Female reproductive energetics in mantled howler monkeys (Alouatta palliata): A follow-up study.
C-peptide
energy expenditure
energy intake
lactation
thyroid hormone
Journal
American journal of physical anthropology
ISSN: 1096-8644
Titre abrégé: Am J Phys Anthropol
Pays: United States
ID NLM: 0400654
Informations de publication
Date de publication:
03 2021
03 2021
Historique:
received:
15
06
2020
revised:
12
11
2020
accepted:
20
12
2020
pubmed:
12
1
2021
medline:
31
3
2021
entrez:
11
1
2021
Statut:
ppublish
Résumé
Reproduction entails several challenges to primate females, among which energetic costs are remarkable at certain stages of the reproductive cycle. Still, females may use behavioral and physiological strategies to cope with those challenges. We had previously reported covariation between female energetic condition through the reproductive cycle and time-budget adjustments in mantled howler monkeys (Alouatta palliata). Accordingly, we suggested that behavioral flexibility allowed coping with the energetic challenges of reproduction. Subsequent evidence from the same population, however, suggested otherwise, so we performed a follow-up study on the variation in female reproductive energetics based on a larger sample of females. We studied 48 free-ranging adult females at Los Tuxtlas (Mexico). We assessed energy balance via urinary C-peptide concentrations (2717 urine samples), behavioral energy intake and expenditure (5728 sampling hours), and physiological energy expenditure via fecal triiodothyronine metabolites (fTH3; 3138 fecal samples). We found that energy balance varied among reproductive states: (a) cycling was a period of low C-peptide concentrations; (b) the highest C-peptide concentrations occurred during gestation; and (c) the beginning of lactation marked a notable decrease in C-peptide concentrations, which then improved at mid-lactation to again decline at lactation offset. These peaks and valleys in energy balance did not seem to be associated with variation in energy acquisition but were rather mirrored by activity levels and fTH3 during lactation. Energy balance was not preserved through the reproductive cycle, supporting previous contentions that the reproductive performance of female mantled howler monkeys may be energetically constrained. The contrast between these and results that we have previously reported, highlights the importance of conducting follow-up studies to continually improve our understanding of the reproductive energetics of primate females.
Substances chimiques
C-Peptide
0
Thyroid Hormones
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
396-406Informations de copyright
© 2021 Wiley Periodicals LLC.
Références
Altmann, J. (1974). Observational study of behavior: Sampling methods. Behaviour, 49, 227-266. https://doi.org/10.1163/156853974X00534
Amato, K. R., & Garber, P. A. (2014). Nutrition and foraging strategies of the black howler monkey (Alouatta pigra) in Palenque National Park, Mexico. American Journal of Primatology, 76, 774-787. https://doi.org/10.1002/ajp.22268
Amato, K. R., Leigh, S. R., Kent, A., Mackie, R. I., Yeoman, C. J., Stumpf, R. M., & Garber, P. A. (2014). The role of gut microbes in satisfying the nutritional demands of adult and juvenile wild, black howler monkeys (Alouatta pigra). American Journal of Physical Anthropology, 155, 652-664. https://doi.org/10.1002/ajpa.22621
Amato, K. R., Leigh, S. R., Kent, A. D., Mackie, R., Yeoman, C. J., et al. (2015). The gut microbiota appears to compensate for seasonal diet variation in the wild black howler monkey (Alouatta pigra). Microbial Ecology, 69, 434-443. https://doi.org/10.1007/s00248-014-0554-7
Anthony, M. R. L., & Kay, R. F. (1993). Tooth form and diet in ateline and alouattine primates: Reflections on the comparative method. American Journal of Science, 293A, 356-382. https://doi.org/10.2475/ajs.293.A.356
Arroyo-Rodríguez, V., Mandujano, S., & Benitez-Malvido, J. (2011). Diversidad y estructura de la vegetación en fragmentos de selva de Los Tuxtlas, Veracruz. In Comisión Nacional para el Conocimiento y Uso de la Biodiversidad (CONABIO), Gobierno del Estado de Veracruz, & Instituto de Ecología A.C. (Eds.), La biodiversidad en Veracruz: Estudio de Estado (1st ed., pp. 239-246). CONABIO.
Arroyo-Rodríguez, V., Serio-Silva, J. C., Álamo-García, J., & Ordano, M. (2007). Exploring immature-to-mother social distances in Mexican mantled howler monkeys at Los Tuxtlas, Mexico. American Journal of Primatology, 69, 173-181. https://doi.org/10.1002/ajp.20344
Back, J. P., & Bicca-Marques, J. C. (2019). Supplemented howler monkeys eat less wild fruits, but do not change their activity budgets. American Journal of Primatology, e23051, 81. https://doi.org/10.1002/ajp.23051
Balcells, C. D., & Veà, J. J. (2009). Developmental stages in the howler monkey, subspecies Alouatta palliata mexicana: A new classification using age-sex categories. Neotropical Primates, 16, 1-8. https://doi.org/10.1896/044.016.0101
Barret, L., Halliday, J., & Henzi, S. P. (2006). The ecology of motherhood: The structuring of lactation costs by chacma baboons. Journal of Animal Ecology, 75, 875-886. https://doi.org/10.1111/j.1365-2656.2006.01105.x
Bergstrom, M. L., Kalbitzer, U., Campos, F. A., Melin, A. D., Emery Thompson, M., & Fedigan, L. M. (2020). Non-invasive estimation of the costs of feeding competition in a Neotropical primate. Hormones and Behavior, 118, 104632. https://doi.org/10.1016/j.yhbeh.2019.104632
Bicca-Marques, J. C. (2003). How do howler monkeys cope with habitat fragmentation. In L. K. Marsh (Ed.), Primates in fragments: Ecology and conservation (pp. 283-303). Kluwer Academics.
Boinski, S. (1993). Vocal coordination of troop movement among white-faced capuchin monkeys, Cebus capucinus. American Journal of Primatology, 30, 85-100. https://doi.org/10.1002/ajp.1350300202
Brockman, D. K., & van Schaik, C. P. (2005). Seasonality and reproductive function. In C. P. van Schaik & D. K. Brockman (Eds.), Seasonality in primates: Studies of living and extinct human and non-human primates (pp. 269-306). Cambridge University Press. https://doi.org/10.1017/CBO9780511542343.011
Bronson, F. H. (1989). Mammalian reproductive biology. University of Chicago Press.
Cano-Huertes, B., Rangel-Negrín, A., Coyohua-Fuentes, A., Chavira-Ramírez, D. R., Canales-Espinosa, D., & Dias, P. A. D. (2017). Reproductive energetics of female mantled howlers (Alouatta palliata). International Journal of Primatology, 38, 942-961. https://doi.org/10.1007/s10764-017-9990-9
Castillo-Campos, G., & Laborde, J. (2004). La vegetación. In S. Guevara, J. Laborde, & G. Sánchez Ríos (Eds.), Los Tuxtlas. El paisaje de la sierra (pp. 231-265). Instituto de Ecología.
Ceccarelli, E., Rangel-Negrín, A., Coyohua-Fuentes, A., Canales-Espinosa, D., & Dias, P. A. D. (2020). Sex differences in leadership during group movement in mantled howler monkeys (Alouatta palliata). American Journal of Primatology, 82, e23099. https://doi.org/10.1002/ajp.23099
Clarke, M. R. (1990). Behavioral development and socialization of infants in a free-ranging group of howling monkeys (Alouatta palliata). Folia Primatologica, 54, 1-15. https://doi.org/10.1159/000156422
Cristóbal-Azkarate, J., & Arroyo-Rodríguez, V. (2007). Diet and activity patterns of howler monkeys (Alouatta palliata) in Los Tuxtlas, Mexico: Effects of habitat fragmentation and implications for conservation. American Journal of Primatology, 69, 1-17. https://doi.org/10.1002/ajp.20420
Cristóbal-Azkarate, J., Dunn, J. C., Balcells, C. D., & Baró, J. V. (2017). A demographic history of a population of howler monkeys (Alouatta palliata) living in a fragmented landscape in Mexico. PeerJ, 5, e3547. https://doi.org/10.7717/peerj.3547
Crockett, C. (2003). Re-evaluating the sexual selection hypothesis for infanticide by Alouatta males. In C. B. Jones (Ed.), Sexual selection and reproductive competition in primates: New perspectives and directions (pp. 327-365). American Society of Primatologists.
Di Fiore, A., & Campbell, C. J. (2007). The atelines: Variation in ecology, behavior, and social organization. In C. J. Campbell, A. Fuentes, K. C. MacKinnon, M. Panger, & S. K. Bearder (Eds.), Primates in perspective (pp. 155-185). Oxford University Press.
Dias, P. A. D., Cano-Huertes, B., Coyohua-Fuentes, A., Chavira-Ramírez, D. R., Canales-Espinosa, D., & Rangel-Negrín, A. (2018). Maternal condition and maternal investment during lactation in mantled howler monkeys. American Journal of Physical Anthropology, 167, 178-184. https://doi.org/10.1002/ajpa.23626
Dias, P. A. D., Coyohua-Fuentes, A., Canales-Espinosa, D., Chavira-Ramírez, R., & Rangel-Negrín, A. (2017). Hormonal correlates of energetic condition in mantled howler monkeys. Hormones and Behavior, 94, 13-20. https://doi.org/10.1016/j.yhbeh.2017.06.003
Dias, P. A. D., & Rangel-Negrín, A. (2015). Diets of howler monkeys. In M. Kowalewski, P. A. Garber, L. Cortés-Ortiz, B. Urbani, & D. Youlatos (Eds.), Howler monkeys: Behavior, ecology, and conservation (pp. 21-56). Springer. https://doi.org/10.1007/978-1-4939-1960-4_2
Dias, P. A. D., Rangel-Negrín, A., & Canales-Espinosa, D. (2011). Effects of lactation on the time-budgets and foraging patterns of female black howlers (Alouatta pigra). American Journal of Physical Anthropology, 145, 137-146. https://doi.org/10.1002/ajpa.21481
Dunn, J. C., Cristóbal-Azkarate, J., Schulte-Herbrüggen, B., Chavira, R., & Veà, J. J. (2013). Travel time predicts fecal glucocorticoid levels in free-ranging howlers (Alouatta palliata). International Journal of Primatology, 34, 246-259. https://doi.org/10.1007/s10764-013-9657-0
Emery Thompson, M. (2013). Comparative reproductive energetics of human and nonhuman primates. Annual Review of Anthropology, 42, 287-304. https://doi.org/10.1146/annurev-anthro-092412-155530
Emery Thompson, M. (2016). C-peptide of insulin. In A. Fuentes (Ed.), The international encyclopedia of primatology. Wiley-Blackwell Press. https://doi.org/10.1002/9781119179313.wbprim0159
Emery Thompson, M. (2017). Energetics of feeding, social behavior, and life history in non-human primates. Hormones and Behavior, 91, 84-96. https://doi.org/10.1016/j.yhbeh.2016.08.009
Emery Thompson, M., Muller, M. N., & Wrangham, R. W. (2012). The energetics of lactation and the return to fecundity in wild chimpanzees. Behavioral Ecology, 23, 1234-1241. https://doi.org/10.1093/beheco/ars107
Erhart, E. M., & Overdorff, D. J. (1999). Female coordination of group travel in wild Propithecus and Eulemur. International Journal of Primatology, 20, 927-940. https://doi.org/10.1023/a:1020830703012
Espinosa-Gómez, F., Gómez-Rosales, S., Wallis, I. R., Canales-Espinosa, D., & Hernández-Salazar, L. (2013). Digestive strategies and food choice in mantled howler monkeys Alouatta palliata mexicana: Bases of their dietary flexibility. Journal of Comparative Physiology B, 183, 1089-1100. https://doi.org/10.1007/s00360-013-0769-9
Espinosa-Gómez, F. C., Serio-Silva, J. C., Santiago-García, J. D., Sandoval-Castro, C. A., Hernández-Salazar, L. T., Mejía-Varas, F., Ojeda-Chávez, J., & Chapman, C. A. (2018). Salivary tannin-binding proteins are a pervasive strategy used by the folivorous/frugivorous black howler monkey. American Journal of Primatology, 80, e22737. https://doi.org/10.1002/ajp.22737
Estrada, A. (1982). Survey and census of howler monkeys (Alouatta palliata) in the rain forest of “Los Tuxtlas,” Veracruz, Mexico. American Journal of Primatology, 2, 363-372. https://doi.org/10.1002/ajp.1350020405
Gesquiere, L. R., Pugh, M., Alberts, S. C., & Markham, A. C. (2018). Estimation of energetic condition in wild baboons using fecal thyroid hormone determination. General and Comparative Endocrinology, 260, 9-17. https://doi.org/10.1016/j.ygcen.2018.02.004
Gittleman, J. L., & Thompson, S. D. (1988). Energy allocation in mammalian reproduction. Integrative and Comparative Biology, 28, 863-875. https://doi.org/10.1093/icb/28.3.863
Glander, K. E. (1980). Reproduction and population growth in free-ranging mantled howling monkeys. American Journal of Physical Anthropology, 53, 25-36. https://doi.org/10.1002/ajpa.1330530106
Grueter, C. C., Deschner, T., Behringer, V., Fawcett, K., & Robbins, M. M. (2014). Socioecological correlates of energy balance using urinary C-peptide measurements in wild female mountain gorillas. Physiology & Behavior, 127, 13-19. https://doi.org/10.1016/j.physbeh.2014.01.009
Gutiérrez-García, G., & Ricker, M. (2011). Climate and climate change in the region of Los Tuxtlas (Veracruz, Mexico): A statistical analysis. Atmosfera, 24, 347-373. https://www.revistascca.unam.mx/atm/index.php/atm/article/view/27738
Havel, P. J. (2001). Peripheral signals conveying metabolic information to the brain: Short-term and long-term regulation of food intake and energy homeostasis. Experimental Biology and Medicine, 226, 963-977. https://doi.org/10.1177/153537020122601102
Hayseen, V., & Orr, T. J. (2017). Reproduction in mammals: The female perspective. John Hopkins University Press.
Janson, C., & Verdolin, J. (2005). Seasonality of primate births in relation to climate. In C. P. van Schaik & D. K. Brockman (Eds.), Seasonality in primates: Studies of living and extinct human and non-human primates (pp. 307-350). Cambridge University Press. https://doi.org/10.1017/CBO9780511542343.012
Jones, C. B. (1980). The functions of status in the mantled howler monkey, Alouatta palliata GRAY: Intraspecific competition for group membership in a folivorous neotropical primate. Primates, 21, 389-405. https://doi.org/10.1007/BF02390468
Martin, R. D. (1995). Phylogenetic aspects of primate reproduction: The context of advanced maternal care. In C. R. Pryce, R. D. Martin, & D. E. Skuse (Eds.), Motherhood in human and nonhuman primates: Biosocial determinants (pp. 16-26). Karger Publishers. https://doi.org/10.1159/000424484
Martin, R. D. (2007). The evolution of human reproduction: A primatological perspective. American Journal of Physical Anthropology, 50, 59-84. https://doi.org/10.1002/ajpa.20734
McCabe, G. M., & Fedigan, L. M. (2007). Effects of reproductive status on energy intake, ingestion rates, and dietary composition of female Cebus capucinus at Santa Rosa, Costa Rica. International Journal of Primatology, 28, 837-851. https://doi.org/10.1007/s10764-007-9159-z
McCabe, G. M., Fernández, D., & Ehardt, C. L. (2013). Ecology of reproduction in Sanje mangabeys (Cercocebus sanjei): Dietary strategies and energetic condition during a high fruit period. American Journal of Primatology, 75, 1196-1208. https://doi.org/10.1002/ajp.22182
Milton, K. (1982). Dietary quality and demographic regulation in a howler monkey population. In E. G. Leigh, A. S. Rand, & D. M. Windsor (Eds.), The ecology of a tropical forest (pp. 273-289). Smithsonian Institution Press. https://ci.nii.ac.jp/naid/10015027513/
Piperata, B. A., & Dufour, D. L. (2007). Diet, energy expenditure, and body composition of lactating Ribeirinha women in the Brazilian amazon. American Journal of Human Biology, 19, 722-734. https://doi.org/10.1002/ajhb.20628
Prentice, A. M., & Prentice, A. (1988). Reproduction against the odds: Women in The Gambia eat too little and work too hard but they still manage to have babies. How do they cope? New Scientist, 118, 42-46.
Rangel-Negrín, A., Coyohua-Fuentes, A., Chavira-Ramírez, D. R., Canales-Espinosa, D., & Dias, P. A. D. (2018). Energetic constraints on the reproduction of female mantled howlers. American Journal of Primatology, 80, e22925. https://doi.org/10.1002/ajp.22925
Rangel-Negrín, A., Flores-Escobar, E., Chavira, R., Canales-Espinosa, D., & Dias, P. A. D. (2014). Physiological and analytical validations of fecal steroid hormone measures in black howler monkeys. Primates, 55, 459-465. https://doi.org/10.1007/s10329-014-0432-4
Reynoso-Cruz, J. E., Rangel-Negrín, A., Coyohua-Fuentes, A., Canales-Espinosa, D., & Dias, P. A. D. (2016). Measures of food intake in mantled howling monkeys. Primates, 57, 161-166. https://doi.org/10.1007/s10329-016-0513-7
Righini, N., Garber, P. A., & Rothman, J. M. (2017). The effects of plant nutritional chemistry on food selection of Mexican black howler monkeys (Alouatta pigra): The role of lipids. American Journal of Primatology, 79, e22524. https://doi.org/10.1002/ajp.22524
Rosetta, L., Lee, P. C., & Garcia, C. (2011). Energetics during reproduction: A doubly labeled water study of lactating baboons. American Journal of Physical Anthropology, 144, 661-668. https://doi.org/10.1002/ajpa.21475
Treves, A., Drescher, A., & Snowdon, C. T. (2003). Maternal watchfulness in black howler monkeys (Alouatta pigra). Ethology, 109, 135-146. https://doi.org/10.1046/j.1439-0310.2003.00853.x
Valeggia, C., & Ellison, P. T. (2009). Interactions between metabolic and reproductive functions in the resumption of postpartum fecundity. American Journal of Human Biology, 21, 559-566. https://doi.org/10.1002/ajhb.20907
Wasser, S. K., Hunt, K. E., Brown, J. L., Cooper, K., Crockett, C. M., Bechert, U., Millspaugh, J. J., Larson, S., & Monfort, S. L. (2000). A generalized fecal glucocorticoid assay for use in a diverse array of nondomestic mammalian and avian species. General and Comparative Endocrinology, 120(3), 260-275. https://doi.org/10.1006/gcen.2000.7557
Wright, P. C. (1990). Patterns of paternal care in primates. International Journal of Primatology, 11, 89-102. https://doi.org/10.1007/BF02192783
Youlatos, D., & Meldrum, J. (2011). Locomotor diversification in New World monkeys: Running, climbing, or clawing along evolutionary branches. Anatomy Records, 294, 1991-2012. https://doi.org/10.1002/ar.21508