Communal nesting, kinship, and maternal success in a social primate

Behavioral Ecology and Sociobiology

Volumn 67, Issue 12, 2013, Pages 1939-1950

  Baden, Andrea L ^a,b   Wright, Patricia C ^b   Louis, Edward E ^c   Bradley, Brenda J ^a  

^a YALE UNIVERSITY   (United States)

^b STONY BROOK UNIVERSITY   (United States)

^c Henry Doorly Zoo   (United States)

Author keywords

Allomaternal care; Communal breeding; Cr ching behavior; Lemurs; Reproductive success

Indexed keywords

COLONIAL BREEDING; KINSHIP; MATERNAL EFFECT; MUTUALISM; NESTING BEHAVIOR; PRIMATE; REARING; RELATEDNESS; REPRODUCTIVE SUCCESS; SOCIAL BEHAVIOR; SURVIVORSHIP;

LEMURIDAE; MAMMALIA; PRIMATES; VARECIA VARIEGATA;

EID: 84887623253     PISSN: 03405443     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00265-013-1601-y     Document Type: Article

References (111)

1. Altmann J (1974) Observational study of behavior: sampling methods. Behaviour 49: 227-267.
2. Baden AL (2011) Communal infant care in black- and-white ruffed lemurs (Varecia variegata). PhD Dissertation, Stony Brook University, Stony Brook, NY.
3. Baden AL, Brenneman RA, Louis EE Jr (2008) Morphometrics of wild black-and-white ruffed lemurs [Varecia variegata; Kerr, 1792]. Am J Primatol 70: 913-926.
4. Balko EA (1998) A behaviorally plastic response to forest composition and logging disturbance by Varecia variegata variegata in Ranomafana National Park, Madagascar. PhD Dissertation, State University of New York, Syracuse, NY.
5. Bled F, Royle JA, Cam E (2011) Assessing hypotheses about nesting site occupancy dynamics. Ecology 92: 938-951.
6. Blouin MS (2003) DNA-based methods for pedigree reconstruction and kinship analysis in natural populations. Trends Ecol Evol 18: 503-511.
7. Bogart MH, Cooper RW, Benirschke K (1977a) Reproductive studies of black and ruffed lemurs. Int Zoo Yearb 17: 177-182.
8. Bogart MH, Kumamoto AT, Lasley BL (1977b) A comparison of the reproductive cycle of three species of Lemur. Folia Primatol 28: 134-143.
9. Borgatti SP (2002) NetDraw: graph visualization software. Harvard Analytic Technologies, Cambridge.
10. Boskoff KJ (1977) Aspects of reproduction in ruffed lemurs (Lemur variegatus). Folia Primatol 28: 241-250.
11. Bradley BJ, Doran-Sheehy DM, Lukas D, Boesch C, Vigilant L (2004) Dispersed male networks in western gorillas. Curr Biol 14: 510-513.
12. Britt A (2000) Diet and feeding behavior of the black-and-white ruffed lemur (Varecia variegata variegata) in the Betampona Reserve, eastern Madagascar. Folia Primatol 71: 133-141.
13. Brockman DK, Willis MS, Karesh WB (1987) Management and husbandry of ruffed lemurs, Varecia variegata, at the San Diego Zoo. II. Reproduction, pregnancy, parturition, litter size, infant care and reintroduction of hand-raised infants. Zoo Biol 6: 349-363.
14. Browning LE, Patrick SC, Rollins LA, Griffith SC, Russell AF (2012) Kin selection, not group augmentation, predicts helping in an obligate cooperatively breeding bird. Proc R Soc Lond B 279: 3861-3869.
15. Cairns SJ, Schwager SJ (1987) A comparison of association indices. Anim Behav 35: 1454-1469.
16. Clutton-Brock T (2002) Breeding together: kin selection and mutualism in cooperative vertebrates. Science 296: 69-72.
17. Clutton-Brock T (2009) Cooperation between non-kin in animal societies. Nature 462: 51-57.
18. Cockburn A (1998) Evolution of helping in cooperatively breeding birds. Annu Rev Ecol Syst 29: 141-177.
19. Cockburn A, Russell AF (2011) Cooperative breeding: A question of climate? Curr Biol 21: R195-R197.
20. Creel SR, Creel NM (1991) Energetics, reproductive suppression and obligate communal breeding in carnivores. Behav Ecol Sociobiol 28: 263-270.
21. Csilléry K, Johnson T, Beraldi D, Clutton-Brock T, Coltman D et al (2006) Performance of marker-based relatedness estimators in natural populations of outbred vertebrates. Genetics 173: 2091-2101.
22. Dewar RE, Richard AF (2007) Evolution in the hypervariable environment of Madagascar. P Natl Acad Sci USA 104: 13723-13727.
23. Dunham AE, Erhart EM, 'Wright PC (2010) Global climate cycles and cyclones: consequences for rainfall patterns and lemur reproduction in southeastern Madagascar. Global Change Biol 17: 219-227.
24. Ebensperger LA, Hurtado MJ, León C (2007) An experimental examination of the consequences of communal versus solitary breeding on maternal condition and the early postnatal growth and survival of degu, Octodon degus, pups. Anim Behav 73: 185-194.
25. Eberle M, Kappeler PM (2006) Family insurance: kin selection and cooperative breeding in a solitary primate (Microcebus murinus). Behav Ecol Sociobiol 60: 582-588.
26. Emlen ST (1991) Evolution of cooperative breeding in birds and mammals. In: Krebs JR, Davies NB (eds) Behavioral ecology: an evolutionary approach, 3rd edn. Blackwell, London, pp 301-337.
27. Erhart EM, Overdorff DJ (2008) Rates of agonism by diurnal lemuroids: implications for female social relationships. Int J Primatol 29: 1227-1247.
28. ESRI (2011) ArcGIS Desktop. Release 9. 3. Environmental Systems Research Institute, Redlands, CA.
29. Fairbanks LA, McGuire MT (1995) Maternal condition and the quality of maternal care in vervet monkeys. Behaviour 132: 733-754.
30. Foerg R (1982) Reproductive behavior in Varecia variegata. Folia Primatol 38: 108-121.
31. Gilchrist JS (2007) Cooperative behavior in cooperative breeders: costs, benefits and communal breeding. Behav Process 76: 100-105.
32. Gittleman JL (1985) Functions of communal care in mammals. In: Greenwood PJ, Harvey PH, Slatkin M (eds) Evolution: essays in honour of John Maynard Smith. Cambridge University Press, Cambridge, pp 181-205.
33. Glander KE (1993) Capture and marking techniques for arboreal primates. In: Estrada A, Rodriguez-Luna E, Lopez-Wilchis R, Coates-Estrada R (eds) Estudios Primatologicos en Mexico, vol 1. Universidad Veracruzana, Veracruz, pp 299-304.
34. Gould L, Sussman RW, Sauther ML (2003) Demographic and life-history patterns in a population of ring-tailed lemurs (Lemur catta) at Beza Mahafaly Reserve, Madagascar: a 15 year perspective. Am J Phys Anthropol 120: 182-194.
35. Hamilton WD (1964) The genetical evolution of social behaviour. I. J Theor Biol 7: 1-52.
36. Harris TR, Chapman CA, Monfort SL (2010) Small folivorous primate groups exhibit behavioral and physiological effects of food scarcity. Behav Ecol 21: 46-56.
37. Hayes LD (2000) To nest communally or not to nest communally: a review of rodent communal nesting and nursing. Anim Behav 59: 677-688.
38. Hill K, Hurtado AM (2009) Cooperative breeding in South American hunter-gatherers. Proc R Soc Lon B 276: 3863-3870.
39. Holm S (1979) A simple sequentially rejective multiple test procedure. Scand J Stat 6: 65-70.
40. Hrdy SB (1999) Mother nature. A history of mothers, infants, and natural selection. Pantheon, New York.
41. Hrdy SB (2006) Evolutionary context of human development: the cooperative breeding model. In: Carter CS, Ahnert L, Grossman KE, Hrdy SB, Lamb ME, Porges SW, Sachser N (eds) Attachment and bonding: a new synthesis. MIT Press, Cambridge, pp 9-32.
42. Hrdy SB (2009) Mothers and others: the evolutionary origins of mutual understandings. Belknap Press of Harvard University Press, Cambridge.
43. Huck M, Löttker P, Heymann EW (2004) Benefits of infant carrying and food transfer in wild moustached tamarins (Saguinus mystax). Behaviour 141: 915-934.
44. Ivey PA (2000) Cooperative reproduction in Ituri Forest hunter-gatherers: who cares for Efe infants? Curr Anthropol 41: 856-866.
45. Jetz W, Rubenstein DR (2011) Environmental uncertainty and the global biogeography of cooperative breeding in birds. Curr Biol 21: 72-78.
46. Johnstone RA (2000) Models of reproductive skew: a review and synthesis (invited article). Ethology 106: 5-26.
47. Kalinowski ST, Wagner AP, Taper ML (2006) ML-Relate: a computer program for maximum likelihood estimation of relatedness and relationship. Mol Ecol Notes 6: 576-579.
48. Kappeler PM, Wimmer B, Zinner D, Tautz D (2002) The hidden matrilineal structure of a solitary lemur: implications for primate social evolution. Proc R Soc Lond B 269: 1755-1763.
49. Kassara C, Dimalexis A, Fric J, Karris G, Barboutis C, Sfenthourakis S (2012) Nest-site preferences in Eleonora's Falcon (Falco eleonorae) on uninhabited islets of the Aegean Sea using GIS and species distribution models. J Ornithol 153: 663-675.
50. König B (1997) Cooperative care of young in mammals. Naturwissenschaften 84: 95-104.
51. König B, Riester J, Markl H (1988) Maternal care in house mice (Mus musculus): II. The energy cost of lactation as a function of litter size. J Zool Lond 216: 195-210.
52. Lahann P, Dausmann KH (2011) Live fast, die young: flexibility of life history traits in the fat tailed dwarf lemur (Cheirogaleus medius). Behav Ecol Sociobiol 65: 381-390.
53. Langergraber KE, Mitani JC, Vigilant L (2007) The limited impact of kinship on cooperation in wild chimpanzees. P Natl Acad Sci USA 104: 7768-7790.
54. Lee PC (1987) Allomothering among African elephants. Anim Behav 35: 278-291.
55. Lehmann J, Boesch C (2009) Sociality of the dispersing sex: the nature of social bonds in West African chimpanzees, Pan troglodytes. Anim Behav 77: 377-387.
56. Lemon WC, Barth RH (1992) The effects of feeding rate on reproductive success in the zebra finch, Taeniopygia guttata. Anim Behav 44: 851-857.
57. Lewis RJ, Kappeler PM (2005) Seasonality, body condition and timing of reproduction in Propithecus verreauxi verreauxi in the Kirindy Forest. Am J Primatol 67: 347-364.
58. Louis EE Jr, Ratsimbazafy JH, Razakamaharauo VR, Pierson DJ, Barber RC, Brenneman RA (2005) Conservation genetics of black-and-white ruffed lemurs, Varecia variegata, from Southeastern Madagascar. Anim Conserv 8: 105-111.
59. Lukas D, Clutton-Brock T (2012) Cooperative breeding and monogamy in mammalian societies. Proc R Soc Lond B 1736: 2151-2156.
60. Lukas D, Reynolds V, Boesch C, Vigilant L (2005) To what extent does living in a group mean living with kin? Mol Ecol 14: 2181-2196.
61. Manly BFJ (1997) A method for the estimation of parameters for natural stage-structured populations. Res Popul Ecol 39: 101-111.
62. Mann J, Watson-Capps JJ (2005) Surviving at sea: ecological and behavioral predictors of calf mortality in Indian Ocean bottlenose dolphins, Tursiops sp. Anim Behav 69: 899-909.
63. Maynard Smith J (1964) Group selection and kin selection. Nature 201: 1145-1147.
64. Meehan CL, Quinlan R, Malcolm CD (2013) Cooperative breeding and maternal energy expenditure among Aka foragers. Am J Hum Biol 25: 42-57.
65. Mitani JC, Watts D (1997) The evolution of non-maternal caretaking among anthropoid primates: do helpers help? Behav Ecol Sociobiol 40: 213-220.
66. Morland HS (1990) Parental behavior and infant development in ruffed lemurs (Varecia variegata) in a northeast Madagascar rain forest. Am J Primatol 20: 253-265.
67. Morland HS (1991) Social organization and ecology of black and white ruffed lemurs (Varecia variegata variegata) in lowland rain forest, Nosy Mangabe, Madagascar. PhD Dissertation, Yale University, New Haven, CT.
68. Morland HS (1993) Reproductive activity of ruffed lemurs (Varecia variegata variegata) in a Madagascar rain forest. Am J Phys Anthropol 91: 71-82.
69. Packer C, Scheel D, Pusey AE (1990) Why lions form groups: food is not enough. Am Nat 136: 1-19.
70. Painter JN, Crozier RH, Poiani A, Robertson RJ, Clarke MF (2000) Complex social organization reflects genetic structure and relatedness in the cooperatively breeding bell miner, Manorina melanophrys. Mol Ecol 9: 1339-1347.
71. Patterson JEH (2012) Nest site characteristics and nest tree use by northern flying squirrels (Glaucomys sabrinus) in Southwestern Alberta, Canada. BioOne 86: 144-150.
72. Pereira ME, Klepper A, Simons EL (1987) Tactics of care for young infants by forest-living ruffed lemurs (Varecia variegata variegata): ground nests, parking and biparental guarding. Am J Primatol 13: 129-144.
73. Prentice AM, Prentice A (1988) Energy costs of lactation. Annu Rev Nutr 8: 63-79.
74. Queller DC, Goodnight KF (1998) Estimating relatedness using genetic markers. Evolution 43: 258-275.
75. Ramos-Fernandez G, Boyer D, Aureli F, Vick LG (2009) Association networks in spider monkeys (Ateles geoffroyi). Behav Ecol Sociobiol 63: 999-1013.
76. Rasmussen DT (1985) A comparative study of breeding seasonality and litter size in eleven taxa of captive lemurs (Lemur and Varecia). Int J Primatol 6: 501-517.
77. Ratsimbazafy JJ (2002) On the brink of extinction and the process of recovery: responses of black-and-white ruffed lemurs (Varecia variegata variegata) to disturbance in Manombo Forest, Madagascar. PhD Dissertation, Stony Brook University, Stony Brook, NY.
78. Rice WR, Gaines SD (1994) 'Heads I win, tails you lose': testing directional alternative hypotheses in ecological and evolutionary research. Trends Ecol Evol 9: 235-237.
79. Richard AF, Dewar RE, Schwartz M, Ratsirarson J (2002) Life in the slow lane? Demography and life histories of male and female sifaka (Propithecus verreauxi verreauxi). J Zool 256: 421-436.
80. Riehl C (2010) Living with strangers: direct benefits favour non-kin cooperation in a communally nesting bird. Proc R Soc Lond B 278: 1728-1735.
81. Riehl C (2012) Mating system and reproductive skew in a communally breeding cuckoo: hard working males do not sire more young. Anim Behav 84: 707-714.
82. Ross C, MacLarnon A (2000) The evolution of non-maternal care in anthropoid primates: a test of the hypotheses. Folia Primatol 71: 93-113.
83. Rowe N (2012) All the Worlds Primates database, www. alltheworldsprimates. com. Accessed 13 Jan 2013.
84. Rubenstein DI (1982) Risk, uncertainty and evolutionary strategies. In: Kings College Sociobiology Group (eds) Current problems in sociobiology. Cambridge University Press, Cambridge, pp 91-111.
85. Scelza B, Bird RB (2008) Group structure and female cooperative networks in Australia's Western Desert. Hum Nature 19: 231-248.
86. Sear R, Mace R (2008) Who keeps children alive? A review of the effects of kin on child survival. Evol Hum Behav 29: 1-18.
87. Shideler SE, Lindburg DG (1982) Selected aspects of Lemur variegatus reproductive biology. Zoo Biol 1: 127-134.
88. Silk JB (2009) Nepotistic cooperation in non-human primate groups. Philos T Roy Soc B 364: 3243-3254.
89. Sokal RR, Rohlf FJ (1995) Biometry, 3rd edn. Freeman, New York.
90. Solomon NG, French JA (1997) Cooperative breeding in mammals. Cambridge University Press, Cambridge.
91. Stacey PB, Koenig WD (1990) Cooperative breeding in birds. Long term studies of ecology and behavior. Cambridge University Press, Cambridge.
92. Stanford CB (1992) The costs and benefits of allomothering in wild capped langurs (Presbytis pileata). Behav Ecol Sociobiol 30: 29-34.
93. Symington MM (1988) Food competition and foraging party size in the black spider monkey (Ateles paniscus chamek). Behaviour 105: 117-134.
94. Taberlet P, Griffin S, Goossens B, Questiau S, Manceau V et al (1996) Reliable genotyping of samples with very low DNA quantities using PCR. Nucleic Acids Res 24: 3189-3194.
95. Tecot SR, Baden AL, Romine NK, Kamilar JM (2012) Infant parking and nesting, not allomaternal care, influence Malagasy primate life histories. Behav Ecol Sociobiol 66: 1375-1386.
96. Tecot SR, Baden AL, Romine N, Kamilar JM (2013) Reproductive strategies and infant care in the Malagasy primates. In: Clancy KBH, Hinde K, Rutherford JN (eds) Building babies: primate development in proximate and ultimate perspetive. Springer, Dordrecht, pp 321-359.
97. Tilden CD (1993) Reproductive energetic of prosimian primates. PhD Dissertation, Duke University, Durham, NC.
98. Tilden CD, Oftedal OT (1997) Milk composition reflects patterns of maternal care in prosimian primates. Am J Primatol 41: 195-211.
99. van Horn RC, Altmann J, Alberts SC (2008) Can't get there from here: inferring kinship from pairwise genetic relatedness. Anim Behav 75: 1173-1180.
100. van Schaik CP, Kappeler PM (1997) Infanticide risk and the evolution of male-female association in primates. Proc R Soc Lond B 264: 1687-1694.
101. Vasey N (1997) Community ecology and behavior of Varecia variegata rubra and Lemur fulvus albifrons on the Masoala Peninsula, Madagascar. PhD thesis, Washington University, St. Louis, MO.
102. Vasey N (2003) Ruffed lemurs (Varecia). In: Goodman SM, Benstead JP (eds) The natural history of Madagascar. University of Chicago Press, Chicago, pp 1332-1336.
103. Vasey N (2006) Impact of seasonality and reproduction on social structure, ranging patterns, and fission-fusion social organization in red ruffed lemurs. In: Gould L, Sauther ML (eds) Lemurs: ecology and adaptation. Springer, Chicago, pp 275-304.
104. Vasey N (2007) The breeding system of wild red ruffed lemurs (Varecia rubra): a preliminary report. Primates 48: 41-54.
105. Watts DP (1988) Environmental influences on mountain gorilla time budgets. Am J Primatol 15: 195-211.
106. White AM, Cameron EZ (2009) Communal nesting is unrelated to burrow availability in the common warthog. Anim Behav 77: 87-94.
107. Wright P, King S, Baden A, Jernvall J (2008) Aging in wild female lemurs: sustained fertility with increased infant mortality. In: Atsalis S, Margulis SW (eds) Primate reproductive aging. Karger, Basel, pp 17-28.
108. Wright PC (1992) Primate ecology, rainforest conservation, and economic development: building a national park in Madagascar. Evol Anthropol 1: 25-33.
109. Wright PC (1999) Lemur traits and Madagascar ecology: coping with an island environment. Am J Phys Anthropol 110: 31-72.
110. Wright PC, Erhart EM, Tecot SR, Baden AL, Arrigo-Nelson S, Herrera J, Morelli TL, Blanco M, Deppe A, Atsalis S, Johnson SE, Ratelolahy F, Tan C, Zohdy S (2012) Long term lemur research at Centre ValBio, Ranomafana National Park, Madagascar. In: Kappeler PM, Watts D (eds) Long-term field studies of primates. Springer, Dordrecht, pp 67-100.
111. Young AL, Richard AF, Aiello LC (1990) Female dominance and maternal investment in strepsirrhine primates. Am Nat 135: 473-488.