Skip to main content

Advertisement

Log in

Do predators modify context-dependent dispersal of red squirrels?

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

Abstract

Natal dispersal, the one-way movement between birth site and first breeding site, is an important determinant of species gene-flow and invasion potential. While dispersing in unfamiliar habitat, individuals may adjust their movement based on possible costs and benefits of moving, termed context-dependent dispersal. The role of factors, such as population density or spatial organisation of habitats, is well studied in the departure, transfer and settlement phases of dispersal. However, the role of predators for context-dependent dispersal remains less studied, particularly for the transfer phase and settlement phase of natal dispersal. We studied natal dispersal of radio-collared Eurasian red squirrels, Sciurus vulgaris, in relation to nest site locations of their main predator, the goshawk, Accipiter gentilis, in Finland. The locations of nest sites of goshawk had no influence on movement made during the transfer phase or on the location of settlement sites of juvenile red squirrels. Limited data on squirrel response to indices of predator presence (call playback of goshawk and faecal odours of mammalian predators) appeared to support the conclusion that predators had limited role in explaining movements of dispersers. We suggest that predators do not modify context-dependent dispersal among red squirrels in our boreal study area. This finding may be due to the low density of squirrel predators in northern boreal forests but may not hold true for species in which dispersers frequently encounter predators. Our study supports the conclusion that the resource and habitat availability are more important factors than predator presence for context-dependent dispersal among red squirrels.

Significance statement

Context-dependent dispersal means that individuals rely on a set of external cues, such as local population density and habitat quality, to adjust their movement tactics. One potentially important but little studied factor for context-dependent dispersal is the presence of predators. We studied movements of radio-collared dispersing Eurasian red squirrels in relation to nest site locations of their main predator, the goshawk. Movements of dispersing red squirrels were not influenced by the presence of predators. Thus, it seems likely that food and habitat availability, which were previously observed to shape dispersal patterns of red squirrels, determine where and how far Eurasian red squirrels disperse in boreal forests.

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

Similar content being viewed by others

References

  • Bernstein C (1984) Prey and predator emigration responses in the acarine system Tetranychus urticae Phytoseiulus persimilis. Oecologia 61:134–142

    Article  CAS  PubMed  Google Scholar 

  • Bestion E, Teyssier A, Aubret F, Clobert J, Cote J (2014) Maternal exposure to predator scents: offspring phenotypic adjustment and dispersal. Proc R Soc B 281:20140701

    Article  PubMed  Google Scholar 

  • Biro PA (2013) Are most samples of animals systematically biased? Consistent individual trait differences bias samples despite random sampling. Oecologia 171:339–345

    Article  PubMed  Google Scholar 

  • Biro PA, Dingemanse NJ (2009) Sampling bias resulting from animal personality. Trends Ecol Evol 24:66–67

    Article  PubMed  Google Scholar 

  • Björklund H, Santangeli AF, Blanchet G, Huitu O, Lehtoranta H, Lindén H, Valkama J, Laaksonen T (2016) Intraguild predation and competition impacts on a subordinate predator. Oecologia 181:257–269

    Article  PubMed  Google Scholar 

  • Bonte D, van Dyck H, Bullock JM, Coulon A, Delgado M, Gibbs M, Lehouck V, Matthysen E, Mustin K, Saastamoinen M, Schtickzelle N, Stevens VM, Vandewoestijne S, Baguette M, Barton K, Benton TG, Chaput-Bardy A, Clobert J, Dytham C, Hovestadt T, Meier CM, Palmer SCF, Turlure C, Travis JMJ (2012) Costs of dispersal. Biol Rev 87:290–312

    Article  PubMed  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 

  • Carlson NV, Pargeter HM, Templeton CN (2017) Sparrowhawk movement, calling, and presence of dead conspecifics differentially impact blue tit (Cyanistes caeruleus) vocal and behavioral mobbing responses. Behav Ecol Sociobiol 71:133

    Article  PubMed Central  PubMed  Google Scholar 

  • Clobert J, Le Galliard J-F, Cote J, Meylan S, Massot M (2009) Informed dispersal, heterogeneity in animal dispersal syndromes and the dynamics of spatially structured populations. Ecol Lett 12:197–209

    Article  PubMed  Google Scholar 

  • Cooper EB, Taylor RW, Kelley AD, Martinig AR, Boutin S, Humphries MM, Dantzer B, Lane JE, McAdam AG (2017) Personality is correlated with natal dispersal in north American red squirrels. Behaviour 154:939–961

    Article  Google Scholar 

  • Cote J, Bestion E, Jacob S, Travis J, Legrand D, Baguette M (2017) Evolution of dispersal strategies and dispersal syndromes in fragmented landscapes. Ecography 40:56–73

    Article  Google Scholar 

  • Cote J, Clobert J (2007) Social information and emigration: lessons from immigrants. Ecol Lett 10:411–441

    Article  CAS  PubMed  Google Scholar 

  • Cote J, Fogarty S, Tymen B, Sih A, Brodin T (2013) Personality dependent dispersal cancelled under predation risk. Proc R Soc B 280:20132349

    Article  PubMed  Google Scholar 

  • De Meester N, Bonte D (2010) Information use and density-dependent emigration in an agrobiont spider. Behav Ecol 21:992–998

    Article  Google Scholar 

  • Dell'Arte GL, Laaksonen T, Norrdahl K, Korpimäki E (2007) Variation in the diet composition of a generalist predator, the red fox, in relation to season and density of main prey. Acta Oecol 31:276–281

    Article  Google Scholar 

  • Descamps S, Boutin S, Berteaux D, McAdam AG, Jean-Michel G (2008) Cohort effects in red squirrels: the influence of density, food abundance and temperature on future survival and reproductive success. J Anim Ecol 77:305–314

    Article  PubMed  Google Scholar 

  • Doligez B, Danchin E, Clobert J (2002) Public information and breeding habitat selection in a wild bird population. Science 297:1168–1170

    Article  CAS  PubMed  Google Scholar 

  • Fey K, Banks PB, Ylönen H, Korpimäki E (2010) Behavioural responses of voles to simulated risk of predation by a native and an alien mustelid: an odour manipulation experiment. Wildlife Res 37:273–282

    Article  Google Scholar 

  • Fey K, Hämäläinen S, Selonen V (2016) Roads are no barrier for dispersing red squirrels in an urban environment. Behav Ecol 27:741–747

    Article  Google Scholar 

  • Forsman JT, Mönkkönen M, Korpimäki E, Thomson RL (2013) Mammalian nest predator feces as a cue in avian habitat selection decisions. Behav Ecol 24:262–266

    Article  Google Scholar 

  • Fronhofer EA, Klecka J, Melián CJ, Altermatt F (2015) Condition-dependent movement and dispersal in experimental metacommunities. Ecol Lett 18:954–963

    Article  PubMed  Google Scholar 

  • Fülling O, Halle S (2004) Breeding suppression in free-ranging grey-sided voles under the influence of predator odour. Oecologia 138:151–159

    Article  Google Scholar 

  • Gendron RP, Staddon JER (1984) A laboratory simulation of foraging behavior: the effect of search rate on the probability of detecting prey. Am Nat 124:407–415

    Article  Google Scholar 

  • Gurnell J (1983) Squirrel numbers and the abundance of tree seeds. Mammal Rev 13:133–148

    Article  Google Scholar 

  • Hakkarainen H, Ilmonen P, Koivunen V, Korpimäki E (2001) Experimental increase of predation risk induces breeding dispersal of Tengmalm’s owl. Oecologia 126:355–359

    Article  PubMed  Google Scholar 

  • Hakkarainen H, Korpimäki E (1994) Nest defence of Tengmalm’s owls reflects offspring survival prospects under fluctuating food conditions. Anim Behav 48:843–849

    Article  Google Scholar 

  • Hakkarainen H, Mykra S, Kurki S, Korpimäki E, Nikula A, Koivunen V (2003) Habitat composition as a determinant of reproductive success of Tengmalm’s owls under fluctuating food conditions. Oikos 100:162–171

    Article  Google Scholar 

  • Hammond JI, Luttbeg B, Sih A (2007) Predator and prey space use: dragonflies and tadpoles in an interactive game. Ecology 88:1525–1535

    Article  PubMed  Google Scholar 

  • Hanski IK, Selonen V (2009) Female-biased natal dispersal in the Siberian flying squirrel. Behav Ecol 20:60–67

    Article  Google Scholar 

  • Hämäläinen A, McAdam AG, Dantzer B, Lane JE, Haines JA, Humphries MM, Boutin S (2017) Fitness consequences of peak reproductive effort in a resource pulse system. Sci Rep 7:9335

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hämäläinen S, Fey K, Selonen V (2018) Habitat and nest use during natal dispersal of the urban red squirrel (Sciurus vulgaris). Landscape Urban Plan 169:269–275

    Article  Google Scholar 

  • Hiddink JG, Kock RP, Wolff WJ (2002) Active pelagic migrations of the bivalve Macoma balthica are dangerous. Mar Biol 140:1149–1156

    Article  Google Scholar 

  • Ims RA, Hjermann DØ (2001) Condition-dependent dispersal. In: Clobert J, Danchin E, Dhondt AA, Nichols JD (eds) Dispersal. Oxford University Press, Oxford, pp 203–216

    Google Scholar 

  • Kauhala K, Talvitie K, Vuorisalo T (2016) Encounters between medium-sized carnivores and humans in the city of Turku, SW Finland, with special reference to the red fox. Mammal Res 61:25–33

    Article  Google Scholar 

  • Korpimäki E, Hakkarainen H (2012) The boreal owl: ecology, behaviour and conservation of a forest-dwelling predator. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Korpimäki E, Sulkava S (1987) Diet and breeding performance of Ural owls Strix uralensis under fluctuating food conditions. Ornis Fenn 64:57–66

    Google Scholar 

  • Kotler BP, Brown JS, Hasson O (1991) Factors affecting gerbil foraging behavior and rates of owl predation. Ecology 72:2249–2260

    Article  Google Scholar 

  • Kuefler D, Avgar T, Fryxell JM (2012) Rotifer population spread in relation to food, density and predation risk in an experimental system. J Anim Ecol 81:323–329

    Article  PubMed  Google Scholar 

  • Larsen KW, Boutin S (1994) Movements, survival, and settlement of red squirrel (Tamiasciurus hudsonicus) offspring. Ecology 75:214–223

    Article  Google Scholar 

  • Laundré JW, Hernández L, Altendorf KB (2001) Wolves, elk, and bison: reestablishing the “landscape of fear” in Yellowstone National Park, USA. Can J Zool 79:1401–1409

    Article  Google Scholar 

  • Le Galliard J-F, Remy A, Ims RA, Lambin X (2012) Patterns and processes of dispersal behaviour in arvicoline rodents. Mol Ecol 21:505–523

    Article  PubMed  Google Scholar 

  • Lima SL (2009) Predators and the breeding bird: behavioral and reproductive flexibility under the risk of predation. Biol Rev 84:485–513

    Article  PubMed  Google Scholar 

  • Lurz PWW, Garson PJ, Wauters LA (1997) Effects of temporal and spatial variation in habitat quality on red squirrel dispersal behaviour. Anim Behav 54:427–435

    Article  CAS  PubMed  Google Scholar 

  • Lurz P, Gurnell J, Magris L (2005) Sciurus vulgaris. Mamm Spec 769:1–10

    Article  Google Scholar 

  • Matthysen E (2005) Density-dependent dispersal in birds and mammals. Ecography 28:403–416

    Article  Google Scholar 

  • McCauley SJ, Rowe L (2010) Notonecta exhibit threat-sensitive, predator-induced dispersal. Biol Lett 6:449–452

    Article  PubMed Central  PubMed  Google Scholar 

  • McIntosh AR, Peckarsky BL, Taylor BW (2002) The influence of predatory fish on mayfly drift: extrapolating from experiments to nature. Freshw Biol 47:1497–1513

    Article  Google Scholar 

  • Merrick MJ, Koprowski JL (2017) Altered natal dispersal at the range periphery: the role of behavior, resources, and maternal condition. Ecol Evol 7:58–72

    Article  PubMed  Google Scholar 

  • Morosinotto C, Thomson RL, Korpimäki E (2010) Habitat selection as an antipredator behaviour in a multi-predator landscape: all enemies are not equal. J Anim Ecol 79:327–333

    Article  PubMed  Google Scholar 

  • Morosinotto C, Villers A, Thomson RL, Varjonen R, Korpimäki E (2017) Competitors and predators alter settlement patterns and reproductive success of an intraguild prey. Ecol Monogr 87:4–20

    Article  Google Scholar 

  • Petty SJ, Lurz PWW, Rushton SP (2003) Predation of red squirrels by northern goshawks in a conifer forest in northern England: can this limit squirrel numbers and create a conservation dilemma? Biol Conserv 111:105–114

    Article  Google Scholar 

  • Poethke HJ, Weisser WW, Hovestadt T (2010) Predator-induced dispersal and the evolution of conditional dispersal in correlated environments. Am Nat 175:577–586

    Article  PubMed  Google Scholar 

  • Ronce O (2007) How does it feel to be like a rolling stone? Ten questions about dispersal evolution. Annu Rev Ecol Evol S 38:231–253

    Article  Google Scholar 

  • Selonen V, Hanski IK (2012) Dispersing Siberian flying squirrels (Pteromys volans) locate preferred habitats in fragmented landscapes. Can J Zool 90:885–892

    Article  Google Scholar 

  • Selonen V, Hanski IK (2015) Occurrence and dispersal of the red squirrel and the Siberian flying squirrel in fragmented landscapes. In: Shuttleworth CM, Lurz P, Hayward MW (eds) Red squirrels: ecology. Conservation & Management in Europe. European Squirrel Initiative, Suffolk, pp 67–82

    Google Scholar 

  • Selonen V, Hanski IK, Desrochers A (2007) Natal habitat-biased dispersal in the Siberian flying squirrel. Proc R Soc Lond B 274:2063–2068

    Article  Google Scholar 

  • Selonen V, Sulkava P, Sulkava R, Sulkava S, Korpimäki E (2010) Decline of flying and red squirrels in boreal forests revealed by long-term diet analyses of avian predators. Anim Conserv 13:579–585

    Article  Google Scholar 

  • Selonen V, Varjonen R, Korpimäki E (2015) Immediate or lagged responses of a red squirrel population to pulsed resources. Oecologia 177:401–411

    Article  PubMed  Google Scholar 

  • Selonen V, Varjonen R, Korpimäki E (2016a) Predator presence, but not food supplementation, affects forest red squirrels in winter. Ann Zool Fenn 53:183–193

    Article  Google Scholar 

  • Selonen V, Wistbacka R (2017) Role of breeding and natal movements in lifetime dispersal of a forest-dwelling rodent. Ecol and Evol 7:2204–2213

    Article  Google Scholar 

  • Selonen V, Wistbacka R, Korpimäki E (2016b) Food abundance and weather modify reproduction of two arboreal squirrel species. J Mamm 97:1376–1384

    Article  Google Scholar 

  • Terraube J, Vasko V, Korpimäki E (2015) Mechanisms and reproductive consequences of breeding dispersal in a specialist predator under temporally varying food conditions. Oikos 124:762–771

    Article  Google Scholar 

  • Thomson RL, Tomas G, Forsman JT, Broggi J, Mönkkönen M (2010) Predator proximity as a stressor in breeding flycatchers: mass loss, stress protein induction, and elevated provisioning. Ecology 91:1832–1840

    Article  PubMed  Google Scholar 

  • Tornberg R, Korpimäki E, Byholm P (2006) Ecology of the northern goshawk in Fennoscandia. Stud Avian Biol-Ser 31:141–157

    Google Scholar 

  • Turkia T, Korpimäki E, Villers A, Selonen V (2018) Predation risk landscape modifies flying and red squirrel nest site occupancy independently of habitat amount. PLoS One 13:e0194624

    Article  PubMed Central  PubMed  Google Scholar 

  • Verhulst S, Perrins CM, Riddington R (1997) Natal dispersal of great tits in a patchy environment. Ecology 78:864–872

    Article  Google Scholar 

  • Wauters L, Dhondt AA (1993) Immigration pattern and success in red squirrels. Behav Ecol Sociobiol 33:159–167

    Article  Google Scholar 

  • Wauters LA, Githiru M, Bertolino S, Molinari A, Tosi G, Lens L (2008) Demography of alpine red squirrel populations in relation to fluctuations in seed crop size. Ecography 31:104–114

    Article  Google Scholar 

  • Wauters LA, Verbeylen G, Preatoni D, Martinoli A, Matthysen E (2010) Dispersal and habitat cuing of Eurasian red squirrels in fragmented habitats. Popul Ecol 52:527–536

    Article  Google Scholar 

Download references

Acknowledgments

We thank Mikko Hänninen, Jorma Nurmi, Rauno Varjonen and Tanja Hannola for great help in the field. Constructive comments by two referees were valuable to improve the manuscript.

Funding

The study was financially supported by the Academy of Finland (no. 259562 to VS).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Vesa Selonen.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. No ethical approval was required from an institutional or national ethics review board.

Additional information

Communicated by A. I. Schulte-Hostedde

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Selonen, V., Fey, K., Hämäläinen, S. et al. Do predators modify context-dependent dispersal of red squirrels?. Behav Ecol Sociobiol 72, 136 (2018). https://doi.org/10.1007/s00265-018-2554-y

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00265-018-2554-y

Keywords

Navigation