Skip to main content
Log in

Temporal shifts in landscape connectivity for an ecosystem engineer, the roe deer, across a multiple-use landscape

  • Research Article
  • Published:
Landscape Ecology Aims and scope Submit manuscript

Abstract

Context

Routine movements of large herbivores, often considered as ecosystem engineers, impact key ecological processes. Functional landscape connectivity for such species influences the spatial distribution of associated ecological services and disservices.

Objectives

We studied how spatio-temporal variation in the risk-resource trade-off, generated by fluctuations in human activities and environmental conditions, influences the routine movements of roe deer across a heterogeneous landscape, generating shifts in functional connectivity at daily and seasonal time scales.

Methods

We used GPS locations of 172 adult roe deer and step selection functions to infer landscape connectivity. In particular, we assessed the influence of six habitat features on fine scale movements across four biological seasons and three daily periods, based on variations in the risk-resource trade-off.

Results

The influence of habitat features on roe deer movements was strongly dependent on proximity to refuge habitat, i.e. woodlands. Roe deer confined their movements to safe habitats during daytime and during the hunting season, when human activity is high. However, they exploited exposed open habitats more freely during night-time. Consequently, we observed marked temporal shifts in landscape connectivity, which was highest at night in summer and lowest during daytime in autumn. In particular, the onset of the autumn hunting season induced an abrupt decrease in landscape connectivity.

Conclusions

Human disturbance had a strong impact on roe deer movements, generating pronounced spatio-temporal variation in landscape connectivity. However, high connectivity at night across all seasons implies that Europe’s most abundant and widespread large herbivore potentially plays a key role in transporting ticks, seeds and nutrients among habitats.

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

Similar content being viewed by others

References

  • Abbas F, Merlet J, Morellet N, Verheyden H, Hewison AJM, Cargnelutti B, Angibault JM, Picot D, Rames JL, Lourtet B (2012) Roe deer may markedly alter forest nitrogen and phosphorus budgets across Europe. Oikos 121:1271–1278

    Article  Google Scholar 

  • Adrados C, Girard I, Gendner J-P, Janeau G (2002) Global positioning system (GPS) location accuracy improvement due to selective availability removal. C R Biol 325:165–170

    Article  PubMed  Google Scholar 

  • Albert A, Auffret AG, Cosyns E, Cousins SAO, D'hondt B, Eichberg C, Eycott, AE, Heinken T, Hoffmann M, Jaroszewicz B (2015) Seed dispersal by ungulates as an ecological filter: a trait-based meta-analysis. Oikos 124:1109–1120

    Article  Google Scholar 

  • Allan BF, Keesing F, Ostfeld RS (2003) Effect of forest fragmentation on lyme disease risk. Conserv Biol 17:267–272

    Article  Google Scholar 

  • Allan BF, Tallis H, Chaplin-Kramer R, Huckett S, Kowal VA, Musengezi J, Okanga S, Ostfeld RS, Schieltz J, Warui CM (2017) Can integrating wildlife and livestock enhance ecosystem services in central Kenya? Front Ecol Environ 15:328–335

    Article  Google Scholar 

  • Baguette M, Van Dyck H (2007) Landscape connectivity and animal behavior: functional grain as a key determinant for dispersal. Landscape Ecol 22:1117–1129

    Article  Google Scholar 

  • Basille M (2015) hab: Habitat and movement functions. URL http://ase-research.org/basille/hab

  • Bélisle M (2005) Measuring landscape connectivity: the challenge of behavioral landscape ecology. Ecology 86:1988–1995

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Benhamou S, Cornélis D (2010) Incorporating movement behavior and barriers to improve kernel home range space use estimates. J Wildl Manag 74:1353–1360

    Article  Google Scholar 

  • Bjorneraas K, Solberg EJ, Herfindal I, Van Moorter B, Rolandsen CM, Tremblay JP, Skarpe C, Saether BE, Eriksen R, Astrup R (2011) Moose Alces alces habitat use at multiple temporal scales in a human-altered landscape. Wildl Biol 17:44–54

    Article  Google Scholar 

  • Bjørneraas K, Van Moorter B, Rolandsen CM, Herfindal I (2010) Screening global positioning system location data for errors using animal movement characteristics. J Wildl Manag 74:1361–1366

    Article  Google Scholar 

  • Bonnot NC, Morellet N, Verheyden H, Cargnelutti B, Lourtet B, Klein F, Hewison AJM (2013) Habitat use under predation risk: hunting, roads and human dwellings influence the spatial behaviour of roe deer. Eur J Wildl Res 59:185–193

    Article  Google Scholar 

  • Bonnot NC, Hewison AJM, Morellet N, Gaillard J-M, Debeffe L, Couriot O, Cargnelutti B, Chaval Y, Lourtet B, Kjellander P (2017) Stick or twist: roe deer adjust their flight behaviour to the perceived trade-off between risk and reward. Anim Behav 124:35–46

    Article  Google Scholar 

  • Brown JS, Laundré JW, Gurung M (1999) The ecology of fear: optimal foraging, game theory, and trophic interactions. J Mammal 80:385–399

    Article  Google Scholar 

  • Brownstein JS, Skelly DK, Holford TR, Fish D (2005) Forest fragmentation predicts local scale heterogeneity of Lyme disease risk. Oecologia 146:469–475

    Article  PubMed  Google Scholar 

  • Burnham KP, Anderson DR (2002) Model selection and multi-model inference: a practical information-theoretic approach. Springer, New York

    Google Scholar 

  • Calenge C (2006) The package “adehabitat” for the R software: a tool for the analysis of space and habitat use by animals. Ecol Model 197:516–519

    Article  Google Scholar 

  • Cargnelutti B, Coulon A, Hewison AJM, Goulard M, Angibault J-M, Morellet N (2007) Testing global positioning system performance for wildlife monitoring using mobile collars and known reference points. J Wildl Manag 71:1380–1387

    Article  Google Scholar 

  • Cat J, Beugnet F, Hoch T, Jongejan F, Prangé A, Chalvet-Monfray K (2017) Influence of the spatial heterogeneity in tick abundance in the modeling of the seasonal activity of Ixodes ricinus nymphs in Western Europe. Exp Appl Acarol 71:115–130

    Article  PubMed  Google Scholar 

  • Cederlund G (1989) Activity patterns in moose and roe deer in a north boreal forest. Ecography 12:39–45

    Article  Google Scholar 

  • Chastagner A, Pion A, Verheyden H, Lourtet B, Cargnelutti B, Picot D, Poux V, Bard E, Plantard O, McCoy KD (2017) Host specificity, pathogen exposure, and superinfections impact the distribution of Anaplasma phagocytophilum genotypes in ticks, roe deer, and livestock in a fragmented agricultural landscape. Infect Genet Evol 55:31–44

    Article  PubMed  Google Scholar 

  • Ciuti S, Northrup JM, Muhly TB, Simi S, Musiani M, Pitt JA, Boyce MS (2012) Effects of humans on behaviour of wildlife exceed those of natural predators in a landscape of Fear. PLoS ONE 7:e50611

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Conner LM, Smith MD, Burger L (2003) A comparison of distance-based and classification-based analyses of habitat use. Ecology 84:526–531

    Article  Google Scholar 

  • Conway J, Eddelbuettel D, Nishiyama T, Kumar Prayaga S, Tiffin N (2017) RPostgreSQL: R interface to the “PostgreSQL” database system [Internet]. Available from: https://cran.r-project.org/web/packages/RPostgreSQL/index.html

  • Côté SD, Rooney TP, Tremblay J-P, Dussault C, Waller DM (2004) Ecological impacts of deer overabundance. Annu Rev Ecol Evol Syst 35:113–147

    Article  Google Scholar 

  • Coulon A, Cosson J, Angibault J, Cargnelutti B, Galan M, Morellet N, Petit E, Aulagnier S, Hewison AJM (2004) Landscape connectivity influences gene flow in a roe deer population inhabiting a fragmented landscape: an individual–based approach. Mol Ecol 13:2841–2850

    Article  PubMed  CAS  Google Scholar 

  • Coulon A, Morellet N, Goulard M, Cargnelutti B, Angibault J-M, Hewison AJM (2008) Inferring the effects of landscape structure on roe deer (Capreolus capreolus) movements using a step selection function. Landscape Ecol 23:603–614

    Article  Google Scholar 

  • Debeffe L, Morellet N, Cargnelutti B, Lourtet B, Bon R, Gaillard J-M, Hewison AJM (2012) Condition-dependent natal dispersal in a large herbivore: heavier animals show a greater propensity to disperse and travel further. J Anim Ecol 81:1327

    Article  PubMed  Google Scholar 

  • Earl JE, Zollner PA (2017) Advancing research on animal-transported subsidies by integrating animal movement and ecosystem modeling. J Anim Ecol 86:987–997

    Article  PubMed  Google Scholar 

  • Ellis EC, Klein Goldewijk K, Siebert S, Lightman D, Ramankutty N (2010) Anthropogenic transformation of the biomes, 1700 to 2000. Glob Ecol Biogeogr 19:589–606

    Google Scholar 

  • Fortin D, Beyer HL, Boyce MS, Smith MS, Duchesne T, Mao JS (2005) Wolves influence elk movements: behavior shapes a trophic cascade in Yellowstone National Park. Ecology 86:1320–1330

    Article  Google Scholar 

  • Fortin D, Fortin M-E, Beyer HL, Duchesne TCourant S, Dancose K (2009) Group-size-mediated habitat selection and group fusion–fission dynamics of bison under predation risk. Ecology 90:2480–2490

    Article  PubMed  Google Scholar 

  • Frid A, Dill LM (2002) Human-caused disturbance stimuli as a form of predation risk. Conserv Ecol 6:11

    Article  Google Scholar 

  • Fryxell JM, Hazell M, Börger L, Dalziel BD, Haydon DT, Morales JM, McIntosh T, Rosatte RC (2008) Multiple movement modes by large herbivores at multiple spatiotemporal scales. Proc Natl Acad Sci 105:19114–19119

    Article  PubMed  PubMed Central  Google Scholar 

  • Gill RMA, Beardall V (2001) The impact of deer on woodlands: the effects of browsing and seed dispersal on vegetation structure and composition. Forestry 74:209–218

    Article  Google Scholar 

  • Grignolio S, Merli E, Bongi P, Ciuti S, Apollonio M (2011) Effects of hunting with hounds on a non-target species living on the edge of a protected area. Biol Conserv 144:641–649

    Article  Google Scholar 

  • Hewison AM, Angibault J-M, Cargnelutti B, Coulon A, Rames J-L, Serrano E, Verheyden H, Morellet N (2007) Using radio-tracking and direct observation to estimate roe deer Capreolus capreolus density in a fragmented landscape: a pilot study. Wildl Biol 13:313–320

    Article  Google Scholar 

  • Hewison A, Morellet N, Verheyden H, Daufresne T, Angibault J-M, Cargnelutti B, Merlet J, Picot D, Rames J-L, Joachim J (2009) Landscape fragmentation influences winter body mass of roe deer. Ecography 32:1062–1070

    Article  Google Scholar 

  • Hobbs NT (1996) Modification of ecosystems by ungulates. J Wildl Manag 60:695–713

    Article  Google Scholar 

  • Jeltsch F, Bonte D, Pe’er G, Reineking B, Leimgruber P, Balkenhol N, Schröder B, Buchmann CM, Mueller T, Blaum N, Zurell D, Böhning-Gaese K, Wiegand T, Eccard JA, Hofer H, Reeg J, Eggers U, Bauer S (2013) Integrating movement ecology with biodiversity research-exploring new avenues to address spatiotemporal biodiversity dynamics. Mov Ecol 1:6

    Article  PubMed  PubMed Central  Google Scholar 

  • Jones CG, Lawton JH, Shachak M (1997) Positive and negative effects of organisms as physical ecosystem engineers. Ecology 78:1946–1957

    Article  Google Scholar 

  • Kiffner C, Lödige C, Alings M, Vor T, Rühe F (2010) Abundance estimation of Ixodes ticks (Acari: Ixodidae) on roe deer (Capreolus capreolus). Exp Appl Acarol 52:73–84

    Article  PubMed  PubMed Central  Google Scholar 

  • Kilpatrick AM, Dobson AD, Levi T, Salkeld DJ, Swei A, Ginsberg HS, Kjemtrup A, Padgett KA, Jensen PM, Fish D (2017) Lyme disease ecology in a changing world: consensus, uncertainty and critical gaps for improving control. Phil Trans R Soc B 372:20160117

    Article  PubMed  Google Scholar 

  • Laundré JW, Hernández L, Ripple WJ (2010) The landscape of fear: ecological implications of being afraid. Open Ecol J 3:1–7

    Article  Google Scholar 

  • Lima SL, Zollner PA (1996) Towards a behavioral ecology of ecological landscapes. Trends Ecol Evol 11:131–135

    Article  PubMed  CAS  Google Scholar 

  • Linnell J, Duncan P, Andersen R (1998) The European roe deer: a portrait of a successful species. In: The European roe deer: the biology of success. Scand Univ Press Oslo, pp. 11–22

  • Lone K, Loe LE, Meisingset EL, Stamnes I, Mysterud A (2015) An adaptive behavioural response to hunting: surviving male red deer shift habitat at the onset of the hunting season. Anim Behav 102:127–138

    Article  Google Scholar 

  • Martin J, Benhamou S, Yoganand K, Owen-Smith N (2015) Coping with spatial heterogeneity and temporal variability in resources and risks: adaptive movement behaviour by a large grazing herbivore. PLoS ONE 10:e0118461

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Mitchell MGE, Bennett EM, Gonzalez A (2013) Linking landscape connectivity and ecosystem service provision: current knowledge and research gaps. Ecosystems 16:894–908

    Article  Google Scholar 

  • Morellet N, Van Moorter B, Cargnelutti B, Angibault J-M, Lourtet B, Merlet J, Ladet S, Hewison AJM (2011) Landscape composition influences roe deer habitat selection at both home range and landscape scales. Landscape Ecol 26:999–1010

    Article  Google Scholar 

  • Mysterud A, Easterday WR, Stigum VM, Aas AB, Meisingset EL, Viljugrein H (2016) Contrasting emergence of Lyme disease across ecosystems. Nat Commun 7:11882

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Nathan R, Getz WM, Revilla E, Holyoak M, Kadmon R, Saltz D, Smouse PE (2008) A movement ecology paradigm for unifying organismal movement research. Proc Natl Acad Sci 105:19052–19059

    Article  PubMed  PubMed Central  Google Scholar 

  • Owen-Smith N, Fryxell J, Merrill E (2010) Foraging theory upscaled: the behavioural ecology of herbivore movement. Philos Trans R Soc Lond B 365:2267–2278

    Article  CAS  Google Scholar 

  • Owen-Smith N, Goodall V, Fatti P (2012) Applying mixture models to derive activity states of large herbivores from movement rates obtained using GPS telemetry. Wildl Res 39:452–462

    Google Scholar 

  • Padié S, Morellet N, Hewison AJM, Martin J-L, Bonnot N, Cargnelutti B, Chamaillé-Jammes S (2015) Roe deer at risk: teasing apart habitat selection and landscape constraints in risk exposure at multiple scales. Oikos 124:1536–1546

    Article  Google Scholar 

  • Pakeman R (2001) Plant migration rates and seed dispersal mechanisms. J Biogeogr 28:795–800

    Article  Google Scholar 

  • Palmer M, Fieberg J, Swanson A, Kosmala M, Packer C (2017) A ‘dynamic’ landscape of fear: prey responses to spatiotemporal variations in predation risk across the lunar cycle. Ecol Lett 20:1364–1373

    Article  PubMed  CAS  Google Scholar 

  • Panzacchi M, Van Moorter B, Strand O, Saerens M, Kivimäki I, St. Clair CC, Herfindal I, Boitani L (2016) Predicting the continuum between corridors and barriers to animal movements using step selection functions and randomized shortest paths. J Anim Ecol 85:32–42

    Article  PubMed  Google Scholar 

  • Perret J-L, Guerin PM, Diehl PA, Vlimant M, Gern L (2003) Darkness induces mobility, and saturation deficit limits questing duration, in the tick Ixodes ricinus. J Exp Biol 206:1809–1815

    Article  PubMed  Google Scholar 

  • Picard M, Papaïx J, Gosselin F, Picot D, Bideau E, Baltzinger C (2015) Temporal dynamics of seed excretion by wild ungulates: implications for plant dispersal. Ecol Evol 5:2621–2632

    Article  PubMed  PubMed Central  Google Scholar 

  • Prokopenko CM, Boyce MS, Avgar T (2017) Extent-dependent habitat selection in a migratory large herbivore: road avoidance across scales. Landscape Ecol 32:313–325

    Article  Google Scholar 

  • Qviller L, Grøva L, Viljugrein H, Klingen I, Mysterud A (2014) Temporal pattern of questing tick Ixodes ricinus density at differing elevations in the coastal region of western Norway. Parasit Vectors 7:179

    Article  PubMed  PubMed Central  Google Scholar 

  • Qviller L, Viljugrein H, Loe LE, Meisingset EL, Mysterud A (2016) The influence of red deer space use on the distribution of Ixodes ricinus ticks in the landscape. Parasit Vectors 9:545

    Article  PubMed  PubMed Central  Google Scholar 

  • R Core Team (2016) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, 2015. https://www.R-project.org/

  • Ruiz-Fons F, Gilbert L (2010) The role of deer as vehicles to move ticks, Ixodes ricinus, between contrasting habitats. Int J Parasitol 40:1013–1020

    Article  PubMed  Google Scholar 

  • Seagle SW (2003) Can ungulates foraging in a multiple-use landscape alter forest nitrogen budgets? Oikos 103:230–234

    Article  CAS  Google Scholar 

  • Sempéré A, Mauget R, Mauget C (1998) Reproductive physiology of roe deer. In: Andersen R, Duncan P, Linnell JDC (eds) The European roe deer: the biology of success. Scandinavian University Press, Oslo, pp 161–188

    Google Scholar 

  • Signer J, Fieberg J, Avgar T (2017) Estimating utilization distributions from fitted step-selection functions. Ecosphere 8:e01771

    Article  Google Scholar 

  • Taylor PD, Fahrig L, Henein K, Merriam G (1993) Connectivity is a vital element of landscape structure. Oikos 68:571–573

    Article  Google Scholar 

  • Therneau TM, Lumley T (2017) survival: Survival Analyses. R-package version 2.41-3. Available from: https://cran.r-project.org/package=survival

  • Thurfjell H, Ciuti S, Boyce MS (2014) Applications of step-selection functions in ecology and conservation. Mov Ecol 2:1–12

    Article  Google Scholar 

  • Trombulak SC, Frissell CA (2000) Review of ecological effects of roads on terrestrial and aquatic communities. Conserv Biol 14:18–30

    Article  Google Scholar 

  • Van Beest FM, Mysterud A, Loe LE, Milner JM (2010) Forage quantity, quality and depletion as scale-dependent mechanisms driving habitat selection of a large browsing herbivore. J Anim Ecol 79:910–922

    PubMed  Google Scholar 

  • Vourc’h G, Abrial D, Bord S, Jacquot M, Masseglia S, Poux V, Pisanu B, Bailly X, Chapuis J-L (2016) Mapping human risk of infection with Borrelia burgdorferi sensu lato, the agent of Lyme borreliosis, in a periurban forest in France. Ticks Tick-Borne Dis 7:644–652

    Article  PubMed  Google Scholar 

  • Zeller KA, McGarigal K, Whiteley AR (2012) Estimating landscape resistance to movement: a review. Landscape Ecol 27:777–797

    Article  Google Scholar 

Download references

Acknowledgements

We thank the local hunting associations, the Fédération Départementale des Chasseurs de la Haute-Garonne for allowing us to work in the Comminges, as well as all coworkers and volunteers for help collecting data. We thank two anonymous referees for constructive comments on a previous version of the manuscript. This work was performed using the facilities of the CC LBBE/PRABI and was supported by the “EUROENET” ANR grant ANR-14-CE02-0017-01 and the “OSCAR” ANR grant ANR-11 AGRO 001 05.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Jodie Martin.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 1496 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Martin, J., Vourc’h, G., Bonnot, N. et al. Temporal shifts in landscape connectivity for an ecosystem engineer, the roe deer, across a multiple-use landscape. Landscape Ecol 33, 937–954 (2018). https://doi.org/10.1007/s10980-018-0641-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10980-018-0641-0

Keywords

Navigation