Accelerating across the landscape: The energetic costs of natal dispersal in a large herbivore.
biologging
circadian rhythm
energy expenditure
movement
philopatric
roe deer
transience
Journal
The Journal of animal ecology
ISSN: 1365-2656
Titre abrégé: J Anim Ecol
Pays: England
ID NLM: 0376574
Informations de publication
Date de publication:
01 2020
01 2020
Historique:
received:
15
03
2019
accepted:
08
08
2019
pubmed:
31
8
2019
medline:
14
8
2020
entrez:
31
8
2019
Statut:
ppublish
Résumé
Dispersal is a key mechanism enabling species to adjust their geographic range to rapid global change. However, dispersal is costly and environmental modifications are likely to modify the cost-benefit balance of individual dispersal decisions, for example, by decreasing functional connectivity. Dispersal costs occur during departure, transience and settlement, and are levied in terms of energy, risk, time and lost opportunity, potentially influencing individual fitness. However, to the best of our knowledge, no study has yet quantified the energetic costs of dispersal across the dispersal period by comparing dispersing and philopatric individuals in the wild. Here, we employed animal-borne biologgers on a relatively large sample (N = 105) of juvenile roe deer to estimate energy expenditure indexed using the vector of dynamic body acceleration and mobility (distance travelled) in an intensively monitored population in the south-west of France. We predicted that energy expenditure would be higher in dispersers compared to philopatric individuals. We expected costs to be (a) particularly high during transience, (b) especially high in the more fragmented areas of the landscape and (c) concentrated during the night to avoid disturbance caused by human activity. There were no differences in energy expenditure between dispersers and philopatric individuals during the pre-dispersal phase. However, dispersers expended around 22% more energy and travelled around 63% further per day than philopatric individuals during transience. Differences in energy expenditure were much less pronounced during the settlement phase. The costs of transience were almost uniquely confined to the dawn period, when dispersers spent 23% more energy and travelled 112% further than philopatric individuals. Finally, the energetic costs of transience per unit time and the total distance travelled to locate a suitable settlement range were higher in areas of high road density. Our results provide strong support for the hypothesis that natal dispersal is energetically costly and indicate that transience is the most costly part of the process, particularly in fragmented landscapes. Further work is required to link dispersal costs with fitness components so as to understand the likely outcome of further environmental modifications on the evolution of dispersal behaviour.
Identifiants
pubmed: 31469178
doi: 10.1111/1365-2656.13098
doi:
Banques de données
Dryad
['10.5061/dryad.mm324rv']
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
173-185Informations de copyright
© 2019 The Authors. Journal of Animal Ecology © 2019 British Ecological Society.
Références
Adrados, C., Girard, I., Gendner, J. P., & Janeau, G. (2002). Global positioning system (GPS) location accuracy improvement due to selective availability removal. Comptes Rendus Biologies, 325, 165-170. https://doi.org/10.1016/S1631-0691(02)01414-2
Arnold, W., Ruf, T., Loe, L. E., Irvine, R. J., Ropstad, E., Veiberg, V., & Albon, S. D. (2018). Circadian rhythmicity persists through the Polar night and midnight sun in Svalbard reindeer. Scientific Reports, 8, 14466. https://doi.org/10.1038/s41598-018-32778-4
Bates, D., Maechler, M., Bolker, B., & Walker, S. (2015). Fitting linear mixed-effects models using lme4. Journal of Statistical Software, 67(1), 1-48. https://doi.org/10.18637/jss.v067.i01
Benoit, L., Hewison, A. J. M., Coulon, A., Debeffe, L., Grémillet, D., Ducros, D., … Morellet, N. (2019). Data from: Accelerating across the landscape: The energetic costs of natal dispersal in a large herbivore. Dryad Digital Repository. https://doi.org/10.5061/dryad.mm324rv
Bjørneraas, K., Van Moorter, B., Rolandsen, C. M., & Herfindal, I. (2010). Screening global positioning system location data for errors using animal movement characteristics. The Journal of Wildlife Management, 74, 1361-1366. https://doi.org/10.1111/j.1937-2817.2010.tb01258.x
Boldt, A., & Ingold, P. (2005). Effects of air traffic, snow cover and weather on altitudinal short-term and medium-term movements of female Alpine chamois Rupicapra rupicapra in winter. Wildlife Biology, 11, 351-363. https://doi.org/10.2981/0909-6396(2005)11[351:EOATSC]2.0.CO;2
Bonnot, N. C., Hewison, A. J. M., Morellet, N., Gaillard, J.-M., Debeffe, L., Couriot, O., … Vanpé, C. (2017). Stick or twist: Roe deer adjust their flight behaviour to the perceived trade-off between risk and reward. Animal Behaviour, 124, 35-46. https://doi.org/10.1016/j.anbehav.2016.11.031
Bonnot, N. C., Morellet, N., Hewison, A. J. M., Martin, J. L., Benhamou, S., & Chamaillé-Jammes, S. (2016). Sitka black-tailed deer (Odocoileus hemionus sitkensis) adjust habitat selection and activity rhythm to the absence of predators. Canadian Journal of Zoology, 94, 385-394. https://doi.org/10.1139/cjz-2015-0227
Bonte, D., Van Dyck, H., Bullock, J. M., Coulon, A., Delgado, M., Gibbs, M., … Travis, J. M. J. (2012). Costs of dispersal. Biological Reviews, 87, 290-312. https://doi.org/10.1111/j.1469-185X.2011.00201.x
Bowler, D. E., & Benton, T. G. (2005). Causes and consequences of animal dispersal strategies: Relating individual behaviour to spatial dynamics. Biological Reviews, 80, 205-225. https://doi.org/10.1017/S1464793104006645
Brown, J. H., Gillooly, J. F., Allen, A. P., Savage, V. M., & West, G. B. (2004). Toward a metabolic theory of ecology. Ecology, 85, 1771-1789. https://doi.org/10.1890/03-9000
Burnham, K. P., & Anderson, D. R. (2002). Model selection and multimodel inference: A practical information-theoretic approach (2nd ed.). New York, NY: Springer.
Calenge, C., Dray, S., & Royer, M. (2009). The concept of animals' trajectories from a data analysis perspective. Ecological Informatics, 4, 34-41. https://doi.org/10.1016/j.ecoinf.2008.10.002
Cargnelutti, B., Coulon, A., Hewison, A. J. M., Goulard, M., Angibault, J. M., & Morellet, N. (2007). Testing GPS performance for wildlife monitoring using mobile collars with known reference points. Journal of Wildlife Management, 71, 1380-1387. https://doi.org/10.2193/2006-257
Clobert, J., Danchin, E., Dhondt, A. A., & Nichols, J. (2001). Dispersal. Oxford, UK: Oxford University Press.
Collins, P. M., Green, J. A., Warwick-Evans, V., Dodd, S., Shaw, P. J., Arnould, J. P., & Halsey, L. G. (2015). Interpreting behaviors from accelerometry: A method combining simplicity and objectivity. Ecology and Evolution, 5, 4642-4654. https://doi.org/10.1002/ece3.1660
Couriot, O., Hewison, A. J. M., Saïd, S., Cagnacci, F., Chamaillé-Jammes, S., Linnell, J. D. C., … Morellet, N. (2018). Truly sedentary? The multi-range tactic as a response to resource heterogeneity and unpredictability in a large herbivore. Oecologia, 187(1), 47-60. https://doi.org/10.1007/s00442-018-4131-5
Crnokrak, P., & Roff, D. A. (2000). The trade-off to macroptery in the cricket Gryllus firmus: A path analysis in males. Journal of Evolutionary Biology, 13, 396-408. https://doi.org/10.1046/j.1420-9101.2000.00188.x
Crooks, K. R., Burdett, C. L., Theobald, D. M., King, S. R., Di Marco, M., Rondinini, C., & Boitani, L. (2017). Quantification of habitat fragmentation reveals extinction risk in terrestrial mammals. Proceedings of the National Academy of Sciences of the United States of America, 114, 7635-7640. https://doi.org/10.1073/pnas.1705769114
Daan, S., Honma, S., & Honma, K. I. (2013). Body temperature predicts the direction of internal desynchronization in humans isolated from time cues. Journal of Biological Rhythms, 28, 403-411. https://doi.org/10.1177/0748730413514357
Debeffe, L., Morellet, N., Cargnelutti, B., Lourtet, B., Bon, R., Gaillard, J.-M., & Hewison, A. J. M. (2012). Condition-dependent natal dispersal in a large herbivore: Heavier animals show a greater propensity to disperse and travel further. Journal of Animal Ecology, 81, 1327-1327. https://doi.org/10.1111/j.1365-2656.2012.02014.x
Debeffe, L., Morellet, N., Cargnelutti, B., Lourtet, B., Coulon, A., Gaillard, J. M., … Hewison, A. (2013). Exploration as a key component of natal dispersal: Dispersers explore more than philopatric individuals in roe deer. Animal Behaviour, 86, 143-151. https://doi.org/10.1016/j.anbehav.2013.05.005
Debeffe, L., Morellet, N., Verheyden-Tixier, H., Hoste, H., Gaillard, J.-M., Cargnelutti, B., … Hewison, A. J. M. (2014). Parasite abundance contributes to condition-dependent dispersal in a wild population of large herbivore. Oikos, 123, 1121-1125. https://doi.org/10.1111/oik.01396
Dibner, C., Schibler, U., & Albrecht, U. (2010). The mammalian circadian timing system: Organization and coordination of central and peripheral clocks. Annual Review of Physiology, 72, 517-549. https://doi.org/10.1146/annurev-physiol-021909-135821
Ensing, E. P., Ciuti, S., de Wijs, F. A., Lentferink, D. H., ten Hoedt, A., Boyce, M. S., & Hut, R. A. (2014). GPS based daily activity patterns in European red deer and North American elk (Cervus elaphus): Indication for a weak circadian clock in ungulates. PLoS ONE, 9, e106997. https://doi.org/10.1371/journal.pone.0106997
Fahrig, L. (2007). Non-optimal animal movement in human-altered landscapes. Functional Ecology, 21, 1003-1015. https://doi.org/10.1111/j.1365-2435.2007.01326.x
Gaillard, J. M., Loison, A., Toïgo, C., Delorme, D., & Van Laere, G. (2003). Cohort effects and deer population dynamics. Ecoscience, 10, 412-420. https://doi.org/10.1080/11956860.2003.11682789
Gaynor, K. M., Hojnowski, C. E., Carter, N. H., & Brashares, J. S. (2018). The influence of human disturbance on wildlife nocturnality. Science, 360, 1232-1235. https://doi.org/10.1126/science.aar7121
Gleiss, A. C., Wilson, R. P., & Shepard, E. L. (2011). Making overall dynamic body acceleration work: On the theory of acceleration as a proxy for energy expenditure. Methods in Ecology and Evolution, 2(1), 23-33. https://doi.org/10.1111/j.2041-210X.2010.00057.x
Graf, P. M., Wilson, R. P., Qasem, L., Hackländer, K., & Rosell, F. (2015). The use of acceleration to code for animal behaviours; a case study in free-ranging Eurasian beavers Castor fiber. PLoS ONE, 10, e0136751. https://doi.org/10.1371/journal.pone.0136751
Grémillet, D., Lescroël, A., Ballard, G., Dugger, K. M., Massaro, M., Porzig, E. L., & Ainley, D. G. (2018). Energetic fitness: Field metabolic rates assessed via 3D accelerometry complement conventional fitness metrics. Functional Ecology, 32, 1203-1213. https://doi.org/10.1111/1365-2435.13074
Hein, A. M., Hou, C., & Gillooly, J. F. (2012). Energetic and biomechanical constraints on animal migration distance. Ecology Letters, 15, 104-110. https://doi.org/10.1111/j.1461-0248.2011.01714.x
Hewison, A. J. M., Angibault, J. M., Cargnelutti, B., Coulon, A., Rames, J. L., Serrano, E., … Morellet, N. (2007). Using radio-tracking and direct observation to estimate roe deer Capreolus capreolus density in a fragmented landscape: A pilot study. Wildlife Biology, 13, 313-320. https://doi.org/10.2981/0909-6396(2007)13[313:URADOT]2.0.CO;2
Hewison, A. J. M., Gaillard, J. M., Delorme, D., Van Laere, G., Amblard, T., & Klein, F. (2011). Reproductive constraints, not environmental conditions, shape the ontogeny of sex-specific mass-size allometry in roe deer. Oikos, 120(8), 1217-1226. https://doi.org/10.1111/j.1600-0706.2011.19316.x
Hewison, A. J. M., Morellet, N., Verheyden, H., Daufresne, T., Angibault, J.-M., Cargnelutti, B., … Cebe, N. (2009). Landscape fragmentation influences winter body mass of roe deer. Ecography, 32, 1062-1070. https://doi.org/10.1111/j.1600-0587.2009.05888.x
Hovestadt, T., Binzenhöfer, B., Nowicki, P., & Settele, J. (2011). Do all inter-patch movements represent dispersal? A mixed kernel study of butterfly mobility in fragmented landscapes. Journal of Animal Ecology, 80, 1070-1077. https://doi.org/10.1111/j.1365-2656.2011.01848.x
Ims, R. A., & Hjermann, D. O. (2001). Condition-dependent dispersal. In J. Clobert, E. Danchin, A. A. Dhondt, & J. D. Nichols (Eds.), Dispersal (pp. 203-216). Oxford, UK: Oxford University Press.
Jeugd, H. P. V. D. (2001). Large barnacle goose males can overcome the social costs of natal dispersal. Behavioral Ecology, 12, 275-282. https://doi.org/10.1093/beheco/12.3.275
Johnson, C. A., Fryxell, J. M., Thompson, I. D., & Baker, J. A. (2009). Mortality risk increases with natal dispersal distance in American martens. Proceedings of the Royal Society B: Biological Sciences, 276, 3361-3367. https://doi.org/10.1098/rspb.2008.1958
Kingma, S. A., Komdeur, J., Hammers, M., & Richardson, D. S. (2016). The cost of prospecting for dispersal opportunities in a social bird. Biology Letters, 12, 20160316. https://doi.org/10.1098/rsbl.2016.0316
Kokko, H., & López-Sepulcre, A. (2006). From individual dispersal to species ranges: Perspectives for a changing world. Science, 313, 789-791. https://doi.org/10.1126/science.1128566
Krop-Benesch, A., Berger, A., Hofer, H., & Heurich, M. (2013). Long-term measurement of roe deer (Capreolus capreolus) (Mammalia: Cervidae) activity using two-axis accelerometers in GPS-collars. Italian Journal of Zoology, 80, 69-81. https://doi.org/10.1080/11250003.2012.725777
Lagos, L., Picos, J., & Valero, E. (2012). Temporal pattern of wild ungulate-related traffic accidents in northwest Spain. European Journal of Wildlife Research, 58, 661-668. https://doi.org/10.1007/s10344-012-0614-6
Lavielle, M. (1999). Detection of multiple changes in a sequence of dependent variables. Stochastic Processes and their Applications, 83, 79-102. https://doi.org/10.1016/S0304-4149(99)00023-X
Linnell, J. D. C., Wahlström, K., & Gaillard, J. M. (1998). From birth to independence. In R. Andersen, P. Duncan, & J. D. C. Linnell (Eds.), The European roe deer: The biology of success (pp. 257-283). Oslo, Norway: Scandinavian University Press.
Martin, J., Vourc’h, G., Bonnot, N., Cargnelutti, B., Chaval, Y., Lourtet, B., … Morellet, N. (2018). Temporal shifts in landscape connectivity for an ecosystem engineer, the roe deer, across a multiple-use landscape. Landscape Ecology, 33, 937-954. https://doi.org/10.1007/s10980-018-0641-0
Massemin, S., Maho, Y. L., & Handrich, Y. (1998). Seasonal pattern in age, sex and body condition of Barn Owls Tyto alba killed on motorways. Ibis, 140(1), 70-75. https://doi.org/10.1111/j.1474-919X.1998.tb04543.x
Maublanc, M.-L., Bideau, E., Willemet, R., Bardonnet, C., Gonzalez, G., Desneux, L., … Gerard, J.-F. (2012). Ranging behaviour of roe deer in an experimental high-density population: Are females territorial? Comptes Rendus Biologies, 335, 735-743. https://doi.org/10.1016/j.crvi.2012.11.003
Miwa, M., Oishi, K., Nakagawa, Y., Maeno, H., Anzai, H., Kumagai, H., …Hirooka, H. (2015). Application of overall dynamic body acceleration as a proxy for estimating the energy expenditure of grazing farm animals: relationship with heart rate. PLoS ONE, 10, e0128042. https://doi.org/10.1371/journal.pone.0128042
Morellet, N., Bonenfant, C., Börger, L., Ossi, F., Cagnacci, F., Heurich, M., …Mysterud, A. (2013). Seasonality, weather and climate affect home range size in roe deer across a wide latitudinal gradient within Europe. Journal of Animal Ecology, 82, 1326-1339. https://doi.org/10.1111/1365-2656.12105
Morellet, N., Van Moorter, B., Cargnelutti, B., Angibault, J.-M., Lourtet, B., Merlet, J., … Hewison, A. J. M. (2011). Landscape composition influences roe deer habitat selection at both home range and landscape scales. Landscape Ecology, 26, 999-1010. https://doi.org/10.1007/s10980-011-9624-0
Morellet, N., Verheyden, H., Angibault, J. M., Cargnelutti, B., Lourtet, B., & Hewison, A. J. M. (2009). The effect of capture on ranging behaviour and activity of the European roe deer Capreolus capreolus. Wildlife Biology, 15, 278-287. https://doi.org/10.2981/08-084
Patin, R., Etienne, M. P., Lebarbier, E., Chamaillé-Jammes, S., & Benhamou, S. (2020). Identifying stationary phases in multivariate time-series for highlighting behavioural modes and home range settlements. Journal of Animal Ecology, 89, 44-56.
Pohl, H. H. (1998). Temperature cycles as zeitgeber for the circadian clock of two burrowing rodents, the normothermic antelope ground squirrel and the heterothermic Syrian hamster. Biological Rhythm Research, 29, 311-325. https://doi.org/10.1076/brhm.29.3.311.1436
Qasem, L., Cardew, A., Wilson, A., Griffiths, I., Halsey, L. G., Shepard, E. L. C., … Wilson, R. (2012). Tri-axial dynamic acceleration as a proxy for animal energy expenditure; should we be summing values or calculating the vector? PLoS ONE, 7, e31187. https://doi.org/10.1371/journal.pone.0031187
R Core Team. (2017) R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing. Retrieved from https://www.R-project.org/.
Ratcliffe, P. R., & Mayle, B. A. (1992). Roe deer biology and management. London, UK: HMSO.
Récapet, C., Zahariev, A., Blanc, S., Arrivé, M., Criscuolo, F., Bize, P., & Doligez, B. (2016). Differences in the oxidative balance of dispersing and non-dispersing individuals: An experimental approach in a passerine bird. BMC Evolutionary Biology, 16, 125. https://doi.org/10.1186/s12862-016-0697-x
Reinhardt, K., Köhler, G., Maas, S., & Detzel, P. (2005). Low dispersal ability and habitat specificity promote extinctions in rare but not in widespread species: The Orthoptera of Germany. Ecography, 28, 593-602. https://doi.org/10.1111/j.2005.0906-7590.04285.x
Ronce, O., Perret, F., & Olivieri, I. (2000). Landscape dynamics and evolution of colonizer syndromes: Interactions between reproductive effort and dispersal in a metapopulation. Evolutionary Ecology, 14, 233-260. https://doi.org/10.1023/A:1011068005057
Rothermel, B. B., & Semlitsch, R. D. (2002). An experimental investigation of landscape resistance of forest versus old-field habitats to emigrating juvenile amphibians. Conservation Biology, 16, 1324-1332. https://doi.org/10.1046/j.1523-1739.2002.01085.x
Sawyer, H., Kauffman, M. J., Middleton, A. D., Morrison, T. A., Nielson, R. M., & Wyckoff, T. B. (2013). A framework for understanding semi-permeable barrier effects on migratory ungulates. Journal of Applied Ecology, 50(1), 68-78. https://doi.org/10.1111/1365-2664.12013
Schtickzelle, N., Mennechez, G., & Baguette, M. (2006). Dispersal depression with habitat fragmentation in the bog fritillary butterfly. Ecology, 87, 1057-1065. https://doi.org/10.1890/0012-9658(2006)87[1057:DDWHFI]2.0.CO;2
Stache, A., Heller, E., Hothorn, T., & Heurich, M. (2013). Activity patterns of European roe deer (Capreolus capreolus) are strongly influenced by individual behaviour. Folia Zoologica, 62(1), 67-75. https://doi.org/10.25225/fozo.v62.i1.a10.2013
Taylor, P. D., Fahrig, L., Henein, K., & Merriam, G. (1993). Connectivity is a vital element of landscape structure. Oikos, 68, 571-573. https://doi.org/10.2307/3544927
Travis, J. M., & Dytham, C. (1999). Habitat persistence, habitat availability and the evolution of dispersal. Proceedings of the Royal Society of London. Series B: Biological Sciences, 266, 723-728. https://doi.org/10.1098/rspb.1999.0696
Tucker, M. A., Böhning-Gaese, K., Fagan, W. F., Fryxell, J. M., Van Moorter, B., Alberts, S. C., … Mueller, T. (2018). Moving in the Anthropocene: Global reductions in terrestrial mammalian movements. Science, 359, 466-469. https://doi.org/10.1126/science.aam9712
Vanpé, C., Kjellander, P., Galan, M., Cosson, J. F., Aulagnier, S., Liberg, O., & Hewison, A. J. M. (2008). Mating system, sexual dimorphism, and the opportunity for sexual selection in a territorial ungulate. Behavioral Ecology, 19, 309-316. https://doi.org/10.1093/beheco/arm132
Wahlström, L. K. (1994). The significance of male-male aggression for yearling dispersal in roe deer (Capreolus capreolus). Behavioral Ecology and Sociobiology, 35, 409-412. https://doi.org/10.1007/BF00165843
Warren, R., Price, J., Graham, E., Forstenhaeusler, N., & VanDerWal, J. (2018). The projected effect on insects, vertebrates, and plants of limiting global warming to 1.5°C rather than 2°C. Science, 360, 791-795. https://doi.org/10.1126/science.aar3646
Wiens, J. D., Noon, B. R., & Reynolds, R. T. (2006). Post-fledging survival of northern goshawks: The importance of prey abundance, weather, and dispersal. Ecological Applications, 16, 406-418. https://doi.org/10.1890/04-1915
Williams, T. M., Wolfe, L., Davis, T., Kendall, T., Richter, B., Wang, Y., … Wilmers, C. C. (2014). Instantaneous energetics of puma kills reveal advantage of felid sneak attacks. Science, 346, 81-85. https://doi.org/10.1126/science.1254885
Wilmers, C. C., Nickel, B., Bryce, C. M., Smith, J. A., Wheat, R. E., & Yovovich, V. (2015). The golden age of bio-logging: How animal-borne sensors are advancing the frontiers of ecology. Ecology, 96, 1741-1753. https://doi.org/10.1890/14-1401.1
Wood, S., & Scheipl, F. (2017). gamm4: Generalized Additive Mixed Models using ‘mgcv’ and ‘lme4’. R package version 0.2-5. Retrieved from https://CRAN.R-project.org/package=gamm4