Marsh LK (2003) Dietary flexibility, behavioural plasticity, and survival in fragments: Lessons from translocated howlers. In: Marsh LK (ed) Primates in fragments: Ecology and conservation. Kluwer, New York.
98. Silver SC, Ostro LET, Young CP, Horwich R (1998) Feeding ecology of the black howler monkeys (Alouatta pigra) in Northern Belize. Am J Primatol 45:263-279.
99. Snaith TV, Chapman CA (2008) Red colobus monkeys display alternative behavioural responses to the costs of scramble competition. Behav Ecol 19:1289-1296.
100. Stanford CB (1991) The diet of the capped langur (Presbytis pileata) in a moist deciduous forest in Bangladesh. Int J Primatol 12:199-216.
101. Stevens CE (1988) Comparative Physiology of the vertebrate digestive system. Cambridge University Press, Cambridge.
102. Stoner KE (1996) Habitat selection and seasonal patterns of activity and foraging of mantled howling monkeys (Alouatta palliata) in northeastern Costa Rica. Int J Primatol 17:1-30.
103. Strier KB, Mendes SL, Santos RR (2001) Timing of births in sympatric brown howler monkeys (Alouatta fusca clamitans) and northern muriquis (Brachyteles arachnoids hypoxanthus). Am J Primatol 55:87-100.
104. Wasserman MB, Chapman CA (2003) Determinants of colobine monkey abundance: The importance of food energy, protein and fiber content. J Anim Ecol 72:650-659.
105. Waterman PG, Ross JAM, Bennett EL, Davies AG (1988) A comparison of the floristics and leaf chemistry on populations of colobine monkeys in the Old World. Biol J Linnean Soc 34:1-32.
106. Williams-Guillen K (2003) The behavioral ecology of mantled howling monkeys (Alouatta palliata) living in a Nicaraguan shade coffee plantation. PhD dissertation. New York University, New York.
107. Ziegler TE, Scheffler G, Snowdon CT (1995) The relationship of cortisol levels to social environment and reproductive functioning in female cotton top tamarins, Saguinus Oedipus. Horm Behav 29:407-424.
108. Zunino GE, Gonzalez V, Kowalewski MM, Bravo SP (2001) Alouatta caraya. Relations among hábitat, density and social organization. Primate Report 61:37-46.