Abstract
The old African proverb, “It takes a village to raise a child,” may extend well beyond the collective effort attributed to human child rearing strategies. In fact, allomaternal care is taxonomically widespread, particularly among mammalian taxa (e.g., rodents: Gubernick and Alberts 1987; Solomon and Getz 1997; chiroptera: O’Farrell and Studier 1973; canids: Moehlman and Hofer 1997; cetaceans: Gero et al. 2009; and primates: Hrdy 1976; Chism 2000). Allomaternal care includes infant care provided by the father (paternal care, Fernandez-Duque et al. 2009) or by conspecifics other than the parents (alloparental care, Wilson 1975). While well represented by a diversity of taxa, allomaternal care is not common among mammals (e.g., 9–10% of taxa display paternal care; Kleiman and Malcolm 1981; Huck and Fernandez-Duque 2012), allomaternal care has been recently noted to occur at relatively high frequencies in the Order Primates, particularly among many haplorhine (e.g., monkey and ape) species (Tardif 1997; Chism 2000; Ross and MacLarnon 2000; Hrdy 2009). While studies have examined the causes and consequences of allomaternal care among haplorhines, to our knowledge, there has yet to be a comprehensive analysis of allomaternal care across the entire primate order (e.g., including the primates of Madagascar, hereafter referred to as lemurs). This is in large part because studies of lemur allomaternal care have lagged behind those of their primate cousins. The most recent attempt at a synthesis of primate allomaternal care found that it was a haplorhine-biased phenomenon, finding no evidence of lemurs participating in allomaternal care-related behaviors (Ross 2003), and thus precluding any analysis of allomaternal care within that taxon. However, recent increases in attention to and sampling effort of lemur care behaviors have revealed that allomaternal care is more common in lemurs than originally thought (Mitchell 1969; Klopfer 1974; Pereira et al. 1987; Wright 1990; Patel 2007; Hrdy 2010; Rowe and Myers 2011; Tecot and Hrdy, unpublished data). Moreover, a number of studies in recent years have added to our understanding of this postnatal care strategy in lemurs, making it possible to include these species in broader taxonomic comparisons of primate reproductive strategies. In light of these recent discoveries, we aim to (1) describe the different types of allomaternal care observed in primates, including a discussion of how each type of care is expressed in monkeys and apes, and a summary of what is currently known for lemurs; (2) discuss the benefits of allomaternal caretaking and whether such behaviors benefit lemur mothers; and (3) outline important gaps in our knowledge of lemur allomaternal care, suggesting future avenues of research.
Keywords
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Altmann J (1980) Baboon mothers and infants. Harvard University Press, Cambridge, p 272
Altmann J, Samuels A (1992) Costs of maternal care: infant-carrying in baboons. Behav Ecol Sociobiol 29:391–398
Andrews J (1998) Infanticide by a female black lemur, Eulemur macaco, in disturbed habitat on Nosy Be, North-Western Madagascar. Folia Primatol 69:14–17
Arrigo-Nelson SJ (2006) The impact of habitat disturbance on the feeding ecology of the Milne-Edwards’ sifaka (Propithecus edwardsi) in Ranomafana National Park. Dissertation, Stony Brook University. 181 p
Baden AL (2009) It takes a village: communal infant care and socialization in wild ruffed lemurs (Varecia variegata) in Ranomafana National Park, Madagascar. Am J Primatol 71(S1):93
Baden AL (2011) Communal infant care in black-and-white ruffed lemurs (Varecia variegata). Dissertation, Stony Brook University, 252 p
Baden AL, Louis EE Jr, Bradley BJ (2011) Cooperation confers fitness benefits in a communally nesting primate. Am J Phys Anthropol 144(S52):79–80
Baden AL, Louis EE Jr, Bradley BJ (in revision) Communal infant care confers maternal success in a social primate
Baldovino M, Di Bitetti M (2008) Allonursing in tufted capuchin monkeys (Cebus nigritus): milk or pacifier? Folia Primatol 79:79–92
Bales K, Dietz J, Baker A, Miller K, Tardif SD (2000) Effects of allocare-givers on fitness of infants and parents in callitrichid primates. Folia Primatol 71:27–38
Balko EA (1998) A behaviorally plastic response to forest composition and logging disturbance by Varecia variegata variegata in Ranomafana National Park, Madagascar. Dissertation, SUNY-CESF. 245 p
Balko EA (2011) Black and white ruffed lemur, Varecia variegata. In: Rowe N (ed) All the world’s primates. Pogonias, Charlestown
Barthold J, Kappeler P, Fichtel C (2009) What is it going to be? Pattern and potential function of natal coat change in sexually dichromatic redfronted lemurs (Eulemur fulvus rufus). Am J Phys Anthropol 138:1–10
Bastian ML, Brockman D (2007) Paternal care in Propithecus verreauxi coquereli. Int J Primatol 28:305–313
Boskoff K (1978) The oestrous cycle of the brown lemur, Lemur fulvus. J Reprod Fertil 54:313–318
Brockman DK, van Schaik CP (2005) Seasonality and reproductive function. In: Brockman DK, van Schaik CP (eds) Seasonality in primates: studies of living and extinct human and non-human primates. Cambridge University Press, New York, pp 269–305
Bronson FH, Heideman PD (1994) Seasonal regulation of reproduction in mammals. In: Knobil E, Neil JD (eds) The physiology of reproduction, 2nd edn. Raven, New York, pp 541–583
Brown GR, Almond REA, van Bergen Y (2004) Begging, stealing, and offering: food transfer in nonhuman primates. Adv Stud Behav 34:265–295
Buchan JC, Alberts SC, Silk JB, Altmann J (2003) True paternal care in a multi-male primate society. Nature 425:179–181
Buss DH, Cooper RW, Wallen K (1976) Composition of lemur milk. Folia Primatol 26:301–305
Carlson AA, Russell AF, Young AJ, Jordan NR, McNeilly AS, Parlow AF, Clutton-Brock T (2006) Elevated prolactin levels immediately precede decisions to babysit by male meerkat helpers. Horm Behav 50:94–100
Catlett KK, Schwartz GT, Godfrey LR, Jungers WL (2010) “Life history space”: a multivariate analysis of life history variation in extant and extinct Malagasy lemurs. Yearb Phys Anthropol 142:391–404
Chism J (2000) Allocare patterns among cercopithecines. Folia Primatol 71:55–66
Chivers DJ (1974) The siamang in Malaya: a field study of a primate in tropical rain forest. Contrib Primatol 4:1–335
Clutton-Brock TH, Gaynor D, Kansky R, MacColl ADC, McIlrath G, Chadwick P, Brotherton PNM, O’Riain JM, Manswer M, Skinner JD (1998) Costs of cooperative behaviour in suricates (Suricates suricatta). Proc R Soc Lond, B 265:185–190
Curtis DJ (1997) The mongoose lemur (Eulemur mongoz): a study in behaviour and ecology. Dissertation, University of Zurich
Curtis DJ, Zaramody A (1998) Group size, home range use, and seasonal variation in the ecology of Eulemur mongoz. Int J Primatol 19:811–837
Curtis DJ, Zaramody A (1999) Social structure and seasonal variation in the behaviour of Eulemur mongoz. Folia Primatol 70:79–96
Dausmann K, Glos J, Ganzhorn JU, Heldmaier G (2004) Hibernation in a tropical primate. Nature 429:825–826
Deag JM, Crook JH (1971) Social behaviour and “agonistic buffering” in the wild Barbary macaque Macaca sylvana. Folia Primatol 15:183–200
Dewar RE, Richard AF (2007) Evolution in the hypervariable environment of Madagascar. Proc Natl Acad Sci 104:13723–13727
Dixson AF, Fleming D (1981) Parental behaviour and infant development in owl monkeys (Aotus trivirgatus griseimembra). J Zool 194:25–39
Dunbar RIM (1995) The mating system of callitrichid primates II: the impact of helpers. Anim Behav 50:1071–1089
Eaglen RH, Boskoff KJ (1978) The birth and early development of a captive sifaka, Propithecus verreauxi coquereli. Folia Primatol 30:206–219
Eberle M, Kappeler PM (2006) Family insurance: kin selection and cooperative breeding in a solitary primate (Microcebus murinus). Behav Ecol Sociobiol 60:582–588
Emlen ST (1984) Cooperative breeding in birds and mammals. In: Krebs JR, Davies NB (eds) Behavioural ecology: an evolutionary approach. Blackwell, Oxford, pp 305–339
Emlen ST (1991) Evolution of cooperative breeding in birds and mammals. In: Krebs JR, Davies NB (eds) Behavioural ecology: an evolutionary approach, 3rd edn. Blackwell, London, pp 301–335
Emlen ST (1997) Predicting family dynamics in social vertebrates. In: Krebs JR, Davies NB (eds) Behavioural ecology, an evolutionary approach, 4th edn. Blackwell Publishing, Oxford, pp 228–253
Erhart EM, Overdorff DJ (1998) Infanticide in Propithecus diadema edwardsi: an evaluation of the sexual selection hypothesis. Int J Primatol 19:73–81
Fairbanks LA (1990) Reciprocal benefits of allomothering for female vervet monkeys. Anim Behav 40:553–562
Feistner ATC, McGrew WC (1989) Food-sharing in primates: a critical review. In: Seth PK, Seth S (eds) Perspectives in primate biology, vol 3. Today and Tomorrow’s Printers and Publishers, New Delhi, pp 21–36
Feistner A, Price E (1991) Food offering in New World primates: two species added. Folia Primatol 57:165–168
Fernandez-Duque E, Valeggia CR, Mendoza SP (2009) The biology of paternal care in human and nonhuman primates. Annu Rev Anthropol 38:115–130
Fietz J (1999) Mating system of Microcebus murinus. Am J Primatol 48:127–133
Fietz J (2003) Pair living and mating strategies in the fat-tailed dwarf lemur (Cheirogaleus medius). In: Reichard UH, Boesch C (eds) Monogamy: mating strategies and partnerships in birds, humans and other mammals. Cambridge University Press, Cambridge, pp 214–231
Fietz J, Dausmann KH (2003) Costs and potential benefits of parental care in the nocturnal fat-tailed dwarf lemur (Cheirogaleus medius). Folia Primatol 74:246–258
Fragaszy DM, Schwarz S, Shimosaka D (1982) Longitudinal observations of care and development of infant titi monkeys (Callicebus moloch). Am J Primatol 2:191–200
Fragaszy DM, Fedigan LM, Visalberghi E (2004) The complete capuchin: the biology of the genus Cebus. Cambridge Univ Press, New York, p 339
Ganzhorn JU, Abraham JP, Razanahoera-Rakotomalala M (1985) Some aspects of the natural history and food selection of Avahi laniger. Primates 26:452–463
Ganzhorn JU, Wright PC, Ratsimbazafy HJ (1999) Primate communities: Madagascar. In: Fleagle JG, Janson CH, Reed K (eds) Primate communities. Cambridge University Press, Cambridge, pp 75–89
Garber PA, Leigh SR (1997) Ontogenetic variation in small-bodied New World primates: implications for patterns of reproduction and infant care. Folia Primatol 68:1–22
Geiser F, Ruf T (1995) Hibernation versus daily torpor in mammals and birds: physiological variables and classification of torpor patterns. Physiol Zool 68:935–966
Génin F (2008) Life in unpredictable environments: first investigation of the natural history of Microcebus griseorufus. Int J Primatol 29:303–321
Gero S, Engelhaupt D, Rendell L, Whitehead H (2009) Who cares? Between-group variation in alloparental caregiving in sperm whales. Behav Ecol 20:838–843
Godfrey LR, Samonds KE, Jungers WL, Sutherland MR, Irwin MT (2004) Ontogenetic correlates of diet in Malagasy lemurs. Am J Phys Anthropol 123:250–276
Goldizen AW (1987a) Facultative polyandry and the role of infant-carrying in wild saddle-back tamarins (Saguinus fuscicollis). Behav Ecol Sociobiol 20:99–109
Goldizen AW (1987b) Tamarins and marmosets: Communal care of offspring. In: Smuts BB, Cheney DL, Seyfarth RM, Wrangham RW, Struhsaker TT (eds) Primate societies. University of Chicago Press, Chicago, pp 34–43
Gould L (1992) Alloparental care in free-ranging Lemur catta at Berenty Reserve, Madagascar. Folia Primatol 58:72–83
Gould L (2011) The Lemuriformes. In: Campbell C, Fuentes CA, MacKinnon K, Bearder SK, Stumpf R (eds) Primates in perspective, 2nd edn. Oxford University Press, Oxford, pp 55–79
Gould L, Sauther ML, Cameron A (2000) Adoption of a wild orphaned ringtailed lemur infant by natal group members: adaptive explanations. Primates 41:413–419
Grassi C (2001) The behavioral ecology of Hapalemur griseus griseus: the influences of microhabitat and population density on this small-bodied prosimian folivore. Dissertation, University of Texas at Austin. 345 p. Available from: University Microfilms, Ann Arbor, MI; AADAA-I3032404
Grieser B (1992) Infant development and parental care in two species of sifakas. Primates 33:305–314
Gubernick DJ, Alberts JR (1987) The biparental care system of the California mouse, Peromyscus californicus. J Comp Psychol 101:169–177
Gursky S (2000) Allocare in a nocturnal primate: data on the spectral tarsier, Tarsius spectrum. Folia Primatol 71:39–54
Hamilton WD (1964) The genetical evolution of social behaviour. I, II. J Theor Biol 7:1–52
Harrington J (1978) Development of behavior in Lemur macaco in the first nineteen weeks. Folia Primatol 29:107–128
Harvey PH, Clutton-Brock TH (1985) Life history variation in primates. Evolution 39:559–581
Harvey PH, Martin RD, Clutton-Brock TH (1987) Life Histories in comparative perspective. In: Smuts BB, Cheney DL, Seyfarth RM, Wrangham RS, Struhsaker TT (eds) Primate societies. Chicago University Press, Chicago, pp 181–196
Hilgartner R, Zinner D, Kappeler PM (2008) Life history traits and parental care in Lepilemur ruficaudatus. Am J Primatol 70:2–11
Hinde K, Milligan LA (2011) Primate milk: proximate mechanisms and ultimate perspectives. Evol Anthropol 20:9–23
Hrdy S (1976) Care and exploitation of nonhuman primate infants by conspecifics other than the mother. In: Rosenblatt J, Hinde R, Shaw E, Beer C (eds) Advances in the study of behavior. Academic, New York, pp 101–158
Hrdy SB (1977) The langurs of Abu: female and male strategies of reproduction. Harvard University Press, Cambridge, p 382
Hrdy S (2009) Mothers and others: the evolutionary origins of mutual understanding. The Belknap Press, Cambridge, p 432
Hrdy S (2010) Estimating the prevalence of shared care and cooperative breeding in the Order Primates, an appendix to mothers and others: the evolutionary origins of human understanding. http://www.citrona.com/hrdy/documents/AppendixI.pdf
Huck M, Fernandez-Duque E (2012) When dads help: male behavioral care during primate infant development. In: Clancy KBH, Hinde K, Rutherford JN (eds) Building babies: primate development in proximate and ultimate perspectives. Springer, New York
Huck M, Lottker P, Heymann EW (2004) The many faces of helping: Possible costs and benefits of infant carrying and food transfer in wild moustached tamarins (Saguinus mystax). Behaviour 141:915–934
Jaeggi AV, van Schaik CP (2011) The evolution of food sharing in primates. Behav Ecol Sociobiol 65:2125–2140
Janson C, Verdolin J (2005) Seasonality of primate births in relation to climate. In: Brockman DK, van Schaik CP (eds) Seasonality in primates: studies of living and extinct human and non-human primates. Cambridge University Press, New York, pp 307–350
Jolly A (1966) Lemur behavior: a Madagascar field study. University of Chicago Press, Chicago, p 187
Jolly A (1967) Breeding synchrony in wild Lemur catta. In: Altmann SA (ed) Social communication among primates. Chicago University Press, Chicago, pp 3–13
Jolly A (1972) The evolution of primate behavior. Macmillan Company, New York, p 397
Jolly A (1984) The puzzle of female feeding priority. In: Small M (ed) Female primates: studies by women primatologists. Alan R. Liss, New York, pp 197–215
Jolly A, Caless S, Cavigelli S, Gould L, Pereira ME, Pitts A, Pride RE, Rabenandrasana HD, Walkder JD, Zafison T (2000) Infant killing, wounding, and predation in Eulemur and Lemur. Int J Primatol 21:21–40
Jones KE, Bielby J, Cardillo M, Fritz SA, O’Dell J, Orme CDL, Safi K, Sechrest W, Boakes EH, Carbone C, Connolly C, Cutts MJ, Foster JK, Grenyer R, Habib M, Plaster CA, Price SA, Rigby EA, Rist J, Teacher A, Bininda-Emonds ORP, Gittleman JL, Mace GM, Purvis A, Michener WK (2009) Pantheria: a species-level database of life history, ecology, and geography of extant and recently extinct mammals. Ecology 90:2648
Kappeler PM (1996) Causes and consequences of life-history variation among strepsirrhine primates. Am Nat 148:868–891
Kappeler PM (1998) Nests, tree holes, and the evolution of primate life histories. Am J Primatol 46:7–33
Kappeler PM, Pereira ME (2003) A primate life history database. In: Kappeler PM, Pereira ME (eds) Primate life histories and socioecology. University of Chicago Press, Chicago, pp 313–330
Kesch K (2009) Allomothering and allonursing behavior in collared lemurs (Eulemur collaris). Lemur News 14:54–55
King SJ, Morelli TL, Arrigo-Nelson S, Ratelolahy FJ, Godfrey LR, Wyatt J, Tecot S, Jernvall J, Wright PC (2011) Morphometrics and pattern of growth in wild sifakas (Propithecus edwardsi) at Ranomafana National Park, Madagascar. Am J Primatol 73:155–172
Kirkwood JK, Underwood SJ (1984) Energy requirements of captive cotton-top tamarins, Saguinus oedipus oedipus. Folia Primatol 42:180–187
Kleiman DG, Malcolm JR (1981) The evolution of male parental investment in mammals. In: Gubernick DJ, Klopfer PH (eds) Parental care in mammals. Plenum, New York, pp 347–387
Klopfer PH (1974) Mother-young relations in lemurs. In: Martin RD, Doyle GA, Walker AC (eds) Prosimian biology. Duckworth, London, pp 273–292
Koenig WD, Pitelka FA, Carmen WJ, Mumme RL, Stanback MT (1992) The evolution of delayed dispersal in cooperative breeders. Q Rev Biol 67:111–150
Kokko H, Johnstone RA (1999) Social queuing in animal societies: a dynamic model of reproductive skew. Proc R Soc Lond B 266:571–578
König B (1997) Cooperative care of young in mammals. Naturwissenschaften 84:95–104
König B (2006) Non-offspring nursing in mammals: general implications from a case study on house mice. In: Kappeler PM, van Schaik CP (eds) Cooperation in primates and humans: mechanisms and evolution. Springer, Berlin, pp 191–205
Lancaster JB (1971) Play-mothering: the relations between juvenile females and young infants among free-ranging vervet monkeys (Cercopithecus aethiops). Folia Primatol 15:161–182
Lappan S (2008) Male care of infants in a siamang (Symphalangus syndactylus) population including socially monogamous and polyandrous groups. Behav Ecol Sociobiol 62:1307–1317
Leigh SR, Terranova CJ (1998) Comparative perspectives on bimaturism, ontogeny, and dimorphism in Lemurid primates. Int J Primatol 19:723–749
Lemon WC, Barth RH (1992) The effects of feeding rate on reproductive success in the zebra finch, Taeniopygia guttata. Anim Behav 44:851–857
Lessnau RG, Taylor LL, Thompson WL (1993) Infant transfer patterns in a captive group of ringtailed lemurs (Lemur catta) at the Detroit zoological park. AAZPA Regional Conference Proceedings 1993, pp 254–259
Leutenegger W (1980) Monogamy in callitrichids: a consequence of phyletic dwarfism? Int J Primatol 1:95–98
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
Lewis SE, Pusey AE (1997) Factors influencing the occurrence of communal care in plural breeding mammals. In: Solomon NG, French JA (eds) Cooperative breeding in mammals. Cambridge University Press, Cambridge, pp 335–363
Ligon JD, Stacey PB (1991) The origin and maintenance of helping behavior in birds. Am Nat 138:254–258
Lindenfors P (2002) Sexually antagonistic selection on primate size. J Evol Biol 15:595–607
Maestripieri D (1994) Social structure, infant handling, and mothering styles in group-living Old World monkeys. Int J Primatol 15:531–553
Martin RD (1972) A preliminary field-study of the lesser mouse lemur (Microceuns murinus J.F. Miller 1777). In: Michael RP, Crook JH (eds) Comparative ecology and behavior of primates. Academic, London
McKenna JJ (1981) Primate infant caregiving behavior: origins, consequences, and variability with emphasis on the common Indian langur monkey. In: Gubernick DJ, Klopfer PH (eds) Parental care in mammals. Plenum, New York, pp 389–416
Meyers DM (1993) The effects of resource seasonality on behavior and reproduction in the golden-crowned sifaka (Propithecus tattersalli, Simons, 1988) in three Malagasy forests. Dissertation, Duke University. 251 p. Available from: University Microfilms, Ann Arbor, MI; AADAA-I9508755
Meyers DM, Wright PC (1993) Resource tracking: food availability and Propithecus seasonal reproduction. In: Kappeler PM, Ganzhorn JU (eds) Lemur social systems and their ecological basis. Plenum Press, New York, pp 179–192
Mitani JC, Watts D (1997) The evolution of non-maternal caretaking among anthropoid primates: do helpers help? Behav Ecol Sociobiol 40:213–220
Mitchell GD (1969) Paternalistic behavior in primates. Psychol Bull 71:399–417
Mittermeier RA, Louis EE Jr, Richardson M, Schwitzer C, Langrand O, Rylands A, Hawkins F, Rajaobelina S, Ratsimbazafy J, Roos C, Kappeler PM, MacKinnon J (2010) Lemurs of Madagascar, 3rd edn. Conservation International, Washington, p 762
Moehlman PD, Hofer H (1997) Cooperative breeding, reproductive suppression, and body mass in canids. In: Solomon NG, French JA (eds) Cooperative breeding in mammals. Cambridge University Press, Cambridge, pp 76–127
Morelli TL, King SJ, Pochron ST, Wright PC (2009) The rules of disengagement: takeovers, infanticide, and dispersal in a rainforest lemur, Propithecus edwardsi. Behaviour 146:499–523
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
Morland HS (1991) Preliminary report on the social organization of ruffed lemurs (Varecia variegata variegata) in a northeast Madagascar rainforest. Folia Primatol 56:157–161
Muldoon KM, Goodman SM (2010) Ecological biogeography of Malagasy non-volant mammals: community structure is correlated with habitat. J Biogeogr 37:1144–1159
Mumme RL (1997) A bird’s eye view of cooperative breeding. In: Solomon NG, French JA (eds) Cooperative breeding in mammals. University Press, Cambridge, pp 164–388
Negus NC, Berger PJ (1972) Environmental factors and reproductive processes in mammalian populations. In: Velardo JT, Kasprow BA (eds) Biology of reproduction: basic and clinical studies. Third Pan American Congress on Anatomy, New Orleans. Pan American Association of Anatomy, pp 89–98
Nekaris KAI, Bearder SK (2011) The Lorisiform primates of Asia and mainland Africa: diversity shrouded in darkness. In: Campbell C, Fuentes CA, MacKinnon K, Bearder SK, Stumpf R (eds) Primates in perspective, 2nd edn. Oxford University Press, Oxford, pp 34–54
Numen M, Insel TR (2003) Neurobiology of parental behavior. Springer, New York, p 418
O’Farrell MJ, Studier EH (1973) Reproduction, growth, and development in Myotis Thysanodes and M. Lucifugus (Chiroptera: Vespertilionidae). Ecology 54:18–30
Overdorff DJ (1991) Ecological correlates to social structure in two prosimian primates: Eulemur fulvus rufous and Eulemur rubriventer in Madagascar. Dissertation, Duke University. 313 p. Available from: University Microfilms, Ann Arbor, MI; AAD92-02491
Overdorff DJ (1996a) Ecological correlates to social structure in two Lemur species in Madagascar. Am J Phys Anthropol 100:487–506
Overdorff DJ (1996b) Ecological correlates to activity and habitat use of two prosimian primates: Eulemur rubriventer and Eulemur fulvus rufus in Madagascar. Am J Primatol 40:327–342
Overdorff DJ, Tecot SR (2006) Social pair-bonding and resource defense in wild red-bellied lemurs (Eulemur rubriventer). In: Gould L, Sauther ML (eds) Lemurs: ecology and adaptation. Springer, New York, pp 235–254
Overdorff DJ, Merenlender A, Talata P, Telo A, Forward Z (1999) Life history of Eulemur fulvus rufus from 1988-1998 in southeastern Madagascar. Am J Phys Anthropol 108:295–310
Packer C, Lewis S, Pusey A (1992) A comparative analysis of non-offspring nursing. Anim Behav 43:265–281
Pagel M (1999) Inferring the historical patterns of biological evolution. Nature 401:877–884
Palombit RA, Seyfarth RM, Cheney DL (1997) The adaptive value of ‘friendships’ to female baboons: experimental and observational evidence. Anim Behav 54:599–614
Patel ER (2007) Non-maternal infant care in wild silky sifakas (Propithecus candidus). Lemur News 12:39–42
Pereira ME (1991) Asynchrony within estrous synchrony among ringtailed lemurs (Primates: Lemuridae). Physiol Behav 49:47–52
Pereira M (1993) Seasonal adustment of growth rate and adult body weight in ringtailed lemurs. In: Kappeler PM, Ganzhorn JU (eds) Lemur social systems and their ecological basis. Plenum, New York, pp 205–221
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
Pereira ME, Russ AS, Cavigelli SA, Hughes CL, Pearson DD (1999) Metabolic strategy and social behavior in Lemuridae. In: Rakotosamimanana B, Rasamimanana H, Ganzhorn JU, Goodman SM (eds) New directions in lemur studies. Plenum Publishers, New York, pp 93–118
Perry S (1995) Social relationships in wild white-faced capuchin monkeys, Cebus capucinus. Dissertation, University of Michigan. 326 p. Available from: University Microfilms, Ann Arbor, MI; AADAA-I9542933
Petter-Rousseaux A (1964) Reproductive physiology and behavior of the Lemuroidea. In: Buettner-Janusch J (ed) Evolutionary and genetic biology of Primates. Academic, New York, pp 92–132
Petter-Rousseaux A (1980) Seasonal activity rhythms, reproduction, and body weight variations in five sympatric nocturnal prosimians, in simulated light and climatic conditions. In: Charles-Dominique P, Cooper HM, Hladik A, Hladik CM, Pages E, Pariente GF, Petter-Rousseaux A, Petter J-J, Schilling A (eds) Nocturnal malagasy primates: ecology, physiology, and behavior. Academic, New York, pp 137–152
Pochron ST, Tucker WT, Wright PC (2004) Demography, life history and social structure in Propithecus edwardsi in Ranomafana National Park, Madagascar. Am J Phys Anthropol 125:61–72
Poirier FE (1968) The Nilgiri langur (Presbytis johnii) mother-infant dyad. Primates 9:45–68
Poirier FE (1970) The Nilgiri Langur (Presbytis johnii) of South India. In: Rosenblum LA (ed) Primate behavior, developments in field and laboratory research, vol I. Academic, New York, pp 251–383
Pollock JI (1975) Field observations on Indri indri: a preliminary report. In: Tattersall I, Sussman RW (eds) Lemur biology. Plenum, New York, pp 287–311
Pollock JI (1977) The ecology and sociology of feeding in Indri indri. In: Clutton-Brock TH (ed) Primate ecology: studies of feeding and ranging behaviour in lemurs, monkeys and apes. Academic, New York, pp 37–69
Pontzer H, Kamilar JM (2009) Great ranging associated with greater reproductive investment in mammals. Proc Natl Acad Sci U S A 106:192–196
Powzyk J (1997) The Socio-ecology of two sympatric indriids: Propithecus diadema diadema and Indri indri, a comparison of feeding strategies and their possible repercussions on species-specific behaviors. Dissertation, Duke University. 307 p
Quiatt D (1979) Aunts and mothers: adaptive implications of allomaternal behavior of nonhuman primates. Am Anthropol 81:310–319
Rasmussen D (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
Ravosa MJ, Meyers DM, Glander KE (1993) Relative growth of the limbs and trunk in sifakas: heterochronic, ecological, and functional considerations. Am J Anthropol 92:499–520
Richard AF (1976) Preliminary observations on the birth and development of Propithecus verreauxi to the age of six months. Primates 17:357–366
Richard A (1978) Behavioral variation: case study of a Malagasy lemur. Bucknell University Press, Lewisburg
Richard AF (1987) Malagasy prosimians: female dominance. In: Smuts B, Cheney D, Seyfarth R, Wrangham R, Struhsaker T (eds) Primate Societies. University of Chicago Press, Chicago, pp 25–33
Richard AF, Dewar RE (1991) Lemur ecology. Annu Rev Ecol Syst 22:145–175
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). J Zool, Lond 256:421–436
Ross C (2001) Park or ride? Evolution of infant carrying in primates. Int J Primatol 22:749–771
Ross C (2003) Life history, infant care strategies, and brain size in primates. In: Kappeler PM, Pereira ME (eds) Primate life histories and socioecology. University of Chicago Press, Chicago, pp 266–284
Ross C, MacLarnon A (1995) Ecological and social correlates of maternal expenditure on infant growth in haplorhine primates. In: Pryce C, Martin R, Skuse D (eds) Motherhood in human and nonhuman primates. Karger, Basel, pp 37–46
Ross C, MacLarnon A (2000) The evolution of non-maternal care in anthropoid primates: a test of the hypotheses. Folia Primatol 71:93–113
Rowe N, Myers M (eds) (2011) All the world’s primates. Primate Conservation Inc, Charlestown, http://www.alltheworldsprimates.org
Russell AF, Clutton-Brock TH, Brotherton PNM, Sharpe LL, McIlrath GM, Dalerum FD, Cameron EZ, Barnard JA (2002) Factors affecting pup growth and survival in co-operatively breeding meerkats Suricata suricata. J Anim Ecol 71:700–709
Sauther ML (1998) The interplay of phenology and reproduction in ringtailed lemurs: implications for ringtailed lemur conservation. Folia Primatol 69:309–320
Schmid J, Kappeler PM (1998) Fluctuating sexual dimorphism and differential hibernation by sex in a primate, the gray mouse lemur (Microcebus murinus). Behav Ecol Sociobiol 43:125–132
Schmid J, Stephenson PJ (2003) Physiological adaptations of Malagasy mammals: lemurs and tenrecs compared. In: Benstead J, Goodman SM (eds) The natural history of Madagascar. University of Chicago Press, Chicago, pp 1198–1203
Schradin C, Anzenberger G (2001) Costs of infant carrying in common marmosets, Callithrix jacchus: an experimental analysis. Anim Behav 62:289–295
Schülke O (2005) Evolution of pair-living in Phaner furcifer. Int J Primatol 26:903–919
Silk J (1980) Kidnapping and female competition among captive bonnet macaques. Primates 21:100–110
Smuts B (1998) What are friends for? In: Ciochon RL, Nisbett RA (eds) The primate anthology: essays on primate behavior, ecology, and conservation from Natural History. Prentice Hall, New York, pp 36–43
Solomon NG, French JA (1997) The study of mammalian cooperative breeding. In: Solomon NG, French JA (eds) Cooperative breeding in mammals. Cambridge University Press, Cambridge, pp 1–10
Solomon NG, Getz LL (1997) Examinations of alternative hypotheses for cooperative breeding in rodents. In: Solomon NG, French JA (eds) Cooperative breeding in mammals. Cambridge University Press, Cambridge, pp 335–363
Sørg J-P, Ganzhorn JU, Kappeler PM (2003) Forestry and research in the Kirindy Forest/Centre de Formation Professionnelle Forestiere. In: Benstead J, Goodman SM (eds) The natural history of Madagascar. University of Chicago Press, Chicago, pp 1512–1519
Stanford CB (1992) The costs and benefits of allomothering in wild capped langurs (Presbytis pileata). Behav Ecol Sociobiol 30:29–34
Storey AE, Delahunty KM, McKay DW, Walsh CJ, Wilhelm SI (2006) Social and hormonal bases of individual differences in the parental behaviour of birds and mammals. Can J Exp Psychol 60:237–245
Sussman RW (1977) Socialization, social structure, and ecology of two sympatric species of lemur. In: Chevalier-Skolnikoff S, Poirier FE (eds) Primate biosocial development: biological, social and ecological determinants. Garland Publishing, New York, pp 515–545
Sussman RW (1991) Demography and social organization of free-ranging Lemur catta in the Beza Mahafaly Reserve, Madagascar. Am J Phys Anthropol 84:43–58
Tan CL (2000) Behavior and ecology of three sympatric bamboo lemur species (genus Hapalemur) in Ranomafana National Park, Madagascar. Dissertation, State University of New York at Stony Brook. 242 p. Available from: University Microfilms, Ann Arbor, MI; AADAA-I3000799
Tan CL (2006) Behavior and ecology of gentle lemurs (Genus Hapalemur). In: Gould L, Sauther ML (eds) Lemurs: ecology and adaptation. Springer, New York, pp 369–381
Tardif SD (1997) The bioenergetics of parental behavior and the evolution of alloparental care in marmoset and tamarins. In: Solomon NG, French JA (eds) Cooperative breeding in mammals. Cambridge University Press, Cambridge, pp 11–32
Tardif SD, Santos CV, Baker AJ, Van Elsacker L, Ruiz-Miranda CR, Moura ACA, Passos FC, Price EC, Rapaport LG, de Vleeschouwer K (2002) Infant care in lion tamarins. In: Kleiman DG, Rylands AB (eds) Lion tamarins: biology and conservation. Smithsonian University Press, Washington, pp 213–232
Tattersall I (1982) The primates of Madagascar. Columbia University Press, New York
Tecot S (2007) Fecal cortisol levels and maintenance behaviors in wild groups of a cooperatively breeding species, the red-bellied lemur (Eulemur rubriventer). Am J Primatol 69:127
Tecot S (2008) Seasonality and predictability: the hormonal and behavioral responses of Eulemur rubriventer in Southeastern Madagascar. Dissertation, University of Texas-Austin. 544 p. Available from: University of Texas Libraries
Tecot S (2010) It’s all in the timing: out of season births and infant survival in Eulemur rubriventer. Int J Primatol 31:715–735
Tecot S (2012) Variable energetic strategies in disturbed and undisturbed rain forest habitats: fecal cortisol levels in southeastern Madagascar. In: Masters J, Gamba M, Génin F (eds) Leaping ahead: advances in prosimian biology. Developments in primatology series. Springer, New York (in press)
Tecot S and Overdorff DJ (2005) Aseasonal births and reproductive patterns in Eulemur rubriventer in southeastern Madagascar. Am J Primatol 66(S1):111–112
Tecot S, Baden A, Romine N, Kamilar J (In revision). Infant parking and nesting, not allomaternal care, influence Malagasy primate life histories
Tilden CD, Oftedal OT (1995) The bioenergetics of reproduction in prosimian primates: is it related to female dominance? In: Alterman L, Doyle GA, Izard MK (eds) Creatures of the dark: the nocturnal prosimians. Plenum, New York, pp 119–131
Tilden CD, Oftedal OT (1997) Milk composition reflects pattern of maternal care in prosimian primates. Am J Primatol 41:195–211
Trivers RL (1972) Parental investment and sexual selection. In: Campbell BG (ed) Sexual selection and the descent of man, 1871–1971. Aldine, Chicago, pp 136–179
van Horn RN (1975) Primate breeding season: photoperiodic regulation in captive Lemur catta. Folia Primatol 24:203–220
van Schaik CP, Kappeler PM (1993) Life history, activity period and lemur social systems. In: Kappeler PM, Ganzhorn JU (eds) Lemur social systems and their ecological basis. Plenum, New York, pp 241–260
van Schaik CP, Kappeler PM (1997) Infanticide risk and the evolution of male-female association in primates. Proc Biol Sci 264:1687–1694
van Schaik CP, Paul A (1996) Male care in primates: does it ever reflect paternity? Evol Anthropol 5:152–156
Vasey N (2007) The breeding system of wild red ruffed lemurs (Varecia rubra): a preliminary report. Primates 48:41–54
Vogel C (1984) Patterns of infant-transfer within two troops of common langurs (Presbytis entellus) near Jodhpur. Testing hypotheses concerning the benefits and risks. In: Roonwal M, Mohnot S, Rathore N (eds) Current primate researches. University of Jodhpur, Jodhpur, pp 361–379
Volampeno MSN, Masters J, Downs C (2011) Life history traits, maternal behavior and infant development of blue-Eyed black lemurs (Eulemur flavifrons). Am J Primatol 73:474–484
White FJ, Burton AS, Buchholz S, Glander KE (1992) Social organization of free-ranging ruffed lemurs, Varecia variegata variegata: mother-adult daughter relationship. Am J Primatol 28:281–287
Whitten PL, Brockman DK (2001) Strepsirrhine reproductive ecology. In: Ellison PT (ed) Reproductive ecology and human evolution. Aldine de Gruyter, New York, pp 321–350
Williams L, Gibson S, McDaniel M, Bazzel J, Barnes S, Abee C (1994) Allomaternal interactions in the Bolivian squirrel monkey (Saimiri boliviensis boliviensis). Am J Primatol 34:145–156
Wilson EO (1975) Sociobiology. Harvard University Press, Cambridge
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
Wright PC (1984) Biparental care in Aotus trivirgatus and Callicebus moloch. In: Small M (ed) Female primates: studies by women primatologists. Alan R. Liss, New York, pp 59–75
Wright PC (1990) Patterns of paternal care in primates. Int J Primatol 11:89–102
Wright PC (1995) Demography and life history of free-ranging Propithecus diadema edwardsi in Ranomafana National Park, Madagascar. Int J Primatol 16:835–854
Wright PC (1999) Lemur traits and Madagascar ecology: coping with an island environment. Yearb Phys Anthropol 42:31–72
Wright PC, Martin LB (1995) Predation, pollination and torpor in two nocturnal prosimians: Cheirogaleus major and Microcebus rufus in the rain forest of Madagascar. In: Alterman L, Doyle GA, Izard MK (eds) Creatures of the dark: the nocturnal prosimians. Plenum, New York, pp 45–60
Wright PC, Razafindratsita T, Pochron ST, Jernvall J (2005) The key to frugivory in Madagascar. In: Dew JL, Boubli JP (eds) Tropical fruits and frugivores: the search for strong interactors. Kluwer Academic/Plenum, New York, pp 118–128
Wright PC, Erhart EM, Tecot SR, Baden AL, Arrigo-Nelson S, Morelli TL, Deppe A, Ratelolahy F, Blanco M, Atsalis S, Johnson SE, Ratolahy F, Tan CLM, Zohdy S (2012) Long-term lemur research at Centre ValBio, Ranomafana National Park, Madagascar. In: Kappeler PM, Watts D (eds) Long-term research in Primates. Springer, Dordrecht (2012)
Young AL, Richard AF, Aiello LC (1990) Female dominance and maternal investment in Strepsirhine primates. Am Nat 135:473–488
Zahed SR, Prudom SL, Snowdon CT, Ziegler TE (2007) Male parenting and response to infant stimuli in the common marmoset (Callithrix jacchus). Am J Primatol 69:1–15
Zehr S, Haring D, Taylor J, Katz A, Williams C, Yoder A (2011) Everything you ever wanted to know about infant growth rates in prosimians but didn’t have a large enough sample size to ask: analyses of infant weight data at the Duke Lemur Center (abstract). Am J Phys Anthropol 144((Suppl)):317
Ziegler TE (2000) Hormones associated with non-maternal infant care: a review of mammalian and avian studies. Folia Primatol 71:6–21
Ziegler TE, Wegner FH, Carlson AA, Lazaro-Perea C, Snowdon CT (2000) Prolactin levels during the periparturitional period in the biparental cotton-top tamarin (Saguinus oedipus): Interactions with gender, androgen levels, and parenting. Horm Behav 38:111–122
Ziegler TE, Washabaugh KF, Snowdon CT (2004) Responsiveness of expectant male cotton-top tamarins, Saguinus oedipus, to mate’s pregnancy. Horm Behav 45:84–92
Acknowledgments
We would like to thank Katie Hinde, Julienne Rutherford, and Kate Clancy for inviting us to contribute to this volume, and for their insightful comments. We are grateful to the three anonymous reviewers for their thoughtful feedback and suggestions, and the numerous lemur researchers who took the time to answer our questions. We appreciate access to unpublished data from the All the World’s Primates database, generously contributed by several researchers and provided by Noel Rowe; the Duke Lemur Center, provided by Sarah Zehr and Julie Taylor; Teague O’Mara, and Erik Patel. SRT would like to thank Toni Ziegler, Pat Wright, Anita Ginther, and Sarah Hrdy for insight and discussions on allomaternal care.
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Glossary
- Allomaternal care
-
Costly behaviors directed toward infants, which are provided by individuals other than the mother. This can include care by the genetic father, siblings, and other distantly related or unrelated group members.
- Allomaternal nursing
-
The behavior of females nursing offspring that are not genetically their own.
- Carrying on fur
-
Also known as infant riding; the infant clings to its mother’s fur during movement between locations.
- Carrying orally
-
Care-providers transport young in their mouths, such as when moving between nests. Oral carrying typically occurs when infants are altricial and cannot cling to their mother’s fur.
- Cheirogaleidae
-
A family within the infraorder Lemuriformes including the genera Allocebus, Cheirogaleus, Microcebus, Mirza, and Phaner.
- Crèching
-
A shared nest or centralized location where the young of several mothers are cared for in a communal fashion (i.e., by one or many individuals other than the mother).
- Daubentoniidae
-
A family within the infraorder Lemuriformes including the genus Daubentonia.
- Energy transfer
-
When group members provision infants with food resources to the energetic benefit of the infant. Includes food sharing and allomaternal nursing.
- Food sharing
-
Transfer of food resources from group members to infants, often due to infant solicitation.
- Haplorhini
-
A suborder of primates including catarrhines (Old World monkeys and apes), platyrrhines (New World monkeys), and tarsiers.
- Helper
-
Infant care-provider other than the mother.
- Indriidae
-
A family within the infraorder Lemuriformes including the genera Avahi, Indri, and Propithecus.
- Infant guarding or “babysitting”
-
When group members other than the mother remain with an infant while its mother is away. This can involve predator protection, protection against infanticide, and general supervision.
- Infant transport
-
When a care-provider moves an infant between locations (transport can be over short or long distances) and includes carrying on fur (i.e., infant clings) and/or oral carrying, as in cases where infants cannot cling.
- Infant mistreatment/“Aunting to death”
-
Exploitative cases of allomaternal care which result in the mishandling, injury, and sometimes death of infants receiving care.
- Lemuridae
-
A family within the infraorder Lemuriformes including the genera Eulemur, Hapalemur, Lemur, Prolemur, and Varecia.
- Lemuriformes
-
An infraorder of strepsirhini primates endemic to the island of Madagascar.
- Lepilemuridae
-
A family within the infraorder Lemuriformes including the genus Lepilemur.
- Nesting
-
When infants are left in actual nests that have been constructed from leaves, lianas, and other materials. Often occurs when infants are altricial and cannot cling, and is common among litter-bearing taxa.
- Parking
-
When infants are left hidden in a tree-hole, amongst lianas and tree tangles, or clinging to a branch while family members feed and forage. Often occurs when infants are altricial and cannot cling.
- Strepsirrhini
-
A suborder of primates including lemurs, lorises, and galagos.
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Tecot, S.R., Baden, A.L., Romine, N., Kamilar, J.M. (2013). Reproductive Strategies and Infant Care in the Malagasy Primates. In: Clancy, K., Hinde, K., Rutherford, J. (eds) Building Babies. Developments in Primatology: Progress and Prospects, vol 37. Springer, New York, NY. https://doi.org/10.1007/978-1-4614-4060-4_15
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