Growth and allometric curves of southern brown howler monkey (Alouatta guariba): Insights on its ontogeny and conservation.
Atlantic forest
New World Monkeys
captivity
ontogenetic allometry
sexual dimorphism
Journal
American journal of primatology
ISSN: 1098-2345
Titre abrégé: Am J Primatol
Pays: United States
ID NLM: 8108949
Informations de publication
Date de publication:
05 Aug 2024
05 Aug 2024
Historique:
revised:
14
07
2024
received:
12
10
2023
accepted:
27
07
2024
medline:
6
8
2024
pubmed:
6
8
2024
entrez:
6
8
2024
Statut:
aheadofprint
Résumé
Ontogenetic sexual dimorphism is observed in different primate species, with ecological and evolutionary relationships explaining this pattern. Understanding the growth of the southern brown howler monkey elucidates not only the ecology and evolution but also contributes to conservation projects for this species. Throughout 20 years of the Centro de Pesquisas Biológicas de Indaial-Projeto Bugio, Brazil, we collected morphological data on 105 howlers of the Alouatta guariba species to identify the growth differences between ontogenetic categories and sexes and generate a growth curve to estimate the age of rescued individuals. Linear measurements were employed to obtain body length as well as the dimensions of the head and limbs. All individuals were also weighed to obtain body mass. We assessed growth rate and duration using allometric analysis based on the individuals' ages. We compared growth rate and duration among infant, juvenile, and adult howlers and between sexes. We provide growth curves for body size for both sexes using the Von Bertalanffy model. Infants have accelerated growth rate in comparison to the juveniles and adults, with no differences between sexes in establishing body length at this ontogenetic stage. Males have a prolonged development duration from the juvenile stage, reaching adulthood later than females, which explains the body length differences found in this species. Variables of head and limbs analyzed also showed differences in growth rate and duration, but not so consistently among ontogenetic stages. Mass was not a good variable to understand the growth differences of the animals, since many arrived feeble in the project and may have lost mass due to different circumstances in old age. Therefore, growth curves were obtained only for body length, allowing the estimation of the age of these animals when rescued from the wild to more effectively provide needed care in captivity.
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
e23675Informations de copyright
© 2024 Wiley Periodicals LLC.
Références
de Abreu, F. V. S., Delatorre, E., dos Santos, A. A. C., Ferreira‐de‐Brito, A., de Castro, M. G., Ribeiro, I. P., Furtado, N. D., Vargas, W. P., Ribeiro, M. S., Meneguete, P., Bonaldo, M. C., Bello, G., & Lourenço‐de‐Oliveira, R. (2019). Combination of surveillance tools reveals that yellow fever virus can remain in the same Atlantic Forest area at least for three transmission seasons. Memórias do Instituto Oswaldo Cruz, 114, e190076. https://doi.org/10.1590/0074-02760190076
Aguiar, L. M., Ludwig, G., Svoboda, W. K., Teixeira, G. M., Hilst, C. L. S., Shiozawa, M. M., Malanski, L. S., Mello, Â. M., Navarro, I. T., & Passos, F. C. (2007). Use of traps to capture black and gold howlers (Alouatta caraya) on the islands of the upper Paraná River, Southern Brazil. American Journal of Primatology, 69(2), 241–247. https://doi.org/10.1002/ajp.20372
Ariana, I., Padeta, I., Rachma Jadi, A., Wijayanto, H., Budipitojo, T., Raharjo, S., Rezeki, A., & Budi Santoso, H. (2020). The correlation of femur length with the body length of proboscis monkey. BIO Web of Conferences, 20, 04001. https://doi.org/10.1051/bioconf/20202004001
Balcells, C. D., & Baró, J. J. V. (2009). Developmental stages in the howler monkey, subspecies Alouatta palliata mexicana: A new classification using age‐sex categories. Neotropical Primates, 16(1), 1–8. https://doi.org/10.1896/044.016.0101
Baty, F., Ritz, C., Charles, S., Brutsche, M., Flandrois, J. P., & Delignette‐Muller, M. L. (2015). A toolbox for nonlinear regression in R: the package nlstools. Journal of Statistical Software, 66(5), 1–21. https://doi.org/10.18637/jss.v066.i05
Berghänel, A., Stevens, J. M. G., Hohmann, G., Deschner, T., & Behringer, V. (2023). Adolescent length growth spurts in bonobos and other primates: mind the scale. bioRxiv, 525764. https://doi.org/10.1101/2023.01.26.525764
Bernstein, R. M. (2017). Hormones and human and nonhuman primate growth. Hormone Research in Paediatrics, 88(1), 15–21. https://doi.org/10.1159/000476065
Bernstein, R. M. (2010). The big and small of it: How body size evolves. American Journal of Physical Anthropology, 143(S51), 46–62. https://doi.org/10.1002/ajpa.21440
Bishop, N. D., Hudson, R., Marlin, J., Pop, T., Rainwater, T., Boylan, S., Atkinson, B., & Carthy, R. R. (2021). Using growth rates to estimate the minimum age and size at sexual maturity in a captive population of the critically endangered Central American river turtle Dermatemys mawii. Journal of Zoo and Aquarium Research, 9(3), 150–156. https://doi.org/10.19227/jzar.v9i3.432
Blomquist, G. E., Kowalewski, M. M., & Leigh, S. R. (2009). Demographic and Morphological Perspectives on Life History Evolution and Conservation of New World Monkeys. In P. A. Garber, A. Estrada, J. C. Bicca‐Marques, E. W. Heymann, & K. B. Strier (Eds.), South American Primates. Developments in primatology: Progress and prospects (pp. 117–138). Springer. https://doi.org/10.1007/978-0-387-78705-3_5
Bonner, J. T. (1963). Morphogenesis and essay on development. Atheneum.
Braza, F., Alvarez, F., & Azcarate, T. (1983). Feeding habits of the red howler monkeys (Alouatta seniculus) in the Llanos of Venezuela. Mammalia, 47(2), 205–214.
Canales‐Espinosa, D., de Jesús Rovirosa‐Hernández, M., de Thoisy, B., Caba, M., & García‐Orduña, F. (2015). Hematology and Serum Biochemistry in Wild Howler Monkeys. In M. Kowalewski, P. Garber, L. Cortés‐Ortiz, B. Urbani, & D. Youlatos (Eds.), Howler Monkeys. Developments in primatology: Progress and prospects (pp. 179–202). Springer. https://doi.org/10.1007/978-1-4939-1957-4_7
Chaves, Ó. M., Júnior, J. C. S., Buss, G., Hirano, Z. M. B., Jardim, M. M. A., Amaral, E. L. S., Godoy, J. C., Peruchi, A. R., Michel, T., & Bicca‐Marques, J. C. (2022). Wildlife is imperiled in peri‐urban landscapes: Threats to arboreal mammals. Science of the Total Environment, 821, 152883. https://doi.org/10.1016/j.scitotenv.2021.152883
Crockett, C. M., & Pope, T. R. (1993). Consequences of sex differences in dispersal for juvenile red howler monkeys. In M. E. Pereira, & L. A. Fairbanks (Eds.), Juvenile Primates: Life History, Development and Behavior, with a New Foreword (pp. 104–118). The University of Chicago Press.
Fox, J., & Weisberg, S. (2019). An {R} Companion to Applied Regression (Third Edition.). Sage. https://socialsciences.mcmaster.ca/jfox/Books/Companion/
Froehlich, J. W., Thorington, R. W., & Otis, J. S. (1981). The demography of howler monkeys (Alouatta palliata) on Barro Colorado Island, Panamá. International Journal of Primatology, 2, 207–236. https://doi.org/10.1007/BF02739331
Geiger, M., Forasiepi, A. M., Koyabu, D., & Sánchez‐Villagra, M. R. (2013). Heterochrony and post‐natal growth in mammals—An examination of growth plates in limbs. Journal of Evolutionary Biology, 27(1), 98–115. https://doi.org/10.1111/jeb.12279
Glander, K. E., Fedigan, L. M., Fedigan, L., & Chapman, C. (1991). Field methods for capture and measurement of three monkey species in Costa Rica. Folia Primatologica, 57(2), 70–82. https://doi.org/10.1159/000156567
Gould, S. J. (1966). Allometry and size in ontogeny and phylogeny. Biological Reviews, 41, 587–638.
Gould, S. J. (1977). Ontogeny and phylogeny. Belknap Press of Harvard University Press.
Hintz, R. L. (1990). Role of growth hormone and insulin‐like growth factor binding proteins. Hormone Research, 33(2–4), 105–110. https://doi.org/10.1159/000181492
ICMBIO. (2018). Livro Vermelho da Fauna Brasileira Ameaçada de Extinção (Vol. IIMamíferos1 ed.). ICMBio/MMA.
Kelley, K. M., Oh, Y., Gargosky, S. E., Gucev, Z., Matsumoto, T., Hwa, V., Ng, L., Simpson, D. M., & Rosenfeld, R. G. (1996). Insulin‐like growth factor‐binding proteins (IGFBPs) and their regulatory dynamics. The International Journal of Biochemistry & Cell Biology, 28(6), 619–637. https://doi.org/10.1016/1357-2725(96)00005-2
Klingenberg, C. P. (1998). Heterochrony and allometry: The analysis of evolutionary change in ontogeny. Biological Reviews, 73(1), 79–123. https://doi.org/10.1017/S000632319800512X
Lee, L., Atkinson, D. Hirst, A. G., & Cornell, S. J. (2020). A new framework for growth curve fitting based on the von Bertalanffy Growth Function. Scientific Reports, 10, 7953. https://doi.org/10.1038/s41598-020-64839-y
Leigh, S. R. (1992). Patterns of variation in the ontogeny of primate body size dimorphism. Journal of Human Evolution, 23(1), 27–50. https://doi.org/10.1016/0047-2484(92)90042-8
Leigh, S. R. (1994). Ontoaenetic correlates of diet in anthropoid primates. American Journal of Physical Anthropology, 94, 499–522. https://doi.org/10.1002/ajpa.1330940406
Leutenegger, W., & Cheverud, J. (1982). Correlates of sexual dimorphism in primates: Ecological and size variables. International Journal of Primatology, 3, 387–402. https://doi.org/10.1007/BF02693740
Marshall, D. J., & White, C. R. (2019). Have we outgrown the existing models of growth? Trends in Ecology & Evolution, 34(2), 102–111. https://doi.org/10.1016/j.tree.2018.10.005
Mendes, S. L. (1989). Estudo ecológico de alouatta fusca (Primates: Cebidae) na Estação Biológica de Caratinga, MG. Revista Nordestina de Biologia, 6(2), 71–104.
Mendoza, P., Velasquez, J., Sanchez, J., Davila, L., Loja, D., Riveros, R., & Vilchez, C. (2019). Growth Curve of Amazonian Manatee (Trichechus ininguis) in Captivity. Aquatic Mammals, 45(4), 389–397.
Neville, M. K., Glander, K. E., Braza, F., & Rylands, A. B. (1988). The howling monkeys, genus Alouatta. In R. A. Mittermeier, A. B. Rylands, A. F. Coimbra‐Filho, & G. A. B. da Fonseca (Eds.), Ecology and Behavior in Neotropical Primates (pp. 349–453). World Wildlife Fund.
Ogle, D. (2013). fishR Vignette—Von Bertalanffy Models. http://derekogle.com/fishR/examples/oldFishRVignettes/VonBertalanffy.pdf
Ogle, D. (2022). FSAmisc: Miscellaneous functions for simple fisheries stock assessment methods. R package version 0.0.3. https://github.com/droglenc/FSAmisc
Ogle, D. H., & Isermann, D. A. (2017). Estimating age at a specified length from the von Bertalanffy growth function. North American Journal of Fisheries Management, 37, 1176–1180. https://doi.org/10.1080/02755947.2017.1342725
Ogle, D. H., Doll, J. C., Wheeler, P., & Dinno, A. (2022). FSA: Fisheries stock analysis. R package version 0.9.3.9000. https://fishr-core-team.github.io/FSA/
Oklander, L. I., Buss, G., Bicca‐Marques, J. C., Hirano, Z. M. B., Chaves, O. M., Jardim, M. M. A., Valença‐Montenegro, M. M., Mendes, S. L., Neves, L. G., Kowalewski, M., Melo, F. R., de Rylands, A. B., & Jerusalinsky, L. (2022). Brown Howler Monkey. In R. A. Mittermeier, K. E. Reuter, A. B. Rylands, L. Jerusalinsky, C. Schwitzer, K. B. Strier, J. Ratsimbazafy, & T. Humble (Eds.), Primates in Peril: The World's 25 Most Endangered Primates 2022‐2023 (pp. 121–125). IUCN SSC Primate Specialist Group, International Primatological Society, Re:wild.
Povill, C., de Oliveira, M. B., de Abreu, F. V. S., de Oliveira, R. L., Perini, F. A., Monticelli, C., Bueno, C., dos Santos, E., Pissinatti, A., & Bonvicino, C. R. (2023). Genetic diversity and insights into the distribution of Brown Howler Monkeys (Alouatta guariba Group) (Atelidae, Alouattinae). International Journal of Primatology, 44, 517–539. https://doi.org/10.1007/s10764-023-00352-z
R Core Team. (2022). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/
Raff, R. A. (1996). The shape of life: Genes, development, and the evolution of animal form. The University of Chicago Press.
Raguet‐Schofield, M., & Pavé, R. (2015). An Ontogenetic Framework for Alouatta: Infant Development and Evaluating Models of Life History. In M. Kowalewski, P. Garber, L. Cortés‐Ortiz, B. Urbani, & D. Youlatos (Eds.), Howler Monkeys. Developments in primatology: Progress and prospects (pp. 289–316). Springer. https://doi.org/10.1007/978-1-4939-1957-4_11
Revell, L. J. (2009). Size‐correction and principal components for interspecific comparative studies. Evolution, 63(12), 3258–3268. https://doi.org/10.1111/j.1558-5646.2009.00804.x
Rezende, C. L., Scarano, F. R., Assad, E. D., Joly, C. A., Metzger, J. P., Strassburg, B. B. N., Tabarelli, M., Fonseca, G. A., & Mittermeier, R. A. (2018). From hotspot to hopespot: An opportunity for the Brazilian atlantic forest. Perspectives in Ecology and Conservation, 16(4), 208–214. https://doi.org/10.1016/j.pecon.2018.10.002
Rodríguez, G. A. C., & Boher, S. B. (1988). Notes on the biology of Cebus nigrivittatus and Alouatta seniculus in Northern Venezuela. Primate Conservation, 9, 61–66. http://www.primate-sg.org/primate_conservation
Rosenberger, A. L., & Strier, K. B. (1989). Adaptive radiation of the ateline primates. Journal of Human Evolution, 18(7), 717–750. https://doi.org/10.1016/0047-2484(89)90102-4
Rumiz, D. I. (1990). Alouatta caraya; Population density and demography in Northern Argentina. American Journal of Primatology, 21, 279–294. https://doi.org/10.1002/ajp.1350210404
Runestad Connour, J., & Glander, K. E. (2020). Sexual dimorphism and growth in Alouatta palliata based on 20+ years of field data. American Journal of Physical Anthropology, 172, 545–566. https://doi.org/10.1002/ajpa.24055
Shea, B. T. (1983). Allometry and heterochrony in the African Apes. American Journal of Physical Anthropology, 62(3), 275–289. https://doi.org/10.1002/ajpa.1330620307
Shea, B. T. (1986). Ontogenetic approaches to sexual dimorphism in anthropoids. Human Evolution, 1, 97–110. https://doi.org/10.1007/BF02437489
Strier, K. B., & Mendes, S. L. (2009). Long‐term field studies of South American Primates. In P. A. Garber, A. Estrada, J. C. Bicca‐Marques, E. W. Heymann, & K. B. Strier (Eds.), South American Primates. Developments in Primatology: Progress and Prospects (pp. 139–155). Springer. https://doi.org/10.1007/978-0-387-78705-3_6
Strier, K. B., Mendes, S. L., & Santos, R. R. (2001). Timing of births in sympatric brown howler monkeys (Alouatta fusca clamitans) and Northern muriquis (Brachyteles arachnoides hypoxanthus). American Journal of Primatology, 55, 87–100. https://doi.org/10.1002/ajp.1042
Thompson, D. W. (1917). On growth and form. Cambridge University Press.
Thorington Jr., R. W., Ruiz, J. C., & Eisenberg, J. F. (1984). A study of a black howling monkey (Alouatta caraya) population in Northern Argentina. American Journal of Primatology, 6, 357–366. https://doi.org/10.1002/ajp.1350060405
Thorington, R. W., Rudran, R., & Mack, D. (1979). Sexual dimorphism of Alouatta seniculus and observations on capture techniques. In J. F. Eisenberg (Ed.), Vertebrate ecology in the northern neotropics (pp. 97–106). Smithsonian Institution Press.
Wang, Q., Shi, C., Liu, D., & Jiang, G. (2022). Estimation of body weight in captive Amur tigers (Panthera tigris altaica). Integrative Zoology, 17(6), 1106–1120. https://doi.org/10.1111/1749-4877.12612
Warton, D. I., Duursma, R. A., Falster, D. S., & Taskinen, S. (2012). smatr 3—An R package for estimation and inference about allometric lines. Methods in ecology and evolution, 3(2), 257–259. https://doi.org/10.1111/j.2041-210X.2011.00153.x
West, G. B., Brown, J. H., & Enquist, B. J. (2001). A general model for ontogenetic growth. Nature, 413, 628–631. https://doi.org/10.1038/35098076
Wood, B. A., & Chamberlain, A. T. (1986). The primate pelvis: Allometry or sexual dimorphism? Journal of Human Evolution, 15(4), 257–263. https://doi.org/10.1016/S0047-2484(86)80053-7