Skip to main content
Log in

Ecological and hormonal correlates of antipredator behavior in adult Belding’s ground squirrels (Spermophilus beldingi)

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

Abstract

Predator–prey relationships provide an excellent opportunity to study coevolved adaptations. Decades of theoretical and empirical research have illuminated the various behavioral adaptations exhibited by prey animals to avoid detection and capture, and recent work has begun to characterize physiological adaptations, such as immune reactions, metabolic changes, and hormonal responses to predators or their cues. A 2-year study quantified the activity budgets and antipredator responses of adult Belding’s ground squirrels (Spermophilus beldingi) living in three different California habitats and likely experiencing different predation pressures. At one of these sites, which is visually closed and predators and escape burrows are difficult to see, animals responding to alarm calls remain alert longer and show more exaggerated responses than adults living in two populations that likely experience less intense predation pressure. They also spend more time alert and less time foraging than adults at the other two sites. A 4-year study using noninvasive fecal sampling of cortisol metabolites revealed that S. beldingi living in the closed site also have lower corticoid levels than adults at the other two sites. The lower corticoids likely reflect that predation risk at this closed site is predictable, and might allow animals to mount large acute cortisol responses, facilitating escape from predators and enhanced vigilance while also promoting glucose storage for the approaching hibernation. Collectively, these data demonstrate that local environments and perceived predation risk influence not only foraging, vigilance, and antipredator behaviors, but adrenal functioning as well, which may be especially important for obligate hibernators that face competing demands on glucose storage and mobilization.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Abbott DH, Keverne EB, Bercovitch FB, Shively CA, Mendoza SP, Saltzman W, Snowdon CT, Ziegler TE, Banjevic M, Garland TJ, Sapolsky RM (2003) Are subordinates always stressed? A comparative analysis of rank differences in cortisol levels among primates. Horm Behav 43:67–82

    Article  PubMed  CAS  Google Scholar 

  • Alberts SC (1994) Vigilance in young baboons: effects of habitat, age, sex and maternal rank on glance rate. Anim Behav 47:749–755

    Article  Google Scholar 

  • Altmann J (1974) Observational study of behavior: sampling methods. Behaviour 49:227–267

    PubMed  CAS  Google Scholar 

  • Apfelbach R, Blanchard CD, Blanchard RJ, Hayes RA, McGregor IS (2005) The effects of predator odors in mammalian prey species: a review of field and laboratory studies. Neurosci Biobehav Rev 29:1123–1144

    Article  PubMed  Google Scholar 

  • Astheimer LB, Buttemer WA, Wingfield JC (1995) Seasonal and acute changes in adrenocortical responsiveness in an arctic-breeding bird. Horm Behav 29:442–457

    Article  Google Scholar 

  • Bachman GC (1993) The effect of body condition on the trade-off between vigilance and foraging in Belding’s ground squirrels. Anim Behav 46:233–244

    Article  Google Scholar 

  • Beehner JC, Whitten PL (2004) Modifications of a field method for fecal steroid analysis in baboons. Physiol Behav 82:269–277

    Article  PubMed  CAS  Google Scholar 

  • Bian JH, Wu Y, Liu J (2005) Effect of predator-induced maternal stress during gestation on growth in root voles Microtus oeconomus. Acta Theriol 50:473–482

    Google Scholar 

  • Blanchard RJ, Nikulina JN, Sakai RR, McKittrick C, McEwen BS, Blanchard DC (1998) Behavioral and endocrine change following chronic predatory stress. Physiol Behav 63:561–569

    Article  PubMed  CAS  Google Scholar 

  • Blumstein DT, Runyan A, Seymour M, Nicodemus A, Ozgul A, Ransler F, Im S, Stark T, Zugmeyer C, Daniel JC (2004) Locomotor ability and wariness in yellow-bellied marmots. Ethology 110:615–634

    Article  Google Scholar 

  • Boonstra R (2005) Equipped for life: the adaptive role of the stress axis in male mammals. J Mammal 86:236–247

    Article  Google Scholar 

  • Boonstra R, McColl CJ (2000) Contrasting stress response of male Arctic ground squirrels and red squirrels. J Exp Zool 286:390–404

    Article  PubMed  CAS  Google Scholar 

  • Boonstra R, Singleton GR (1993) Population declines in the snowshoe hare and the role of stress. Gen Comp Endocrinol 91:126–143

    Article  PubMed  CAS  Google Scholar 

  • Boonstra R, Hik D, Singleton GR, Tinnikov A (1998) The impact of predator-induced stress on the snowshoe hare cycle. Ecol Monogr 68:371–394

    Article  Google Scholar 

  • Boswell T, Woods SC, Kenagy GJ (1994) Seasonal changes in body mass, insulin, and glucocorticoids of free-living golden-mantled ground squirrels. Gen Comp Endocrinol 96:339–346

    Article  PubMed  CAS  Google Scholar 

  • Brown C, Gardner C, Braithwaite VA (2005) Differential stress responses in fish from areas of high- and low-predation pressure. J Comp Physiol B 175:305–312

    Article  Google Scholar 

  • Caro TM (1994) Cheetahs of the Serengeti Plains: group living in an asocial species. University of Chicago Press, Chicago

    Google Scholar 

  • Casolini P, Cigliana G, Alema GS, Ruggieri V, Angelucci L, Catalani A (1997) Effect of increased maternal corticosterone during lactation on hippocampal corticosteroid receptors, stress response and learning in offspring in the early stages of life. Neuroscience 79:1005–1012

    Article  PubMed  CAS  Google Scholar 

  • Cavigelli SA (1999) Behavioural patterns associated with faecal cortisol levels in free-ranging female ring-tailed lemurs, Lemur catta. Anim Behav 57:935–944

    Article  PubMed  Google Scholar 

  • Cavigelli SA, Monfort SL, Whitney TK, Mechref YS, Novotny M, McClintock MK (2005) Frequent serial fecal corticoid measures from rats reflect circadian and ovarian corticosterone rhythms. J Endocrinol 184:153–163

    Article  PubMed  CAS  Google Scholar 

  • Clinchy M, Zanette L, Boonstra R, Wingfield JC, Smith JNM (2004) Balancing food and predator pressure induces chronic stress in songbirds. Proc R Soc Lond B Biol Sci 271:2473–2479

    Article  Google Scholar 

  • Cockrem JF, Silverin B (2002) Sight of a predator can stimulate a corticosterone response in the great tit (Parus major). Gen Comp Endocrinol 125:248–255

    Article  PubMed  CAS  Google Scholar 

  • Creel S (2005) Dominance, aggression and glucocorticoid levels in social carnivores. J Mammal 86:255–264

    Article  Google Scholar 

  • Cresswell W, Quinn JL (2004) Faced with a choice, sparrow hawks more often attack the more vulnerable prey group. Oikos 104:71–76

    Article  Google Scholar 

  • Downes SJ, Adams M (2001) Geographic variation in antisnake tactics: the evolution of scent-mediated behavior in a lizard. Evolution 55:605–615

    Article  PubMed  CAS  Google Scholar 

  • Dufty AM, Crandall MB (2005) Corticosterone secretion in response to adult alarm calls in American kestrels. J Field Ornithol 76:319–325

    Google Scholar 

  • Ebensperger LA, Hurtado MJ (2005) On the relationship between herbaceous cover and vigilance activity of degus (Octodon degus). Ethology 111:593–608

    Article  Google Scholar 

  • Edmunds M (1974) Defense in animals: a survey of anti-predator defenses. Longmans, London

    Google Scholar 

  • Eilam D, Dayan T, Ben-Eliyahu S, Schulman I, Shefer G, Hendrie CA (1999) Differential behavioural and hormonal responses of voles and spiny mice to owl calls. Anim Behav 58:1085–1093

    Article  PubMed  Google Scholar 

  • Elgar MA (1989) Predator vigilance and group size in mammals and birds: a critical review of the empirical evidence. Biol Rev 64:13–33

    PubMed  CAS  Google Scholar 

  • Endler JA (1995) Multiple-trait coevolution and environmental gradients in guppies. Trends Ecol Evol 10:22–29

    Article  Google Scholar 

  • Foster SA (1999) The geography of behaviour: an evolutionary perspective. Trends Ecol Evol 14:190–195

    Article  PubMed  Google Scholar 

  • Fraser DF, Gilliam JF (1987) Feeding under predation hazard: response of the guppy and Hart’s rivulus from sites with contrasting predation hazard. Behav Ecol Sociobiol 21:203–209

    Article  Google Scholar 

  • Goldsmith AE (1990) Vigilance behavior of pronghorns in different habitats. J Mammal 71:460–462

    Article  Google Scholar 

  • Goymann W, East ML, Wachter B, Honer OP, Möstl E, Van’t Hof TJ, Hofer H (2001) Social, state-dependent and environmental modulation of faecal corticosteroid levels in free-ranging female spotted hyenas. Proc R Soc Lond B Biol Sci 268:2453–2459

    Article  CAS  Google Scholar 

  • Griffin AS, Evans CS, Blumstein DT (2001) Learning specificity in acquired predator recognition. Anim Behav 62:577–589

    Article  Google Scholar 

  • Hayward LS, Wingfield JC (2004) Maternal corticosterone is transferred to avian yolk and may alter offspring growth and adult phenotype. Gen Comp Endocrinol 135:365–371

    Article  PubMed  CAS  Google Scholar 

  • Herzog HA, Schwartz JM (1990) Geographical variation in the anti-predator behaviour of neonate garter snakes, Thamnophis sirtalis. Anim Behav 40:597–598

    Article  Google Scholar 

  • Hik DS, McColl CJ, Boonstra R (2001) Why are Arctic ground squirrels more stressed in the boreal forest than in alpine meadows? Ecoscience 8:275–288

    Google Scholar 

  • Holmes WG (1984) Predation risk and foraging behavior of the hoary marmot in Alaska. Behav Ecol Sociobiol 15:293–301

    Article  Google Scholar 

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

    Google Scholar 

  • Hubbs AH, Millar JS, Wiebe JP (2000) Effect of brief exposure to a potential predator on cortisol concentrations in female Columbian ground squirrels (Spermophilus columbianus). Can J Zool 78:578–587

    Article  CAS  Google Scholar 

  • Khan MZ, Altmann J, Isani SS, Yu J (2002) A matter of time: evaluating the storage of fecal samples for steroid analysis. Gen Comp Endocrinol 128:57–64

    Article  PubMed  CAS  Google Scholar 

  • Kotrschal K, Hirschenhauser K, Möstl E (1998) The relationship between social stress and dominance is seasonal in greylag geese. Anim Behav 55:171–176

    Article  PubMed  Google Scholar 

  • LaGory KE (1986) Habitat, group size, and the behaviour of white-tailed deer. Behaviour 98:168–179

    Google Scholar 

  • Lima SL (1998) Stress and decision making under the risk of predation: recent developments from behavioral, reproductive, and ecological perspectives. Adv Study Behav 27:215–290

    Google Scholar 

  • Longland WS, Price MV (1991) Direct observations of owls and heteromyid rodents: can predation risk explain microhabitat use? Ecology 72:2261–2273

    Article  Google Scholar 

  • Loughry WJ (1988) Population differences in how black-tailed prairie dogs deal with snakes. Behav Ecol Sociobiol 22:61–67

    Article  Google Scholar 

  • Magurran AE (1990) The inheritance and development of minnow anti-predator behaviour. Anim Behav 39:834–842

    Article  Google Scholar 

  • Mateo JM (1995) The development of alarm-call responses in free-living and captive Belding’s ground squirrels, Spermophilus beldingi. Ph.D. thesis, University of Michigan

  • Mateo JM (1996) The development of alarm-call response behaviour in free-living juvenile Belding’s ground squirrels. Anim Behav 52:489–505

    Article  Google Scholar 

  • Mateo JM (2006) Developmental and geographic variation in stress hormones in wild Belding’s ground squirrels (Spermophilus beldingi). Horm Behav 50:718–725

    Article  PubMed  CAS  Google Scholar 

  • Mateo JM, Cavigelli SA (2005) A validation of extraction methods for non-invasive sampling of glucocorticoids in free-living ground squirrels. Physiol Biochem Zool 78:1069–1084

    Article  PubMed  CAS  Google Scholar 

  • Mateo JM, Holmes WG (1997) Development of alarm-call responses in Belding’s ground squirrels: the role of dams. Anim Behav 54:509–524

    Article  PubMed  Google Scholar 

  • Mateo JM, Holmes WG (1999) Plasticity of alarm-call response development in Belding’s ground squirrels (Spermophilus beldingi, Sciuridae). Ethology 105:193–206

    Article  Google Scholar 

  • McCormick MI (1998) Behaviorally induced maternal stress in a fish influences progeny quality by a hormonal mechanism. Ecology 79:1873–1883

    Google Scholar 

  • Metcalfe NB (1984) The effect of habitat on the vigilance of shorebirds: is visibility important? Anim Behav 32:981–985

    Article  Google Scholar 

  • Mills MGL, Broomhall LS, du Toit JT (2004) Cheetah Acinonyx jubatus feeding ecology in the Kruger National Park and a comparison across African savanna habitats: is the cheetah only a successful hunter on open grassland plains? Wildlife Biol 10:177–186

    Google Scholar 

  • Miner BG, Sultan SE, Morgan SG, Padilla DK, Relyea RA (2005) Ecological consequences of phenotypic plasticity. Trends Ecol Evol 20:685–692

    Article  PubMed  Google Scholar 

  • Mirza RS, Mathis A, Chivers DP (2006) Does temporal variation in predation risk influence the intensity of antipredator responses? A test of the risk allocation hypothesis. Ethology 112:44–51

    Article  Google Scholar 

  • Morton ML (1975) Seasonal cycles of body weights and lipids in Belding ground squirrels. Bull South Calif Acad Sci 74:128–143

    Google Scholar 

  • Murie JO, Boag DA (1984) The relationship of body weight to overwinter survival in Columbian ground squirrels. J Mammal 65:688–690

    Article  Google Scholar 

  • Owings DH, Coss RG (2007) Social and antipredator systems: intertwining links in multiple time frames. In: Wolff JO, Sherman PW (eds) Rodent societies. University of Chicago Press, Chicago

    Google Scholar 

  • Owings DH, Virginia RA (1978) Alarm calls of California ground squirrels (Spermophilus beecheyi). Z Tierpsychol 46:58–70

    Google Scholar 

  • Owings DH, Coss RG, McKernon D, Rowe MP, Arrowood PC (2001) Snake-directed antipredator behavior of rock squirrels (Spermophilus variegatus): population differences and snake-species discrimination. Behaviour 138:575–595

    Article  Google Scholar 

  • Palme R, Rettenbacher S, Touma C, El-Bahr SM, Möstl E (2005) Stress hormones in mammals and birds: comparative aspects regarding metabolism, excretion, and noninvasive measurement in fecal samples. Ann N Y Acad Sci 1040:162–171

    Article  PubMed  CAS  Google Scholar 

  • Partecke J, Schwabl I, Gwinner E (2006) Stress and the city: urbanization and its effects on the stress physiology in European blackbirds. Ecology 87:1945–1952

    Article  PubMed  Google Scholar 

  • Poran NS, Coss RG, Benjamini E (1987) Resistance of California ground squirrels (Spermophilus beecheyi) to the venom of the Northern Pacific rattlesnake (Crotalus viridis oreganus): a study of adaptive variation. Toxicon 25:767–777

    Article  PubMed  CAS  Google Scholar 

  • Pride RE (2005) Foraging success, agonism, and predator alarms: behavioral predictors of cortisol in Lemur catta. Int J Primatol 26:295–319

    Article  Google Scholar 

  • Reeder DM, Kramer KM (2005) Stress in free-ranging mammals: integrating physiology, ecology, and natural history. J Mammal 86:225–235

    Article  Google Scholar 

  • Richards DG, Wiley RH (1980) Reverberations and amplitude fluctuations in the propagation of sound in a forest: implications for animal communication. Am Nat 115:381–399

    Article  Google Scholar 

  • Rogovin K, Randall JA, Kolosova I, Moshkin M (2004) Predation on a social desert rodent, Rhombomys opimus: effect of group size, composition, and location. J Mammal 85:723–730

    Article  Google Scholar 

  • Romero LM (2002) Seasonal changes in plasma glucocorticoid concentrations in free-living vertebrates. Gen Comp Endocrinol 128:1–24

    Article  PubMed  CAS  Google Scholar 

  • Ruxton GD, Sherratt TM, Speed MP (2004) Avoiding attack: the evolutionary ecology of crypsis, warning signals and mimicry. Oxford University Press, Oxford

    Google Scholar 

  • Sapolsky RM, Romero LM, Munck AU (2000) How do glucocorticoids influence stress-responses? Integrating permissive, suppressive, stimulatory, and adaptive actions. Endocr Rev 21:55–89

    Article  PubMed  CAS  Google Scholar 

  • Schooley RL, Sharpe PB, Van Horne B (1996) Can shrub cover increase predation risk for a desert rodent? Can J Zool 74:157–163

    Article  Google Scholar 

  • Schwagmeyer PL, Brown CH (1981) Conspecific reaction to playback of thirteen-lined ground squirrel vocalizations. Z Tierpsychol 56:25–32

    Google Scholar 

  • Sharpe PB, Van Horne B (1998) Influence of habitat on behavior of Townsend’s ground squirrels (Spermophilus townsendii). J Mammal 79:906–918

    Article  Google Scholar 

  • Sherman PW (1976) Natural selection among some group-living organisms. Ph.D. thesis, University of Michigan

  • Sherman PW, Morton ML (1984) Demography of Belding’s ground squirrels. Ecology 65:1617–1628

    Article  Google Scholar 

  • Siegel S, Castellan NJ (1988) Nonparametric statistics for the behavioral sciences. McGraw-Hill, New York

    Google Scholar 

  • Virgin CE, Sapolsky RM (1997) Styles of male social behavior and their endocrine correlates among low-ranking baboons. Am J Primatol 42:25–39

    Article  PubMed  CAS  Google Scholar 

  • Wingfield JC (2004) Control of behavioural strategies for capricious environments. Anim Behav 66:807–816

    Article  Google Scholar 

  • Ylönen H, Eccard JA, Jokinen I, Sundell J (2006) Is the antipredatory response in behaviour reflected in stress measured in faecal corticosteroids in a small rodent? Behav Ecol Sociobiol

Download references

Acknowledgements

I thank Melanie Brooks, Jared Bruck, Jason Bruck, Matthew Heintz, Anne Janas, Becca Kordas, Ella Malamud, Meredith Nelson, Kara Nuss, Caroline Pitt, and Wendy Tidhar for assistance in the field, Jocelyn Bryant for conducting the hormone assays, and Sonia Cavigelli, Warren Holmes, Nancy Peters, and anonymous reviewers for critical readings of the manuscript. I also thank Dan Leger for providing some of the S. beldingi alarm-call recordings used here. These studies were approved by Cornell University (4/20/00; # 00-32), the University of Chicago (11/26/02; # 71255), and University of California at Santa Barbara (3/30/00; # 4-00-532; 5-03-532) and adhere to standards set forth by the US NIH for animal research. This work was supported by the NIMH.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Jill M. Mateo.

Additional information

Communicated by P. Heeb and T. Czeschlik

Rights and permissions

Reprints and permissions

About this article

Cite this article

Mateo, J.M. Ecological and hormonal correlates of antipredator behavior in adult Belding’s ground squirrels (Spermophilus beldingi). Behav Ecol Sociobiol 62, 37–49 (2007). https://doi.org/10.1007/s00265-007-0436-9

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00265-007-0436-9

Keywords

Navigation