Effects of logging, hunting, and forest fragment size on physiological stress levels of two sympatric ateline primates in Colombia

Conservation Physiology

Volumn 1, Issue 1, 2013, Pages

  Rimbach, Rebecca ^a,b   Link, Andrés ^b,c   Heistermann, Michael ^a   Gómez Posada, Carolina ^d   Galvis, Nelson ^b,c   Heymann, Eckhard W ^a  

^a GERMAN PRIMATE CENTER   (Germany)

^b Fundacion Proyecto Primates   (Colombia)

^c UNIVERSIDAD DE LOS ANDES   (Colombia)

^d UNIVERSITY OF WASHINGTON   (United States)

Author keywords

Alouatta seniculus; Ateles hybridus; Faecal glucocorticoid metabolites; Habitat fragmentation; Hunting; Logging

Indexed keywords

EID: 84983509321     PISSN: None     EISSN: 20511434     Source Type: Journal    
DOI: 10.1093/conphys/cot031     Document Type: Article

References (104)

1. Aguilar-Melo AR, Andresen E, Cristóbal-Azkarate J, Arroyo-Rodríguez V, Chavira R, Schondube J, Serio-Silva JC, Cuarón AD (2013) Behavioral and physiological responses to subgroup size and number of people in howler monkeys inhabiting a forest fragment used for naturebased tourism. Am J Primatol 75: 1108-1116.
2. Aldana AM, Beltrán M, Torres-Neira J, Stevenson PR (2008) Habitat characterization and population density of brown spider monkeys (Ateles hybridus) in Magdalena Valley, Colombia. Neotrop Primates 15: 46-50.
3. Arroyo-Rodríguez V, Mandujano S (2006) Forest fragmentation modifies habitat quality for Alouatta palliata. Int J Primatol 27: 1079-1096.
4. Baayen RH (2010) Analyzing Linguistic Data: A Practical Introduction to Statistics. Cambridge University Press, Cambridge, UK.
5. Baayen RH (2011) language R: data sets and functions with "Analyzing linguistic data: a practical introduction to statistics", R package version 1.4. http://cran.r-project.org/package=languageR
6. 1.4. http://cran.r-project.org/package=languageR Barja I, Silván G, Rosellinic S, Piñeiroc A, González-Gilb A, Camachob L, Illera JC (2007) Stress physiological responses to tourist pressure in a wild population of European pine marten. J Steroid Biochem Mol Biol 104: 136-142.
7. Bates D, Maechler M (2010) lme4: Linear mixed-effects models using S4 classes. http://cran.r-project.org/package=lme4
8. Bateson P, Bradshaw EL (1997) Physiological effects of hunting red deer (Cervus elaphus). Proc Biol Sci 264: 1707-1714.
9. Behie AM, Pavelka MSM, Chapman CA (2010) Sources of variation in fecal cortisol levels in howler monkeys in Belize. Am J Primatol 72: 600-606.
10. Bernstein I, Balcaen P, Dresdale L, Gouzoules H, Kavanagh M, Patterson T, Neyman-Warner P (1976) Differential effects of forest degradation on primate populations. Primates 17: 401-411.
11. Bicca-Marques JC (2003) How do howler monkeys cope with habitat fragmentation?. In LK Marsh, ed., Primates in Fragments: Ecology and Conservation. Kluwer Academic/Plenum Publishers, New York, pp 283-303.
12. Blumstein DT, Fernández-Juricic E, Zollner PA, Garity SC (2005) Interspecific variation in avian responses to human disturbance. J Appl Ecol 42: 943-953.
13. Boonstra R (2005) Equipped for life: the adaptive role of the stress axis in male mammals. J Mammal 86: 236-247.
14. Boonstra R (2013) Reality as the leading cause of stress: rethinking the impact of chronic stress in nature. Funct Ecol 27: 11-12.
15. Boubli J-P, Di Fiore A, Rylands AB, Mittermeier RA (2008) Alouatta seniculus. In: IUCN 2013. IUCN Red List of Threatened Species. Version 2013.1. http://www.iucnredlist.org. (last accessed 25 July 2013).
16. Breazile JE (1987) Physiologic basis and consequences of distress in animals. J Am Vet Med Assoc 191: 1212-1215.
17. Busch DS, Hayward LS (2009) Stress in a conservation context: a discussion of glucocorticoid actions and how levels change with conservation-relevant variables. Biol Conserv 142: 2844-2853.
18. Cardillo M, Mace GM, Jones KE, Bielby J, Bininda-Emonds ORP, Sechrest W, Orme CDL, Purvis A (2005) Multiple causes of high extinction risk in large mammal species. Science 309: 1239-1241.
19. Cavigelli SA (1999) Behavioural patterns associated with faecal cortisol levels in free-ranging female ring-tailed lemurs, Lemur catta. Anim Behav 57: 935-944.
20. Chapman CA, Saj TL, Snaith TV (2007) Temporal dynamics of nutrition, parasitism, and stress in colobus monkeys: implications for population regulation and conservation. Am J Phys Anthropol 134: 240-250.
21. Charbonnel N, Chaval Y, Berthier K, Deter J, Morand S, Palme R, Cosson JF (2008) Stress and demographic decline: a potential effect mediated by impairment of reproduction and immune function in cyclic vole populations. Physiol Biochem Zool 81: 63-73.
22. Cordeiro NJ, Howe HF (2001) Low recruitment of trees dispersed by animals in African forest fragments. Conserv Biol 15: 1733-1741.
23. Cosson JF, Ringuet S, Claessens O, de Massary JC, Dalecky A, Villiers JF, Granjon L, Pons JM (1999) Ecological changes in recent land-bridge islands in French Guiana, with emphasis on vertebrate communities. Biol Conserv 91: 213-222.
24. 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.
25. Crockett CM (1998) Conservation biology of the genus Alouatta. Int J Primatol 19: 549-578.
26. Cyr NE, Romero ML (2007) Chronic stress in free-living European starlings reduces corticosterone concentrations and reproductive success. Gen Comp Endocrinol 151: 82-89.
27. Di Fiore A, Campbell CJ (2007) The atelines: variation in ecology, behavior, and social organization. In CJ Campbell, A Fuentes, KC MacKinnon, M Panger, SK Bearder, eds, Primates in Perspective. Oxford University Press, New York, pp 155-185.
28. Di Fiore A, Link A, Campbell CJ (2010) The atelines: behavioral and socioecological diversity in a New World radiation. In CJ Campbell, A Fuentes, KC MacKinnon, M Panger, SK Beader, eds, Primates in Perspective, Ed 2. Oxford University Press, Oxford, pp 155-188.
29. Dunn JC, Cristóbal-Azkarate J, Veà 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.
30. Dunn JC, Cristóbal-Azkarate J, Schulte-Herbrüggen B, Chavira R, Veà JJ (2013) Travel time predicts fecal glucocorticoid levels in free-ranging howlers (Alouatta palliata). Int J Primatol 34: 246-259.
31. Ellenberg U, Mattern T, Seddon PJ, Luna Jorquera G (2006) Physiological and reproductive consequences of human disturbance in Humboldt Penguins: the need for species-specific visitor management. Biol Conserv 133: 95-106.
32. Ellenberg U, Setiawan AN, Cree A, Houston DM, Seddon PJ (2007) Elevated hormonal stress response and reduced reproductive output in Yellow-eyed Penguins exposed to unregulated tourism. Gen Comp Endocrinol 152: 54-63.
33. Fahrig L (2003) Effects of habitat fragmentation on biodiversity. Annu Rev Ecol Evol Syst 34: 487-515.
34. Field A (2005) Discovering Statistics using SPSS. Sage Publications, London.
35. Foley JA, Defries R, Asner GP, Barford C, Bonan G, Carpenter SR, Chapin FS, Coe MT, Daily GC, Gibbs HK et al. (2005) Global consequences of land use. Science 309: 570-574.
36. Fowler GS (1999) Behavioral and hormonal responses of Magellanic Penguins (Spheniscus magellanicus) to tourism and nest site visitation. Biol Conserv 90: 143-149.
37. Fox J, Weisberg S (2011) An R Companion to Applied Regression. Sage Publications, London.
38. French SS, Denardo DF, Greives TJ, Strand CR, Demas GE (2010) Human disturbance alters endocrine and immune responses in the Galapagos marine iguana (Amblyrhynchus cristatus). Horm Behav 58: 792-799.
39. Ganswindt A, Palme R, Heistermann M, Borragan S, Hodges JK (2003) Non-invasive assessment of adrenocortical function in the male African elephant (Loxodonta africana) and its relation to musth. Gen Comp Endocrinol 134: 156-166.
40. Ganzhorn JU (1995) Low-level forest disturbance effects on primary production, leaf chemistry, and lemur populations. Ecology 76: 2084-2096.
41. Gobush KS, Mutayoba BM, Wasser SK (2008) Long-term impacts of poaching on relatedness, stress physiology, and reproductive output of adult female African elephants. Conserv Biol 22: 1590-1599.
42. Gómez-Posada C, Roncancio N, Hincapie P, Betancourt A (2010) Densidad y composición de grupos en tres poblaciones de mono aullador rojo (Alouatta seniculus) en Valle y Cauca, Colombia. Boletín Científico del Centro de Museos, Universidad de Caldas 14: 79-91.
43. González-Solís J, Guix JC, Mateos E, Llorens L (2001) Population density of primates in a large fragment of the Brazilian Atlantic rainforest. Biodivers Conserv 10: 1267-1282.
44. Goymann W (2012) On the use of non-invasive hormone research in uncontrolled, natural environments: the problem with sex, diet, metabolic rate and the individual. Methods Ecol Evol 3: 757-765.
45. Hannah L, Carr JL, Lankerani A (1995) Human disturbance and natural habitat: a biome level analysis of a global data set. Biodivers Conserv 4: 128-155.
46. Harcourt AH, Coppeto SA, Parks SA (2002) Rarity, specialization and extinction in primates. J Biogeogr 29: 445-456.
47. Heistermann M, Ademmer C, Kaumanns W (2004) Ovarian cycle and effect of social changes on adrenal and ovarian function in Pygathrix nemaeus. Int J Primatol 25: 689-708.
48. Henle K, Davie KF, Kleyer M, Margules C, Settele J (2004) Predictors of species sensitivity to fragmentation. Biodivers Conserv 13: 207-251.
49. Hinam HL, St Clair CC (2008) High levels of habitat loss and fragmentation limit reproductive success by reducing home range size and provisioning rates of Northern Saw-whet Owls. Biol Conserv 141: 524-535.
50. 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.
51. Hunt KE, Wasser SK (2003) Effect of long-term preservation methods on fecal glucocorticoid concentrations of grizzly bear and African elephant. Physiol Biochem Zool 76: 918-928.
52. Irwin MT (2008) Diademed sifaka (Propithecus diadema) ranging and habitat use in continuous and fragmented forest: higher density but lower viability in fragments? Biotropica 40: 231-240.
53. IUCN (2012) The IUCN Red List of Threatened Species. Version 2012.2. http://www.iucnredlist.org (last accessed 5 December 2012).
54. Jaimez NA, Bribiescas RG, Aronsen GP, Anestis SA, Watts DP (2012) Urinary cortisol levels of gray-cheeked mangabeys are higher in disturbed compared to undisturbed forest areas in Kibale National Park, Uganda. Anim Conserv 15: 242-247.
55. Janin A, Léna J-P, Joly P (2011) Beyond occurrence: body condition and stress hormone as integrative indicators of habitat availability and fragmentation in the common toad. Biol Conserv 144: 1008-1016.
56. Johns AD (1988) Effects of "selective" timber extraction on rain forest structure and composition and some consequences for frugivores and folivores. Biotropica 20: 31-37.
57. Johns AD, Skorupa JP (1987) Responses of rain-forest primates to habitat disturbance: a review. Int J Primatol 8: 157-191.
58. Julliot C, Sabatier D (1993) Diet of the red howler monkey (Alouatta seniculus) in French Guiana. Int J Primatol 14: 527-550.
59. Keay JM, Singh J, Gaunt MC, Kaur T (2006) Fecal glucocorticoids and their metabolites as indicators of stress in various mammalian species: a literature review. J Zoo Wildl Med 37: 234-244.
60. Keselman HJ, Algina J, Kowalchuk RK (2001) The analysis of repeated measures designs: a review. Br J Math Stat Psychol 54: 1-20.
61. Klein LL, Klein DJ (1977) Feeding behaviour of the Colombian spider monkey, Ateles belzebuth. In TH Clutton-Brock, ed., Primate Ecology: Studies of Feeding and Ranging Behavior in Lemurs, Monkeys, and Apes. Academic Press, London, pp 153-181.
62. Landys MM, Ramenofsky M, Wingfield JC (2006) Actions of glucocorticoids at a seasonal baseline as compared to stress-related levels in the regulation of periodic life processes. Gen Comp Endocrinol 148: 132-149.
63. Link A, de Luna AG, Alfonso F, Giraldo-Beltran P, Ramirez F (2010) Initial effects of fragmentation on the density of three neotropical primate species in two lowland forests of Colombia. Endang Species Res 13: 41-50.
64. 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.
65. Lucas JR, Freeberg TM, Egbert J, Schwabl H (2006) Fecal corticosterone, body mass, and caching rates of Carolina chickadees (Poecile carolinensis) from disturbed and undisturbed sites. Horm Behav 49: 634-643.
66. Martínez-Mota R, Valdespino C, Sánchez-Ramos MA, Serio-Silva JC (2007) Effects of forest fragmentation on the physiological stress response of black howler monkeys. Anim Conserv 10: 374-379.
67. Menon S, Poirier FE (1996) Lion-tailed macaques (Macaca silenus) in a disturbed forest fragment: activity patterns and time budget. Int J Primatol 17: 969-985.
68. Michalski F, Peres CA (2005) Anthropogenic determinants of primate and carnivore local extinctions in a fragmented forest landscape of southern Amazonia. Biol Conserv 124: 383-396.
69. Millspaugh JJ, Washburn BE (2004) Use of fecal glucocorticoid metabolite measures in conservation biology research: considerations for application and interpretation. Gen Comp Endocrinol 138: 189-99.
70. Milton K (1980) The Foraging Strategy of Howler Monkeys: A Study of Primate Economics. Columbia University Press, New York.
71. Mittermeier RA, Rylands AB, Taylor LA, Chiozza F, Williamson EA, Wallis J, Schwitzer C (2012) Primates in Peril: The World's 25 Most Endangered Primates 2012-2014. IUCN/SSC Primate Specialist Group (PSG), International Primatological Society (IPS), Conservation International (CI), and Bristol Conservation and Science Foundation, Bristol, UK.
72. Monclús R, Rödel HG, Von Holst D, De Miguel J (2005) Behavioural and physiological responses of naïve European rabbits to predator odour. Anim Behav 70: 753-761.
73. Muehlenbein MP, Ancrenaz M, Sakong R, Ambu L, Prall S, Fuller G, Raghanti MA (2012) Ape conservation physiology: fecal glucocorticoid responses in wild Pongo pygmaeus morio following human visitation. PLoS One 7: e33357. doi:10.1371/journal.pone.0033357.
74. Muller MN, Wrangham RW (2004) Dominance, cortisol and stress in wild chimpanzees (Pan troglodytes schweinfurthii). Behav Ecol Sociobiol 55: 332-340.
75. Müllner A, Linsenmair EK, Wikelski M (2004) Exposure to ecotourism reduces survival and affects stress response in hoatzin chicks (Opisthocomus hoazin). Biol Conserv 118: 549-558.
76. Munshi-South J, Tchignoumba L, Brown J, Abbondanza N, Maldonado JE, Henderson A, Alonso A (2008) Physiological indicators of stress in African forest elephants (Loxodonta africana cyclotis) in relation to petroleum operations in Gabon, Central Africa. Divers Distrib 14: 995-1003.
77. Neville MK (1972) The population structure of red howler monkeys (Alouatta seniculus) in Trinidad and Venezuela. Folia Primatol 17: 56-86.
78. Ostro LET, Silver SC, Koontz FW, Horwich RH, Brockett R (2001) Shifts in social structure of black howler (Alouatta pigra) groups associated with natural and experimental variation in population density. Int J Primatol 22: 733-748.
79. Peres CA (2001) Synergistic effects of subsistence hunting and habitat fragmentation on Amazonian forest vertebrates. Conserv Biol 15: 1490-1505.
80. Pickering AD, Pottinger TG, Sumpter JP, Carragher JF, Le Bail PY (1991) Effects of acute and chronic stress on the levels of circulating growth hormone in the rainbow trout, Oncorhynchus mykiss. Gen Comp Endocrinol 83: 86-93.
81. Piñeiro A, Barja I, Silván G, Illera JC (2012) Effects of tourist pressure and reproduction on physiological stress response in wildcats: management implications for species conservation. Wildl Res 39: 532-539.
82. Purvis A, Gittleman JL, Cowlishaw G, Mace GM (2000) Predicting extinction risk in declining species. Proc Biol Sci 267: 1947-1952.
83. Putz FE, Leigh EGJ, Wright SJ (1990) Solitary confinement in Panama. Garden 2: 18-23.
84. R Development Core Team (2012) A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org
85. Rangel-Negrín A, Alfaro JL, Valdez RA, Romano MC, Serio-Silva JC (2009) Stress in Yucatan spider monkeys: effects of environmental conditions on fecal cortisol levels in wild and captive populations. Anim Conserv 12: 496-502.
86. Rimbach R, Heymann EW, Link A, Heistermann M (2013) Validation of an enzyme immunoassay for assessing adrenocortical activity and characterization of factors that affect fecal glucocorticoid metabolite levels in two New World primates. Gen Comp Endocrinol 191: 13-23.
87. Rumiz DI (1990) Alouatta caraya: population density and demography. Am J Primatol 21: 279-294.
88. Sapolsky RM, Romero ML, Munck AU (2000) How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions. Endocr Rev 21: 55-89.
89. Selye H (1956) The Stress of Life. McGraw-Hill, New York.
90. Setchell JM, Smith T, Wickings EJ, Knapp LA (2010) Stress, social behaviour, and secondary sexual traits in a male primate. Horm Behav 58: 720-728.
91. Shutt K, Setchell JM, Heistermann M (2012) Non-invasive monitoring of physiological stress in the Western lowland gorilla (Gorilla gorilla gorilla): validation of a fecal glucocorticoid assay and methods for practical application in the field. Gen Comp Endocrinol 179: 167-177.
92. Strasser EH, Heath JA (2013) Reproductive failure of a human-tolerant species, the American kestrel, is associated with stress and human disturbance. J Appl Ecol 50: 912-919.
93. Stratakis CA, Chrousos GP (1995) Neuroendocrinology and pathophysiology of the stress system. Ann N Y Acad Sci 77: 1-18.
94. Sumner J, Moritz C, Shine R (1999) Shrinking forest shrinks skink: morphological change in response to rainforest fragmentation in the prickly forest skink (Gnypetoscincus queenslandiae). Biol Conserv 91: 159-167.
95. Symington MM (1988) Food competition and foraging party size in the black spider monkey (Ateles paniscus chamek). Behaviour 105: 117-134.
96. Tecot SR (2008) Seasonality and predictability: the hormonal and behavioral responses of the red-bellied lemur, Eulemur rubriventer, in southeastern Madagascar. PhD thesis. University of Texas at Austin.
97. Thiel D, Palme R, Jenni L, Jenni-Eiermann S (2011) Winter tourism increases stress hormone levels in the Capercaillie Tetrao urogallus. Ibis 153: 122-133.
98. Umapathy G, Hussain S, Shivaji S (2011) Impact of habitat fragmentation on the demography of lion-tailed macaque (Macaca silenus) populations in the rainforest of Anamalai Hills, Western Ghats, India. Int J Primatol 32: 889-900.
99. Urbani B, Morales AL, Link A, Stevenson PR (2008) Ateles hybridus. In: IUCN 2013. IUCN Red List of Threatened Species. Version 2013.1. http://www.iucnredlist.org. (last accessed 25 July 2013).
100. von der Ohe CG, Wasser SK, Hunt KE, Servheen C (2004) Factors associated with fecal glucocorticoids in Alaskan brown bears (Ursus arctos horribilis). Physiol Biochem Zool 77: 313-320.
101. Wasser SK, Bevis K, King G, Hanson E (1997) Noninvasive physiological measures of disturbance in the Northern Spotted Owl. Conserv Biol 11: 1019-1022.
102. Wasser SK, Davenport B, Ramage ER, Hunt KE, Parker M, Clarke C, Stenhouse G (2004) Scat detection dogs in wildlife research and management: application to grizzly and black bears in the Yellowhead Ecosystem, Alberta, Canada. Can J Zool 82: 475-492.
103. Wingfield JC, Maney DL, Breuner CW, Jacobs JD, Lynn S, Ramenofsky M, Richardson RD (1998) Ecological bases of hormone-behavior interactions: the "emergency life history stage". Integr Comp Biol 38: 191-206.
104. Zwijacz-Kozica T, Selva N, Barja I, Silván G, Martínez-Fernández L, Illera JC, Jodlowski M (2012) Concentration of fecal cortisol metabolites in chamois in relation to tourist pressure in Tatra National Park (South Poland). Acta Theriol 58: 215-222.