Skip to main content

Advertisement

SpringerLink
Log in

Trade-offs between maternal foraging and fawn predation risk in an income breeder

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

Abstract

The choice of neonatal hiding place is critical for ungulates adopting hiding anti-predator strategies, but the consequences of different decisions have rarely been evaluated with respect to offspring survival. First, we investigated how landscape-scale choices made by roe deer fawns and their mothers affected predation risk by red foxes in a forest–farmland mosaic in southeastern Norway. After, we examined the effect of site-specific characteristics and behaviour (i.e. visibility, mother–fawn distance and abundance of the predator’s main prey item—small rodents) on predation risk. The study of habitat use, selection and habitat-specific mortality revealed that roe deer utilised the landscape matrix in a functional way, with different habitats used for feeding, providing maternal care and as refugia from predation. Mothers faced a trade-off between foraging and offspring survival. At the landscape-scale decisions were primarily determined by maternal energetic constraints and only secondarily by risk avoidance. Indeed, forage-rich habitats were strongly selected notwithstanding the exceptionally high densities of rodents which increased fawn predation. At fine spatial scales, a high visibility of the mother was the major factor determining predation risk; however, mothers adjusted their behaviour to the level of risk at the bed site to minimise predation. Fawns selected both landscape-scale refugia and concealed bed sites, but failure to segregate from the main prey of red foxes led to higher predation. This study provides evidence for the occurrence of spatial heterogeneity in predation risk and shows that energetically stressed individuals can tackle the foraging-safety trade-off by adopting scale-dependent anti-predator responses.

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
Fig. 4

Similar content being viewed by others

References

  • Ackerman JT (2002) Of mice and mallards: positive indirect effects of coexisting prey on waterfowl nest success. Oikos 99:469–480

    Article  Google Scholar 

  • Andersen R, Gaillard JM, Linnell JDC, Duncan P (2000) Factors affecting maternal care in an income breeder, the European roe deer. J Anim Ecol 69:672–682

    Article  Google Scholar 

  • Bates D, Sarkar D (2006) lme4: linear mixed-effects models using S4 classes. R package version 0.9975-10. Available at: http://cran.r-project.org/web/packages/lme4/index.html. Accessed 13 Sept 2009

  • Benhaiem S, Delon M, Lourtet B, Cargnelutti B, Aulagnier S, Hewison M, Morellet N, Verheyden H (2008) Hunting increases vigilance levels in roe deer and modifies feeding site selection. Anim Behav 76(3):611–618

    Article  Google Scholar 

  • Bongi P, Ciuti S, Grignolio S, Del Frate M, Simi S, Gandelli D, Apollonio M (2008) Anti-predator behavior, space use and habitat selection in female roe deer during the fawning season in a wolf area. J Zool 276:242–251

    Article  Google Scholar 

  • Bowyer RT, Van Ballenberghe V, Kie JG, Maier JA (1999) Birth-site selection by Alaskan moose: maternal strategies for coping with a risky environment. J Mammal 80:1070–1083

    Article  Google Scholar 

  • Brown JS, Kotler BP (2004) Hazardous duty pay and the foraging cost of predation. Ecol Lett 7(10):999–1014

    Article  Google Scholar 

  • Byers JA, Byers KZ (1983) Do pronghorn mothers reveal the locations of their hidden fawns? Behav Ecol Sociobiol 13:147–156

    Article  Google Scholar 

  • Caro T (2005) Antipredator defenses in birds and mammals. University of Chicago Press, Chicago

    Google Scholar 

  • Chen Z, Kuo L (2001) A note on the estimation of the multinomial logit model with random effects. Am Stat 55:89–94

    Article  Google Scholar 

  • Ciuti S, Bongi S, Vassale M, Apollonio S (2006) Influence of fawning on the spatial behavior and habitat selection of female fallow deer (Dama dama) during late pregnancy and early lactation. J Zool 268:97–107

    Google Scholar 

  • Charnov EL (1976) Optimal foraging, marginal value theorem. Theor Popul Biol 9:129–136

    Article  CAS  PubMed  Google Scholar 

  • Clutton-Brock TH, Albon SD, Guinness FE (1989) Fitness cost of gestation and lactation in wild mammals. Nature 337(6024):260–262

    Article  CAS  PubMed  Google Scholar 

  • Crawley MJ (2002) Statistical computing: an introduction to data analysis using S-Plus. Wiley, Chichester

    Google Scholar 

  • Creel S, Winnie J, Maxwell B, Hamlin K, Creel M (2005) Elk alter habitat selection as an antipredator response to wolves. Ecology 86:3387–3397

    Article  Google Scholar 

  • Delibes M, Gaona P, Ferreras P (2001) Effects of an attractive sink leading into maladaptive habitat selection. Am Nat 158(3):277–284

    Article  CAS  PubMed  Google Scholar 

  • Festa-Bianchet M (1988) Seasonal range selection in bighorn sheep: conflicts between forage quality, forage quantity, and predator avoidance. Oecologia 75:580–586

    Article  Google Scholar 

  • Fitzgibbon CD (1993) Antipredator strategies of female Thomson gazelle with hidden fawns. J Mammal 74:758–762

    Article  Google Scholar 

  • Fretwell SD, Lucas HL (1970) On territorial behavior and other factors influencing habitat distribution in birds. I. Theoretical development. Acta Biotheor 19:16–36

    Article  Google Scholar 

  • Grignolio S, Rossi I, Bertolotto E, Bassano B, Apollonio M (2007) Influence of the kid on space use and habitat selection of female Alpine ibex. J Wildl Manage 71:713–719

    Article  Google Scholar 

  • Gustine DD, Parker K, Lay RJ, Gillingham MP, Heard DC (2006) Calf survival of Woodland Caribou in a multi-predator ecosystem. Wildl Monogr 165:1–32

    Article  Google Scholar 

  • Hamlin KL, Riley SJ, Pyrah D, Dood AR, Mackie RJ (1984) Relationship among mule deer fawns mortality, coyotes and alternative prey species during summer. J Wildl Manage 48(2):489–499

    Article  Google Scholar 

  • Herfindal I, Tremblay JP, Hansen BB, Solberg EJ, Heim M, Sæther BE (2009) Scale dependency and functional response in moose habitat selection. Ecography 32:849–859

    Article  Google Scholar 

  • Hochman V, Kotler B (2007) Patch use, apprehension, and vigilance behaviour of Nubian ibex under perceived risk of predation. Behav Ecol 18:368–374

    Article  Google Scholar 

  • Hofmann RR, Stewart DRM (1972) Grazer or browser: a classification based on the stomach structure and feeding habits of East African ruminants. Mammalia 36:226–240

    Article  Google Scholar 

  • Jarnemo A (2004) Predation processes: behavioral interactions between red fox and roe deer during the fawning season. J Ethol 22(2):167–173

    Article  Google Scholar 

  • Jarnemo A, Liberg O (2005) Red fox removal and roe deer fawns survival—a 14 years study. J Wildl Manage 69(3):1090–1098

    Article  Google Scholar 

  • Kjellander P, Nordström J (2003) Cyclic voles, prey switching in red fox and roe deer dynamics—a test of the alternative prey hypothesis. Oikos 101:338–344

    Article  Google Scholar 

  • Kjellander P, Gaillard JM, Hewison M, Liberg O (2004) Predation risk and longevity influence variation in fitness of female roe deer (Capreolus capreolus L.). Proc R Soc Lond [Biol] 271(5):338–340

    Article  Google Scholar 

  • Lent PC (1974) Mother–infant relationship in ungulates. In: Geist V, Walther F (eds) The behavior of ungulates and its relation to management. Publication series 24(1). IUCN, Morges, pp 14–54

    Google Scholar 

  • Lima SL, Bednekoff PA (1999) Temporal variation in danger drives antipredator behavior: the predation risk allocation hypothesis. Am Nat 153:649–659

    Article  Google Scholar 

  • Lindström ER (1994) Large prey for small cubs—on crucial resources of a boreal red fox population. Ecography 17:17–22

    Article  Google Scholar 

  • Lingle S (2000) Seasonal variation in coyote feeding behaviour and mortality of white-tailed deer and mule deer. Can J Zool 78(1):85–99

    Article  Google Scholar 

  • Lingle S, Pellis SM, Wilson WF (2005) Interspecific variation in antipredator behaviour leads to differential vulnerability of mule deer and white-tailed deer fawns early in life. J Anim Ecol 74:1140–1149

    Article  Google Scholar 

  • Lingle S, Feldman A, Boyce M, Wilson WF (2008) Prey behaviour, age-dependent vulnerability and predation rates. Am Nat 172(5):712–725

    Article  PubMed  Google Scholar 

  • Linnell JDC (1994) Reproductive tactics and parental care in Norwegian roe deer. Dissertation, National University of Ireland

  • Linnell JDC, Aanes R, Andersen R (1995) Who killed Bambi? The role of predation in the neonatal mortality of temperate ungulates. Wildl Biol 1:209–224

    Google Scholar 

  • Linnell JDC, Nijhuis P, Teurlings I, Andersen R (1999) Selection of bed sites by neonatal roe deer fawns in a boreal forest landscape. Wildl Biol 5:225–231

    Google Scholar 

  • Linnell JDC, Nilsen E, Andersen R (2004) Selection for bed-sited by roe deer Capreolus capreolus fawns in agricultural landscape. Acta Theriol 49(1):103–111

    Google Scholar 

  • Manly BFJ, McDonald LL, Thomas DL, McDonald TL, Erickson WP (2002) Resource selection by animals. Statistical design and analysis for field studies. Kluwer Academic, Dordrecht

    Google Scholar 

  • McLoughlin PD, Dunford JS, Boutin S (2005) Relating predation mortality to broad-scale habitat selection. J Anim Ecol 74:701–707

    Article  Google Scholar 

  • McLoughlin PD, Boyce MS, Coulson T, Clutton-Brock T (2006) Lifetime reproductive success and density-dependent, multi-variable resource selection. Proc Biol Sci 273(1593):1449–1454

    Article  PubMed  Google Scholar 

  • McLoughlin PD, Gaillard JM, Boyce MS, Bonenfant C, Messier F, Duncan P, Delorme D, Van Moorter B, Saïd S, Klein F (2007) Lifetime reproductive success and composition of the home range in a large herbivore. Ecology 88(12):3192–3201

    Article  CAS  PubMed  Google Scholar 

  • Miyashita T, Suzuki M, Ando D, Go F, Ochiai K, Asada M (2008) Forest edges creates small-scale variation in reproductive rate of sika deer. Popul Ecol 50:111–120

    Article  Google Scholar 

  • Myllmäki A, Paasikallio A, Pankakoski E, Kanervo V (1971) Removal experiments on small quadrates as a mean of rapid assessment of the abundance of small mammals. Ann Zool Fennici 8:177–185

    Google Scholar 

  • Mysterud A (2000) The relationship between ecological segregation and sexual body size dimorphism in large herbivores. Oecologia 124:40–54

    Article  Google Scholar 

  • Mysterud A, Lian LB, Hjermann DO (1999) Scale-dependant trade-offs in foraging by European roe deer (Capreolus capreolus) during winter. Can J Zool 77:1486–1493

    Article  Google Scholar 

  • Nilsen EB, Linnell JDC, Andersen R (2004) Individual access to preferred habitat affects fitness components in female roe deer Capreolus capreolus. J Anim Ecol 73:44–50

    Article  Google Scholar 

  • Nilsen EB, Gaillard JM, Andersen R, Odden J, Delorme D, Van Laere G, Linnell JDC (2009a) A slow life in hell or a fast life in heaven: demographic analyses of contrasting roe deer populations. J Anim Ecol 78:585–594

    Article  PubMed  Google Scholar 

  • Nilsen EB, Linnell JDC, Odden J, Andersen R (2009b) Climate, season, and social status modulate the functional response of an efficient stalking predator: the Eurasian lynx. J Anim Ecol 78(4):741–751

    Article  PubMed  Google Scholar 

  • Palomares F, Delibes M, Revilla E, Calzada J, Fedriani JM (2001) Spatial ecology of Iberian lynx and abundance of European rabbits in southwestern Spain. Wildl Monogr 148:1–36

    Google Scholar 

  • Panzacchi M, Linnell J, Melis C, Odden M, Odden J, Andersen R (2010) Effect of land-use on small mammals’ abundance and diversity in a forest-farmland mosaic landscape in south-eastern Norway. Forest Ecol Manag 259:1536–1545

    Google Scholar 

  • Panzacchi M, Linnell JDC, Odden J, Odden M, Andersen R (2008a) When a generalist becomes a specialist: patterns of red fox predation on roe deer fawns under contrasting conditions. Can J Zool 86(2):116–126

    Article  Google Scholar 

  • Panzacchi M, Linnell JDC, Odden M, Serrao G, Eie S, Odden J, Andersen R (2008b) Evaluation of the importance of roe deer fawns in the spring–summer diet of red foxes in south-eastern Norway. Ecol Res 23(5):889–896

    Article  Google Scholar 

  • Panzacchi M, Linnell J, Odden M, Odden J, Andersen R (2009) Habitat and roe deer fawn vulnerability to red fox predation. J Anim Ecol 78:1124–1133

    Article  CAS  PubMed  Google Scholar 

  • Pettorelli N, Gaillard JM, Duncan P, Ouellet JP, Van Laere G (2001) Population density and small-scale variations in habitat quality affect phenotypic quality in roe deer. Oecologia 128:400–405

    Article  Google Scholar 

  • Pettorelli N, Gaillard JM, Duncan P, Maillard D, Van Laere G, Delorme D (2003) Age and density modify the effects of habitat quality on survival and movements of roe deer. Ecology 84(12):3307–3316

    Article  Google Scholar 

  • Pettorelli N, Gaillard JM, Yoccoz NG, Duncan P, Maillard D, Delorme D, Van Laere G, Toigo C (2005) The response of fawn survival to changes in habitat quality varies according to cohort quality and spatial scale. J Anim Ecol 74:972–981

    Article  Google Scholar 

  • Ratikainen I, Panzacchi M, Mysterud A, Odden J, Linnell JDC, Andersen R (2007) Use of winter habitat by roe deer at a northern latitude where Eurasian lynx are present. J Zool 273:192–199

    Article  Google Scholar 

  • Rettie JW, Messier F (2000) Hierarchical habitat selection by woodland caribou: its relationship to limiting factors. Ecography 23:466–478

    Article  Google Scholar 

  • Rohm JH, Nielsen CK, Woolf A (2006) Survival of white-tailed deer fawns in southern Illinois. J Wildl Manage 71(3):851–860

    Article  Google Scholar 

  • Rosef L, Bele B (2005) Knowledge of traditional farming practices as a tool for management of semi-natural grassland. Tools for management of natural grasslands. Vista-WP5 7:6–8

    Google Scholar 

  • Spong G (2002) Space use in lions, Panthera leo, in the Selous Game Reserve: social and ecological factors. Behav Ecol Sociobiol 52:303–307

    Article  Google Scholar 

  • Van Moorter B, Gaillard JM, McLoughlin PD, Delorme D, Klein F, Boyce M (2009) Maternal and individual effects in selection of bed sites and their consequences for fawn survival at different spatial scales. Oecologia 159(3):669–678

    Article  PubMed  Google Scholar 

  • Vreeland JK, Diefenbach DR, Wallingford BD (2004) Survival rates, mortality causes, and habitat of Pennsylvania white-tailed deer fawns. Wildl Soc Bull 32(2):542–553

    Article  Google Scholar 

  • White GC, Burnham KP (1999) Program MARK: survival estimation from populations of marked animals. Bird Study 46(Supplement):120–138

    Article  Google Scholar 

  • White M, Knowlton FF, Glazener WC (1972) Effects of dam-newborn fawn behavior on capture and mortality. J Wildl Manage 36:897–906

    Article  Google Scholar 

Download references

Acknowledgements

Ø Høgseth, A Bryan, C Melis, E Ness, G Serrao, H Andersen, I Teurlings, JM Arnemo, K Fische, L Gangås, M Hauger, P Nijhuis, S Lerheim, T Tveter, T Wegge, V Årnes and many others helped in the field. The various stages of the project have been funded by the Research Council of Norway (2 × 5 year project grants and an individual scholarship to the lead author), the Norwegian Directorate for Nature Management and the Norwegian Institute for Nature Research.

Ethical standards

The project complies with the current Norwegian laws on ethics and animal welfare.

Conflict of interest

None.

Author information

Author notes

  1. Morten Odden

    Present address: Faculty of Forestry and Wildlife Management, Hedmark University College, 2418, Elverum, Norway

Authors and Affiliations

  1. Norwegian Institute for Nature Research, Tungasletta-2, 7485, Trondheim, Norway

    Manuela Panzacchi, John D. C. Linnell, John Odden & Reidar Andersen

  2. Centre for Conservation Biology, Biology Department, Norwegian University of Science and Technology, 7491, Trondheim, Norway

    Ivar Herfindal

  3. Department of Ecology and Natural Resource Management, Norwegian University of Life Sciences, 1432, Ǻs, Norway

    Morten Odden

  4. Section of Natural History, Museum of Natural History and Archaeology, Norwegian University of Science and Technology, 7491, Trondheim, Norway

    Reidar Andersen

Authors
  1. Manuela Panzacchi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ivar Herfindal
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. John D. C. Linnell
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Morten Odden
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. John Odden
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Reidar Andersen
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Manuela Panzacchi.

Additional information

Communicated by M. Festa-Bianchet

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

(DOC 41.5 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Panzacchi, M., Herfindal, I., Linnell, J.D.C. et al. Trade-offs between maternal foraging and fawn predation risk in an income breeder. Behav Ecol Sociobiol 64, 1267–1278 (2010). https://doi.org/10.1007/s00265-010-0941-0

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00265-010-0941-0

Keywords

Search

Navigation