While howlers are the most ecologically flexible of the atelines, they must still respond to issues arising from anthropogenic modifications, such as fragmentation or dietary changes. A group of Alouatta palliata living in a highly modified landscape (commensal group) at the Curú Wildlife Refuge in Costa Rica was compared to howlers with limited human influence (control group). The commensal group had a more frugivorous diet than the control group (H = 9.23, p = 0.002) due to crop-foraging of mango fruits. The commensal group maintained a larger home range than the control group, at 39 and 10 ha, respectively. The commensal group also had increased travel (H = 7.37, p = 0.007) and feeding (H = 7.34, p = 0.007) time, as well as reduced proximity to conspecifics (H = 44.77, p = 0.000). There were no significant differences in rates of either aggressive or affiliative social behaviours. The increased home range, shift in diet, increased travel and foraging time and reduced group cohesion demonstrated by these animals represent responses to the varied utility of available landscapes and the more widely dispersed resources in their range. These data contribute to our understanding of Alouatta, one of the most successful of Neotropical primates in modified landscapes.

Keywords:
Alouatta, Howler monkeys, Anthropogenic impacts, Dietary flexibility, Group cohesion, Activity budget
1.
Aguilar-Melo A, 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 nature-based tourism. American Journal of Primatology 75: 1108–1116.
2.
Altmann J (1974). Observational study of behavior: sampling methods. Behaviour 49: 227–267.
3.
Altmann J, Muruthi P (1988). Differences in daily life between semiprovisioned and wild-feeding baboons. American Journal of Primatology 15: 213–221.
4.
Arroyo-Rodríguez V, Dias PAD (2010). Effects of habitat fragmentation and disturbance on howler monkeys: a review. American Journal of Primatology72: 1–16.
5.
Asensio N, Arroyo-Rodríguez V, Dunn JC, Cristóbal-Azkarate J (2009). Conservation value of landscape supplementation for howler monkeys living in forest patches. Biotropica 41: 768–773.
6.
Benchimol M, Peres CA (2013). Anthropogenic modulators of species-area relationships in Neotropical primates: a continental-scale analysis of fragmented forest landscapes. Diversity and Distributions 19: 1339–1352.
7.
Bicca-Marques JC (2003). How do howler monkeys cope with habitat fragmentation? In Primates in Fragments (Marsh LK, ed.), pp 283–303. Boston, Springer.
8.
Brotcorne F, Maslarov C, Wandia IN, Fuentes A, Beudels-Jamar R, Huynen M-C (2014). The role of anthropic, ecological, and social factors in sleeping site choice by long-tailed macaques (Macaca fascicularis). American Journal of Primatology 76: 1140–1150.
9.
Chapman C (1987). Flexibility in diets of three species of Costa Rican primates. Folia Primatologica 49: 90–105.
10.
Chaves OM, Bicca-Marques MC (2017). Crop feeding by brown howlers (Alouatta guariba clamitans) in forest fragments: the conservation value of cultivated species. International Journal of Primatology 38: 263–281.
11.
Clarke MR, Glander KE (2010). Secondary transfer of adult mantled howlers (Alouatta palliata) on Hacienda La Pacifica, Costa Rica: 1975–2009. Primates 51: 241–249.
12.
Clarke MR, Collins DA, Zucker EL (2002). Responses to deforestation in a group of mantled howlers (Alouatta palliata) in Costa Rica. International Journal of Primatology 23: 365–381.
13.
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. American Journal of Primatology 69: 1013–1029.
14.
Crockett C (1998). Conservation biology of the genus Alouatta. International Journal of Primatology 19: 549–578.
15.
De la Torre S (2014). Effects of tourism on Ecuadorian primates: is there a need for responsible primate tourism? In Primate Tourism: A Tool for Conservation? (Russon AE, Wallis J, eds.), pp 245–255. Cambridge, Cambridge University Press.
16.
Dias PAD, Rangel-Negrín A (2015). Diets of howler monkeys. In Howler Monkeys: Behavior, Ecology, and Conservation (Kowalewski MM, Garber PA, Cortés-Ortiz L, Urbani B, Youlatos D, eds.), pp 21–56. New York, Springer.
17.
Di Fiore A, Campbell CJ (2007). The atelines: variation in ecology, behaviour, and social organisation. In Primates in Perspective (Campbell CJ, Fuentes A, Mackinnon KC, Panger M, Bearder SK, eds.), pp 155–185. New York, Oxford University Press.
18.
Espinosa-Gómez F, Gómez-Rosales S, Wallis IR, Canales-Espinosa D, Hernández-Salazar L (2013). Digestive strategies and food choices in mantled howler monkeys Alouatta palliata mexicana: bases of their dietary flexibility. Journal of Comparative Physiology B 183: 1089–1100.
19.
Estrada A (2015). Conservation of Alouatta: social and economic drivers of habitat loss, information vacuum, and mitigating population declines. In Howler Monkeys: Behavior, Ecology, and Conservation (Kowalewski MM, Garber PA, Cortés-Ortiz L, Urbani B, Youlatos D, eds.), pp 383–409. New York, Springer.
20.
Estrada A, Raboy BE, Oliveira LC (2012). Agroecosystems and primate conservation in the tropics: a review. American Journal of Primatology 74: 696–711.
21.
Garber PA, Kowalewski MM (2015). New challenges in the study of howler monkeys’ behavioural ecology and conservation: where we are and where we need to go. In Howler Monkeys: Behavior, Ecology, and Conservation (Kowalewski MM, Garber PA, Cortés-Ortiz L, Urbani B, Youlatos D, eds.), pp 413–428. New York, Springer.
22.
Grossberg R, Treves A, Naughton-Treves L (2003). The incidental ecotourist: measuring visitor impacts on endangered howler monkeys at a Belizean archaeological site. Environmental Conservation 30: 40–51.
23.
Ho L, Cortés-Ortiz L, Dias PAD, Canales-Espinosa D, Kitchen DM, Bergman TJ (2014). Effects of ancestry on behavioural variation in two species of howler monkeys (Alouatta pigra and A. palliata) and their hybrids. American Journal of Primatology 76: 855–867.
24.
Hoffman TS, O’Riain MJ (2012). Troop size and human-modified habitat affect the ranging patterns of a chacma baboon population in the Cape Peninsula, South Africa. American Journal of Primatology 74: 853–863.
25.
Instituto Meteorológico Nacional de Costa Rica (2018). Datos climáticos: Puntarenas. www.imn.ac.cr/web/imn/inicio.
26.
Irwin MT (2007). Living in forest fragments reduces group cohesion in diademed sifakas (Propithecus diadema) in Eastern Madagascar by reducing food patch size. American Journal of Primatology 69: 434–447.
27.
Jaimez NA, Bribiescas RG, Aronsen GP, Anestis SA, Watts DP (2011). Urinary cortisol levels of gray-cheeked mangabeys are higher in disturbed compared to undisturbed forest areas in Kibale National Park, Uganda. Animal Conservation 15: 242–247.
28.
Kowalewski MM, Zunino GE (1999). Impact of deforestation on a population of Alouatta caraya in Northern Argentina. Folia Primatologica 70: 163–166.
29.
Kowalewski MM, Garber PA, Cortés-Ortiz L, Urbani B, Youlatos D (2015). Why is it important to continue studying the behavioral ecology and conservation management of howler monkeys? In Howler Monkeys: Behavior, Ecology, and Conservation (Kowalewski MM, Garber PA, Cortés-Ortiz L, Urbani B, Youlatos D, eds.), pp 3–17. New York, Springer.
30.
Krebs CJ (1999). Ecological Methodology, 2nd ed. Menlo Park, Addison-Welsey Education Publishers.
31.
LaFleur M, Gould L (2009). Feeding outside the forest: the importance of crop raiding and an invasive weed in the diet of gallery forest ring-tailed lemurs (Lemur catta) following a cyclone at the Beza Mahafaly Special Reserve, Madgascar. Folia Primatologica 80: 233–246.
32.
Lehner P (1996). Handbook of Ethological Methods, 2nd ed. Cambridge, Cambridge University Press.
33.
Lootvoet AC, Phillippon J, Bessa-Gomes C (2015). Behavioral correlates of primates’ conservation status: intrinsic vulnerability to anthropogenic threats. PLOS One 10: e0135585.
34.
McKinney T (2010). Social and Ecological Impact of Anthropogenic Disturbance on the Sympatric White-Faced Capuchin ( Cebus capucinus) and Mantled Howler Monkey ( Aouatta palliata). Doctoral dissertation, Ohio State University.
35.
McKinney T (2011). The effects of provisioning and crop-raiding on the diet and foraging activities of human-commensal white-faced capuchins (Cebus capucinus). American Journal of Primatology 73: 439–448.
36.
McKinney T (2014). Species-specific responses to tourist interactions by white-faced capuchins (Cebus imitator) and mantled howlers (Alouatta palliata) in a Costa Rican wildlife refuge. International Journal of Primatology35: 573–589.
37.
McKinney T (2015). A classification system for describing anthropogenic influence on nonhuman primate populations. American Journal of Primatology77: 715–726.
38.
McKinney T, Westin JL, Serio-Silva JC (2015). Anthropogenic habitat modification, tourist interactions and crop-raiding in howler monkeys. In Howler Monkeys: Behavior, Ecology, and Conservation (Kowalewski MM, Garber PA, Cortés-Ortiz L, Urbani B, Youlatos D, eds.), pp 281–311. New York, Springer.
39.
McLennan MR, Spagnoletti N, Hockings KJ (2017). The implications of primate behavioral flexibility for sustainable human-primate coexistence in anthropogenic habitats. International Journal of Primatology 38: 105–121.
40.
Michalski F, Peres CA (2005). Anthropogenic determinants of primate and carnivore local extinctions in a fragmented forest landscape of southern Amazonia. Biological Conservation 124: 383–396.
41.
Nowak K, Lee PC (2013). “Specialist” primates can be flexible in response to habitat alteration. In Primates in Fragments: Complexity and Resilience(Marsh LK, Chapman CA, eds.), pp 199–211. New York, Springer.
42.
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.
43.
Peres CA (2001). Synergistic effects of subsistence hunting and habitat fragmentation on Amazonian forest vertebrates. Conservation Biology 15: 1490–1505.
44.
Perry S (1995). Social Relationships in Wild White-Faced Capuchin Monkeys, Cebus capucinus. Doctoral dissertation, University of Michigan.
45.
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. Animal Biodiversity and Conservation 26: 39–49.
46.
Powell RA (2000). Animal home ranges and territories and home range estimators. In Research Techniques in Animal Ecology: Controversies and Consequences (Boitani L, Fuller TK, eds.), pp 65–110. New York, Columbia University Press.
47.
Pozo-Montuy G, Serio-Silva JC, Chapman CA, Bonilla-Sánchez YM (2013). Resource use in a landscape matrix by an arboreal primate: evidence of supplementation in black howlers (Alouatta pigra). International Journal of Primatology 34: 714–731.
48.
Rangel Negrín A, Fuentes AC, Espinosa DC, Dias PAD (2016). The loss of behavioral diversity as a consequence of anthropogenic habitat disturbance: the social interactions of black howler monkeys. Primates 57: 9–15.
49.
Rodrigues MA (2017). Female spider monkeys (Ateles geoffroyi) cope with anthropogenic disturbance through fission-fusion dynamics. International Journal of Primatology 38: 838–855.
50.
Ryan SJ, Starks PT, Milton K, Getz WM (2008). Intersexual conflict and group size in Alouatta palliata: a 23-year evaluation. International Journal of Primatology 29: 405–420.
51.
Saj T, Sicotte P, Paterson JD (1999). Influence of human food consumption on the time budget of vervets. International Journal of Primatology 20: 977–994.
52.
Sha JCM, Hanya G (2013). Diet, activity, habitat use, and ranging of two neighboring groups of food-enhanced long-tailed macaques (Macaca fascicularis). American Journal of Primatology 75: 581–592.
53.
Sinha A, Mukhopadhyay K (2013). The monkey in the town’s commons, revisited: an anthropogenic history of the Indian bonnet macaque. In The Macaque Connection: Cooperation and Conflict between Humans and Macaques (Radhakrishna S, Huffman MA, Sinha A, eds.), pp 187–208. New York, Springer.
54.
Stevenson PR, Quiñones MJ, Ahumada JA (1998). Effects of fruit patch availability on feeding subgroup size and spacing patterns in four primate species at Tinigua National Park, Colombia. International Journal of Primatology 19: 313–324.
55.
Thoisy B, Richard-Hansen C (1997). Diet and social behaviour changes in a red howler monkey (Alouatta seniculus) troop in a highly degraded rain forest. Folia Primatologica68: 357–361.
56.
Wang E, Milton K (2003). Intragroup social relationships of male Alouatta palliata on Barro Colorado Island, Republic of Panama. International Journal of Primatology 24: 1227–1243.
57.
Williamson EA, Feistner ATC (2003). Habituating primates: processes, techniques, variables, and ethics. In Field and Laboratory Methods in Primatology: A Practical Guide (Setchell JM, Curtis DJ, eds.), pp 25–39. Cambridge, Cambridge University Press.
58.
Wright PC (2006). Considering climate change effects in lemur ecology and conservation. In Lemurs: Ecology and Adaptation (Gould L, Sauther ML, eds.), pp 385–401. New York, Springer.
59.
Yiming L (2006). Seasonal variation of diet and food availability in a group of Sichuan snub-nosed monkeys in Shennongjia Nature Reserve, China. American Journal of Primatology68: 217–233.
60.
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. American Journal of Primatology 69: 966–975.
© 2019 S. Karger AG, Basel
2019
Copyright / Drug Dosage / Disclaimer
Copyright: All rights reserved. No part of this publication may be translated into other languages, reproduced or utilized in any form or by any means, electronic or mechanical, including photocopying, recording, microcopying, or by any information storage and retrieval system, without permission in writing from the publisher.
Drug Dosage: The authors and the publisher have exerted every effort to ensure that drug selection and dosage set forth in this text are in accord with current recommendations and practice at the time of publication. However, in view of ongoing research, changes in government regulations, and the constant flow of information relating to drug therapy and drug reactions, the reader is urged to check the package insert for each drug for any changes in indications and dosage and for added warnings and precautions. This is particularly important when the recommended agent is a new and/or infrequently employed drug.
Disclaimer: The statements, opinions and data contained in this publication are solely those of the individual authors and contributors and not of the publishers and the editor(s). The appearance of advertisements or/and product references in the publication is not a warranty, endorsement, or approval of the products or services advertised or of their effectiveness, quality or safety. The publisher and the editor(s) disclaim responsibility for any injury to persons or property resulting from any ideas, methods, instructions or products referred to in the content or advertisements.
You do not currently have access to this content.