The relative impact of forest patch and landscape attributes on black howler monkey populations in the fragmented Lacandona rainforest, Mexico

Landscape Ecology

Volumn 28, Issue 9, 2013, Pages 1717-1727

  Arroyo Rodríguez, Víctor ^a   González Perez, Iraida M ^a   Garmendia, Adriana ^a   Solà, Mireia ^b   Estrada, Alejandro ^c  

^a INSTITUTO DE INVESTIGACIONES EN ECOSISTEMAS Y SUSTENTABILIDAD   (Mexico)

^b UNIVERSITAT AUTÒNOMA DE BARCELONA   (Spain)

^c UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO   (Mexico)

Author keywords

Alouatta pigra; Habitat fragmentation; Habitat loss; Matrix quality; Population status; Primates

Indexed keywords

FOREST COVER; HABITAT; HABITAT CONSERVATION; HABITAT FRAGMENTATION; HABITAT LOSS; LANDSCAPE; MATRIX; PATCH SIZE; PERMEABILITY; PRIMATE; RAINFOREST; SURVIVAL;

CHIAPAS; LACANDON FOREST; MEXICO [NORTH AMERICA];

EID: 84887872915     PISSN: 09212973     EISSN: 15729761     Source Type: Journal    
DOI: 10.1007/s10980-013-9929-2     Document Type: Article

References (74)

1. Alexander SM, Pavelka MSM, Bywater NH (2006) Quantifying fragmentation of black howler (Alouatta pigra) habitat after hurricane Iris (2001), Southern Belize. In: Estrada A, Garber PA, Pavelka M, Luecke L (eds) New Perspectives in the study of Mesoamerican primates. Springer, Chicago, pp 539-560.
2. Anzures-Dadda A, Manson RH (2007) Patch and landscape scale effects on howler monkey distribution and abundance in rainforest fragments. Anim Conserv 10: 66-77.
3. Arriaga L, Espinoza JM, Aguilar C, Martínez E, Gómez L, Loa E (2000) Lacandona. In: Regiones Terrestres Prioritarias de México. Comisión Nacional para el Conocimiento y Uso de la Biodiversidad, Mexico city, pp 537-540.
4. Arroyo-Rodríguez V, Dias PAD (2009) Effects of habitat fragmentation and disturbance on howler monkeys: a review. Am J Primatol 71: 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, Mandujano S (2009) Conceptualization and measurement of rainforest fragmentation from the primates' perspective. Int J Primatol 30: 497-514.
7. Arroyo-Rodríguez V, Mandujano S, Benítez-Malvido J, Cuende-Fantón C (2007) The influence of large tree density on howler monkey (Alouatta palliata mexicana) presence in very small rainforest fragments. Biotropica 39: 760-766.
8. Arroyo-Rodríguez V, Cuesta-del Moral E, Mandujano S, Chapman CA, Reyna-Hurtado R, Fahrig L (2013) Assessing habitat fragmentation effects for primates: the importance of evaluating questions at the correct scale. In: Marsh L, Chapman CA (eds) Primates in Fragments II. Kluwer Academic, London (in press).
9. Arroyo-Rodríguez V, Andresen E, Bravo SP, Stevenson PR (in press) Seed dispersal by howler monkeys: current knowledge, conservation implications and future directions. In: Kowalewski M, Garber PA, Cortés-Ortiz L, Urbani B, Youlatos D (eds) Howler monkeys: examining the biology, adaptive radiation, and behavioral ecology of the most widely distributed genus of Neotropical primate. Springer developments in primatology: progress and prospects book series. Chicago.
10. Asensio N, Arroyo-Rodríguez V, Dunn J, Cristóbal-Azkarate J (2009) Conservation value of landscape supplementation for howler monkeys living in forest patches. Biotropica 41: 768-773.
11. Bicca-Marquez JC (2003) How do howler monkeys cope with habitat fragmentation? In: Marsh LK (ed) Primates in fragments: ecology and conservation. Kluwer Academic/Plenum Publishers, New York, pp 283-303.
12. Burnham KP, Anderson DR (2002) Model selection and multi-model inference: a practical information-theoretic approach. Springer-Verlag, New York.
13. Camara G, Souza RCM, Freitas UM, Garrido J (1996) Spring: integrating remote sensing and GIS by object-oriented data modelling. Comput Gr 20: 395-403.
14. Castellón TD, Sieving KE (2006) An experimental test of matrix permeability and corridor use by an endemic understory bird. Conserv Biol 20: 135-145.
15. Chapman CA, Peres CA (2001) Primate conservation in the new millennium: the role of scientists. Evol Anthropol 10: 16-33.
16. Chazdon RL, Harvey CA, Komar O, Griffith DM, Ferguson BG, Martínez-Ramos M, Morales H, Nigh R, Soto-Pinto L, van Breugel M, Philpott SM (2011) Beyond reserves: a research agenda for conserving biodiversity in human-modified tropical landscapes. Biotropica 41: 142-153.
17. Chiarello AG (2003) Primates of the Brazilian Atlantic forest: the influence of forest fragmentation on survival. In: Marsh LK (ed) Primates in fragments: ecology and conservation. Kluwer Academic/Plenium Publishers, New York, pp 99-121.
18. Cowlishaw G (1999) Predicting the pattern of decline of African primate diversity: an extinction debt from historical deforestation. Conserv Biol 13: 1183-1193.
19. Crawley MJ (2002) Statistical computing: an introduction to data analysis using S-Plus. John Wiley & Sons, London.
20. Cristóbal-Azkarate J, Vea J, Asensio N, Rodríguez-Luna E (2005) Biogeographical and floristic predictors of the presence and abundance of mantled howlers (Alouatta palliata mexicana) in rainforest fragments at Los Tuxtlas, Mexico. Am J Primatol 67: 209-222.
21. Cristóbal-Azkarate J, Chavira R, Boeck L, Rodríguez-Luna E, Vèa J (2007) Glucocorticoid levels in free ranging resident mantled howlers: a study of coping strategies. Am J Primatol 69: 866-876.
22. Dirzo R (1994) Diversidad de la flora mexicana. Agrupación Sierra Madre, Mexico city.
23. Dirzo R, Raven PH (2003) Global state of biodiversity and loss. Annu Rev Env Resour 28: 137-167.
24. Dunning JB, Danielson BJ, Pulliam R (1992) Ecological processes that affect populations in complex landscapes. Oikos 65: 169-175.
25. Estrada A, Coates-Estrada R (1996) Tropical rain forest fragmentation and wild populations of primates at Los Tuxtlas, Mexico. Int J Primatol 17: 759-783.
26. Estrada A, Mendoza A, Castellanos L, Pacheco R, van Belle S, García Y, Muñoz D (2002) Population of the black howler monkey (Alouatta pigra) in a fragmented landscape in Palenque, Chiapas, Mexico. Am J Primatol 58: 45-55.
27. Estrada A, Garber PA, Pavelka M, Luecke L (eds) (2006) New perspectives in the study of Mesoamerican primates. Springer, Chicago.
28. Estrada A, Raboy BE, Oliveira LC (2012) Agroecosystems and primate conservation in the tropics: a review. Am J Primatol 74: 696-711.
29. Ethier K, Fahrig L (2011) Positive effects of forest fragmentation, independent of forest amount, on bat abundance in eastern Ontario, Canada. Landscape Ecol 26: 865-876.
30. Ewers RM, Didham RK (2006) Confounding factors in the detection of species responses to habitat fragmentation. Biol Rev 81: 117-142.
31. Fahrig L (1999) Forest loss and fragmentation: which has the greater effect on persistence of forest-dwelling animals? In: Rochelle JA, Lehmann LA, Wisniewski J (eds) Forest fragmentation; wildlife and management implications. Leiden, The Netherlands, pp 87-95.
32. Fahrig L (2003) Effects of habitat fragmentation on biodiversity. Annu Rev Ecol Evol Syst 34: 487-515.
33. FAO (2011) State of the World's forests 2011. Food and Agriculture Organization of the United Nations, Rome.
34. Fischer J, Lindenmayer DB (2007) Landscape modification and habitat fragmentation: a synthesis. Global Ecol Biogeogr 16: 265-280.
35. Forman RTT, Godron M (1986) Landscape ecology. John Wiley & Sons, New York.
36. Gardner TA, Barlow J, Chazdon R, Ewers RM, Harvey CA, Peres CA, Sodhi NS (2009) Prospects for tropical forest biodiversity in a human-modified world. Ecol Lett 12: 561-582.
37. Gavazzi AJ, Cornick LA, Markowitz TM, Green D, Markowitz H (2008) Density, distribution, and home range of the black howler monkey (Alouatta pigra) at Lamanai, Belize. J Mammal 89: 1105-1112.
38. Goodenough AE, Hart AG, Stafford R (2012) Regression with empirical variable selection: description of a new method and application to ecological datasets. PLoS One 7(3): e34338.
39. GRASS Development Team (2011) Geographic Resources Analysis Support System (GRASS) Software. Springer, New York.
40. Hanski I (1999) Metapopulation ecology. Oxford University Press, New York.
41. Harcourt AH, Doherty DA (2005) Species-area relationships of primates in tropical forest fragments: a global analysis. J Appl Ecol 42: 630-637.
42. Kowalewski MM, Zunino GE (1999) Impact of deforestation on a population of Alouatta caraya in northern Argentina. Folia Primatol 70: 163-166.
43. Laurance WF, Laurance SG, Hilbert DW (2008) Long-term dynamics of a fragmented rainforest mammal assemblage. Conserv Biol 22: 1154-1164.
44. Lindenmayer DB, Fischer J (2007) Tackling the habitat fragmentation panchreston. Trends Ecol Evol 22: 127-132.
45. Lovejoy TE, Bierregaard RO Jr, Rylands AB, Malcolm JR, Quintela CE, Harper LH, Brown KS, Powell AH, Schubart HOR, Hays MB (1986) Edge and other effects of isolation on Amazon forest fragments. In: Soulé ME (ed) Conservation biology. The science of scarcity and diversity, Sinauer Associates, pp 257-285.
46. Lumley T (2009) Package 'LEAPS': Regression subset selection. Available: cran. r-project. org/web/packages/leaps/leaps. pdf. Accessed 05 Feb 2013.
47. Marsh LK, Cuarón AD, Cortés-Ortiz L, Shedden A, Rodríguez-Luna E, de Grammont PC (2008) Alouatta pigra. In: IUCN 2012. IUCN Red List of Threatened Species. Version 2012. 1. www. iucnredlist. org. Accessed 02 July 2012.
48. 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.
49. Mcgarigal K, Cushman SA (2002) Comparative evaluation of experimental approaches to the study of habitat fragmentation. Ecol Appl 12: 335-345.
50. Metzger JP, Martensen AC, Dixo M, Bernacci LC, Ribeiro MC, Teixeira AMG, Pardini R (2009) Time-lag in biological responses to landscape changes in a highly dynamic Atlantic forest region. Biol Conserv 142: 1166-1177.
51. Mora F (2008) Caracterización de la cobertura forestal en el Corredor Biológico Mesoamericano-México: patrones espaciales en la pérdida y fragmentación de bosques. In: Importancia del capital ecológico de la región del Corredor Biológico Mesoamericano-México. Centro de Investigación en Geografía y Geomática & CONABIO, Mexico city, pp 55-83.
52. Neter J, Wasserman W, Kutner MH (1990) Applied linear statistical models. Irwin, Chicago.
53. Neville MK, Glander KE, Braza F, Rylands AB (1988) The howling monkeys, genus Alouatta. In: Mittermeier RA, Rylands AB, Coimbra-Filho AF, da Fonseca GAB (eds) Ecology and behavior of neotropical primates, vol 2. World Wildlife Fund, Washington D. C., pp 349-453.
54. Ostro LET, Silver SC, Koontz FW, Young TP, Horwich RH (1999) Ranging behavior of translocated and established groups of black howler monkeys Alouatta pigra in Belize, Central America. Biol Conserv 87: 181-190.
55. Pardini R, Bueno AA, Gardner TA, Prado PI, Metzger JP (2010) Beyond the fragmentation threshold hypothesis: regime shifts in biodiversity across fragmented landscapes. PLoS One 5: e13666.
56. Peres CA (2001) Synergistic effects of subsistence hunting and habitat fragmentation on Amazonian forest vertebrates. Conserv Biol 15: 1490-1505.
57. Peres CA, Barlow J, Laurance WF (2006) Detecting anthropogenic disturbance in tropical forests. Trends Ecol Evol 21: 227-229.
58. Pozo-Montuy G, Serio-Silva JC (2007) Movement and resource use by a group of Alouatta pigra in a forest fragment in Balancán, Mexico. Primates 48: 102-107.
59. Pulliam HR (1988) Sources, sinks, and population regulation. Am Nat 132: 652-661.
60. 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 (eds) New Perspectives in the study of Mesoamerican primates. Springer, Chicago, pp 189-211.
61. Rosales-Meda M, Estrada A, López JE (2007) Demographic survey of black howler monkey (Alouatta pigra) in the Lachuá Eco-region in Alta Verapaz, Guatemala. Am J Primatol 70: 231-237.
62. Rylands AB, Groves CP, Mittermeier RA, Cortés-Ortíz L, Hines JH (2006) Taxonomy and distribution of Mesoamerican primates. In: Estrada A, Garber PA, Pavelka M, Luecke L (eds) New Perspectives in the study of Mesoamerican primates. Springer, Chicago, pp 29-79.
63. Smith AC, Koper N, Francis CM, Fahrig L (2009) Confronting collinearity: comparing methods for disentangling the effects of habitat loss and fragmentation. Landscape Ecol 24: 1271-1285.
64. Smith AC, Fahrig L, Francis CM (2011) Landscape size affects the relative importance of habitat amount, habitat fragmentation, and matrix quality on forest birds. Ecography 34: 103-113.
65. Sutherland WJ, Pullin AS, Dolman PM, Knight TM (2004) The need for evidence-based conservation. Trends Ecol Evol 19: 305-308.
66. Terborgh J, López L, Nuñez P, Rao M, Shahabuddin G, Orihuela G, Riveros M, Ascanio R, Adler GH, Lambert TD, Balbas L (2001) Ecological meltdown in predator-free forest fragments. Science 294: 1923-1926.
67. Thornton DH, Branch LC, Sunquist ME (2011) The relative influence of habitat loss and fragmentation: do tropical mammals meet the temperate paradigm? Ecol Appl 21: 2324-2333.
68. Trejo-Macías G, Estrada A (2012) Risk factors connected to gastrointestinal parasites in mantled (Alouatta palliata mexicana) and black howler monkeys (Alouatta pigra) living in continuous and in fragmented rainforests in Mexico. Current Zool 58: 375-383.
69. van Belle S, Estrada A (2006) Demographic features of Alouatta pigra populations in extensive and fragmented forests. In: Estrada A, Garber PA, Pavelka M, Luecke L (eds) New Perspectives in the study of Mesoamerican primates. Springer, Chicago, pp 121-142.
70. Villard MA, Trzcinski MK, Merriam G (1999) Fragmentation effects on forest birds: relative influence of woodland cover and configuration on landscape occupancy. Conserv Biol 13: 774-783.
71. Wahungu GM, Muoria PK, Moinde NN, Oguge NO, Kirathe JN (2005) Changes in forest fragment sizes and primate population trends along the River Tana floodplain, Kenya. Afr J Ecol 43: 81-90.
72. Watts ES, Rico-Gray V, Chan C (1986) Monkeys in the Yucatan peninsula, Mexico: preliminary survey of their distribution and status. Primate Conserv 7: 17-22.
73. Wieczkowski J (2004) Ecological correlates of abundance in the Tana Mangabey (Cercocebus galeritus). Am J Primatol 63: 125-138.
74. Zunino GE, Kowalewski MM, Oklander LI, González V (2007) Habitat fragmentation and population size of the black and gold howler monkey (Alouatta caraya) in a semideciduous forest in northern Argentina. Am J Primatol 69: 966-975.