Comparative life history patterns of female gorillas.


Journal

American journal of biological anthropology
ISSN: 2692-7691
Titre abrégé: Am J Biol Anthropol
Pays: United States
ID NLM: 101770171

Informations de publication

Date de publication:
08 2023
Historique:
revised: 16 03 2023
received: 20 10 2022
accepted: 24 05 2023
medline: 23 10 2023
pubmed: 22 6 2023
entrez: 22 6 2023
Statut: ppublish

Résumé

Several theories have been proposed to explain the impact of ecological conditions on differences in life history variables within and between species. Here we compare female life history parameters of one western lowland gorilla population (Gorilla gorilla gorilla) and two mountain gorilla populations (Gorilla beringei beringei). We compared the age of natal dispersal, age of first birth, interbirth interval, and birth rates using long-term demographic datasets from Mbeli Bai (western gorillas), Bwindi Impenetrable National Park and the Virunga Massif (mountain gorillas). The Mbeli western gorillas had the latest age at first birth, longest interbirth interval, and slowest surviving birth rate compared to the Virunga mountain gorillas. Bwindi mountain gorillas were intermediate in their life history patterns. These patterns are consistent with differences in feeding ecology across sites. However, it is not possible to determine the evolutionary mechanisms responsible for these differences, whether a consequence of genetic adaptation to fluctuating food supplies ("ecological risk aversion hypothesis") or phenotypic plasticity in response to the abundance of food ("energy balance hypothesis"). Our results do not seem consistent with the extrinsic mortality risks at each site, but current conditions for mountain gorillas are unlikely to match their evolutionary history. Not all traits fell along the expected fast-slow continuum, which illustrates that they can vary independently from each other ("modularity model"). Thus, the life history traits of each gorilla population may reflect a complex interplay of multiple ecological influences that are operating through both genetic adaptations and phenotypic plasticity.

Identifiants

pubmed: 37345324
doi: 10.1002/ajpa.24792
doi:

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

564-574

Subventions

Organisme : Max Planck Society
Organisme : United States Fish and Wildlife Service Great Ape Fund
Organisme : Berggorilla Regenwald Direkthilfe
Organisme : National Science Foundation
ID : BCS 1753651

Informations de copyright

© 2023 The Authors. American Journal of Biological Anthropology published by Wiley Periodicals LLC.

Références

Altmann, J., & Alberts, S. C. (2005). Growth rates in a wild primate population: Ecological influences and maternal effects. Behavioral Ecology and Sociobiology, 57, 490-501.
Antón, S. C., Taboada, H. G., Middleton, E. R., Rainwater, C. W., Taylor, A. B., Turner, T. R., Turnquist, J. E., Weinstein, K. J., & Williams, S. A. (2016). Morphological variation in Homo erectus and the origins of developmental plasticity. Philosophical Transactions of the Royal Society B: Biological Sciences, 371, 20150236.
Altmann, S. A., & Altmann, J. (1977). Analysis of rates of behaviour. Animal Behaviour, 25, 364-372.
Bădescu, I., Katzenberg, M. A., Watts, D. P., & Sellen, D. W. (2017). A novel fecal stable isotope approach to determine the timing of age-related feeding transitions in wild infant chimpanzees. American Journal of Physical Anthropology, 162(2), 285-299.
Barrett, L., Henzi, S. P., & Lycett, J. E. (2006). Whose life is it anyway? Maternal investment, developmental trajectories, and life history strategies in baboons. In Reproduction and fitness in baboons: Behavioral, ecological, and life history perspectives. Springer.
Borries, C., Lodwick, J. L., Salmi, R., & Koenig, A. (2022). Phenotypic plasticity rather than ecological risk aversion or folivory can explain variation in gorilla life history. Frontiers in Ecology and Evolution, 10, 873557.
Borries, C., Lu, A., Ossi-Lupo, K., Larney, E., & Koenig, A. (2011). Primate life histories and dietary adaptations: A comparison of Asian colobines and Macaques. American Journal of Physical Anthropology, 144(2), 286-299.
Bray, J., Emery Thompson, M., Muller, M. N., Wrangham, R. W., & Machanda, Z. P. (2018). The development of feeding behavior in wild chimpanzees (Pan troglodytes schweinfurthii). American Journal of Physical Anthropology, 165, 34-46.
Breuer, T., Hockemba, M. B.-N., Olejniczak, C., Parnell, R. J., & Stokes, E. J. (2009). Physical maturation, life-history classes and age estimates of free-ranging western gorillas-insights from Mbeli Bai, Republic of Congo. American Journal of Primatology, 71, 106-119.
Breuer, T., Robbins, A. M., Olejniczak, C., Parnell, R. J., Stokes, E. J., & Robbins, M. M. (2010). Variance in the male reproductive success of western gorillas: Acquiring females is just the beginning. Behavioral Ecology and Sociobiology, 64, 515-528.
Breuer, T., Robbins, A. M., Boesch, C., & Robbins, M. M. (2012). Phenotypic correlates of male reproductive success in western gorillas. Journal of Human Evolution, 62, 466-472.
Caillaud, D., Eckardt, W., Vecellio, V., Ndagijimana, F., Mucyo, J.-P., Hirwa, J. P., & Stoinski, T. (2020). Violent encounters between social units hinder the growth of a high-density mountain gorilla population. Science Advances, 6, eaba0724.
Charnov, E., & Berrigan, D. (1993). Why do female primates have such long lifespans and so few babies? Evolutionary Anthropology, 1, 191-194.
Cipolletta, C. (2004). Effects of group dynamics and diet on the ranging patterns of a western gorilla group (Gorilla gorilla gorilla) at Bai Hokou, Central African Republic. American Journal of Primatology, 64(2), 193-205.
Colchero, F., Aburto, J. M., Archie, E. A., Boesch, C., Breuer, T., Campos, F. A., Collins, A., Conde, D. A., Cords, M., Crockford, C., Thompson, M. E., Fedigan, L. M., Fichtel, C., Groenenberg, M., Hobaiter, C., Kappeler, P. M., Lawler, R. R., Lewis, R. J., Machanda, Z. P., … Alberts, S. C. (2021). The long lives of primates and the ‘invariant rate of ageing’ hypothesis. Nature Communications, 12, 3666.
Doran-Sheehy, D. M., Greer, D., Mongo, P., & Schwindt, D. (2004). Impact of ecological and social factors on ranging in western gorillas. American Journal of Primatology, 64, 207-222.
Doran-Sheehy, D. M., Mongo, P., Lodwick, J., & Conklin-Brittain, N. L. (2009). Male and female western gorilla diet: Preferred foods, use of fallback resources, and implications for ape versus old world monkey foraging strategies. American Journal of Physical Anthropology, 140, 727-738.
Eckardt, W., Fawcett, K., & Fletcher, A. W. (2016). Weaned age variation in the Virunga mountain gorillas (Gorilla beringei beringei): Influential factors. Behavioral Ecology and Sociobiology, 70, 493-507.
Ellis, B. J., Figueredo, A. J., Brumbach, B. H., & Schlomer, G. L. (2009). Fundamental dimensions of environmental risk: The impact of harsh versus unpredictable environments on the evolution and development of life history strategies. Human Nature, 20, 204-268.
Emery Thompson, M. (2013). Reproductive ecology of female chimpanzees. American Journal of Primatology, 75, 22-237.
Emery Thompson, M. (2017). Energetics of feeding, social behavior, and life history in non-human primates. Hormones and Behavior, 91, 84-96.
Furuichi, T. (1989). Social interactions and the life history of female Pan paniscus in Wamba, Zaire. International journal of Primatology, 10, 173-197.
Galbany, J., Abavandimwe, D., Vakiener, M., Eckardt, W., Mudakikwa, A., Ndagijimana, F., Stoinski, T. S., & McFarlin, S. C. (2017). Body growth and life history in wild mountain gorillas (Gorilla beringei beringei) from Volcanoes National Park, Rwanda. American Journal of Physical Anthropology, 163, 570-590.
Ganas, J., Robbins, M. M., Nkurunungi, J. B., Kaplin, B. A., & McNeilage, A. (2004). Dietary variability of mountain gorillas in Bwindi Impenetrable National Park, Uganda. International Journal of Primatology, 25, 1043-1072.
Granjon, A. C., Robbins, M. M., Arinaitwe, J., Cranfield, M. R., Eckardt, W., Mburanumwe, I., Musana, A., Robbins, A. M., Roy, J., Sollmann, R., Vigilant, L., & Hickey, J. R. (2020). Estimating abundance and growth rates in a wild mountain gorilla population. Animal Conservation, 23a.12559.
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.
Grützmacher, K. S., Köndgen, S., Keil, V., Todd, A., Feistner, A., Herbinger, I., Petrzelkova, K., Fuh, T., Leendertz, S. A., Calvignac-Spencer, S., & Leendertz, F. H. (2016). Codetection of respiratory syncytial virus in habituated wild western lowland gorillas and humans during a respiratory disease outbreak. EcoHealth, 13, 499-510.
Gurven, M. D., Trumble, B. C., Stieglitz, J., Yetish, G., Cummings, D., Blackwell, A. D., Beheim, B., Kaplan, H. S., & Pontzer, H. (2016). High resting metabolic rate among Amazonian forager-horticulturalists experiencing high pathogen burden. American Journal of Physical Anthropology, 161(3), 414-425.
Harcourt, A. H. (1995). Sexual selection and sperm competition in primates: what are male genitalia good for? Evolutionary Anthropology, 4, 121-129.
Harcourt, A. H., & Stewart, K. J. (2007). Gorilla society: Conflict, compromise, and cooperation between the sexes. University of Chicago Press.
Head, J. S., Boesch, C., Makaga, L., & Robbins, M. M. (2011). Sympatric chimpanzees (Pan troglodytes troglodytes) and gorillas (Gorilla gorilla gorilla) in Loango National Park, Gabon: Dietary composition, seasonality, and intersite comparisons. International Journal of Primatology, 32, 755-775.
Janson, C. H., & van Schaik, C. P. (1993). Ecological risk aversion in juvenile primates: Slow and steady wins the race. In Juvenile primates: Life history, development, and behavior (pp. 57-74). Oxford University Press.
Jones, J. H. (2011). Primates and the evolution of long, slow life histories. Current Biology, 21, R708-R717.
Kalan, A. K., Kulik, L., Arandjelovic, M., Boesch, C., Haas, F., Dieguez, P., Barratt, C. D., Abwe, E. E., Agbor, A., Angedakin, S., Aubert, F., Ayimisin, E. A., Bailey, E., Bessone, M., Brazzola, G., Buh, V. E., Chancellor, R., Cohen, H., Coupland, C., … Kühl, H. S. (2020). Environmental variability supports chimpanzee behavioural diversity. Nature Communications, 11, 4451.
Klailova, M., Casanova, C., Henschel, P., Lee, P., Rovero, F., & Todd, A. (2012). Non-human predator interactions with wild great apes in Africa and the use of camera traps to study their dynamics. Folia Primatologica, 83, 312-328.
Knott, C. D., & Harwell, F. (2021). Ecological risk and the evolution of great ape life histories. In Chimpanzees in context: A comparative perspective on chimpanzee behavior, cognition, conservation and welfare. University of Chicago Press.
Kuzawa, C. W., & Bragg, J. M. (2012). Plasticity in human life history strategy: Implications for contemporary human variation and the evolution of genus Homo. Current Anthropology, 53(S6), S369-S382.
Lee, P., & Kappeler, P. M. (2003). Socioecological correlates of phenotypic plasticity of primate life histories. In Primate life histories and socioecology (pp. 41-65). University of Chicago Press.
Leigh, S., & Bernstein, R. (2006). Ontogeny, life history, and maternal investment in baboons. In Reproduction and fitness in babbons (pp. 225-256). Springer Press.
Leigh, S., & Shea, B. (1996). Ontogeny of body size variation in African apes. American Journal of Physical Anthropology, 99, 43-65.
Lodwick, J. L., & Salmi, R. (2019). Nutritional composition of the diet of the western gorilla (Gorilla gorilla): Interspecific variation in diet quality. American Journal of Primatology, 81, e23044.
Lonsdorf, E. V., Stanton, M. A., Pusey, A. E., & Murray, C. M. (2020). Sources of variation in weaned age among wild chimpanzees in Gombe National Park, Tanzania. American Journal of Physical Anthropology, 171, 419-429.
Manguette, M. L., Robbins, A. M., Breuer, T., Stokes, E. J., Parnell, R. J., & Robbins, M. M. (2019). Intersexual conflict influences female reproductive success in a female-dispersing primate. Behavioral Ecology and Sociobiology, 73, 118.
Manguette, M. L., Robbins, A. M., Breuer, T., Stokes, E. J., Parnell, R. J., & Robbins, M. M. (2020). Female dispersal patterns influenced by male tenure duration and group size in western lowland gorillas. Behavioral Ecology and Sociobiology, 74, 81.
Masi, S., Cipolletta, C., & Robbins, M. M. (2009). Western Lowland Gorillas (Gorilla gorilla gorilla) change their activity patterns in response to frugivory. American Journal of Primatology, 71, 91-100.
Masi, S., Mundry, R., Ortmann, S., Cipolletta, C., Boitani, L., & Robbins, M. M. (2015). The influence of seasonal frugivory on nutrient and energy intake in wild western gorillas. PLoS One, 10, e0129254.
Matsumoto, T. (2017). Developmental changes in feeding behaviors of infant chimpanzees at Mahale, Tanzania: Implications for nutritional independence long before cessation of nipple contact. American Journal of Physical Anthropology, 163, 356-366.
Morgan, D., & Sanz, C. (2006). Chimpanzee feeding ecology and comparisons with sympatric gorillas in the Goualougo Triangle, Republic of Congo. In G. Hohmann, M. M. Robbins, & C. Boesch (Eds.), Feeding ecology in apes and other primates (pp. 97-122). Cambridge University Press.
Nishida, T., Corp, N., Hamai, M., Hasegawa, T., Hiraiwa-Hasegawa, M., & Hosaka, K. (2003). Demography, female life history, and reproductive profiles among the chimpanzees of Mahale. American Journal of Primatology, 59, 99-121.
Nowell, A. A., & Fletcher, A. W. (2007). Development of Independence from the Mother in Gorilla gorilla gorilla. International Journal of Primatology, 28(2), 441-455.
Oates, J. F., McFarland, K. L., Groves, J. L., Bergl, R. A., Linder, J. M., & Disotell, T. R. (2003). The Cross River gorilla: Natural history and status of a neglected and critically endangered subspecies. In A. B. Taylor & M. L. Goldsmith (Eds.), Gorilla biology: A multidisciplinary approach (pp. 472-497). Cambridge University Press.
Ostrofsky, K. R., & Robbins, M. M. (2020). Fruit-feeding and activity patterns of mountain gorillas (Gorilla beringei beringei) in Bwindi Impenetrable National Park, Uganda. American Journal of Physical Anthropology, 173, 3-20.
Parnell, R. J. (2002). Group size and structure in western lowland gorillas (Gorilla gorilla gorilla) at Mbeli Bai, Republic of Congo. American Journal of Primatology, 56, 193-206.
Promislow, D., & Harvey, P. (1990). Living fast and dying young: A comparative analysis of life-history variation among mammals. Journal of Zoology, 220, 417-438.
R Core Team. (2020). R: A language and environment for statistical computing.Vienna: R Foundation for Statistical Computing. https://www.Rproject.org
Ravosa, M. J., Meyers, D. M., & Glander, K. E. (1993). Relative growth of the limbs and trunk in sifakas: Heterochronic, ecological, and functional considerations. American Journal of Physical Anthropology, 92, 499-520.
Reichard, U. H., & Barelli, C. (2008). Life history and reproductive strategies of Khao Yai Hylobates lar: Implications for social evolution in apes. International Journal of Primatology, 29, 823-844.
Reynolds, V. (2005). The chimpanzees of Budongo Forest: Ecology, behaviour, and conservation. Oxford University Press.
Robbins, A. M., Gray, M., Basabose, A., Uwingeli, P., Mburanumwe, I., Kagoda, E., & Robbins, M. M. (2013). Impact of male infanticide on the social structure of mountain gorillas. PLoS One, 8(11), e78256.
Robbins, A. M., Gray, M., Breuer, T., Manguette, M., Stokes, E., Uwingeli, P., Mburanumwe, I., Kagoda, E., & Robbins, M. M. (2016). Mothers may shape the variations in social organization among gorillas. Royal Society Open Science, 3, 160533.
Robbins, A. M., Stoinski, T. S., Fawcett, K. A., & Robbins, M. M. (2009). Does dispersal cause reproductive delays in female mountain gorillas? Behaviour, 146, 525-549.
Robbins, M. M., Akantorana, M., Arinaitwe, J., Kabano, P., Kayijamahe, C., Gray, M., Guschanski, K., Richardson, J., Roy, J., Tindimwebwa, V., Vigilant, L., & Robbins, A. M. (2019). Dispersal and reproductive careers of male mountain gorillas in Bwindi Impenetrable National Park, Uganda. Primates, 60, 133-142.
Robbins, M. M., Gray, M., Fawcett, K. A., Nutter, F. B., Uwingeli, P., Mburanumwe, I., Kagoda, E., Basabose, A., Stoinski, T. S., Cranfield, M. R., Byamukama, J., Spelman, L. H., & Robbins, A. M. (2011). Extreme conservation leads to recovery of the Virunga mountain gorillas. PLoS One, 6, e19788.
Robbins, M. M., Gray, M., Kagoda, E., & Robbins, A. M. (2009). Population dynamics of the Bwindi mountain gorillas. Biological Conservation, 142, 2886-2895.
Robbins, M. M., Ortmann, S., & Seiler, N. (2022). Dietary variability of western gorillas (Gorilla gorilla gorilla). PLoS One, 17, e0271576.
Robbins, M. M., & Robbins, A. M. (2021). Variability of weaning age in mountain gorillas (Gorilla beringei beringei). American Journal of Physical Anthropology, 174, 776-784.
Robbins, M. M., Robbins, A. M., Gerald-Steklis, N., & Steklis, H. D. (2007). Socioecological influences on the reproductive success of female mountain gorillas (Gorilla beringei beringei). Behavioral Ecology and Sociobiology, 61, 919-931.
Robbins, M. M. (2003). Behavioral aspects of sexual selection in mountain gorillas. In C. L. Jones (Ed.), Sexual Selection & Reproductive Competition in Primates: New Perspectives and Directions (pp. 477-501). American Society of Primatologists.
Robbins, M. M., Ortmann, S., & Seiler, N. (2022). Dietary variability of western gorillas (Gorilla gorilla gorilla). Plos One, 17, e0271576.
Rogers, M. E., Abernethy, K., Bermejo, M., Cipolletta, C., Doran, D., Mcfarland, K., Nishihara, T., Remis, M., & Tutin, C. E. G. (2004). Western gorilla diet: A synthesis from six sites. American Journal of Primatology, 64, 173-192.
Rothman, J. M., Plumptre, A. J., Dierenfeld, E. S., & Pell, A. N. (2007). Nutritional composition of the diet of the gorilla (Gorilla beringei): A comparison between two montane habitats. Journal of Tropical Ecology, 23, 673-682.
Roy, J., Arandjelovic, M., Bradley, B. J., Guschanski, K., Stephens, C. R., Bucknell, D., Cirhuza, H., Kusamba, C., Kyungu, J. C., Smith, V., Robbins, M. M., & Vigilant, L. (2014). Recent divergences and size decreases of eastern gorilla populations. Biology Letters, 10, 20140811.
Schaller, G. (1963). The mountain gorilla: Ecology and behavior. University of Chicago Press.
Seiler, N., Boesch, C., Ortmann, S., Mundry, R., & Robbins, M. M. (2018). Ecological and social influences on space use behavior in a large non-territorial mammal. American Journal of Primatology, 80, e22754.
Seiler, N., & Robbins, M. M. (2020). Ecological correlates of space use patterns in wild western lowland gorillas. American Journal of Primatology, 82, e23168.
Sibly, R. M., & Brown, J. H. (2007). Effects of body size and lifestyle on evolution of mammal life histories. Proceedings of the National Academy of Sciences, 104, 17707-17712.
Spelman, L. H., Gilardi, K. V. K., Lukasik-Braum, M., Kinani, J.-F., Nyirakaragire, E., Lowenstine, L. J., & Cranfield, M. R. (2013). Respiratory disease in mountain gorillas (Gorilla beringei beringei) in Rwanda, 1990-2010: Outbreaks, clinical course, and medical management. Journal of Zoo and Wildlife Medicine, 44, 1027-1035.
Stearns, S. C. (1992). The evolution of life histories. Oxford University Press.
Stoinski, T. S., Perdue, B., Breuer, T., & Hoff, M. P. (2013). Variability in the developmental life history of the genus Gorilla: Gorilla developmental life history. American Journal of Physical Anthropology, 152, 165-172.
Stoinski, T. S., Vecellio, V., Ngaboyamahina, T., Ndagijimana, F., Rosenbaum, S., & Fawcett, K. A. (2009). Proximate factors influencing dispersal decisions in male mountain gorillas, Gorilla beringei beringei. Animal Behaviour, 77, 1155-1164.
Stokes, E. J., Parnell, R. J., & Olejniczak, C. (2003). Female dispersal and reproductive success in wild western lowland gorillas (Gorilla gorilla gorilla). Behavioral Ecology and Sociobiology, 54, 329-339.
Sugiyama, Y. (2004). Demography and life history parameters of chimpanzees at Boussou., Guinea. American Journal of Physical Anthropology, 124, 154-165.
van Noordwijk, M. A., Utami Atmoko, S. S., Knott, C. D., Kuze, N., Morrogh-Bernard, H. C., Oram, F., Schuppli, C., van Schaik, C. P., & Willems, E. P. (2018). The slow ape: High infant survival and long interbirth intervals in wild orangutans. Journal of Human Evolution, 125, 38-49.
van Noordwijk, M. A., Willems, E. P., Utami Atmoko, S. S., Kuzawa, C. W., & van Schaik, C. P. (2013). Multi-year lactation and its consequences in Bornean orangutans (Pongo pygmaeus wurmbii). Behavioral Ecology and Sociobiology, 67, 805-814.
Vogel, E. R., Harrison, M. E., Zulfa, A., Bransford, T. D., Alavi, S. E., Husson, S., Morrogh-Bernard, H., Santiano, Firtsman, T., Utami-Atmoko, S. S., van Noordwijk, M. A., & Farida, W. R. (2015). Nutritional differences between two orangutan habitats: Implications for population density. PLoS One, 10, e0138612.
Walker, K. K., Walker, C. S., Goodall, J., & Pusey, A. E. (2018). Maturation is prolonged and variable in female chimpanzees. Journal of Human Evolution, 114, 131-140.
Walker, R., Gurven, M., Hill, K., Migliano, A., Chagnon, N., De Souza, R., Djurovic, G., Hames, R., Hurtado, A. M., Kaplan, H., Kramer, K., Oliver, W. J., Valeggia, C., & Yamauchi, T. (2006). Growth rates and life histories in twenty-two small-scale societies. American Journal of Human Biology, 18, 295-311.
Walker, R. S., & Hamilton, M. J. (2008). Life-history consequences of density dependence and the evolution of human body size. Current Anthropology, 49, 8.
Wallis, J. (1997). A survey of reproductive parameters in the free-ranging chimpanzees of Gombe National Park. Journal of Reproduction and Fertility, 109, 297-307.
Watts, D. P. (1984). Composition and variability of mountain gorilla diets in the Central Virungas. American Journal of Primatology, 7, 323-356.
Watts, D. P. (1989). Infanticide in mountain gorillas: New cases and a reconsideration of the evidence. Ethology, 81, 1-18.
Watts, D. P. (1990). Mountain gorilla life histories, reproductive competition, and sociosexual behavior and some implications for captive husbandry. Zoo Biology, 9, 185-200.
Watts, D. P. (1998). Seasonality in the ecology and life histories of mountain gorillas (Gorilla gorilla beringei). International Journal of Primatology, 19, 929-948.
Watts, D. P. (2012). The apes: Taxonomy, biogeography, life histories, and behavioral ecology. In The evolution of primate societies (pp. 113-142). University of Chicago Press.
Wich, S. A., Utami-Atmoko, S. S., Setia, T. M., Rijksen, H. D., Schürmann, C., van Hooff, J. A. R. A. M., & van Schaik, C. P. (2004). Life history of wild Sumatran orangutans (Pongo abelii). Journal of Human Evolution, 47(6), 385-398.
Wittig, R., & Boesch, C. (2019). Demography and life history of five chimpanzee communities in Tai National Park. In The chimpanzees of the Taï forest: 40 years of research. Cambridge University Press.
Wrangham, R., Conklin-Brittain, N. L., & Hunt, K. D. (1998). Dietary response of chimpanzees and cercopithecines to seasonal variation in fruit abundance I. Antifeedants. International Journal of Primatology, 19, 949-970.
Wright, E., Grueter, C. C., Seiler, N., Abavandimwe, D., Stoinski, T. S., Ortmann, S., & Robbins, M. M. (2015). Energetic responses to variation in food availability in the two mountain gorilla populations (Gorilla beringei beringei). American Journal of Physical Anthropology, 158, 487-500.
Xue, Y., Prado-Martinez, J., Sudmant, P. H., Narasimhan, V., Ayub, Q., Szpak, M., Frandsen, P., Chen, Y., Yngvadottir, B., Cooper, D. N., de Manuel, M., Hernandez-Rodriguez, J., Lobon, I., Siegismund, H. R., Pagani, L., Quail, M. A., Hvilsom, C., Mudakikwa, A., Eichler, E. E., … Scally, A. (2015). Mountain gorilla genomes reveal the impact of long-term population decline and inbreeding. Science, 348, 242-245.
Yamagiwa, J., Kahekwa, J., & Basabose, A. K. (2003). Intra-specific variation in social organization of gorillas: Implications for their social evolution. Primates, 44, 359-369.

Auteurs

Martha M Robbins (MM)

Department of Primate Behavior and Evolution, Max Planck Institute for Evolutionary Anthropology, Leipzig, Germany.

Moses Akantorana (M)

Department of Primate Behavior and Evolution, Max Planck Institute for Evolutionary Anthropology, Leipzig, Germany.

Joseph Arinaitwe (J)

Uganda Wildlife Authority, Kampala, Uganda.

Thomas Breuer (T)

Mbeli Bai Study, Wildlife Conservation Society Congo Program, Brazzaville, Democratic Republic of the Congo.
World Wide Fund for Nature, Berlin, Germany.

Marie Manguette (M)

Mbeli Bai Study, Wildlife Conservation Society Congo Program, Brazzaville, Democratic Republic of the Congo.

Shannon McFarlin (S)

Department of Anthropology, Center for the Advanced Study of Human Paleobiology, The George Washington University, Washington, DC, USA.

Angela Meder (A)

Berggorilla Regenwald Direkthilfe, Hoevelhof, Germany.

Richard Parnell (R)

Mbeli Bai Study, Wildlife Conservation Society Congo Program, Brazzaville, Democratic Republic of the Congo.

Jack L Richardson (JL)

Department of Anthropology, Center for the Advanced Study of Human Paleobiology, The George Washington University, Washington, DC, USA.

Claudia Stephan (C)

Mbeli Bai Study, Wildlife Conservation Society Congo Program, Brazzaville, Democratic Republic of the Congo.
Nouabalé-Ndoki Foundation, Brazzaville, Democratic Republic of the Congo.

Emma J Stokes (EJ)

Mbeli Bai Study, Wildlife Conservation Society Congo Program, Brazzaville, Democratic Republic of the Congo.

Tara S Stoinski (TS)

Dian Fossey Gorilla Fund International, Atlanta, Georgia, USA.

Veronica Vecellio (V)

Dian Fossey Gorilla Fund International, Atlanta, Georgia, USA.

Andrew M Robbins (AM)

Department of Primate Behavior and Evolution, Max Planck Institute for Evolutionary Anthropology, Leipzig, Germany.

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1.00
Humans Yoga Low Back Pain Female Male
Humans Meals Time Factors Female Adult

Classifications MeSH