Skip to main content

Advertisement

SpringerLink
Log in

Does lactation lead to resource allocation trade-offs in the spotted hyaena?

  • Original Paper
  • Published:
Behavioral Ecology and Sociobiology Aims and scope Submit manuscript

Abstract

Life history theory predicts that when food intake and body reserves are insufficient to maintain all life processes, resource allocation trade-offs should occur. Lactation is costly and requires increased food intake. In spotted hyaenas, energy expenditure on lactation is high, particularly for mothers rearing twin litters, and foraging effort and food intake are influenced by social status. We investigated whether lactation in this species results in a reduction in resource allocation to immune processes sufficient to increase parasite infection. We expected higher parasite infection in lactating than non-lactating females, in mothers nursing twin than singleton litters, in females of lower than higher social status and in less than more experienced foragers. We quantified Ancylostoma egg load (AEL) and the presence of oocysts of Cystoisospora spp. as a proxy measure of immune function in 58 females. Lactating females were significantly more often infected with Ancylostoma, and their AEL was higher than in non-lactating females. Females nursing twins had significantly higher AELs than those nursing singletons. As social status increased, AELs significantly declined. This relationship was modulated by lactation status and litter size, being strongest in non-lactating females, moderate in females with twin litters and weakest in females with singleton litters. The decrease in AEL with increasing social status was greater for experienced than inexperienced females. Concurrent infection with Cystoisospora significantly increased with increasing AEL. Our results provide evidence for a resource allocation trade-off in lactating spotted hyaenas.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Anderson RM, Schad GA (1985) Hookworm burdens and faecal egg counts: an analysis of the biological basis of variation. Trans R Soc Trop Med Hyg 79:812–825

    Article  CAS  PubMed  Google Scholar 

  • Anthony RM, Rutitzky LI, Urban JF, Stadecker MJ, Gause WC (2007) Protective immune mechanisms in helminth infection. Nat Rev Immunol 7:975–987

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Apanius V, Deerenberg C, Visser H, Daan S (1994) Reproductive effort and parasite resistance: evidence of an energy based trade-off. J Ornithol 135:404

    Google Scholar 

  • Archie EA, Altmann J, Alberts SC (2014) Costs of reproduction in a long-lived female primate: injury risk and wound healing. Behav Ecol Sociobiol 68:1183–1193

    Article  PubMed  Google Scholar 

  • Ardia DR, Parmentier HK, Vogel LA (2011) The role of constrains and limitations in driving individual variation in immune response. Funct Ecol 25:61–73

    Article  Google Scholar 

  • Barclay RMR (1989) The effect of reproductive condition on the foraging behaviour of female hoary bats, Lasiurus cinereus. Behav Ecol Sociobiol 24:31–37

    Article  Google Scholar 

  • Baylis HA (1937) Records of some helminths from the spotted hyaena. Ann Mag Nat Hist 20:438–441

    Article  Google Scholar 

  • Beldomenico PM, Telfer S, Gebert S, Lukomski L, Bennett M, Begon M (2008) Poor condition and infection: a vicious circle in natural populations. Proc R Soc Lond B 275:1753–1759

    Article  Google Scholar 

  • Besedovsky HO, Del Rey A (1996) Immune–neuroendocrine interactions: facts and hypotheses. Endocr Rev 17:64–102

    Article  CAS  PubMed  Google Scholar 

  • Bowman DD (2002) Feline clinical parasitology. Iowa State Univ. Press, Ames

    Book  Google Scholar 

  • Boyd IL (1999) Foraging and provisioning in arctic fur seals: interannual variability in time–energy budgets. Behav Ecol 10:198–208

    Article  Google Scholar 

  • Bulmer MG (1974) On fitting the Poisson lognormal distribution to species-abundance data. Biometrics 30:101–110

    Article  Google Scholar 

  • Burke TM, Roberson EL (1985) Prenatal and lactational transmission of Toxocara canis and Ancylostoma caninum: experimental infection of the bitch before pregnancy. Int J Parasitol 15:71–75

    Article  CAS  PubMed  Google Scholar 

  • Cattadori IM, Boag B, Bjørnstad, Cornell SJ, Hudson PJ (2005) Peak shift and epidemiology in a seasonal host–nematode system. Proc R Soc Lond B 272:1163–1169

    Article  CAS  Google Scholar 

  • Cattadori IM, Albert R, Boag B (2007) Variation in host susceptibility and infectiousness generated by co-infection: the myxoma-Trichostrongylus retortaeformis case in rabbits. J R Soc Interface 4:831–840

    Article  PubMed Central  PubMed  Google Scholar 

  • Christe P, Arlettaz R, Vogel P (2000) Variation in intensity of a parasitic mite (Spinturnix myoti) in relation to the reproductive cycle and immunocompetence of its bat host (Myotis myotis). Ecol Lett 3:207–212

    Article  Google Scholar 

  • Clutton-Brock TH, Huchard E (2013) Social competition and its consequences in female mammals. J Zool 289:151–171

    Article  Google Scholar 

  • Coop RL, Kyriazakis I (1999) Nutrition–parasite interactions. Vet Parasitol 84:187–204

    Article  CAS  PubMed  Google Scholar 

  • Curno O, Behnke JM, McElligott AG, Reader T, Barnard CJ (2008) Mothers produce less aggressive sons with altered immunity where there is a threat of disease during pregnancy. Proc R Soc Lond B 276:1047–1054

    Article  Google Scholar 

  • Debeffe L, Morellet N, Verheyden-Tixier H, Hoste H, Gaillard J-M, Cargnelutti B, Picot D, Sevila J, Hewison AJM (2014) Parasite abundance contributes to condition-dependent dispersal in a wild population of large herbivore. Oikos 123:1121–1125

    Google Scholar 

  • East ML, Hofer H (2001) Male spotted hyaenas Crocuta crocuta queue for status in social groups dominated by females. Behav Ecol 12:558–568

    Article  Google Scholar 

  • East ML, Hofer H (2002) Conflict and cooperation in a female dominated society: a reassessment of the ‘hyperaggressive’ image of spotted hyena. Adv Study Behav 31:1–30

    Article  Google Scholar 

  • East ML, Hofer H (2013) Crocuta crocuta spotted hyaena. In: Kingdon J, Happold DCD, Butynski TM, Hoffmann M, Happold M, Kalina J (eds) Mammals of Africa, vol V. Bloomsbury, London, pp 273–281

    Google Scholar 

  • East ML, Hofer H, Wickler W (1993) The erect ‘penis’ as a flag of submission in a female dominated society: greetings in Serengeti spotted hyenas. Behav Ecol Sociobiol 33:355–370

    Article  Google Scholar 

  • East ML, Burke T, Wilhelm K, Greig C, Hofer H (2003) Sexual conflict in spotted hyenas: male and female mating tactics and their reproductive outcome with respect to age, social status and tenure. Proc R Soc Lond B 270:1247–1254

    Article  Google Scholar 

  • Eckert J, Friedhoff KT, Zahner H, Deplazes P (2008) Lehrbuch der Parasitologie für die Tiermedizin, 2nd edn. Enke, Stuttgart

    Google Scholar 

  • Engh LA, Nelson KG, Peebles R, Hernandez AD, Hubbard KK, Holekamp KE (2003) Coprologic survey of parasites of spotted hyenas (Crocuta crocuta) in the Masai Mara National Reserve, Kenya. J Wildl Dis 39:224–227

    Article  PubMed  Google Scholar 

  • Eziefula AC, Brown M (2008) Intestinal nematodes: disease burden, deworming and the potential importance of co-infection. Curr Opin Infect Dis 21:516–522

    Article  PubMed  Google Scholar 

  • Festa-Bianchet M (1989) Individual differences, parasites, and the cost of reproduction for bighorn ewes (Ovis canadensis). J Anim Ecol 58:785–795

    Article  Google Scholar 

  • Foreyt WJ (2001) Veterinary parasitology reference manual, 5th edn. Iowa State University Press, Ames

    Google Scholar 

  • French SS, DeNardo DF, Moore MC (2007) Trade-offs between reproductive and immune systems: facultative responses to reproduction. Am Nat 170:79–89

    Article  PubMed  Google Scholar 

  • Fujiwara TRT, Geiger SM, Bethony J, Mendez S (2006) Comparative immunology of human and animal models of hookworm infection. Parasite Immunol 28:285–293

    Article  CAS  PubMed  Google Scholar 

  • Gadgil M, Bossert WH (1970) Life historical consequences of natural selection. Am Nat 104:1–24

    Article  Google Scholar 

  • Germain RN (2001) The art of the probable: system control in the adaptive immune system. Science 293:240–245

    Article  CAS  PubMed  Google Scholar 

  • Glaser R, Kiecott-Glaser J (2005) Stress induced immune dysfunction: implications for health. Nat Rev Immunol 5:243–251

    Article  CAS  PubMed  Google Scholar 

  • Goymann W, East ML, Wachter B, Höner O, MöstlE V’t HTJ, Hofer H (2001) Social, state-dependent and environmental modulation of faecal corticosteroid levels in free-ranging female spotted hyaenas. Proc R Soc Lond B 268:2453–2459

    Article  CAS  Google Scholar 

  • Graber M, Blanc JP (1979) Ancylostoma duodenale (Dubini, 1843) Creplin, 1843 (Nematoda: Ancylostomidae) parasite de l’hyenetachetee Crocuta crocuta (Erxleben), en Ethiopie. Rev Elev Med Vet Pay 32:155–160

    CAS  Google Scholar 

  • Hamel S, Gaillard J-M, Yoccoz NG, Loison A, Bonenfant C, Descamps S (2010) Fitness costs of reproduction depend on life speed: empirical evidence from mammal populations. Ecol Lett 13:915–935

    Article  PubMed  Google Scholar 

  • Hayward AD (2013) Causes and consequences of intra- and inter-host heterogeneity in defence against nematodes. Parasite Immunol 35:362–373

    Google Scholar 

  • Heesen M, Rogahn S, Ostner J, Schülke (2013) Food abundance affects energy intake and reproduction in frugivorous female Assamese macaques. Behav Ecol Sociobiol 67:1053–1066

    Article  Google Scholar 

  • Hilbe JM (2009) Logistic regression models. Chapman & Hall, London

    Google Scholar 

  • Hilbe JM (2011) Negative binomial regression. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Hillegrass MA, Waterman JM, Roth JD (2010) Parasite removal increases reproductive success in a social African ground squirrel. Behav Ecol 21:696–700

    Article  Google Scholar 

  • Hofer H, East ML (1993a) The commuting system of Serengeti spotted hyaenas: how a predator copes with migratory prey. I. Social organization. Anim Behav 46:547–557

    Article  Google Scholar 

  • Hofer H, East ML (1993b) The commuting system of Serengeti spotted hyaenas: how a predator copes with migratory prey. II. Intrusion pressure and how predators cope with migratory prey. Anim Behav 46:559–574

    Article  Google Scholar 

  • Hofer H, East ML (1993c) The commuting system of Serengeti spotted hyaenas: how a predator copes with migratory prey. III. Attendance and maternal care. Anim Behav 46:575–589

    Article  Google Scholar 

  • Hofer H, East ML (1995) Population dynamics, population size, and the commuting system of Serengeti spotted hyaenas. In: Sinclair ARE, Arcese P (eds) Serengeti II: dynamics, conservation and management of an ecosystem. University of Chicago Press, Chicago, pp 332–363

    Google Scholar 

  • Hofer H, East ML (2003) Behavioural processes and costs of co-existence in female spotted hyaenas: a life history perspective. Evol Ecol 17:315–331

    Article  Google Scholar 

  • Hofer H, East ML (2008) Siblicide in Serengeti spotted hyenas: a long-term study of maternal input and cub survival. Behav Ecol Sociobiol 62:341–351

    Article  Google Scholar 

  • Hofer H, East ML (2012) Stress and immunosuppression as factors in the decline and extinction of wildlife populations. Concepts, evidence and challenges. In: Aguirre AA, Ostfeld RS, Daszak P (eds) New directions in conservation medicine: applied cases of ecological health. Oxford University Press, New York, pp 82–107

    Google Scholar 

  • Holekamp KE, Smale L, Szykman M (1996) Rank and reproduction in the female spotted hyaena. J Reprod Fertil 108:229–237

    Article  CAS  PubMed  Google Scholar 

  • Hosmer DW, Lemeshow S, Sturdivant RX (2013) Applied logistic regression, 3rd edn. Wiley, Chichester

    Book  Google Scholar 

  • Houdijk JGM, Jessop NS, Kyriazakis I (2001) Nutrient partitioning between reproductive and immune functions in animals. Proc Nutr Soc 60:515–525

    Article  CAS  PubMed  Google Scholar 

  • Houdijk JGM, Kyriazakis I, Jackson F, Huntley JF, Coop RL (2003) Is the allocation of metabolisable protein prioritised to milk production rather than to immune functions in Teladorsagia circumcincta-infected lactating ewes? Int J Parasitol 33:327–338

    Article  CAS  PubMed  Google Scholar 

  • Houston AI, Stephens PA, Boyd IL, Harding KC, McNamara JM (2006) Capital and income breeding? A theoretical model of female reproductive strategies. Behav Ecol 18:241–250

    Article  Google Scholar 

  • Houston AI, McNamara JM, Barta Z, Klasing KC (2007) The effect of energy reserves and food availability on optimal immune defence. Proc R Soc Lond B 274:2835–2842

    Article  Google Scholar 

  • Jacobs JD, Wingfield JC (2000) Endocrine control of life-cycle stages: a constraint on response to the environment. Condor 102:35–51

    Article  Google Scholar 

  • Jolles AE, Ezenwa VO, Etienne RS, Turner WC, Olff H (2008) Interactions between macroparasites and microparasites drive infection patterns in free-ranging African buffalo. Ecology 89:2239–2250

    Article  PubMed  Google Scholar 

  • Jones LA, Houdijk JGM, Sakkas P, Bruce AD, Mitchell M, Knox DP, Kyriazakis I (2011) Dissecting the impact of protein versus energy host nutrition on the expression of immunity to gastrointestinal parasites during lactation. Int J Parasitol 41:711–719

    Article  CAS  PubMed  Google Scholar 

  • Jones LA, Sakkas P, Houdijk JGM, Knox DP, Kyriazakis I (2012) Amelioration of the periparturient relaxation of immunity to parasites through a reduction in mammalian reproductive effort. Int J Parasitol 42:1127–1134

    Article  CAS  PubMed  Google Scholar 

  • Lindsay DS, Blagburn BL (1994) Biology of mammalian Isospora. Parasitol Today 10:214–220

    Article  CAS  PubMed  Google Scholar 

  • Lochmiller RL, Deerenberg C (2000) Trade-offs in evolutionary immunology: just what is the cost of immunity? Oikos 88:87–98

    Article  Google Scholar 

  • Marcus AD, Higgins DP, Gray R (2014) Epidemiology of hookworm (Uncinaria sanguinis) infection in free-ranging Australian sea lion (Neophoca cinerea) pups. Parasitol Res 113:3341–3353

    Article  PubMed  Google Scholar 

  • Martin LB, Weil ZM, Nelson RJ (2008) Seasonal change in vertebrate immune activity: mediated by physiological trade-offs. Philos Trans Roy Soc B 363:321–339

    Article  Google Scholar 

  • McEwen BS, Brunson KW, Bullock K, Chambers WH, Dhabhar FS, Goldfarb RH, Kitson RP, Miller AH, Spencer RL, Weis JM (1997) The role of adrenocorticoids as modulators of immune function in health anddisease: neural, endocrine and immune interactions. Brain Res Rev 23:79–133

    Article  CAS  PubMed  Google Scholar 

  • McNamara JM, Houston AI (1996) State-dependent life histories. Nature 380:215–221

    Article  CAS  PubMed  Google Scholar 

  • Meyer-Lucht Y, Sommer S (2005) MHC diversity and the association to nematode parasitism in the yellow-necked mouse (Apodemus flavicollis). Mol Ecol 14:2233–2244

    Article  CAS  PubMed  Google Scholar 

  • Morrison DA (2009) Evolution of Apicomplexa: where are we now? Trends Parasitol 25:375–382

    Article  PubMed  Google Scholar 

  • Oftedal OT (1984) Milk composition, milk yield and energy output at peak lactation: a comparative review. Symp Zool Soc Lond 51:33–85

    Google Scholar 

  • Oftedal OT, Gittleman JG (1989) Patterns of energy output during reproduction in carnivores. In: Gittleman JG (ed) Carnivore behavior, ecology, and evolution. Chapman & Hall, London, pp 355–378

    Chapter  Google Scholar 

  • Patterson JEH, Neuhaus P, Kutz SJ, Ruckstuhl KE (2013) Parasite removal improves reproductive success of female North American red squirrels (Tamiasciurus hudsonicus). PLoS ONE 8:e55779

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Plowright RK, Field HE, Smith C, Divljan A, Palmer C, Tabor G, Daszak P, Foley JE (2008) Reproduction and nutritional stress are risk factors for hendra virus in little red flying foxes (Pteropus scapulatus). Proc R Soc Lond B 275:861–869

    Article  Google Scholar 

  • Pond CM (1977) The significance of lactation in the evolution of mammals. Evolution 31:177–199

    Article  Google Scholar 

  • Prentice AM, Goldberg GR (2000) Energy adaptations in human pregnancy: limits and long-term consequences. Am J Clin Nutr 71:1226S–1232S

    CAS  PubMed  Google Scholar 

  • Prentice AM, Whitehead RG (1987) The energetics of human reproduction. Symp Zool Soc Lond 57:275–304

    Google Scholar 

  • R Development Core Team (2014) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Available at http://www.R-project.org

  • Råberg L, Grahn M, Hasselquist D, Svensson E (1998) On the adaptive significance of stress-induced immunosuppression. Proc R Soc Lond B 265:1637–1641

    Article  Google Scholar 

  • Roff DA (1992) The evolution of life histories: theory and analysis. Chapman & Hall, London

    Google Scholar 

  • Romagnani S (1996) Understanding the role of Th1/Th2 cells in infection. Trends Microbiol 4:470–473

    Article  CAS  PubMed  Google Scholar 

  • Sheldon BC, Verhulst S (1996) Ecological immunology: costly parasite defences and trade-offs in evolutionary ecology. Trends Ecol Evol 11:317–321

    Article  CAS  PubMed  Google Scholar 

  • Speakman JR (2008) The physiological cost of reproduction in small mammals. Philos Trans Roy Soc B363:375–398

    Article  Google Scholar 

  • Stark D, Barratt JLN, van Hal S, Marriott D, Harkness J, Ellis TJ (2009) Clinical significance of enteric protozoa in the immunosuppressed human population. Clin Microbiol Rev 22:634–650

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Stearns SC (1992) The evolution of life histories. Oxford University Press, Oxford

    Google Scholar 

  • Turner WC, Versfeld WD, Kilian JW, Getz WM (2012) Synergistic effects of seasonal rainfall, parasites and demography on fluctuations in springbok body condition. J Anim Ecol 81:58–69

    Article  PubMed Central  PubMed  Google Scholar 

  • Viney ME, Riley EM, Buchanan KL (2005) Optimal immune responses: immunocompetence revisited. Trends Ecol Evol 20:665–669

    Article  PubMed  Google Scholar 

  • Wilhelm CL, Yarovinsky F (2014) Apicomplexan infections in the gut. Parasite Immunol 35:409–420

    Article  Google Scholar 

  • Wingfield JC, Maney DLI, Breuner CW, Jacobs JD, Lynn S, Ramenofsky M, Richardson RD (1998) Ecological bases of hormone–behavior interactions: the ‘emergency life history stage’. Am Zool 38:191–206

    CAS  Google Scholar 

  • Yee TW (2010) The VGAM package for categorical data analysis. J Stat Softw 32:1–34

    Google Scholar 

  • Yee TW, Wild CJ (1996) Vector generalized additive models. J Roy Stat Soc B58:481–493

    Google Scholar 

  • Zajac AM, Conboy GA (2012) Veterinary clinical parasitology, 8th edn. Blackwell, Oxford

    Google Scholar 

Download references

Acknowledgments

We thank the Tanzania Commission of Science and Technology, Tanzania National Parks and the Tanzania Wildlife Research Institute for their support of our long-term research project. We also thank the editor and two anonymous reviewers for their helpful comments and Malvina Andris, Nelly Boyer and Kerstin Wilhelm for their assistance. This work was financed by a grant awarded from the Leibniz Competitive Fund (“Pakt für Forschung und Innovation”), made possible by the Federal German government through its Ministry for Education and Research and the community of German states (“Länder”), and the Leibniz Institute for Zoo and Wildlife Research.

Ethical standards

All protocols were non-invasive and adhered to the laws and guidelines of Tanzania. Permission to conduct research in Tanzania was granted to JH, HH and MLE by the Tanzania Commission for Science and Technology. Permission to undertake research within the Serengeti National Park was granted by the Tanzanian National Parks Authority, and the research was approved by the Tanzanian Wildlife Research Institute. The research was also approved by the Ethical Committee of the Leibniz Institute for Zoo and Wildlife Research.

Author information

Authors and Affiliations

  1. Department of Evolutionary Ecology, Leibniz Institute for Zoo and Wildlife Research, Alfred-Kowalke-Strasse 17, 10315, Berlin, Germany

    Marion L. East, Ellen Otto, Janine Helms, Dagmar Thierer & Heribert Hofer

  2. School of Biosciences, Cardiff University, CF10 3AX, Cardiff, UK

    Ellen Otto & Joanne Cable

Authors
  1. Marion L. East
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ellen Otto
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Janine Helms
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Dagmar Thierer
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Joanne Cable
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Heribert Hofer
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Marion L. East.

Additional information

Communicated by M. Festa-Bianchet

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

East, M.L., Otto, E., Helms, J. et al. Does lactation lead to resource allocation trade-offs in the spotted hyaena?. Behav Ecol Sociobiol 69, 805–814 (2015). https://doi.org/10.1007/s00265-015-1897-x

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00265-015-1897-x

Keywords

Search

Navigation