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Children of divorce: effects of adult replacements on previous offspring in Argentinean owl monkeys

Behavioral Ecology and Sociobiology volume 66, pages 505–517 (2012)Cite this article

Abstract

According to the Evolutionary Theory of the Family, the replacement of one pair-member by an intruder may have profound consequences for the existing offspring. Step-parents are expected to provide less care towards unrelated immatures than to genetic offspring, unless caring also serves as a mating strategy. Furthermore, because an intruder will be a potential mate for opposite-sexed offspring, relationships between offspring and same-sex parents are predicted to deteriorate. To test these predictions, we studied an Azara’s owl monkey (Aotus azarai) population in Argentina exhibiting serial monogamy and bi-parental care. Since 1997, we have collected demographic data from ca. 25 groups and inter-individual distance data from ca. 150 marked individuals. First, we compared survival and dispersal age of immatures in groups with and without replacements to investigate whether parental care serves as a mating strategy. Second, we compared sex-specific age at dispersal for groups with replacement of opposite-sex parents, same-sex parents, or in stable groups in order to test whether relationships between offspring and same-sex parents deteriorated after the replacement of the other parent. Survival and dispersal ages were not negatively associated with replacements, suggesting that male care might serve, at least partly, as a mating strategy. The time lag between a replacement and the subsequent dispersal of female offspring was greater if the intruder was a male, while the offspring and same-sex parents were less often nearest neighbors after replacements than before. Our results suggest that family disruption through the replacement of a parent is not associated with decreased offspring survival or early dispersion of juveniles, but deteriorates parent–offspring relationships.

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References

  • Achenbach GG, Snowdon CT (2002) Costs of caregiving: weight loss in captive adult male cotton-top tamarins (Saguinus oedipus) following the birth of infants. Int J Primatol 23:179–189

    PubMed  Article  Google Scholar 

  • Aktipis CA, Fernandez-Duque E (2011) Parental investment without kin recognition: simple conditional rules for parent–offspring behavior. Behav Ecol Sociobiol 65:1079–1091

    Article  Google Scholar 

  • Allison TM, Wilhelm SI, Cameron-MacMillan ML, Walsh CJ, Storey AE (2005) Divorce in common murres (Uria aalge): relationship to parental quality. Behav Ecol Sociobiol 57:224–230

    Article  Google Scholar 

  • Alvergne A, Faurie C, Raymond M (2008) Developmental plasticity of human reproductive development: effects of early family environment in modern-day France. Physiol Behav 95:625–632

    PubMed  Article  CAS  Google Scholar 

  • Anderson KG, Kaplan H, Lam D, Lancaster J (1999a) Paternal care by genetic fathers and stepfathers II: reports by Xhosa high school students. Evol Hum Behav 20:433–451

    Article  Google Scholar 

  • Anderson KG, Kaplan H, Lancaster J (1999b) Paternal care by genetic fathers and stepfathers I: reports from Albuquerque men. Evol Hum Behav 20:405–431

    Article  Google Scholar 

  • Aquino R, Encarnación F (1986) Population structure of Aotus nancymai (Cebidae: Primates) in Peruvian Amazon lowland forest. Am J Primatol 11:1–7

    Article  Google Scholar 

  • Austad SN, Rabenold KN (1986) Demography and the evolution of cooperative breeding in the bicolored wren, Campylorhynchus griseus. Behaviour 97:308–324

    Article  Google Scholar 

  • Babb P, Fernandez-Duque E, Schurr T (2010) AVPR1A sequence variation in monogamous owl monkeys (Aotus azarai) and its implications for the evolution of Platyrrhine social behavior. J Mol Evol 71:279–297

    PubMed  Article  CAS  Google Scholar 

  • Babb PL, Fernandez-Duque E, Baiduc CA, Gagneux P, Evans S, Schurr TG (2011a) MtDNA diversity in Azara’s owl monkeys (Aotus azarai azarai) of the Argentinean Chaco. Am J Phys Anthropol 146:209–224

    PubMed  Article  Google Scholar 

  • Babb PL, McIntosh AM, Fernandez-Duque E, Di Fiore A, Schurr TG (2011b) An optimized microsatellite genotyping strategy for assessing genetic identity and kinship in Azara’s owl monkeys (Aotus azarai). Folia Primatol 82:107–117

    PubMed  Article  Google Scholar 

  • Boggess J (1980) Intermale relations and troop male membership changes in langurs Presbytis entellus in Nepal. Int J Primatol 1:233–274

    Article  Google Scholar 

  • Brant CL, Schwab TM, Vandenbergh JG, Schaefer RL, Solomon NG (1998) Behavioural suppression of female pine voles after replacement of the breeding male. Anim Behav 55:615–627

    PubMed  Article  Google Scholar 

  • Brockelmann WY, Reichard U, Treesucon U, Raemaekers JJ (1998) Dispersal, pair formation and social structure in gibbons (Hylobates lar). Behav Ecol Sociobiol 42:329–339

    Article  Google Scholar 

  • Brown AD, Zunino GE (1994) Hábitat, densidad y problemas de conservación de los primates en Argentina. Vida Silv Neotrop 3:30–40

    Google Scholar 

  • Caine NG (1993) Flexibility and co-operation as unifying themes in Saguinus social organization and behaviour: the role of predation pressures. In: Rylands A (ed) Marmosets and tamarins. Systematics, behaviour, and ecology. Oxford Science, Oxford, pp 200–219

    Google Scholar 

  • Charpentier MJE, Van Horn RC, Altmann J, Alberts SC (2008) Paternal effects on offspring fitness in a multimale primate society. Proc Natl Acad Sci USA 105:1988–1992

    PubMed  Article  CAS  Google Scholar 

  • Choudhury S (1995) Divorce in birds: a review of the hypotheses. Anim Behav 50:413–429

    Article  Google Scholar 

  • Clutton-Brock TH (1989) Mammalian mating systems. Proc Roy Soc Lond B 236:339–372

    Article  CAS  Google Scholar 

  • Cords M (1997) Friendship, alliances, reciprocity and repair. In: Whiten A, Byrne R (eds) Machiavellian intelligence II. Cambridge University Press, Cambridge, pp 24–49

    Chapter  Google Scholar 

  • Crawley MJ (2007) The R book. Wiley, Chichester

    Book  Google Scholar 

  • Daly M, Wilson M (1999) Stepparental investment. Evol Hum Behav 20:365–366

    Article  Google Scholar 

  • Eikenaar C, Richardson DS, Brouwer L, Komdeur J (2007) Parent presence, delayed dispersal, and territory acquisition in the Seychelles warbler. Behav Ecol 18:874–879

    Article  Google Scholar 

  • Emlen ST (1995) An evolutionary theory of the family. Proc Natl Acad Sci USA 92:8092–8099

    PubMed  Article  CAS  Google Scholar 

  • Emlen ST (1997) Predicting family dynamics in social vertebrates. In: Krebs JR, Davies NB (eds) Behavioural ecology—an evolutionary approach, 4th edn. Blackwell, Oxford, pp 228–253

    Google Scholar 

  • Erkert HG, Cramer B (2006) Chronobiological background to cathemerality: circadian rhythms in Eulemur fulvus albifrons (Prosimii) and Aotus azarai boliviensis (Anthropoidea). Folia Primatol 77:87–103

    PubMed  Article  Google Scholar 

  • Fedigan LM (2003) Impact of male takeovers on infant deaths, births, and conceptions in Ceubus capucinus at Santa Rosa, Costa Rica. Int J Primatol 24:723–741

    Article  Google Scholar 

  • Fernandez-Duque E (2002) Environmental determinants of birth seasonality in night monkeys (Aotus azarai) of the Argentinian Chaco. Int J Primatol 23:639–656

    Article  Google Scholar 

  • Fernandez-Duque E (2009) Natal dispersal in monogamous owl monkeys (Aotus azarai) of the Argentinean Chaco. Behaviour 146:583–606

    Article  Google Scholar 

  • Fernandez-Duque E (2011a) Aotinae: social monogamy in the only nocturnal anthropoid. In: Campbell CJ, Fuentes A, MacKinnon KC, Bearder SK, Stumpf R (eds) Primates in perspective, 2nd edn. Oxford University Press, Oxford, pp 139–154

    Google Scholar 

  • Fernandez-Duque E (2011b) Rensch’s rule, Bergmann’s effect and adult sexual dimorphism in wild monogamous owl monkeys (Aotus azarai) of Argentina. Am J Phys Anthropol 146:38–48

    PubMed  Article  Google Scholar 

  • Fernandez-Duque E, Erkert HG (2006) Cathemerality and lunar periodicity of activity rhythms in owl monkeys of the Argentinian Chaco. Folia Primatol 77:123–138

    PubMed  Article  Google Scholar 

  • Fernandez-Duque E, Rotundo M (2003) Field methods for capturing and marking azarai night monkeys. Int J Primatol 24:1113–1120

    Article  Google Scholar 

  • Fernandez-Duque E, Rotundo M, Sloan C (2001) Density and population structure of owl monkeys (Aotus azarai) in the Argentinean Chaco. Am J Primatol 53:99–108

    PubMed  Article  CAS  Google Scholar 

  • Fernandez-Duque E, Juárez CP, Di Fiore A (2008) Adult male replacement and subsequent infant care by male and siblings in socially monogamous owl monkeys (Aotus azarai). Primates 49:81–84

    PubMed  Article  Google Scholar 

  • Fernandez-Duque E, Valeggia CR, Mendoza SP (2009) The biology of paternal care in human and nonhuman primates. Annu Rev Anthropol 38:115–130

    Article  Google Scholar 

  • Fernandez-Duque E, de la Iglesia H, Erkert HG (2010) Moonstruck primates: owl monkeys (Aotus) need moonlight for nocturnal activity in their natural environment. PLoS One 5:e12572

    PubMed  Article  Google Scholar 

  • Fernández-Gil A, Swenson JE, Granda C, Pérez T, Domínguez A, Ordiz A, Naves J, Delibes M (2010) Evidence of sexually selected infanticide in an endangered brown bear population. Anim Behav 79:521–527

    Article  Google Scholar 

  • Gubernick DJ, Teferi T (2000) Adaptive significance of male parental care in a monogamous mammal. Proc Roy Soc Lond B 267:147–150

    Article  CAS  Google Scholar 

  • Hannon SJ, Mumme RL, Koenig WD, Pitelka FA (1985) Replacement of breeders and within-group conflict in the cooperatively breeding acorn woodpecker. Behav Ecol Sociobiol 17:303–312

    Article  Google Scholar 

  • Härdling R, Kaitala A (2004) Male brood care without paternity increases mating success. Behav Ecol 15:715–721

    Article  Google Scholar 

  • Hendrichs H (1978) Die soziale organisation von Säugetierpopulationen. Säugetierkd Mitt 26:81–116

    Google Scholar 

  • Hrdy SB (1974) Male–male competition and infanticide among the langurs (Presbytis entellus) of Abu, Rajasthan. Folia Primatol 22:19–58

    PubMed  Article  CAS  Google Scholar 

  • Huck M, Fernandez-Duque E (2011) Building babies when dads help: infant development of owl monkeys and other primates with allo-maternal care. In: Clancy K, Hinde K, Rutherford J (eds) Building babies: primate development in proximate and ultimate perspective. Springer, Heidelberg

  • Huck M, Löttker P, Heymann EW (2004) Proximate mechanisms of reproductive monopolization in male moustached tamarins (Saguinus mystax). Am J Primatol 64:39–56

    PubMed  Article  Google Scholar 

  • Huck M, Rotundo M, Fernandez-Duque E (2011) Growth and development in wild owl monkeys (Aotus azarai) of Argentina. Int J Primatol 32:1133–1152

    Article  Google Scholar 

  • Jack KM, Fedigan L (2004) Male dispersal patterns in white-faced capuchins, Cebus capucinus—part 1: patterns and causes of natal emigration. Anim Behav 67:761–769

    Article  Google Scholar 

  • Jantschke B, Welker C, Klaiber-Schuh A (1998) Rearing without paternal help in the Bolivian owl monkey Aotus azarae boliviensis: a case study. Folia Primatol 69:115–120

    Article  Google Scholar 

  • Jeschke J, Kokko H (2008) Mortality and other determinants of bird divorce rate. Behav Ecol Sociobiol 63:1–9

    Article  Google Scholar 

  • Juárez CP, Rotundo MA, Berg W, Fernández-Duque E (2011) Costs and benefits of radio-collaring on the behavior, demography and conservation of owl monkeys (Aotus azarai) in Formosa, Argentina. Int J Primatol 32:69–82

    Article  Google Scholar 

  • Keddy Hector AC, Seyfarth RM, Raleigh MJ (1989) Male parental care, female choice and the effect of an audience in vervet monkeys. Anim Behav 38:262–271

    Article  Google Scholar 

  • Kent JP (1992) Maternal aggression and inter-individual distance in the broody hen (Gallus gallus). Behav Process 27:37–43

    Article  Google Scholar 

  • Kingma SA, Hall ML, Arriero E, Peters A (2010) Multiple benefits of cooperative breeding in purple-crowned fairy-wrens: a consequence of fidelity? J Anim Ecol 79:757–768

    PubMed  Google Scholar 

  • Koenig WD (1990) Opportunity of parentage and nest destruction in polygynandrous acorn woodpeckers, Melanerpes formidvorus. Behav Ecol 1:55–61

    Article  Google Scholar 

  • Majolo B, de Bortoli VA, Schino G (2008) Costs and benefits of group living in primates: group size effects on behaviour and demography. Anim Behav 76:1235–1247

    Article  Google Scholar 

  • Marlowe F (1999) Showoffs or providers? The parenting effort of Hadza men. Evol Hum Behav 20:391–404

    Article  Google Scholar 

  • McNamara JM, Forslund P (1996) Divorce rates in birds: predictions from an optimization model. Am Nat 147:609–640

    Article  Google Scholar 

  • Morcillo A, Sánchez S, Fidalgo A, Gil-Bürman C, Peláez F (2003) Effects of enclosure size on weight loss after the birth of infants in cotton-top tamarins (Saguinus oedipus). Primate Rep 66-1:32–33

    Google Scholar 

  • Moreno J, Veiga JP, Cordero PJ, Mínguez E (1999) Effects of paternal care on reproductive success in the polygynous spotless starling Sturnus unicolor. Behav Ecol Sociobiol 47:47–53

    Article  Google Scholar 

  • Packer C (2000) Infanticide is no fallacy. Am Anthropol 102:829–857

    Article  Google Scholar 

  • Piper WH, Slater G (1993) Polyandry and incest avoidance in the cooperative stripe-backed wren of Venezuela. Behaviour 124:227–247

    Article  Google Scholar 

  • Price EC (1990) Infant carrying as a courtship strategy of breeding male cotton-top tamarins. Anim Behav 40:784–786

    Article  Google Scholar 

  • Price EC (1992a) The benefits of helpers: effects of group and litter size on infant care in tamarins (Saguinus oedipus). Am J Primatol 26:179–190

    Article  Google Scholar 

  • Price EC (1992b) The costs of infant carrying in captive cotton-top tamarins. Am J Primatol 26:23–33

    Article  Google Scholar 

  • R Development Core Team (2008) R: a language and environment for statistical computing. In. R Foundation for Statistical Computing, Vienna, Austria

  • Rendall D (2004) “Recognizing” kin: mechanisms, media, minds, modules, and muddles. In: Chapais B, Berman CM (eds) Kinship and behavior in primates. Oxford University Press, Oxford, pp 295–316

    Google Scholar 

  • Rotundo M, Fernandez-Duque E, Dixon AF (2005) Infant development and parental care in free-ranging Aotus azarai azarai in Argentina. Int J Primatol 26:1459–1473

    Article  Google Scholar 

  • Rudran R (1973) Adult male replacement in one-male troops of purple-faced langurs (Presbytis senex senex) and its effect on population structure. Folia Primatol 19:166–192

    PubMed  Article  CAS  Google Scholar 

  • Sánchez S, Peláez F, Gil-Bürmann C, Kaumanns W (1999) Costs of infant-carrying in cotton-top tamarin (Saguinus oedipus). Am J Primatol 48:99–111

    PubMed  Article  Google Scholar 

  • Silk JB, Altmann J, Alberts SC (2006) Social relationships among adult female baboons (Papio cynocephalus) I. Variation in the strength of social bonds. Behav Ecol Sociobiol 61:183–195

    Article  Google Scholar 

  • Smuts BB, Gubernick DJ (1992) Male–infant relationships in nonhuman primates: paternal investment or mating effort? In: Hewlett BS (ed) Father–child relations. Cultural and biosocial contexts. de Gruyter, New York, pp 1–30

    Google Scholar 

  • Sommer V (1994) Infanticide among the langurs of Jodhpur: testing the sexual selection hypothesis with a long-term record. In: Parmigiani S, vom Saal FS (eds) Infanticide and parental care. Harwood Academic, Philadelphia

    Google Scholar 

  • Sommer V (2000) The holy wars about infanticide. Which side are you on? And why? In: van Schaik CP, Janson C (eds) Infanticide by males and its implications. Cambridge University Press, Cambridge

    Google Scholar 

  • Stallcup JA, Woolfenden GE (1978) Family status and contributions to breeding by Florida scrub jays. Anim Behav 26:1144–1156

    Article  Google Scholar 

  • Tang-Martinez Z (2001) The mechanisms of kin discrimination and the evolution of kin recognition in vertebrates: a critical re-evaluation. Behav Process 53:21–40

    Article  Google Scholar 

  • Tardif S, Bales K (1997) Is infant-carrying a courtship strategy in callitrichid primates? Anim Behav 53:1001–1007

    Article  Google Scholar 

  • Tilson RL (1981) Family formation strategies of Kloss’s gibbons. Folia Primatol 35:259–287

    PubMed  Article  CAS  Google Scholar 

  • Valcu M, Kempenaers B (2008) Causes and consequences of breeding dispersal and divorce in a blue tit, Cyanistes caeruleus, population. Anim Behav 75:1949–1963

    Article  Google Scholar 

  • van Schaik CP (1983) Why are diurnal primates living in groups? Behaviour 87:120–144

    Article  Google Scholar 

  • Welker C, Schäfer-Witt C (1986) On the carrying behaviour of basic South American primates. Hum Evol 2:459–473

    Article  Google Scholar 

  • Wolovich CK, Perea-Rodriguez JP, Fernandez-Duque E (2007) Food transfers to young and mates in wild owl monkeys (Aotus azarai). Am J Primatol 69:1–16

    Google Scholar 

  • Wright PC (1984) Biparental care in Aotus trivirgatus and Callicebus moloch. In: Small MF (ed) Female primates: studies by women primatologists. Liss, New York, pp 59–75

    Google Scholar 

  • Wright PC (1989) The nocturnal primate niche in the New World. J Hum Evol 18:635–658

    Article  Google Scholar 

  • Wuensch KL (1985) Effects of early paternal presence upon nonhuman offsprings’ development. Am Zool 25:911–923

    Google Scholar 

  • Zhao Q, Borries C, Pan W (2011) Male takeover, infanticide, and female countertactics in white-headed leaf monkeys (Trachypithecus leucocephalus). Behav Ecol Sociobiol 65:1535–1547

    Article  Google Scholar 

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Acknowledgments

Thanks to all the students, volunteers, and assistants who helped with data collection. We also thank Mr. F. Middleton, Manager of Estancia Guaycolec, and Alfredo Casaretto (Director of Bellamar Estancias) for the continued support of the Owl Monkey Project. We would like to thank the two anonymous reviewers and editor Elise Huchard for their very thoughtful comments that helped to improve the manuscript.

Ethical standards

This study conformed to laws of both the USA and Argentina. The Ministerio de la Producción, Subsecretaría de Ecología and Recursos Naturales and Dirección de Fauna from Formosa Province provided permits to conduct the study. The Owl Monkey Project has had continued approval for all research presented here by the Formosa Province Council of Veterinarian Doctors, the Directorate of Wildlife, the Subsecretary of Ecology and Natural Resources, and the Ministry of Production. At the national level, the procedures were approved by the National Wildlife Directorate in Argentina and by the IACUC committees of the Zoological Society of San Diego (2000–2005) and of the University of Pennsylvania (2006–2011).

Conflict of interest

The authors declare that they have no conflict of interest. MH was funded by the Deutsche Forschungsgemeinschaft (HU 1746/2-1). EFD acknowledges the financial support during all these years from the Wenner-Gren Foundation, the L.S.B. Leakey Foundation, the National Geographic Society, the National Science Foundation (BCS-0621020), the University of Pennsylvania Research Foundation, and the Zoological Society of San Diego.

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Authors and Affiliations

  1. Department of Anthropology, University of Pennsylvania, 429 University Museum, 3260 South Street, Philadelphia, PA, 19104, USA

    Maren Huck & Eduardo Fernandez-Duque

  2. Centro de Ecología Aplicada del Litoral, CONICET, Corrientes, Argentina

    Eduardo Fernandez-Duque

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  1. Maren Huck
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  2. Eduardo Fernandez-Duque
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Correspondence to Maren Huck.

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Communicated by T. Bakker

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Huck, M., Fernandez-Duque, E. Children of divorce: effects of adult replacements on previous offspring in Argentinean owl monkeys. Behav Ecol Sociobiol 66, 505–517 (2012). https://doi.org/10.1007/s00265-011-1297-9

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  • DOI: https://doi.org/10.1007/s00265-011-1297-9

Keywords

  • Aotus azarai
  • Dispersal
  • Evolutionary theory of the family
  • Night monkeys
  • Parent–offspring conflict
  • Survival