Adverse Effects of Ball-Chain Radio-Collars on Female Mantled Howlers (Alouatta palliata) in Panama
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Abstract
The placement of radio- and GPS-collars on primates has advanced the fields of primate behavior and ecology and yielded considerable conservation gains. However, to ensure that the placement of tracking collars remains a humane practice, the reporting of both positive and negative outcomes is required. Here, we evaluate the impacts of radio-collars on the reproduction, behavior, and health of female mantled howlers (Alouatta palliata) on Barro Colorado Island, Panama. In June 2005, as part of a behavioral study, we fitted 16 female howlers with ball-chain radio-collars weighing 1.2% of the mean adult female weight. We monitored these 16 collared females and 64 noncollared females across an annual cycle, and recaptured the collared females in July 2006 for collar removal. The mortality rate for collared females across the study year was 6.3% (N=1), while the net loss of noncollared females from study groups was 15.6% (N=10). All collared females reproduced. The behaviors of collared and noncollared females were not significantly different. However, on recapture to remove all remaining collars (N = 13), 38% of recaptured collared females presented with damage to the dermal layer on the back of the neck and 31% presented with more severe damage extending into the subcutaneous tissue and muscle. Given this physical damage, which was not apparent through binoculars, we cannot recommend using ball-chain radio-collars on female mantled howlers without careful welfare monitoring.
Keywords
Adverse impacts Alouatta Ball-chain Howler Radio-collarNotes
Acknowledgments
We thank the Smithsonian Tropical Research Institute and the Autoridad Nacional del Ambiente of Panama (ANAM) for their help and facilitation of this research. In addition, we thank the following individuals for assistance with research: F. Rodrigues, V. Jaramillo, A. Wendt, M. Senf, P. Thompson, K. Ellis, B. Gaard, L. Rich, R. Kays, M. Wikelski, D. Obando, O. Acevedo, and B. Jiménez. We also thank J. Setchell and two anonymous reviewers for their helpful suggestions. Funding was provided to M. Hopkins by the following organizations: the National Science Foundation (#0622611), The Wenner–Gren Foundation, The Leakey Foundation, the Smithsonian Tropical Research Institute, and the University of California at Berkeley. Funding for K. Milton was provided by the California Agricultural Experimental Station.
References
- Altmann, J. (1974). Baboons, space, time, and energy. American Zoologist, 14, 221–248.CrossRefGoogle Scholar
- Calderón-Arguedas, O., Troyo, A., Solano, M., Sánchez, R., Chinchilla, M., & Gutiérez-Espeleta, G. (2004). Infección por larvas de Alouattamyia baeri (Diptera: Cuterebridae) en monos aulladores, Alouatta palliata (Primates: Cebidae), de la costa Caribe de Costa Rica. Neotropical Primates, 12, 21–24.Google Scholar
- Cid, B., Costa, R. D. C. D., Balthazar, D. D. A., Augusto, A. M., Pires, A. S., & Fernandez, F. A. (2013). Preventing injuries caused by radio-telemetry collars in reintroduced red-rumped agoutis, Dasyprocta leporine, in Atlantic Forest, southeastern Brazil. Zoologia (Curitiba), 30(1), 115–118.CrossRefGoogle Scholar
- Clarke, M. R., & Glander, K. E. (2010). Secondary transfer of adult mantled howlers (Alouatta palliata) on Hacienda La Pacifica, Costa Rica: 1975–2009. Primates, 51, 241–249.CrossRefPubMedGoogle Scholar
- Cristobal-Azkarate, J., Colwell, D. D., Kenny, D., Solórzano, B., Sheeden, A., Cassaigne, I., & Rodríguez-Luna, E. (2012). First report of bot fly (Cuterebra baeri) infestation in howler monkeys (Alouatta palliata) from Mexico. Journal of Wildlife Diseases, 48(3), 822–825.CrossRefPubMedGoogle Scholar
- Cunningham, E. P., Unwin, S., & Setchell, J. M. (2015). Darting primates in the field: a review of reporting trends and a survey of practices and their effect on the primates involved. International Journal of Primatology, 36(5), 894–915.CrossRefGoogle Scholar
- De Thoisy, B., Vogel, I., Reynes, J. M., Pouliquen, J. F., Carme, B., Kazanji, M., & Vié, J. (2001). Health evaluation of translocated free ranging primates in French Guiana. American Journal of Primatology, 54, 1–16.CrossRefPubMedGoogle Scholar
- Díaz-Muñoz, S. L. (2011). Paternity and relatedness in a polyandrous nonhuman primate: testing adaptive hypotheses of male reproductive cooperation. Animal Behaviour, 82(3), 563–571.CrossRefGoogle Scholar
- Fedigan, L. M. (2010). Ethical issues faced by field primatologists: asking the relevant questions. American Journal of Primatology, 72(9), 754–771.CrossRefPubMedGoogle Scholar
- Fedo, B. (1991). Ball chain collars. Telonics Quarterly, 4, 2.Google Scholar
- Fernandez-Duque, E., & Rotundo, M. (2003). Field methods for capturing and marking Azarai night monkeys. International Journal of Primatology, 24(5), 1113–1120.CrossRefGoogle Scholar
- Glander, K. E. (1992). Dispersal patterns in Costa Rican mantled howling monkeys. International Journal of Primatology, 13(4), 415–435.CrossRefGoogle Scholar
- Glander, K. E. (1993). Capture and marking techniques for arboreal primates. In A. Estrada, E. Rodriguez-Luna, R. Lopez-Wilchis, & R. Coates-Estrada (Eds.), Estudios primatalogicos en Mexico (Vol. 1, pp. 299–304). Veracruz, Mexico: Universidad Veracruzana.Google Scholar
- Glander, K. E. (2006). Average body weight for mantled howling monkeys (Alouatta palliata): An assessment of average values and variability. In A. Estrada, P. A. Garber, M. Pavelka, & L. Luecke (Eds.), New perspectives in the study of Mesoamerican primates (pp. 247–263). New York: Springer Science+Business Media.Google Scholar
- Glander, K. E., Fedigan, L. M., & Chapman, C. (1991). Field methods for capture and measurement in three monkey species in Costa Rica. Folia Primatologica, 57, 70–82.CrossRefGoogle Scholar
- Gursky, S. (1998). Effects of radio transmitter weight on a small nocturnal primate. American Journal of Primatology, 46(2), 145–155.CrossRefPubMedGoogle Scholar
- Hilpert, A. L., & Jones, C. B. (2005). Possible costs of radio-tracking a young adult female mantled howler monkey (Alouatta palliata) in deciduous habitat of Costa Rican tropical dry forest. Journal of Applied Animal Welfare Science, 8(3), 227–232.CrossRefPubMedGoogle Scholar
- Honess, P. E., & MacDonald, D. W. (2011). Marking and radio-tracking primates. In J. M. Setchell & D. J. Curtis (Eds.), Field & laboratory methods in primatology: A practical guide (pp. 189–206). Cambridge: Cambridge University Press.CrossRefGoogle Scholar
- Hopkins, M. E. (2011). Mantled howler (Alouatta palliata) arboreal pathway networks: relative impacts of resource availability and forest structure. International Journal of Primatology, 32, 238–258.CrossRefGoogle Scholar
- Hopkins, M. E. (2013). Relative dominance and resource availability mediate mantled howler monkey (Alouatta palliata) spatial responses to neighbors’ loud calls. International Journal of Primatology, 5, 1032–1054.CrossRefGoogle Scholar
- Horwich, R. H., Koontz, F., Saqui, E., Saqui, H., & Glander, K. (1993). A reintroduction program for the conservation of the black howler monkey in Belize. Endangered Species Update, 10(6), 1–6.Google Scholar
- Juarez, C. P., Rotundo, M. A., Berg, W. J., & Fernandez-Duque, E. (2011). Costs and benefits of radio-collaring on the behavior, demography, and conservation of owl monkeys (Aotus azarai) in Formosa, Argentina. International Journal of Primatology, 32(1), 69–82.CrossRefGoogle Scholar
- Kenward, R. (2000). A manual for wildlife radio tagging. London: Academic Press.Google Scholar
- Kierulff, M. C. M., Canale, G., & Gouveia, P. S. (2005). Monitoring the yellow-breasted capuchin monkey (Cebus xanthosternos) with radiotelemetry: choosing the best radio-collar. Neotropical Primates, 13(1), 32–33.CrossRefGoogle Scholar
- Krausman, P. R., Bleich, V. C., Cain, J. W., III, Stephenson, T. R., DeYoung, D. W., McGrath, P. W., Swift, P. K., Pierce, B. M., & Jansen, B. D. (2004). Neck lesions in ungulates from collars incorporating satellite technology. Wildlife Society Bulletin, 32(3), 987–991.CrossRefGoogle Scholar
- Madden, R. C., & Giacalone-Madden, J. (1982). A method for radio-tagging flying squirrels. The Journal of Wildlife Management, 46(2), 525–527.CrossRefGoogle Scholar
- Marques, A. A. B. D., Schneider, M., & Alho, C. J. R. (2011). Translocation and radiotelemetry monitoring of black-tailed marmosets, Callithrix (Mico) melanura (É. Geoffroy in Humboldt), in a wildlife rescue operation in Brazil. Brazilian Journal of Biology, 71(4), 983–989.CrossRefGoogle Scholar
- Merker, S. (2006). Habitat-specific ranging patterns of Dian’s tarsiers (Tarsius dianae) as revealed by radiotracking. American Journal of Primatology, 68(2), 111–125.CrossRefPubMedGoogle Scholar
- Milton, K. (1996). Effects of bot fly (Alouattamyia baeri) parasitism on a free-ranging howler monkey (Alouatta palliata) population in Panama. Journal of Zoology, 239, 39–63.CrossRefGoogle Scholar
- Milton, K., Lozier, J. D., & Lacey, E. A. (2009). Genetic structure of an isolated population of mantled howler monkeys (Alouatta palliata) on Barro Colorado Island, Panama. Conservation Genetics, 10(2), 347–358.CrossRefGoogle Scholar
- Muller, K. H., & Schildger, J. (1994). Capture and radio-telemetry of masked titi monkeys, Callicebus personatus melanochir. Neotropical Primates, 2(4), 7–8.Google Scholar
- Olupot, W., & Waser, P. M. (2005). Patterns of male residency and intergroup transfer in gray-cheeked mangabeys (Lophocebus albigena). American Journal of Primatology, 66(4), 331–349.CrossRefPubMedGoogle Scholar
- Peignot, P., Charpentier, M. J., Bout, N., Bourry, O., Massima, U., Dosimont, O., Terramorsi, R., & Wickings, E. J. (2008). Learning from the first release project of captive-bred mandrills Mandrillus sphinx in Gabon. Oryx, 42(1), 122–131.CrossRefGoogle Scholar
- Richard-Hansen, C., Vié, J. C., & de Thoisy, B. (2000). Translocation of red howler monkeys (Alouatta seniculus) in French Guiana. Biological Conservation, 93(2), 247–253.CrossRefGoogle Scholar
- Riley, E. P., MacKinnon, K. C., Fernandez-Duque, E., Setchell, J. M., Garber, P. A., et al. (2014). Code of best practices for field primatology. Resource document. International Primatological Society & American Society of Primatologists. Retrieved from https://www.asp.org/resources/docs/Code%20of_Best_Practices%20Oct%202014.pdf. Accessed 4 November 2014.
- Sikes, R. S., Gannon, W. L., & Animal Care and Use Committee of the American Society of Mammalogists. (2011). Guidelines of the American Society of Mammalogists for the use of wild animals in research. Journal of Mammalogy, 92, 235–253.CrossRefGoogle Scholar
- Trayford, H. R., & Farmer, K. H. (2012). An assessment of the use of telemetry for primate reintroductions. Journal for Nature Conservation, 20(6), 311–325.CrossRefGoogle Scholar
- Vargas-Terán, M., Hofmann, H. C., & Tweddle, N. E. (2005). Impact of screwworm eradication programmes using the sterile insect technique. In Sterile insect technique (pp. 629–650). Dordrecht, the Netherlands: Springer.Google Scholar
- Vie, J. C., Richard-Hansen, C., & Fournier-Chambrillon, C. (2001). Abundance, use of space, and activity patterns of white-faced sakis (Pithecia pithecia) in French Guiana. American Journal of Primatology, 55(4), 203–221.CrossRefPubMedGoogle Scholar
- Zeledón, R., Jiménez-Quirós, O., & Brenes, R. R. Z. (1957). Cuterebra baeri en el mono aullador de Costa Rica. Revista de Biología Tropical, 5, 129–134.Google Scholar