Abstract
The mother-offspring relationship is paramount in most mammals and infant survival often depends on maternal investment. In species with prolonged periods of development or co-residence, mothers may continue to influence their offspring’s outcomes beyond nutritional independence with benefits biased towards the philopatric sex. Chimpanzees (Pan troglodytes) are long-lived mammals with a protracted period of immaturity during which offspring continue to travel with their mothers. In contrast to most mammals, chimpanzees are also typically male philopatric. Here, we use over 50 years of demographic data from two communities in Gombe National Park, Tanzania, to examine the survival and longevity of both male and female chimpanzees that experienced maternal loss during three different age categories. Males who were orphaned between the ages of 0–4.99 years, 5–9.99 years, and 10–14.99 years all faced significantly lower survival than non-orphans and died earlier than expected. Females faced similarly reduced survival probabilities when orphaned between 0–4.99 and 5–9.99 years of age; however, females who experienced maternal loss between 10 and 14.99 years of age were no more likely to die than non-orphans. Females orphaned in this later age class also lived significantly longer beyond maternal loss than their male counterparts. As observed in other mammals, philopatric male chimpanzees may continue to benefit from their mother’s ecological knowledge, whereas maternal influence on female offspring likely fades as they prepare to emigrate. These results emphasize how maternal influence on offspring outcomes can extend well beyond weaning, particularly for the philopatric sex.
Significance statement
Mammalian mothers are crucial to their infant’s survival and in species where offspring continue to live with their mothers after weaning, maternal influence may extend beyond dependence on mother’s milk. While in most group-living mammals females remain in their natal group, chimpanzees typically display the opposite pattern with males residing alongside their mothers into adulthood. Using over 50 years of data on wild chimpanzees, we investigated the consequences of maternal loss both before and after weaning. We found that both males and females orphaned up to 10 years of age were less likely to survive than non-orphans; however, only males orphaned between 10 and 15 years also faced lower survival. These results emphasize how chimpanzee mothers continue to matter for offspring beyond infancy and provide novel data on reduced maternal influence on survival for daughters compared to sons.
Similar content being viewed by others
Explore related subjects
Discover the latest articles, news and stories from top researchers in related subjects.Data availability
The data analyzed during the current study are available in supplementary material: Online Resource 2.
References
Alberts SC, Altmann J, Brockman DK, Cords M, Fedigan LM, Pusey AE, Stoinski T, Strier KB, Morris WF, Bronikowski AM (2013) Reproductive aging patterns in primates reveal that humans are distinct. P Natl Acad Sci USA 110:13440–13445. https://doi.org/10.1073/pnas.1311857110
Allison PD (2010) Survival analysis using SAS: a practical guide, 2nd edn. SAS Institute, Cary, NC
Altmann J (1980) Baboon mothers and infants. Harvard University Press, Cambridge, MA
Altmann J, Alberts SC (2005) Growth rates in a wild primate population: ecological influences and maternal effects. Behav Ecol Sociobiol 57:490–501. https://doi.org/10.1007/s00265-004-0870-x
Andres D, Clutton-Brock TH, Kruuk LEB, Pemberton JM, Stopher KV, Ruckstuhl KE (2013) Sex differences in the consequences of maternal loss in a long-lived mammal, the red deer (Cervus elaphus). Behav Ecol Sociobiol 67:1249–1258. https://doi.org/10.1007/s00265-013-1552-3
Archie E, Tung J, Clark M, Altmann J, Alberts SC (2014) Social affiliation matters: both same-sex and opposite-sex relationships predict survival in wild female baboons. Proc R Soc B 281:20141261. https://doi.org/10.1098/rspb.2014.1261
Berkman LF, Melchior M, Chastang JF, Niedhammer I, Leclerc A, Goldberg M (2004) Social integration and mortality: a prospective study of French employees of Electricity of France-Gas of France: the GAZEL Cohort. Am J Epidemiol 159:167–174. https://doi.org/10.1093/aje/kwh020
Boesch C, Boesh-Achermann H (2000) The chimpanzees of the Taï forest: behavioural ecology and evolution. Oxford University Press, Oxford
Boesch C, Bole C, Eckhardt N, Boesch H (2010) Altruism in forest chimpanzees: the case of adoption. PLoS One 5:e8901. https://doi.org/10.1371/journal.pone.0008901
Botero M, Macdonald SE, Miller RS (2013) Anxiety-related behavior of orphan chimpanzees (Pan troglodytes schweinfurthii) at Gombe National Park, Tanzania. Primates 54:21–26. https://doi.org/10.1007/s10329-012-0327-1
Bray J, Emery Thompson M, Muller MN, Wrangham RW, Machanda ZP (2018) The development of feeding behavior in wild chimpanzees (Pan troglodytes schweinfurthii). Am J Phys Anthropol 165:34–46. https://doi.org/10.1002/ajpa.23325
Brent LJN, Franks DW, Cant MA, Croft DP (2015) Ecological knowledge, leadership, and the evolution of menopause in killer whales. Curr Biol 25:1–5. https://doi.org/10.1016/j.cub.2015.01.037
Bronikowski AM, Cords M, Alberts SC, Altmann J, Brockman DK, Fedigan LM, Pusey AE, Stoinski T, Strier KB, Morris WF (2016) Female and male life tables for seven wild primate species. Sci Data 3:160006. https://doi.org/10.1038/sdata.2016.6
Cameron EZ, Setsaas TH, Linklater WL (2009) Social bonds between unrelated females increase reproductive success in feral horses. P Natl Acad Sci USA 106:13850–13853. https://doi.org/10.1073/pnas.0900639106
Cheney DL (1977) The acquisition of rank and the development of reciprocal alliances among free-ranging immature baboons. Behav Ecol Sociobiol 2:303–318. https://doi.org/10.1007/BF00299742
Clark C (1977) A preliminary report on weaning among chimpanzees of the Gombe National Park, Tanzania. In: Chevalier-Skolinkoff S, Poirer F (eds) Primate biosocial development: biological, social and ecological determinants. Garland, New York, pp 235–260
Clutton-Brock TH (1991) The evolution of parental care. Princeton University Press, Princeton
Conklin-Brittain NL, Knott CD, Wrangham RW (2001) The feeding ecology of apes. In: The apes: challenges for the 21st century. Conference Proceedings of the Brookfield Zoo. Chicago Zoological Society, Brookfield, II, pp 167–174
Croft DP, Brent LJN, Franks DW, Cant MA (2015) The evolution of prolonged life after reproduction. Trends Ecol Evol 30:407–416. https://doi.org/10.1016/j.tree.2015.04.011
East ML, Höner OP, Wachter B, Wilhelm K, Burke T, Hofer H (2009) Maternal effects on offspring social status in spotted hyenas. Behav Ecol 20:478–483. https://doi.org/10.1093/beheco/arp020
Emery Thompson M, Jones JH, Pusey AE, Brewer-Marsden S, Goodall J, Marsden D, Matsuzawa T, Nishida T, Reynolds V, Sugiyama Y, Wrangham RW (2007) Aging and fertility patterns in wild chimpanzees provide insights into the evolution of menopause. Curr Biol 17:2150–2156. https://doi.org/10.1016/j.cub.2007.11.033
Engh AL, Beehner JC, Bergman TJ, Whitten PL, Hoffmeier RR, Seyfarth RM, Cheney DL (2006) Behavioural and hormonal responses to predation in female chacma baboons (Papio hamadryas ursinus). Proc R Soc Lond B 273:707–712. https://doi.org/10.1098/rspb.2005.3378
Fairbanks L (2000) Maternal investment throughout the life span. In: Whitehead P, Jolly C (eds) Old World monkeys. Cambridge University Press, Cambridge, pp 341–367
Foerster S, Franz M, Murray CM, Gilby IC, Feldblum JT, Walker KK, Pusey AE (2016a) Chimpanzee females queue but males compete for social status. Sci Rep 6:35404. https://doi.org/10.1038/srep35404
Foerster S, Zhong Y, Pintea L, Carson CM, Wilson ML, Mjungu DC, Pusey AE (2016b) Feeding habitat quality and behavioral trade-offs in chimpanzees: a case for species distribution models. Behav Ecol 27:1004–1016. https://doi.org/10.1093/beheco/arw004
Foley C, Pettorelli N, Foley L (2008) Severe drought and calf survival in elephants. Biol Lett 4:541–544. https://doi.org/10.1098/rsbl.2008.0370
Foster EA, Franks DW, Mazzi S, Darden SK, Balcomb KC, Ford JKB, Croft DP (2012) Adaptive prolonged postreproductive life span in killer whales. Science 337:1313. https://doi.org/10.1126/science.1224198
Frère CH, Krützen M, Mann J, Connor RC, Bejder L, Sherwin WB (2010) Social and genetic interactions drive fitness variation in a free-living dolphin population. P Natl Acad Sci USA 107:19949–19954. https://doi.org/10.1073/pnas.1007997107
Greenwood PJ (1980) Mating systems, philopatry and dispersal in birds and mammals. Anim Behav 28:1140–1162
Goldenberg SZ, Wittemyer G (2017) Orphaned female elephant social bonds reflect lack of access to mature adults. Sci Rep 7:14408. https://doi.org/10.1038/s41598-017-14712-2
Goldenberg SZ, Wittemyer G (2018) Orphaning and natal group dispersal are associated with social costs in female elephants. Anim Behav 143:1–8. https://doi.org/10.1016/j.anbehav.2018.07.002
Goodall J (1986) The chimpanzees of Gombe: patterns of behavior. Harvard University Press, Cambridge, MA
Harlow HF, Dodsworth RO, Harlow MK (1965) Total social isolation in monkeys. P Natl Acad Sci USA 54:90–97
Hill K, Boesch C, Goodall J, Pusey A, Williams J, Wrangham R (2001) Mortality rates among wild chimpanzees. J Hum Evol 40:437–450. https://doi.org/10.1006/jhev.2001.0469
Hobaiter C, Schel AM, Langergraber K, Zuberbühler K (2014) “Adoption” by maternal siblings in wild chimpanzees. PLoS One 9:e103777. https://doi.org/10.1371/journal.pone.0103777
Holand Ø, Weladji RB, Mysterud A, Røed K, Reimers E, Nieminen M (2012) Induced orphaning reveals post-weaning maternal care in reindeer. Eur J Wildlife Res 58:589–596. https://doi.org/10.1007/s10344-012-0608-4
Holt-Lunstad J, Smith TB, Layton JB (2010) Social relationships and mortality risk: a meta-analytic review. PLoS Med 7:e1000316. https://doi.org/10.1371/journal.pmed.1000316
Horrocks J, Hunte W (1983) Maternal rank and offspring rank in vervet monkeys: an appraisal of the mechanisms of rank acquisition. Anim Behav 31:772–782
Hothorn T, Hornik K, van de Wiel MA, Zeileis A (2008) Implementing a class of permutation tests: J Stat Softw 28:1-23. doi:https://doi.org/10.18637/jss.v028.i08
Kahlenberg SM, Thompson ME, Muller MN, Wrangham RW (2008) Immigration costs for female chimpanzees and male protection as an immigrant counterstrategy to intrasexual aggression. Anim Behav 76:1497–1509. https://doi.org/10.1016/j.anbehav.2008.05.029
Kalcher-Sommersguter E, Preuschoft S, Franz-Schaider C, Hemelrijk CK, Crailsheim K, Massen JJM (2015) Early maternal loss affects social integration of chimpanzees throughout their lifetime. Sci Rep 5:16439. https://doi.org/10.1038/srep16439
Kruuk H (1972) The spotted hyena: a study of predation and social behavior. The University of Chicago Press, Chicago
Langergraber K, Mitani J, Vigilant L (2009) Kinship and social bonds in female chimpanzees (Pan troglodytes). Am J Primatol 71:840–851. https://doi.org/10.1002/ajp.20711
Lee P, Oliver J (1979) Competition, dominance and the acquisition of rank in juvenile yellow baboons (Papio cyanocephalus). Anim Behav 27:576–585
Lee PC, Fishlock V, Webber CE, Moss CJ (2016) The reproductive advantages of a long life: longevity and senescence in wild female African elephants. Behav Ecol Sociobiol 70:337–345. https://doi.org/10.1007/s00265-015-2051-5
Lonsdorf EV (2012) The role of mothers in the development of complex skills in chimpanzees. In: Clancy KBH, Hinde K, Rutherford JN (eds) Building babies: primate development in proximate and ultimate perspective. Springer New York, New York, NY, pp 303–318
Lonsdorf EV, Ross SR (2012) Socialization and development of behavior. In: Palombit RA, Mitani JC, Call J (eds) The evolution of primate societies. The University of Chicago Press, Chicago, pp 245–268
Lonsdorf EV, Stanton MA, Pusey AE, Murray CM (2019) Sources of variation in weaned age among wild chimpanzees in Gombe National Park, Tanzania. Am J Phys Anthropol (published online, doi:https://doi.org/10.1002/ajpa.23986)
Maestripieri D (2018) Maternal influences on primate social development. Behav Ecol Sociobiol 72:130–112. https://doi.org/10.1007/s00265-018-2547-x
Maestripieri D, Mateo JM (eds) (2009) Maternal effects in mammals. The University of Chicago Press, Chicago
Markham AC, Lonsdorf EV, Pusey AE, Murray CM (2015) Maternal rank influences the outcome of aggressive interactions between immature chimpanzees. Anim Behav 100:192–198. https://doi.org/10.1016/j.anbehav.2014.12.003
Matsumoto T (2017) Developmental changes in feeding behaviors of infant chimpanzees at Mahale, Tanzania: implications for nutritional independence long before cessation of nipple contact. Am J Phys Anthropol 163:356–366. https://doi.org/10.1002/ajpa.23212
McComb K, Moss C, Durant SM, Baker L, Sayialel S (2001) Matriarchs as repositories of social knowledge in African elephants. Science 292:491–494. https://doi.org/10.1126/science.1057895
Mitani JC (2009) Cooperation and competition in chimpanzees: current understanding and future challenges. Evol Anthropol 18:215–227. https://doi.org/10.1002/evan.20229
Muller MN, Wrangham RW (2014) Mortality rates among Kanyawara chimpanzees. J Hum Evol 66:107–114. https://doi.org/10.1016/j.jhevol.2013.10.004
Murray CM, Gilby IC, Mane SV, Pusey AE (2008) Adult male chimpanzees inherit maternal ranging patterns. Curr Biol 18:20–24. https://doi.org/10.1016/j.cub.2007.11.044
Nakamura M, Hayaki H, Hosaka K, Itoh N, Zamma K (2014) Brief communication: orphaned male chimpanzees die young even after weaning. Am J Phys Anthropol 153:139–143. https://doi.org/10.1002/ajpa.22411
Nakamura M, Hosaka K (2015) Orphans and allomothering. In: Nakamura M, Hosaka K, Itoh N, Zamma K (eds) Mahale chimpanzees: 50 years of research. Cambridge University Press, Cambridge, pp 421–432
Nishida T (1968) The social group of wild chimpanzees in the Mahali mountains. Primates 9:167–224
Nishida T, Corp N, Hamai M, Hasegawa T, Hiraiwa-Hasegawa M, Hosaka K, Hunt KD, Itoh N, Kawanaka K, Matsumoto-Oda A, Mitani JC, Nakamura M, Norikoshi K, Sakamaki T, Turner L, Uehara S, Zamma K (2003) Demography, female life history, and reproductive profiles among the chimpanzees of Mahale. Am J Primatol 59:99–121. https://doi.org/10.1002/ajp.10068
Nowak R, Porter RH, Lévy F, Orgeur P, Schaal B (2000) Role of mother-young interactions in the survival of offspring in domestic mammals. Rev Reprod 5:153–163. https://doi.org/10.1530/ror.0.0050153
Nunez C, Aldeman J, Rubenstein D (2015) Sociality increases juvenile survival after a catastrophic event in the feral horse (Equus caballus). Behav Ecol 26:138–147. https://doi.org/10.1093/beheco/aru163
Pintea L (2007) Applying remote sensing and GIS for chimpanzee habitat changedetection, behaviour, and conservation. University of Minnesota, PhD Dissertation
Pusey AE (1979) Intercommunity transfer of chimpanzees in Gombe National Park. In: Hamburg D, McCown E (eds) The great apes. Benjamin-Cummings, Menlo Park, pp 464–479
Pusey AE (1983) Mother-offspring relationships in chimpanzees after weaning. Anim Behav 31:363–377
Pusey A (1990) Behavioural changes at adolescence in chimpanzees. Behaviour 115:203–246
Pusey A, Oehlert G, Williams J (2005) Influence of ecological and social factors on body mass of wild chimpanzees. Int J Primatol 26:2–31. https://doi.org/10.1007/s10764-005-0721-2
Pusey A, Schroepfer-Walker K (2013) Female competition in chimpanzees. Phil Trans R Soc B 368:20130077. https://doi.org/10.1098/rstb.2013.0077
Pusey A, Williams J, Goodall J (1997) The influence of dominance rank on the reproductive success of female chimpanzees. Science 277:828–831. https://doi.org/10.1126/science.277.5327.828
R Core Team (2019) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria http://www.R-project.org
Reddy RB, Mitani JC (2019) Social relationships and caregiving behavior between recently orphaned chimpanzee siblings. Primates (published online, doi:https://doi.org/10.1007/s10329-019-00732-1)
Schülke O, Bhagavatula J, Vigilant L, Ostner J (2010) Social bonds enhance reproductive success in male macaques. Curr Biol 20:2207–2210. https://doi.org/10.1016/j.cub.2010.10.058
Silk JB (2007) The adaptive value of sociality in mammalian groups. Phil Trans R Soc B 362:539–559. https://doi.org/10.1098/rstb.2006.1994
Silk JB, Alberts SC, Altmann J (2003) Social bonds of female baboons enhance infant survival. Science 302:1231–1234. https://doi.org/10.1126/science.1088580
Silk JB, Beehner JC, Bergman TJ, Crockford C, Engh AL, Moscovice LR, Wittig RM, Seyfarth RM, Cheney DL (2009) The benefits of social capital: close social bonds among female baboons enhance offspring survival. Proc R Soc Lond B 276:3099–3104. https://doi.org/10.1098/rspb.2009.0681
Silk JB, Beehner JC, Bergman TJ, Crockford C, Engh AL, Moscovice LR, Wittig RM, Seyfarth RM, Cheney DL (2010) Strong and consistent social bonds enhance the longevity of female baboons. Curr Biol 20:1359–1361. https://doi.org/10.1016/j.cub.2010.05.067
Stanton MA, Lonsdorf EV, Pusey AE, Murray CM (2017) Do juveniles help or hinder? Influence of juvenile offspring on maternal behavior and reproductive outcomes in wild chimpanzees (Pan troglodytes). J Hum Evol 111:152–162. https://doi.org/10.1016/j.jhevol.2017.07.012
Stanton MA, Mann J (2012) Early social networks predict survival in wild bottlenose dolphins. PLoS One 7:e47508. https://doi.org/10.1371/journal.pone.0047508
Strier KB, Altmann J, Brockman DK, Bronikowski AM, Cords M, Fedigan LM, Lapp H, Liu X, Morris WF, Pusey AE, Stoinski TS, Alberts SC (2010) The Primate Life History Database: a unique shared ecological data resource. Methods Ecol Evol 1:199–211. https://doi.org/10.1111/j.2041-210X.2010.00023.x
Stumpf RM, Thompson ME, Muller MN, Wrangham RW (2009) The context of female dispersal in Kanyawara chimpanzees. Behaviour 146:629–656
Suomi SJ (1997) Early determinants of behaviour: evidence from primate studies. Brit Med Bull 53:170–184. https://doi.org/10.1093/oxfordjournals.bmb.a011598
Surbeck M, Boesch C, Crockford C, Thompson ME, Furuichi T, Fruth B, Hohmann G, Ishizuka S, Machanda Z, Muller MN, Pusey A, Sakamaki T, Tokuyama N, Walker K, Wrangham R, Wroblewski E, Zuberbühler K, Vigilant L, Langergraber K (2019) Males with a mother living in their group have higher paternity success in bonobos but not chimpanzees. Curr Biol 29:R354–R355. https://doi.org/10.1016/j.cub.2019.03.040
Surbeck M, Mundry R, Hohmann G (2011) Mothers matter! Maternal support, dominance status and mating success in male bonobos (Pan paniscus). Proc R Soc Lond B 278:590–598. https://doi.org/10.1098/rspb.2010.1572
Therneau T (2015) A package for survival analysis in S, version 2.38, https://CRAN.R-project.org/package=survival
Tung J, Archie EA, Altmann J, Alberts SC (2016) Cumulative early life adversity predicts longevity in wild baboons. Nat Commun 7:11181. https://doi.org/10.1038/ncomms11181
van de Rijt-Plooij H, Plooij F (1987) Growing independence, conflict and learning in mother-infant relations in free-ranging chimpanzees. Behaviour 101:1–86
van Leeuwen EJC, Mulenga IC, Chidester DL (2013) Early social deprivation negatively affects social skill acquisition in chimpanzees (Pan troglodytes). Anim Cogn 17:407–414. https://doi.org/10.1007/s10071-013-0672-5
van Noordwijk MA (2012) From maternal investment to lifetime maternal care. In: Mitani J, Call J, Kappeler PM, Palombit RA, Silk JB (eds) Evolution of primate societies. The University of Chicago Press, Chicago, pp 321–342
Walker KK, Pusey AE (in press) Inbreeding risk and maternal support have opposite effects on female chimpanzee dispersal. Curr Biol
Walker KK, Walker CS, Goodall J, Pusey AE (2018) Maturation is prolonged and variable in female chimpanzees. J Hum Evol 114:131–140. https://doi.org/10.1016/j.jhevol.2017.10.010
Wallis J (1997) A survey of reproductive parameters in the free-ranging chimpanzees of Gombe National Park. J Reprod Fertil 109:297–307. https://doi.org/10.1530/jrf.0.1090297
Watts D, Pusey A (2002) Behavior of juvenile and adolescent great apes. In: Pereira M, Fairbanks L (eds) Juvenile primates: life history, development, and behavior. University of Chicago Press, Chicago, pp 148–167
Watts HE, Tanner JB, Lundrigan BL, Holekamp KE (2009) Post-weaning maternal effects and the evolution of female dominance in the spotted hyena. Proc R Soc Lond B 276:2291–2298. https://doi.org/10.1098/rspb.2009.0268
Wood BM, Watts DP, Mitani JC, Langergraber KE (2017) Favorable ecological circumstances promote life expectancy in chimpanzees similar to that of human hunter-gatherers. J Hum Evol 105:41–56. https://doi.org/10.1016/j.jhevol.2017.01.003
Wroblewski EE (2008) An unusual incident of adoption in a wild chimpanzee (Pan troglodytes) population at Gombe National Park. Am J Primatol 70:995–998. https://doi.org/10.1002/ajp.20582
Wroblewski EE, Murray CM, Keele B, Schumacher-Stankey JC, Hahn BH, Pusey AE (2009) Male dominance rank and reproductive success in chimpanzees, Pan troglodytes schweinfurthii. Anim Behav 77:873–885. https://doi.org/10.1016/j.anbehav.2008.12.014
Zipple MN, Archie EA, Tung J, Altmann J, Alberts SC (2019) Intergenerational effects of early adversity on survival in wild baboons. eLife 8:e47433. https://doi.org/10.7554/eLife.47433
Acknowledgments
We thank the Jane Goodall Institute for their continued support of research at Gombe with special thanks to Dr. Jane Goodall for initiating research at Gombe. We are also extremely grateful to the Gombe Stream Research Centre staff, the Government of Tanzania, Tanzania National Parks, Tanzania Commission for Science and Technology, and Tanzania Wildlife Research Institute for their continued support of and permission to conduct this project. We also thank the numerous researchers and assistants who participated in long-term data entry and maintenance, as well as the associate editor and three anonymous reviewers for their comments on this manuscript.
Funding
This research was supported by the Jane Goodall Institute funding of data collection at Gombe. Additional funding support was provided by the National Science Foundation grants DBS-9021946, SBR-9319909, BCS-0452315, IOS-LTREB-1052693, the National Institutes of Health grant R01 AI 058715, Harris Steel, University of Minnesota, and Duke University.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflicts of interest.
Ethical approval
All applicable international, national, and institutional guidelines for the use of animals were followed. Permission to conduct data collection at Gombe National Park was granted and approved by all applicable governing bodies in Tanzania, including Tanzania National Parks, the Tanzanian Wildlife Research Institute, and the Tanzanian Commission for Science and Technology.
Additional information
Communicated by M. A van Noordwijk
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Stanton, M.A., Lonsdorf, E.V., Murray, C.M. et al. Consequences of maternal loss before and after weaning in male and female wild chimpanzees. Behav Ecol Sociobiol 74, 22 (2020). https://doi.org/10.1007/s00265-020-2804-7
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00265-020-2804-7