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Nursing of own and foster offspring by Utah prairie dogs (Cynomys parvidens)

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Abstract

From 1995 through 2005, I studied nursing among Utah prairie dogs (Cynomys parvidens) living under natural conditions at Bryce Canyon National Park, UT, USA. I observed 850 aboveground nursings, which involved 122 mothers and 248 juveniles from 134 litters. Most of the mothers that nursed aboveground were middle-aged, and most nursing juveniles had been coming aboveground for 1–3 weeks. Most nursings involved a single juvenile, lasted 1–10 min, and occurred between 1800 hours and 2000 hours. Seventy-five percent of nursings (598/796) involved a mother suckling her own juvenile offspring; the other 24.9% (198/796) involved a mother suckling another mother’s offspring (i.e., communal nursing). Communal nursings involved juveniles of the home territory, and many communal nursings (74/198 = 37.4%) involved close kin such as half-siblings, grandoffspring, full-nieces, and full-nephews; other communal nursings (37/198 = 18.7%) involved more distant kin such as full-second cousins and full-third cousins. Of seven hypotheses that might explain the evolution of communal nursing, evidence supports the importance of two: elevated inclusive fitness via indirect selection and communal nursing as a cost of coloniality.

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References

  • Alexander RD (1974) The evolution of social behavior. Annu Rev Ecol Syst 5:325–383

    Article  Google Scholar 

  • Armitage KB (1984) Recruitment in yellow-bellied marmot populations: kinship, philopatry, and individual variability. In: Murie JO, Michener GR (eds) The biology of ground-dwelling squirrels. University of Nebraska Press, Lincoln, NE, pp 377–403

    Google Scholar 

  • Auldist B, Carlson D, Morrish L, Wakefield CM, King RH (2000) The influence of suckling interval on milk production of sows. J Anim Sci 78:2026–2031

    PubMed  CAS  Google Scholar 

  • Axelrod R, Hamilton WD (1981) The evolution of cooperation. Science 211:1390–1396

    Article  PubMed  CAS  Google Scholar 

  • Baker JR (1984) Mortality and morbidity in grey seal pups (Halichoerus grypus). Studies on its causes of environment, the nature and sources of infectious agents and the immunological status of pups. J Zool 203:23–48

    Google Scholar 

  • Balcombe JP (1990) Vocal recognition of pups by mother Mexican free-tailed bats, Tadarida brasiliensis mexicana. Anim Behav 39:960–966

    Article  Google Scholar 

  • Balcombe JP, McCracken GF (1992) Vocal recognition in Mexican free-tailed bats: do pups recognize mothers? Anim Behav 43:79–87

    Article  Google Scholar 

  • Barash DP (1989) Marmots: social behavior and ecology. Stanford University Press, Stanford, CA

    Google Scholar 

  • Beck CA, Bowen WD, Iverson SJ (2000) Seasonal changes in buoyancy and diving behaviour of adult grey seals. J Exp Biol 203:2323–2330

    PubMed  CAS  Google Scholar 

  • Beecher MD, Medvin MB, Stoddard PK, Loesche P (1986) Acoustic adaptations for parent-offspring recognition in swallows. Exp Biol 45:179–183

    PubMed  CAS  Google Scholar 

  • Bertram BCR (1976) Kin selection in lions and evolution. In: Bateson PPG, Hinde RA (eds) Growing points in ethology. Cambridge University Press, Cambridge, UK, pp 281–301

    Google Scholar 

  • Bertram BCR (1978) Living in groups: predators and prey. In: Krebs JR, Davies NB (eds) Behavioural ecology: an evolutionary approach, 1st edn. Sinauer, Sunderland, MA, pp 64–96

    Google Scholar 

  • Birgersson B, Ekvall J, Temrin H (1991) Allosuckling in fallow deer, Dama dama. Anim Behav 42:326–327

    Article  Google Scholar 

  • Blumstein DT, Armitage KB (1999) Cooperative breeding in marmots. Oikos 84:369–382

    Article  Google Scholar 

  • Boyd IL (1998) Time and energy constraints in pinniped lactation. Am Nat 152:717–728

    Article  PubMed  CAS  Google Scholar 

  • Brown JL (1987) Helping and communal breeding in birds. Princeton University Press, Princeton, NJ

    Google Scholar 

  • Brown CR, Brown MB (1996) Coloniality in the cliff swallow: the effect of group size on social behavior. University of Chicago Press, Chicago, IL

    Google Scholar 

  • Cameron EZ (1998) Is suckling behavior a useful predictor of milk intake? A review. Anim Behav 56:521–532

    Article  PubMed  Google Scholar 

  • Clark TW (1977) Ecology and ethology of the white-tailed prairie dog (Cynomys leucurus), Publications in biology and geology No. 3. Milwaukee Public Museum, Milwaukee, WI, pp 1–97

    Google Scholar 

  • Clutton-Brock TH, Albon SD, Guinness FE (1989) Fitness costs of gestation and lactation in wild mammals. Nature 337:260–262

    Article  PubMed  CAS  Google Scholar 

  • Creel SR, Montfort SL, Wildt DE, Waser PM (1991) Spontaneous lactation is an adaptive result of pseudopregnancy. Nature 351:660–662

    Article  PubMed  CAS  Google Scholar 

  • Dittrich L (1968) Keeping and breeding gazelles at Hanover Zoo. Int Zoo Yrbk 8:139–143

    Article  Google Scholar 

  • Dobson FS, Risch TS, Murie JO (1999) Increasing returns in the life history of Columbian ground squirrels. J Anim Ecol 68:73–86

    Article  Google Scholar 

  • Dublin HT (1983) Cooperation and reproductive competition among female African elephants. In: Wasser SK (ed) Social behavior of female vertebrates. Academic, New York, NY, pp 291–313

    Google Scholar 

  • Festa-Bianchet M (1988) Nursing behaviour of bighorn sheep: correlates of ewe age, parasitism, lamb age, birthdate and sex. Anim Behav 36:1445–1454

    Article  Google Scholar 

  • Fogden SCL (1971) Mother-young behaviour at grey seal breeding beaches. J Zool (Lond) 164:61–92

    Google Scholar 

  • Grafen A (1982) How not to measure inclusive fitness. Nature 298:425–426

    Article  PubMed  CAS  Google Scholar 

  • Hamilton WD (1964) The genetical evolution of social behaviour. J Theor Biol 7:1–52

    Article  PubMed  CAS  Google Scholar 

  • Hamilton WD (1971) Geometry for the selfish herd. J Theor Biol 31:295–311

    Article  PubMed  CAS  Google Scholar 

  • Harcourt AH, Fossey D, Sabater-Pi J (1981) Demography of Gorilla gorilla. J Zool (Lond) 195:215–233

    Article  Google Scholar 

  • Hayes LD (2000) To nest communally or not to nest communally: a review of rodent communal nesting and nursing. Anim Behav 59:677–688

    Article  PubMed  Google Scholar 

  • Haynie ML, van den Bussche RA, Hoogland JL, Gilbert DA (2003) Parentage, multiple paternity, and breeding success in Gunnison’s and Utah prairie dogs. J Mammal 84:1244–1253

    Article  Google Scholar 

  • Holmes WG, Mateo JM (2007) Kin recognition in rodents: issues and evidence. In: Wolff JO, Sherman PW (eds) Rodent societies. University of Chicago Press, Chicago, IL, pp 216–228

    Google Scholar 

  • Holmes WG, Sherman PW (1982) The ontogeny of kin recognition in two species of ground squirrels. Am Zool 22:491–517

    Google Scholar 

  • Hoogland JL (1979) Aggression, ectoparasitism, and other possible costs of prairie dog (Sciuridae: Cynomys spp.) coloniality. Behaviour 69:1–35

    Article  Google Scholar 

  • Hoogland JL (1981) The evolution of coloniality in white-tailed and black-tailed prairie dogs (Sciuridae: Cynomys leucurus and C. ludovicianus). Ecology 62:252–272

    Article  Google Scholar 

  • Hoogland JL (1995) The black-tailed prairie dog: social life of a burrowing mammal. University of Chicago Press, Chicago, IL

    Google Scholar 

  • Hoogland JL (1999) Philopatry, dispersal, and social organization of Gunnison’s prairie dogs. J Mammal 80:243–251

    Article  Google Scholar 

  • Hoogland JL (2001) Black-tailed, Gunnison’s, and Utah prairie dogs all reproduce slowly. J Mammal 82:917–927

    Article  Google Scholar 

  • Hoogland JL (2003a) Prairie dogs. In: Feldhamer GA, Thompson BC, Chapman JA (eds) Wild mammals of North America. Johns Hopkins University Press, Baltimore, MD, pp 232–247

    Google Scholar 

  • Hoogland JL (2003b) Sexual dimorphism in five species of prairie dogs. J Mammal 84:1254–1266

    Article  Google Scholar 

  • Hoogland JL (2007) Alarm calling, multiple mating, and infanticide among black-tailed Gunnison’s, and Utah prairie dogs. In: Wolff JO, Sherman PW (eds) Rodent societies. University of Chicago Press, Chicago, IL, pp 438–452

    Google Scholar 

  • Hoogland JL, Sherman PW (1976) Advantages and disadvantages of Bank Swallow (Riparia riparia) coloniality. Ecol Monogr 46:33–58

    Article  Google Scholar 

  • Hoogland JL, Tamarin RH, Levy CK (1989) Communal nursing in prairie dogs. Behav Ecol Sociobiol 24:91–95

    Article  Google Scholar 

  • Hoogland JL, Davis S, Benson-Amram S, LaBruna D, Goossens B, Hoogland MA (2004) Pyraperm halts plague among Utah prairie dogs. Southwest Nat 49:376–383

    Article  Google Scholar 

  • Hoogland JL, Cannon KE, DeBarbieri LM, Manno TG (2006) Selective predation on Utah prairie dogs. Am Nat 168:546–552

    Article  PubMed  Google Scholar 

  • Hrdy SB (1977) The langurs of Abu. Harvard University Press, Cambridge, MA

    Google Scholar 

  • Knight MH, Vanjaarsveld AS, Mills MGL (1992) Allo-suckling in spotted hyaenas (Crocuta crocuta): an example of behavioural flexibility in carnivores. Afr J Ecol 30:245–251

    Article  Google Scholar 

  • Konig B (1994a) Communal nursing in mammals. Verh Dtsch Zool Ges 87:115–127

    Google Scholar 

  • Konig B (1994b) Fitness effects of communal rearing in house mice: the role of relatedness versus familiarity. Anim Behav 48:1449–1457

    Article  Google Scholar 

  • Lawick H (1974) Solo: the story of an African wild dog. Collins, London, UK

    Google Scholar 

  • LeBoeuf BJ, Briggs KT (1977) The cost of living in a seal harem. Mammalia 41:168–195

    Google Scholar 

  • Lee PC (1987) Allomothering among African elephants. Anim Behav 35:275–291

    Google Scholar 

  • Leger DW, Owings DH (1978) Responses to alarm calls by California ground squirrels: effects of call structure and maternal status. Behav Ecol Sociobiol 3:177–186

    Article  Google Scholar 

  • Loudon ASI (1985) Lactation and neonatal survival of mammals. Symp Zool Soc Lond 54:183–207

    Google Scholar 

  • Loudon ASI, McNeilly AS, Milne JA (1983) Nutrition and lactational control of fertility in red deer. Nature 302:145–147

    Article  PubMed  CAS  Google Scholar 

  • MacDonald DW, Moehlman PD (1983) Cooperation, altruism, and restraint in the reproduction of carnivores. In: Bateson PPG, Klopfer P (eds) Perspectives in ethology and ontogeny, volume 5. Plenum Press, New York, NY, pp 433–467

    Google Scholar 

  • Manning CJ, Dewsbury DA, Wakeland EK, Potts WK (1995) Communal nesting and communal nursing in house mice, Mus musculus domesticus. Anim Behav 50:741–751

    Article  Google Scholar 

  • Matera L (1996) Action of pituitary and lymphocyte prolactin. Neuroimmunomodulation 4:171–180

    Google Scholar 

  • Maynard Smith J (1964) Group selection and kin selection. Nature 201:1145–1147

    Article  Google Scholar 

  • McCarley H (1966) Annual cycle, population dynamics and adaptive behavior of Citellus tridecemlineatus. J Mammal 47:294–316

    Article  Google Scholar 

  • McCracken GF (1984) Communal nursing in Mexican free-tailed bat maternity colonies. Science 223:1090–1091

    Article  PubMed  CAS  Google Scholar 

  • McCracken GF, Gustin MK (1991) Nursing behavior in Mexican free-tailed bat maternity colonies. Ethology 89:305–321

    Article  Google Scholar 

  • McKaye KR (1981) Natural selection and the evolution of interspecific brood care in fishes. In: Alexander R, Tinkle D (eds) Natural selection and social behavior. Chiron Press, New York, NY, pp 177–183

    Google Scholar 

  • McKaye KR, McKaye NM (1977) Communal care and kidnapping of young by parental cichlids. Evolution 31:674–681

    Article  Google Scholar 

  • Mendl M, Paul ES (1989) Observations of nursing and sucking behaviour as an indicator of milk transfer and parental investment. Anim Behav 37:513–515

    Article  Google Scholar 

  • Michener GR (1973) Field observations on the social relationships between adult female and juvenile Richardson’s ground squirrels. Can J Zool 15:33–38

    Article  Google Scholar 

  • Michener GR (1974) Development of adult-young identification in Richardson’s ground squirrel. Dev Psychobiol 7:375–384

    Article  PubMed  CAS  Google Scholar 

  • Michener GR (1989) Reproductive effort during gestation and lactation by Richardson’s ground squirrels. Oecologia 78:77–86

    Article  Google Scholar 

  • Murphey RM, Paranhos da Costa MJR, da Silva RG, de Souza RC (1995) Allonursing in river buffalo, Bubalus bubalis: nepotism, incompetence, or thievery? Anim Behav 49:1611–1616

    Article  Google Scholar 

  • O’Brien TG, Robinson JG (1991) Allomaternal care by female wedge-capped capuchin monkeys: effects of age, rank and relatedness. Behaviour 119:30–50

    Article  Google Scholar 

  • Packard JM, Seal US, Mech LD, Plotka ED (1985) Causes of reproductive failure in two family groups of wolves (Canis lupus). Z Tierpsychol 68:24–40

    Google Scholar 

  • Packer C, Lewis S, Pusey A (1992) A comparative analysis of non-offspring nursing. Anim Behav 43:265–281

    Article  Google Scholar 

  • Patterson IJ (1965) Timing and spacing of broods in the black-headed gull Larus ridibundus. Ibis 107:433–459

    Article  Google Scholar 

  • Pizzimenti JJ (1975) Evolution of the prairie dog genus Cynomys. Occas Pap Mus Nat Hist Univ Kans 39:1–73

    Google Scholar 

  • Pizzimenti JJ, Collier GD (1975) Cynomys parvidens. Mamm Spec 52:1–3

    Article  Google Scholar 

  • Plesner Jensen S, Siefert L, Okori JJL, Clutton-Brock TH (1999) Age-related participation in allosuckling by nursing warthogs (Phacochoerus africanus). J Zool 248:443–449

    Article  Google Scholar 

  • Pusey AE, Packer C (1994) Non-offspring nursing in social carnivores: minimizing the costs. Behav Ecol 5:362–374

    Article  Google Scholar 

  • Rayor LS (1988) Social organization and space-use in Gunnison’s prairie dog. Behav Ecol Sociobiol 22:69–78

    Article  Google Scholar 

  • Reiter J, Stinson NL, LeBoeuf BJ (1978) Northern elephant seal development: the transition from weaning to nutritional independence. Behav Ecol Sociobiol 3:337–367

    Article  Google Scholar 

  • Reiter J, Panken KJ, LeBoeuf BJ (1981) Female competition and reproductive success in northern elephant seals. Anim Behav 29:670–687

    Article  Google Scholar 

  • Riedman ML (1982) The evolution of alloparental care and adoption in mammals and birds. Q Rev Biol 57:405–435

    Article  Google Scholar 

  • Riedman ML, LeBoeuf BJ (1982) Mother-pup separation and adoption in northern elephant seals. Behav Ecol Sociobiol 11:203–215

    Article  Google Scholar 

  • Roberts WM, Rodriguez JP, Good TC, Dobson AP (2000) Population viability analysis of the Utah prairie dog. Environmental Defense Report, Washington, DC pp 1–49

  • Rood J (1980) Mating relationships and breeding suppression in the dwarf mongoose. Anim Behav 28:143–150

    Article  Google Scholar 

  • Rood JP (1990) Group size, survival, reproduction, and routes to breeding in dwarf mongooses. Anim Behav 39:566–572

    Article  Google Scholar 

  • Roulin A (2002) Why do lactating females nurse foster offspring? A review of hypotheses and empirical evidence. Anim Behav 63:201–208

    Article  Google Scholar 

  • Roulin A (2003) The neuroendocrine function of allosuckling. Ethology 109:185–195

    Article  Google Scholar 

  • Roulin A, Hager R (2003) Indiscriminate nursing in communal breeders: a role for genomic imprinting. Ecol Lett 6:165–166

    Article  Google Scholar 

  • Roulin A, Heeb P (1999) The immunological function of allosuckling. Ecol Lett 2:319–324

    Article  Google Scholar 

  • Sams MG, Lochmiller RL Jr, Qualls CW Jr, Leslie DM, Payton ME (1996) Physiological correlates of neonatal mortality in an overpopulated herd of white-tailed deer. J Mammal 77:179–190

    Article  Google Scholar 

  • Saylor A, Salmon M (1971) An ethological analysis of communal nursing by the house mouse (Mus musculus). Behaviour 40:62–85

    Article  Google Scholar 

  • Slade NA, Balph DF (1974) Population ecology of Uinta ground squirrels. Ecology 55:989–1003

    Article  Google Scholar 

  • Taber AB, Macdonald DW (1992) Communal breeding in the mara, Dolichotis patagonum. J Zool 227:439–452

    Article  Google Scholar 

  • Trillmich F (1981) Mutual mother-pup recognition in Galapagos fur seals and sea lions: cues used and functional significance. Behaviour 78:21–42

    Article  Google Scholar 

  • Trivers RL (1971) The evolution of reciprocal altruism. Q Rev Biol 46:35–57

    Article  Google Scholar 

  • Vine I (1971) Risk of visual detection and pursuit by a predator and the selective advantage of flocking behaviour. J Theor Biol 30:405–422

    Article  PubMed  CAS  Google Scholar 

  • Watkins LC, Shump KA (1981) Roosting behavior in the evening bat, Nycteceius humeralis. Am Midl Nat 105:258–268

    Article  Google Scholar 

  • West SA, Pen I, Griffin AS (2002) Conflict and cooperation—cooperation and competition between relatives. Science 296:72–75

    Article  PubMed  CAS  Google Scholar 

  • West-Eberhard MJ (1975) The evolution of social behavior by kin selection. Q Rev Biol 50:1–33

    Article  Google Scholar 

  • Wilkinson GS (1992) Communal nursing in the evening bat, Nycticeius humeralis. Behav Ecol Sociobiol 31:225–235

    Article  Google Scholar 

  • Williams TD (1994) Adoption in a precocial species, the lesser snow goose: intergenerational conflict, altruism or a mutually beneficial strategy? Anim Behav 47:101–107

    Article  CAS  Google Scholar 

  • Wright-Smith MA (1978) The ecology and social organization of Cynomys parvidens (Utah prairie dog) in south central Utah. MS thesis. Indiana University, Bloomington, IN

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Acknowledgments

For financial assistance, I thank the Denver Zoological Foundation, the National Geographic Society, the National Science Foundation, and the University of Maryland. For help with the manuscript, I thank Dan Blumstein, Gerald Wilkinson, and two anonymous referees. For help with observing nursing of own and foster offspring, I thank my research assistants from 1995 through 2005, and I especially thank Elaine Bond, Kristin Cannon, Lili DeBarbieri, Sarah Druy, Theo Manno, and Alyssa Taylor. My research complies with current laws of the USA and was approved by the Institutional Animal Care and Use Committee of the University of Maryland Center for Environmental Science.

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Hoogland, J.L. Nursing of own and foster offspring by Utah prairie dogs (Cynomys parvidens). Behav Ecol Sociobiol 63, 1621–1634 (2009). https://doi.org/10.1007/s00265-009-0763-0

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