Constraints on population growth of blue monkeys (Cercopithecus mitis) in Kibale National Park, Uganda
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School of Agriculture and Environmental Science, Mountains of the Moon University, Fort Portal, Uganda
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Department for the Ecology of Animal Societies, Max Planck Institute of Animal Behavior, Konstanz, Germany
Department of Biology, University of Konstanz, Konstanz, Germany
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Abstract
Changes in population size are driven by environmental and social factors. In spite of repeated efforts to identify the constraints on an unusually low-density population of blue monkeys (Cercopithecus mitis), it remains unclear why this generalist species fails to thrive in Kibale National Park in Uganda. While an unidentified disease may occasionally obstruct conception, it does not seem to limit overall reproductive rates. Infanticide at this site is infrequent due to the long tenures of resident males. Our analyses indicate that the single biggest constraint on blue monkey densities may be feeding competition with grey-cheeked mangabeys (Lophocebus albigena): across Kibale, the densities of these two species are strongly and negatively correlated. Though further analysis is needed to understand the timing and strength of feeding competition between them, we conclude that blue monkeys at Ngogo experience competitive exclusion from grey-cheeked mangabeys, possibly resolving the 50-year mystery surrounding this population.
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-
Almeida, M.A.B., Cardoso, J.D.C., dos Santos, E., da Fonseca, D.F., Cruz, L.L., Faraco, F.J.C., Bercini, M.A., Vettorello, K.C., Porto, M.A., Mohrdieck, R., Ranieri, T.M.S., Schermann, M.T., Sperb, A.F., Paz, F.Z., Nunes, Z.M.A., Romano, A.P.M., Costa, Z.G., Gomes, S.L. & Flannery, B. (2014). Surveillance for Yellow Fever virus in non-human primates in southern Brazil, 2001–2011: a tool for prioritizing human populations for vaccination. — PLOS Neglect. Trop. Dis. 8: e2741.
-
Angedakin, S. & Lwanga, J. (2011). Changes in group size and composition of the blue monkeys (Cercopithecus mitis stuhlmanni) between 1984 and 2009 at Ngogo, Kibale National Park, Uganda. — Afr. J. Ecol. 49: 362-366.
-
Azeem, S., Bengis, R., Aarde, R.V. & Bastos, A.D.S. (2020). Mass die-off of African elephants in Botswana: pathogen, poison or a perfect storm? — Afr. J. Wildl. Res. 50: 149-156.
-
Balcomb, S.R., Chapman, C.A. & Wrangham, R.W. (2000). Relationship between chimpanzee (Pan troglodytes) density and large, fleshy-fruit tree density: conservation implications. — Am. J. Primatol. 51: 197-203.
-
Barton, R.A. & Whiten, A. (1993). Feeding competition among female olive baboons, Papio anubis. — Anim. Behav. 46: 777-789.
-
Bronikowski, A., Cords, M., Alberts, S.C., Altmann, J., Brockman, D., Fedigan, L.M., Pusey, A., Stoinski, T., Strier, K.B. & Morris, W.F. (2016). Female and male life tables for seven wild primate species. — Sci. Data 3: 160006.
-
Brown, J.H. (1984). On the relationship between abundance and distribution of species. — Am. Nat. 124: 255-279.
-
Brown, M. (2013). Food and range defense in group-living primates. — Anim. Behav. 85: 807-816.
-
Brown, M. & Waser, P.M. (2018). Group movements in response to competitors’ calls indicate conflicts of interest between male and female grey-cheeked mangabeys. — Am. J. Primatol. 80: e22918.
-
Butynski, T.M. (1990). Comparative ecology of blue monkeys (Cercopithecus mitis) in high- and low-density subpopulations. — Ecol. Monogr. 60: 1-26.
-
Caillaud, D., Levréro, F., Cristescu, R., Gatti, S., Dewas, M., Douadi, M., Gautier-Hion, A., Raymond, M. & Ménard, N. (2006). Gorilla susceptibility to Ebola virus: the cost of sociality. — Curr. Biol. 16: 489-491.
-
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. — Sci. Adv. 6: eaba0724.
-
Caughley, G., Grice, D., Barker, R. & Brown, B. (1988). The edge of the range. — J. Anim. Ecol. 57: 771-785.
-
Chapman, C., Balcomb, S.R., Gillespie, T.R., Skorupa, J.P. & Struhsaker, T.T. (2000). Long-term effects of logging on African primate communities: a 28-year comparison from Kibale National Park, Uganda. — Conserv. Biol. 14: 207-217.
-
Chapman, C.A. & Chapman, L.J. (2000). Constraints on group size in red colobus and red-tailed guenons: examining the generality of the ecological constraints model. — Int. J. Primatol. 21: 565-585.
-
Chapman, C.A. & Lambert, J.E. (2000). Habitat alteration and the conservation of African primates: case study of Kibale National Park, Uganda. — Am. J. Primatol. 50: 169-185.
-
Chapman, C.A., Chapman, L.J., Cords, M., Gathua, J.M., Gautier-Hion, A., Lambert, J.E., Rode, K., Tutin, C.E.G. & White, L.J.T. (2002). Variation in the diets of Cercopithecus species: differences within forests, among forests, and across species. — In: The guenons: diversity and adaptation in African monkeys (Glenn, M.E. & Cords, M., eds). Kluwer Academic/Plenum Publishers, New York, NY, p. 319-344.
-
Chapman, C.A., Chapman, L.J., Zanne, A.E., Poulsen, J.R. & Clark, C.W. (2005). A 12-year phenological record of fruiting: implications for frugivore populations and indicators of climate change. — In: Tropical fruits and frugivores: the search for strong interactors (Dew, J.L. & Boubli, J.P., eds). Springer, Amsterdam, p. 75-92.
-
Chapman, C.A., Struhsaker, T.T., Skorupa, J.P., Snaith, T.V. & Rothman, J.M. (2010). Understanding long-term primate community dynamics: implications of forest change. — Ecol. Appl. 20: 179-191.
-
Chapman, C.A., Schoof, V.A.M., Bonnell, T.R., Gogarten, J.F. & Calmé, S. (2015). Competing pressures on populations: long-term dynamics of food availability, food quality, disease, stress and animal abundance. — Phil. Trans. Roy. Soc. B: Biol. Sci. 370: 20140112.
-
Chapman, C.A., Bortolamiol, S., Matsuda, I., Omeja, P.A., Paim, F.P., Reyna-Hurtado, R., Sengupta, R. & Valenta, K. (2017). Primate population dynamics: variation in abundance over space and time. — Biodivers. Conserv. 27: 1221-1238.
-
Chapman, C.A., Omeja, P.A., Kalbitzer, U., Fan, P. & Lawes, M.J. (2018). Restoration provides hope for faunal recovery: changes in primate abundance over 45 years in Kibale National Park, Uganda. — Trop. Conserv. Sci. 11: 1940082918787376.
-
Clutton-Brock, T.H. & Coulson, T. (2002). Comparative ungulate dynamics: the devil is in the details. — Phil. Trans. Roy. Soc. B: Biol. Sci. 357: 1285-1298.
-
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., Manguette, M.L., Muller, M.N., Packer, C., Parnell, R.J., Perry, S., Pusey, A.E., Robbins, M.M., Seyfarth, R.M., Silk, J.B., Staerk, J., Stoinski, T.S., Stokes, E.J., Strier, K.B., Strum, S.C., Tung, J., Villavicencio, F., Wittig, R.M., Wrangham, R.W., Zuberbühler, K., Vaupel, J.W. & Alberts, S.C. (2021). The long lives of primates and the ‘invariant rate of ageing’ hypothesis. — Nature Commun. 12: 3666.
-
Conklin-Brittain, N.L., Wrangham, R.W. & Hunt, K.D. (1998). Dietary response of chimpanzees and cercopithecines to seasonal variation in fruit abundance. II. macronutrients. — Int. J. Primatol. 19: 971-998.
-
Cords, M. (1987). Forest guenons and patas monkeys: male-male competition in one-male groups. — In: Primate societies (Smuts, B.B., Cheney, D.L., Seyfarth, R.M., Wrangham, R.W. & Struhsaker, T.T., eds). University of Chicago Press, Chicago, IL, p. 98-111.
-
Cords, M. (2012). The thirty-year blues: what we know and don’t know about life history, group size and group fission of blue monkeys in the Kakamega forest, Kenya. — In: Long term studies of primates (Kappeler, P.M. & Watts, D.P., eds). Springer, Berlin, p. 289-312.
-
Cords, M. & Chowdhury, S. (2010). Life history of Cercopithecus mitis stuhlmanni in the Kakamega forest, Kenya. — Int. J. Primatol. 3: 433-455.
-
Cords, M. & Fuller, J.L. (2010). Infanticide in Cercopithecus mitis stuhlmanni in the Kakamega forest, Kenya: variation in the occurrence of an adaptive behaviour. — Int. J. Primatol. 31: 409-431.
-
Cords, M. & Rowell, T.E. (1986). Group Fission in Blue Monkeys of the Kakamega forest, Kenya. — Folia Primatol. 46: 70-82.
-
Daszak, P. & Cunningham, A.A. (1999). Extinction by infection. — Trends Ecol. Evol. 14: 279.
-
Fashing, P.J. & Cords, M. (2000). Diurnal primate densities and biomass in the Kakamega forest: an evaluation of census methods and a comparison with other forests. — Am. J. Primatol. 50: 139-152.
-
Fedigan, L.M., Hogan, J.D., Campos, F.A., Kalbitzer, U. & Jack, K.M. (2021). Costs of male infanticide for female capuchins: when does an adaptive male reproductive strategy become costly for females and detrimental to population viability? — Am. J. Phys. Anthropol. 176: 349-360.
-
Gao, L. & Cords, M. (2020). Effects of female group size on the number of males in blue monkey (Cercopithecus mitis) groups. — Int. J. Primatol. 41: 665-682.
-
Garamszegi, L.Z. (2006). Comparing effect sizes across variables: generalization without the need for Bonferroni correction. — Behav. Ecol. 17: 682-687.
-
Gillespie, T.R., Greiner, E.C. & Chapman, C.A. (2004). Gastrointestinal parasites of the guenons of western Uganda. — J. Parasitol. 90: 1356-1360.
-
Gogarten, J.F., Jacob, A.L., Ghai, R.R., Rothman, J.M., Twinomugisha, D., Wasserman, M.D. & Chapman, C.A. (2015). Group size dynamics over 15+ years in an African forest primate community. — Biotropica 47: 101-112.
-
Hanya, G., Stevenson, P., van Noordwijk, M., Wong, S.T., Kanamori, T., Kuze, N., Aiba, S., Chapman, C.A. & van Schaik, C. (2011). Seasonality in fruit availability affects frugivorous primate biomass and species richness. — Ecography 34: 1009-1017.
-
Houle, A., Vickery, W.L. & Chapman, C.A. (2006). Testing mechanisms of coexistence among two species of frugivorous primates. — J Anim Ecol 75: 1034-1044.
-
Houle, A., Chapman, C.A. & Vickery, W.L. (2010). Intratree vertical variation of fruit density and the nature of contest competition in frugivores. — Behav. Ecol. Sociobiol. 64: 429-441.
-
Hudson, P.J., Dobson, A.P., Cattadori, I.M., Newborn, D., Haydon, D.T., Shaw, D.J., Benton, T.G. & Grenfell, B.T. (2002). Trophic interactions and population growth rates: describing patterns and identifying mechanisms. — Phil. Trans. Roy. Soc. B: Biol. Sci. 357: 1259-1271.
-
Kamilar, J.M. & Ledogar, J.A. (2011). Species co-occurrence patterns and dietary resource competition in primates. — Am. J. Phys. Anthropol. 144: 131-139.
-
Köndgen, S., Kühl, H., N’Goran, P.K., Walsh, P.D., Schenk, S., Ernst, N., Biek, R., Formenty, P., Mätz-Rensing, K., Schweiger, B., Junglen, S., Ellerbrok, H., Nitsche, A., Briese, T., Lipkin, W.I., Pauli, G., Boesch, C. & Leendertz, F.H. (2008). Pandemic human viruses cause decline of endangered great apes. — Curr. Biol. 18: 260-264.
-
Lawes, M.J. & Henzi, S.P. (1995). Inter-group encounters in blue monkeys: how territorial must a territorial species be? — Anim. Behav. 49: 240-243.
-
Lawes, M.J., Cords, M. & Lehn, C. (2013). Cercopithecus mitis gentle monkey (diademed monkey, blue monkey, Syke’s monkey). — In: Primates vol. II (Butynski, T.M., Kingdon, J. & Kalina, J., eds). Bloomsbury, London, p. 354-362.
-
Leendertz, F.H., Ellerbrok, H., Boesch, C., Couacy-Hymann, E., Mätz-Rensing, K., Hakenbeck, R., Bergmann, C., Abaza, P., Junglen, S., Moebius, Y., Vigilant, L., Formenty, P. & Pauli, G. (2004). Anthrax kills wild chimpanzees in a tropical rainforest. — Nature 430: 451-452.
-
Lukas, D. & Huchard, E. (2014). The evolution of infanticide by males in mammalian societies. — Science 346: 841.
-
Lwanga, J. (1987). Group fission in blue monkeys (Cercopithecus mitis stuhlmanni): effects on the socioecology in Kibale Forest, Uganda. — M.Sc. Thesis. Makerere University, Kampala.
-
Lwanga, J.S., Struhsaker, T.T., Struhsaker, P.J., Butynski, T.M. & Mitani, J.C. (2011). Primate population dynamics over 32.9 years at Ngogo, Kibale National Park, Uganda. — Am. J. Primatol. 73: 997-1011.
-
Milton, K. (1996). Effects of bot fly (Alouattamyia baeri) parasitism on a free-ranging howler monkey (Alouatta palliata) population in Panama. — J. Zool. 239: 39-63.
-
Milton, K. & Giacalone, J. (2014). Differential effects of unusual climatic stress on capuchin (Cebus capucinus) and howler monkey (Alouatta palliata) populations on barro Colorado island, Panama. — Am. J. Primatol. 76: 249-261.
-
Moore, J. (1999). Population density, social pathology, and behavioral ecology. — Primates 40: 1-22.
-
Nakagawa, S. (2004). A farewell to Bonferroni: the problems of low statistical power and publication bias. — Behav. Ecol. 15: 1044-1045.
-
Negrey, J.D., Reddy, R.B., Scully, E.J., Phillips-Garcia, S., Owens, L.A., Langergraber, K.E., Mitani, J.C., Emery Thompson, M., Wrangham, R.W., Muller, M.N., Otali, E., Machanda, Z., Hyeroba, D., Grindle, K.A., Pappas, T.E., Palmenberg, A.C., Gern, J.E. & Goldberg, T.L. (2019). Simultaneous outbreaks of respiratory disease in wild chimpanzees caused by distinct viruses of human origin. — Emerg. Microb. Infect. 8: 139-149.
-
Nunn, C.L. (2012). Primate disease ecology in comparative and theoretical perspective. — Am. J. Primatol. 74: 497-509.
-
Ochieng, J.R., Rwego, I.B., Kisakye, J.J.M. & Brown, M. (2020). Gastrointestinal parasites of blue monkeys (Cercopithecus mitis) and grey-cheeked mangabeys (Lophocebus albigena) at the Ngogo research site in Kibale National Park, Uganda. — Afr. J. Ecol. 59: 489-496.
-
Olupot, W. & Waser, P.M. (2013). Lophocebus albigena (also L. osmani, L. johnstoni, L. ugandae) Grey-Cheeked Mangabey. — In: Primates, vol. II (Butynski, T.M., Kingdon, J. & Kalina, J., eds). Bloomsbury, London, p. 206-209.
-
Owen, J.C., Landwerlen, H.R., Dupuis, A.P., 2nd, Belsare, A.V., Sharma, D.B., Wang, S., Ciota, A.T. & Kramer, L.D. (2021). Reservoir hosts experiencing food stress alter transmission dynamics for a zoonotic pathogen. — Proc. Roy. Soc. Lond. B: Biol. Sci. 288: 20210881.
-
Packer, C., Hilborn, R., Mosser, A., Kissui, B., Borner, M., Hopcraft, G., Wilmshurst, J., Mduma, S. & Sinclair, A.R.E. (2005). Ecological change, group territoriality, and population dynamics in Serengeti lions. — Science 307: 390-393.
-
Plumptre, A.J. & Cox, D. (2006). Counting primates for conservation: primate surveys in Uganda. — Primates 47: 65-73.
-
Rowell, T.E. (1970). Reproductive cycles of two Cercopithecus monkeys. — J. Reprod. Fertil. 22: 321-338.
-
Rudran, R. (1978). Socioecology of the blue monkeys (Cercopithecus mitis stuhlmanni) of the Kibale forest, Uganda. — Smith. Contrib. Zool. 249: 1-88.
-
Sapolsky, R.M. & Share, L.J. (2004). A Pacific culture among wild baboons: its emergence and transmission. — PLoS ONE 2: e106.
-
Scully, E.J., Basnet, S., Wrangham, R.W., Muller, M.N., Otali, E., Hyeroba, D., Grindle, K.A., Pappas, T.E., Thompson, M.E., Machanda, Z., Watters, K.E., Palmenberg, A.C., Gern, J.E. & Goldberg, T.L. (2018). Lethal respiratory disease associated with human rhinovirus C in wild chimpanzees, Uganda, 2013. — Emerg. Infect. Dis. 24: 267-274.
-
Sibly, R.M. & Hone, J. (2002). Population growth rate and its determinants: an overview. — Phil. Trans. Roy. Soc. B: Biol. Sci. 357: 1153-1170.
-
Sterck, E.H.M., Watts, D.P. & van Schaik, C.P. (1997). The evolution of female social relationships in nonhuman primates. — Behav. Ecol. Sociobiol. 4: 291-309.
-
Struhsaker, T.T. (1978). Food habits of five monkey species in the Kibale forest, Uganda. — In: Recent advances in primatology. 1. Behaviour. (Chivers, D.J. & Herbert, J., eds). Academic Press, London, p. 225-248.
-
Struhsaker, T.T. (1981). Polyspecific associations among tropical rain-forest primates. — Z. Tierpsychol. 57: 268-304.
-
Struhsaker, T.T. (1997). Ecology of an African rainforest: logging in Kibale and the conflict between conservation and exploitation. — University Press of Florida, Gainesville, FL.
-
Struhsaker, T.T. (2010). The red colobus monkeys: variation in demography, behavior, and ecology of endangered species. — Oxford University Press, Oxford.
-
Struhsaker, T.T. & Leland, L. (1979). Socioecology of five sympatric monkey species in the Kibale forest, Uganda. — In: Advances in the study of behavior (Rosenblatt, J., Hinde, R.A., Beer, C. & Busnel, M.C., eds). Academic Press, New York, NY, p. 158-228.
-
Struhsaker, T.T. & Leland, L. (1988). Group fission in redtail monkeys (Cercopithecus ascanius) in the Kibale forest, Uganda. — In: A primate radiation: evolutionary biology of the African guenons (Gautier-Hion, A., Bourliere, F., Gautier, P. & Kingdon, J., eds). Cambridge University Press, Cambridge, p. 364-388.
-
Struhsaker, T.T. & Leakey, M. (1990). Prey selectivity by crowned hawk-eagles on monkeys in the Kibale forest, Uganda. — Behav. Ecol. Sociobiol. 26: 435-443.
-
Struhsaker, T.T., Angedakin, S. & Landsmann, A. (2019). Facial and genital lesions in baboons (Papio anubis) of Kibale National Park, Uganda. — Primates 60: 109-112.
-
Teelen, S. (2007). Primate abundance along five transect lines at Ngogo, Kibale National Park, Uganda. — Am. J. Primatol. 69: 1-15.
-
Watts, D.P. & Mitani, J.C. (2015). Hunting and prey switching by chimpanzees (Pan troglodytes schweinfurthii) at Ngogo. — Int. J. Primatol. 36: 728-748.
-
Watts, D.P., Potts, K.B., Lwanga, J.S. & Mitani, J.C. (2012). Diet of chimpanzees (Pan troglodytes schweinfurthii) at Ngogo, Kibale National Park, Uganda, 1. diet composition and diversity. — Am. J. Primatol. 74: 114-129.
-
Windfelder, T. & Lwanga, J. (2004). Group fission in red-tailed monkeys (Cercopithecus ascanius) in Kibale National Park, Uganda. — In: The guenons: diversity and adaptation in African monkeys (Glenn, M.E. & Cords, M., eds). Kluwer Academic/Plenum Publishers, New York, NY, p. 147-159.
-
Worman, C.O. & Chapman, C.A. (2005). Seasonal variation in the quality of a tropical ripe fruit and the response of three frugivores. — J. Trop. Ecol. 21: 689-697.
-
Worman, C.O. & Chapman, C.A. (2006). Densities of two frugivorous primates with respect to forest and fragment tree species composition and fruit availability. — Int. J. Primatol. 27: 203-225.
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Constraints on population growth of blue monkeys (Cercopithecus mitis) in Kibale National Park, Uganda
In: BehaviourSearch for other papers by Hannah Frogge in
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Search for other papers by Revee A. Jones in
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School of Agriculture and Environmental Science, Mountains of the Moon University, Fort Portal, Uganda
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Department for the Ecology of Animal Societies, Max Planck Institute of Animal Behavior, Konstanz, Germany
Department of Biology, University of Konstanz, Konstanz, Germany
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Abstract
Changes in population size are driven by environmental and social factors. In spite of repeated efforts to identify the constraints on an unusually low-density population of blue monkeys (Cercopithecus mitis), it remains unclear why this generalist species fails to thrive in Kibale National Park in Uganda. While an unidentified disease may occasionally obstruct conception, it does not seem to limit overall reproductive rates. Infanticide at this site is infrequent due to the long tenures of resident males. Our analyses indicate that the single biggest constraint on blue monkey densities may be feeding competition with grey-cheeked mangabeys (Lophocebus albigena): across Kibale, the densities of these two species are strongly and negatively correlated. Though further analysis is needed to understand the timing and strength of feeding competition between them, we conclude that blue monkeys at Ngogo experience competitive exclusion from grey-cheeked mangabeys, possibly resolving the 50-year mystery surrounding this population.
| All Time | Past Year | Past 30 Days | |
|---|---|---|---|
| Abstract Views | 662 | 215 | 17 |
| Full Text Views | 91 | 22 | 0 |
| PDF Views & Downloads | 189 | 41 | 0 |