Reproductive seasonality in wild Sanje mangabeys (Cercocebus sanjei), Tanzania: Relationship between the capital breeding strategy and infant survival
äºBehaviourbDepartment of Anthropology, University of Texas at San Antonio, San Antonio, TX 78249, USA
Search for other papers by Gráinne Michelle McCabe in
Current site
Google Scholar
Search for other papers by Melissa Emery Thompson in
Current site
Google Scholar
The reproductive seasonality model states that it is adaptive for species in seasonally variable environments to temporally cluster reproductive events around periods of resource availability. Many studies have examined links between seasonal reproduction and phenological events, though few studies have fully tested the adaptive hypothesis by examining the effects of reproductive timing on outcomes. Our study tests the predictions of the model in an African cercopithecine, the Sanje mangabey, by examining the impact of food availability on the timing of conception, birth and weaning, and the relationship of reproductive timing and female energy balance (urinary C-peptide) to infant survival. From September 2008 through 2010, 28 infants were born. Distribution of conceptions was non-uniform, with a peak between January and March. There was a significant positive correlation between mean monthly fruit availability and number of conceptions per month. An increased food supply supports a positive energy balance, maximizing the potential for conception; a pattern found among many cercopithecines. Mothers that conceived within the peak period also exhibited higher levels of urinary C-peptide during preconception and early gestation, compared to conceptions outside the peak period. This strategy increased the probability of survival to year one, as it was significantly higher for infants conceived during the peak conceptive season. These results support the reproductive seasonality model and demonstrate that the timing of conception is critical for mangabey reproductive success.
Purchase
Buy instant access (PDF download and unlimited online access):
Institutional Login
Log in with Open Athens, Shibboleth, or your institutional credentials
Personal login
Log in with your brill.com account
-
Altmann J. (1974). Observational study of behavior: sampling methods. â Behaviour 49: 227-267.
-
Altmann J. (1980). Baboon mothers and others. â University of Chicago Press, Chicago, IL.
-
Altmann S.A. (1998). Foraging for survival: yearling baboons in Africa. â University of Chicago Press, Chicago, IL.
-
Anderson D.P., Nordheim E., Boesch C. (2006). Environmental factors influencing the seasonality of estrus in chimpanzees. â Primates 47: 43-50.
-
Anyamba A., Tucker C.J., Mahoney R. (2002). From El Niño to La Niña: vegetation response patterns over East and Southern Africa during the 1977â2000 period. â J. Climate 15: 3096-3103.
-
Babicky A., Ostadalova I., Parizek J., Kolar J., Bibr B. (1973). Onset and duration of the physiological weaning period for infant rats reared in nests of different sizes. â Physiol. Bohemoslov. 22: 449-456.
-
Barrett L., Halliday J., Henzi S. (2006). The ecology of motherhood: the structuring of lactation costs by chacma baboons. â J. Anim. Ecol. 75: 875-886.
-
Beehner J., Onderdonk D.A., Alberts S., Altmann J. (2006). The ecology of conception and pregnancy failure in wild baboons. â Behav. Ecol. 17: 741-750.
-
Bentley-Condit V.K., Smith E.O. (1997). Female reproductive parameters of Tana River yellow baboons. â Int. J. Primatol. 18: 581-596.
-
Borries C., Koenig A., Winkler P. (2001). Variation of life history traits and mating patterns in female langur monkeys (Semnopithecus entellus). â Behav. Ecol. Sociobiol. 50: 391-402.
-
Bowman J.E., Lee P.C. (1995). Growth and threshold weaning weights among captive rhesus macaques. â Am. J. Phys. Anthropol. 96: 159-175.
-
Boyd I.L. (2000). State-dependent fertility in pinnipeds: contrasting capital and income breeders. â Funct. Ecol. 14: 623-630.
-
Brockman D.K., van Schaik C.P. (2005). Seasonality and reproductive function. â In: Seasonality in primates: studies of living and extinct human and non-human primates ( Brockman D.K., van Schaik C.P., eds). Cambridge University Press, Cambridge, p. 269-305.
-
Bronson F.H. (1989). Mammalian reproductive biology. â University of Chicago Press, Chicago, IL.
-
Carnegie S., Fedigan L., Melin A. (2011). Reproductive seasonality in female capuchins (Cebus capucinus) in Santa Rosa (Area de Conservación Guanacaste), Costa Rica. â Int. J. Primatol. 32: 1076-1090.
-
Carrai V., Borgognini-Tarli S.M., Huffman M.A., Bardi M. (2003). Increase in tannin consumption by sifaka (Propithecus verreauxi verreauxi) females during the birth season: a case for self-medication in prosimians? â Primates 44: 61-66.
-
Chandra R.K. (1974). Rosette-forming T lymphocytes and cell-mediated immunity in malnutrition. â Br. Med. J. 3: 608-609.
-
Chandra R.K. (1975). Fetal malnutrition and postnatal immunocompetence. â Am. J. Dis. Child 129: 450-454.
-
Chandra R.K. (1991). 1990 McCollum Award lecture. Nutrition and immunity: lessons from the past and new insights into the future. â Am. J. Clin. Nutr. 53: 1087-1101.
-
Chapman C.A., Fedigan L.M. (1990). Dietary differences between neighboring Cebus capucinus groups: local traditions, food availability or responses to food profitability. â Folia Primatol. 54: 177-186.
-
Comiskey J., Dallmeier F., Mistry S. (2000). Vegetation sampling protocols for the Korup NP, Cameroon. â Smithsonian Institution, Monitoring and Assessment of Biodiversity Program, Washington, DC.
-
Cramer C.P., Thiels E., Alberts J.R. (1990). Weaning in rats: I. Maternal behavior. â Dev. Psychobiol. 23: 479-493.
-
Crockett C.M., Rudran R. (1987). Red howler monkey birth data I: seasonal variation. â Am. J. Primatol. 13: 347-368.
-
Deschner T., Kratzsch J., Hohmann G. (2008). Urinary C-peptide as a method for monitoring body mass changes in captive bonobos (Pan paniscus). â Horm. Behav. 54: 620-626.
-
Di Bitetti M.S., Janson C.H. (2000). When will the stork arrive? Patterns of birth seasonality in Neotropical primates. â Am. J. Primatol. 50: 109-130.
-
Drent R.H., Daan S. (1980). The prudent parent: energetic adjustments in avian breeding. â In: The integrated study of bird populations ( Klomp H., Woldendrop J.W., eds). North Holland, New York, NY, p. 225-252.
-
Dunbar R.I.M. (1984). Reproductive decisions: an economic analysis of gelada baboon social strategies. â Princeton University Press, Princeton, NJ.
-
Ehardt C.L., Butynski T.M. (2013). The Sanje mangabey (Cercocebus sanjei). â In: The mammals of Africa, Vol. 2 ( Butynski T., Kingdon J., Kalina J., eds). Bloomsbury, London, p. 177-180.
-
Ehardt C.L., McCabe G.M. (2011). Seed consumption in the Sanje mangabey (Cercocebus sanjei) of Tanzania: age/sex parameters and the fallback food concept [abstract]. â Am. J. Primatol. 73: 106.
-
Ehardt C.L., Jones T., Butynski T. (2005). Protective status, ecology and strategies for improving conservation of Cercocebus sanjei in the Udzungwa Mountains, Tanzania. â Int. J. Primatol. 26: 557-583.
-
Ehardt C.L., Butynski T.M., Struhsaker T. (2008). Cercocebus sanjei. â In: IUCN 2011. IUCN Red List of Threatened Species. Version 2011.2, available online at: http://www.iucnredlist.org (accessed 31 May 2012).
-
Ellison P.T. (1990). Human ovarian function and reproductive ecology: new hypotheses. â Am. Anthropol. 92: 933-952.
-
Ellison P.T. (2001). Reproductive ecology and human evolution. â Aldine de Gruyter, New York, NY.
-
Ellison P.T. (2003). Energetics and reproductive effort. â Am. J. Hum. Biol. 15: 342-351.
-
Ellison P.T., Valeggia C. (2003). C-peptide levels and the duration of lactational amenorrhea. â Fertil. Steril. 80: 1279-1280.
-
Emery Thompson M., Knott C.D. (2008). Urinary C-peptide of insulin as a non-invasive marker of energy balance in wild orangutans. â Horm. Behav. 53: 526-535.
-
Emery Thompson M., Wrangham R. (2008). Diet and reproductive function in wild female chimpanzees (Pan troglodytes schweinfurthii) at Kibale National Park, Uganda. â Am. J. Phys. Anthropol. 135: 171-181.
-
Emery Thompson M., Muller M.N., Wrangham R.W., Lwanga J.S., Potts K.B. (2009). Urinary C-peptide tracks seasonal and individual variation in energy balance in wild chimpanzees. â Horm. Behav. 55: 299-305.
-
Emery Thompson M., Muller M.N., Kahlenberg S.M., Wrangham R.W. (2010). Dynamics of social and energetic stress in wild female chimpanzees. â Horm. Behav. 58: 440-449.
-
Fernández D. (2011). Life history traits of wild Sanje mangabeys (Cercocebus sanjei) in the Udzungwa Mountains National Park, Tanzania (abstract). â Am. J. Primatol. 73(S1): 105.
-
Fernández D. (2013). Reproduction, sexual swellings and mating behavior in Sanje mangabeys (Cercocebus sanjei). â Dissertation, Stony Brook University, Stony Brook, NY.
-
Fernandez-Duque E., Rotundo M., Ramirez-Llorens P. (2002). Environmental determinants of birth seasonality in night monkeys (Aotus azarai) of the Argentinean Chaco. â Int. J. Primatol. 23: 639-656.
-
Georgiev A.V., Emery Thompson M., Lokasola A.L., Wrangham R.W. (2011). Seed predation by bonobos (Pan paniscus) at Kokolopori, Democratic Republic of the Congo. â Primates 52: 309-314.
-
Girard-Buttoz C., Higham J.P., Heistermann M., Wedegärtner S., Maestripieri D., Engelhardt A. (2011). Urinary C-peptide measurement as a marker of nutritional status in macaques. â PLoS One 6: 1-9.
-
Godfrey K.M. (1998). Maternal regulation of fetal development and health in adult life. â Eur. J. Obstet. Gynecol. Reprod. Biol. 78: 141-150.
-
Gordon T.P., Gust D.A., Busse C.D., Wilson M.E. (1991). Hormones and sexual behavior associated with postconception perineal swelling in the sooty mangabey (Cereocebus torquatus atys). â Int. J. Primatol. 12: 585-597.
-
Harris T.R., Chapman C.A., Monfort S.L. (2010). Small folivorous primate groups exhibit behavioral and physiological effects of food scarcity. â Behav. Ecol. 21: 46-56.
-
Hau M. (2001). Timing of breeding in variable environments: tropical birds as model systems. â Horm. Behav. 40: 281-290.
-
Higham J.P., Heistermann M., Maestripieri D. (2011). The energetics of maleâmale endurance rivalry in free-ranging rhesus macaques, Macaca mulatta. â Anim. Behav. 81: 1001-1007.
-
Hoet J.J., Hanson M.A. (1999). Intrauterine nutrition: its importance during critical periods for cardiovascular and endocrine development. â J. Physiol. 514: 617-627.
-
Homewood K.M., Rodgers W.A. (1981). A previously undescribed mangabey from Southern Tanzania. â Int. J. Primatol. 2: 47-55.
-
Houdijk J., Jessop N., Kyriazakis I. (2001). Nutrient partitioning between reproductive and immune functions in animals. â Proc. Nutr. Soc. 60: 515-525.
-
Janson C., Verdolin J. (2005). Seasonality of primate births in relation to climate. â In: Seasonality in primates: studies of living and extinct human and non-human primates ( Brockman D.K., van Schaik C.P., eds). Cambridge University Press, Cambridge, p. 307-350.
-
Jin T., Wang D.Z., Zhao Q., Yin L.J., Qin D.G., Ran W.Z., Pan W.S. (2009). Reproductive parameters of wild Trachypithecus leucocephalus: seasonality, infant mortality and interbirth interval. â Am. J. Primatol. 71: 558-566.
-
Jönsson K.I. (1997). Capital and income breeding as alternative tactics of resource use in reproduction. â Oikos 78: 57-66.
-
Knott C.D. (1997). Field collection and preservation of urine in orangutans and chimpanzees. â Trop. Biodivers. 4: 95-102.
-
Knott C.D. (2001). Female reproductive ecology of the apes: implications for human evolution. â In: Reproductive ecology and human evolution ( Ellison P., ed.). Aldine de Gruyter, New York, p. 429-463.
-
Knott C.D., Emery Thompson M., Wich S.A. (2009). The ecology of reproduction in wild orangutans. â In: Orangutans compared: ecology, evolution, behaviour and conservation ( Wich S.A., Utami S.S., Mitra Setia T., van Schaik C., eds). Oxford University Press, New York, NY, p. 171-188.
-
Lee P.C. (1987). Nutrition, fertility, and maternal investment in primates. â J. Zool. 213: 409-422.
-
Lee P.C. (1996). The meanings of weaning: growth, lactation, and life history. â Evol. Anthropol. 5: 87-98.
-
Lee P.C. (1999). Comparative ecology of postnatal growth and weaning among haplorhine primates. â In: Comparative primate socioecology ( Lee P.C., ed.). Cambridge University Press, Cambridge, p. 111-139.
-
Lee P.C., Majluf P., Gordon I.J. (1991). Growth, weaning and maternal investment from a comparative perspective. â J. Zool. 225: 99-114.
-
Leslie P.W., Fry P.H. (1989). Extreme seasonality of births among nomadic Turkana pastoralists. â Am. J. Phys. Anthropol. 79: 103-115.
-
Lovett J.C. (1996). Elevational and latitudinal changes in tree association and diversity in the Eastern Arc mountains of Tanzania. â J. Trop. Ecol. 12: 629-650.
-
Lovett J.C., Marshall A.R., Carr J. (2006). Changes in tropical forest vegetation along an altitudinal gradient in the Udzungwa Mountains National Park, Tanzania. â Afr. J. Ecol. 44: 478-490.
-
Martin P. (1984). The meaning of weaning. â Anim. Behav. 32: 1257-1259.
-
Martin P., Bateson P. (1993). Measuring behaviour: an introductory guide, 2nd edn. â Cambridge University Press, Cambridge.
-
McCabe G.M. (2011). Reproductive seasonality in relation to food availability in wild female Sanje mangabeys, Udzungwa Mountains National Park, Tanzania (abstract). â Am. J. Primatol. 73(S1): 104.
-
Miller K., Bales K., Ramos J., Dietz J. (2006). Energy intake, energy expenditure, and reproductive costs of female wild golden lion tamarins (Leontopithecus rosalia). â Am. J. Primatol. 68: 1037-1053.
-
Mittermeier R.A., Robles Gil P., Hoffmann M., Pilgrim J., Brooks T., Mittermeier C.G., Lamoreux J., da Fonseca G.A.B. (2004). Hotspots revisited. â CEMEX, Mexico City.
-
Moore S.E. (1998). Nutrition, immunity and the fetal and infant origins of disease hypothesis in developing countries. â Proc. Nutr. Soc. 57: 241-247.
-
Oi T. (1996). Sexual behavior and mating system of the wild pig-tailed macaque in West Sumatra. â In: Evolution and ecology of macaque societies ( Fa J.E., Lindburg D.G., eds). Oxford University Press, New York, NY, p. 342-368.
-
Paavola J. (2008). Livelihoods, vulnerability and adaptation to climate change in Morogoro, Tanzania. â Environm. Sci. Policy 11: 642-654.
-
Power M. (1999). Aspects of energy expenditure of callitrichid primates: physiology and behavior. â In: The non-human primates ( Dolhinow P., Fuentes A., eds). Mayfield, Mountain View, CA, p. 225-230.
-
Richard A.F., Dewar R.E., Schwartz M., Ratsirarson J. (2000). Mass change, environmental variability and female fertility in wild Propithecus verreauxi. â J. Hum. Evol. 39: 381-391.
-
Ridley M. (1986). The number of males in a primate troop. â Anim. Behav. 34: 1848-1858.
-
Rojansky N., Brzezinski A., Schenker J.G. (1992). Seasonality in human reproduction: an update. â Hum. Reprod. 7: 735-745.
-
Rosso P. (1990). Nutrition and metabolism in pregnancy. â Oxford University Press, New York, NY.
-
Rovero F., Marshall A.R., Jones T., Perkin A. (2009). The primates of the Udzungwa Mountains: diversity, ecology and conservation. â J. Anthropol. Sci. 87: 93-126.
-
Rowhani P., Lobell D.B., Linderman M., Ramankutty N. (2011). Climate variability and crop production in Tanzania. â Agr. Forest Meteorol. 151: 449-460.
-
Schneider M.L., Roughton E.C., Koehler A.J., Lubach G.R. (1999). Growth and development following prenatal stress exposure in primates: an examination of ontogenetic vulnerability. â Child Dev. 70: 263-274.
-
Sherry D.S., Ellison P.T. (2007). Potential applications of urinary C-peptide of insulin for comparative energetics research. â Am. J. Phys. Anthropol. 133: 771-778.
-
Stearns S.C. (1989). Trade-offs in life-history evolution. â Funct. Ecol. 3: 259-268.
-
Stearns S.C. (1992). The evolution of life histories. â Oxford University Press, New York, NY.
-
Strier K. (2001). Reproductive ecology of New World monkeys. â In: Reproductive ecology and human evolution ( Ellison P.T., ed.). Aldine Transaction, Edison, NJ, p. 351-368.
-
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). â Am. J. Primatol. 55: 87-100.
-
Struhsaker T.T., Marshall A.R., Detwiler K., Siex K., Ehardt C., Lisbjerg D.D., Butynski T.M. (2004). Demographic variation among Udzungwa red colobus in relation to gross ecological and sociological parameters. â Int. J. Primatol. 25: 615-658.
-
Taussky H.H. (1954). A microcolorimetric determination of creatine in urine by the Jaffe reaction. â J. Biol. Chem. 208: 853-862.
-
Tecot S. (2010). Itâs all in the timing: birth seasonality and infant survival in Eulemur rubriventer. â Int. J. Primatol. 31: 715-735.
-
Trivers R., Willard D.E. (1973). Natural selection of parental ability to vary the sex ratio of offspring. â Science 179: 90-92.
-
Ullrey D., Allen M., Ausman L., Conklin-Brittain N., Edwards M., Erwin J., Holick M., Hopkins D., Lewis S., Lonnerdal B., Rudel L. (2003). Nutritional requirements of non-human primates, 2nd revised edn. â National Research Council: Committee on Animal Nutrition. The National Academies Press, Washington, DC.
-
van Schaik C.P., van Noordwijk M.A. (1985). Interannual variability in fruit abundance and the reproductive seasonality in Sumatran long-tailed macaques (Macaca fascicularis). â J. Zool. 206: 533-549.
-
Visser M.E., Both C. (2005). Shifts in phenology due to global climate change: the need for a yardstick. â Proc. Roy. Soc. Lond. B: Biol. 272: 2561-2569.
-
Visser M.E., van Noordwijk A.J., Tinbergen J.M., Lessells C.M. (1998). Warmer springs lead to mistimed reproduction in great tits (Parus major). â Proc. Roy. Soc. Lond. B: Biol. 265: 1867-1870.
-
Vitzthum V.J. (2001). Why not so great is still good enough: flexible responsiveness in human reproductive functioning. â In: Reproductive ecology and human evolution ( Ellison P.T., ed.). Aldine Transaction, Edison, NJ, p. 179-202.
-
Walker S.E., Strasser M.E., Field L.P. (2004). Reproductive parameters and life-history variables in captive golden-bellied mangabeys (Cercocebus agilis chrysogaster). â Am. J. Primatol. 64: 123-131.
-
Widdowson E.M. (1977). Nutrition and lactation. â In: Nutritional disorders of American women ( Winick M., ed.). Wiley, New York, NY, p. 67-75.
-
Wieczkowski J., Kinnaird M. (2008). Shifting forest composition and primate diets: a 13-year comparison of the Tana River mangabey and its habitat. â Am. J. Primatol. 70: 339-348.
-
Wrangham R.W. (1980). An ecological model of female-bonded primate groups. â Behaviour 75: 262-300.
-
Zar J.H. (1999). Biostatistical analysis. â Prentice Hall, Upper Saddle River, NJ.
| å ¨é¨æé´ | è¿å»ä¸å¹´ | è¿å»30天 | |
|---|---|---|---|
| æè¦æµè§æ¬¡æ° | 783 | 76 | 5 |
| å ¨ææµè§æ¬¡æ° | 328 | 9 | 0 |
| PDFä¸è½½æ¬¡æ° | 116 | 5 | 0 |
Reproductive seasonality in wild Sanje mangabeys (Cercocebus sanjei), Tanzania: Relationship between the capital breeding strategy and infant survival
äºBehaviourbDepartment of Anthropology, University of Texas at San Antonio, San Antonio, TX 78249, USA
Search for other papers by Gráinne Michelle McCabe in
Current site
Google Scholar
PubMed
Search for other papers by Melissa Emery Thompson in
Current site
Google Scholar
PubMed
The reproductive seasonality model states that it is adaptive for species in seasonally variable environments to temporally cluster reproductive events around periods of resource availability. Many studies have examined links between seasonal reproduction and phenological events, though few studies have fully tested the adaptive hypothesis by examining the effects of reproductive timing on outcomes. Our study tests the predictions of the model in an African cercopithecine, the Sanje mangabey, by examining the impact of food availability on the timing of conception, birth and weaning, and the relationship of reproductive timing and female energy balance (urinary C-peptide) to infant survival. From September 2008 through 2010, 28 infants were born. Distribution of conceptions was non-uniform, with a peak between January and March. There was a significant positive correlation between mean monthly fruit availability and number of conceptions per month. An increased food supply supports a positive energy balance, maximizing the potential for conception; a pattern found among many cercopithecines. Mothers that conceived within the peak period also exhibited higher levels of urinary C-peptide during preconception and early gestation, compared to conceptions outside the peak period. This strategy increased the probability of survival to year one, as it was significantly higher for infants conceived during the peak conceptive season. These results support the reproductive seasonality model and demonstrate that the timing of conception is critical for mangabey reproductive success.
| å ¨é¨æé´ | è¿å»ä¸å¹´ | è¿å»30天 | |
|---|---|---|---|
| æè¦æµè§æ¬¡æ° | 783 | 76 | 5 |
| å ¨ææµè§æ¬¡æ° | 328 | 9 | 0 |
| PDFä¸è½½æ¬¡æ° | 116 | 5 | 0 |
