Abstract
Context
Understanding how rare and threatened species respond to habitat heterogeneity at different spatial scales requires unbiased population-level parameters incorporating individual variability in occurrence and detection probabilities.
Objectives
We used a Bayesian approach integrating capture-recapture data into an occupancy framework. We assessed the response of Darwin’s fox—a forest-specialist mesocarnivore—to habitat heterogeneity in landscapes with low and moderate fragmentation levels in Chiloé Island, Southern Chile. Our model accounted for differences in capture, occupancy and detection probability among individuals.
Results
We captured 33 Darwin’s foxes, totaling 65 captures/recaptures in 62 different traps (720 trap/nights). Foxes’ detection increased across years and females (n = 15; mean detection probability ± SE 0.07 ± 0.03) were less detected than males (n = 18; 0.11 ± 0.04). Mean [95% BCI] of Darwin’s fox occupancy (\(\uppsi\)) varied from 0.59 [0.43–0.75] in the landscape with the largest mean of forest patch size, to 0.24 [0.22–0.28] in the less heterogeneous landscape. Species occupancy decreased with distance from freshwater bodies. We also found a significant interaction between distance from freshwater bodies and total edges at landscape level, resulting in high occupancy values (> 0.5) in landscapes dominated by forest ecotones.
Conclusions
Our findings suggest the effect of habitat heterogeneity on local populations of the threaten Darwin’s fox in Chiloé Island is modulated by the individual response to habitat attributes at local and landscape scales, but also by emergent cross-scale interactions.
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References
Aarts G, MacKenzie M, McConnell B, Fedak M, Matthiopoulos J (2008) Estimating space use and environmental preference from telemetry data. Ecography 31:140–160
Andrén H (1994) Effects of habitat fragmentation on birds and mammals in landscapes with different proportions of suitable habitat—a review. Oikos 71:355–366
Aravena JC, Carmona MR, Pérez CA, Armesto JJ (2002) Changes in tree species richness, stand structure and soil properties in a successional chronosequence in northern Chiloé Island Chile. Rev Chil Hist Nat 75:339–360
Armesto JJ, Willson MF, Diaz I, Reid S (2005) Ecologia del paisaje rural de la isla de Chiloe: diversidad de aves en fragmentos de bosque nativo. In: Smith-Ramírez C, Armesto JJ, Valdovinos C (eds) Historia, biodiversidad y ecologia de los bosques costeros de Chile. Editorial Universitaria, Santiago, pp 585–599
Atwood TC, Fry TL, Leland BR (2011) Partitioning of anthropogenic watering sites by desert carnivores. J Wildl Manage 75(7):1609–1615
Bannister JR, Donoso PJ (2013) Forest typification to characterize the structure and composition of old-growth evergreen forests on Chiloe island, North Patagonia (Chile). Forests 4:1087–1105
Boyce MS (2006) Scale for resource selection functions. Divers Distrib 12:269–276
Burnham KP, Anderson DR, Huyvaert KP (2011) AIC model selection and multimodel inference in behavioral ecology: some background, observations, and comparisons. Behav Ecol Sociobiol 65(1):23–35
Burton AC, Neilson E, Moreira D, Ladle A, Steenweg R, Fisher JT, Bayne E, Boutin S (2015) Wildlife camera trapping: a review and recommendations for linking surveys to ecological processes. J Appl Ecol 52(3):675–685
Cardillo M, Purvis A, Sechrest W, Gittleman JL, Bielby J, Mace GM (2004) Human population density and extinction risk in the world’s carnivores. PLoS Biol 2:e197
Cardillo M, Mace GM, Jones KE, Bielby J, Bininda-Emonds ORP, Sechrest W, Orme CDL, Purvis A (2005) Multiple causes of high extinction risk in large mammal species. Science 309:1239–1241
Carmona A, Nahuelhual L (2012) Combining land transitions and trajectories in assessing forest cover change. Appl Geogr 32(2):904–915
Celis-Diez JL, Hetz J, Marın-Vial PA, Fuster G, Necochea P, Vasquez RA, Jaksic FM, Armesto JJ (2012) Population abundance, natural history, and habitat use by the arboreal marsupial Dromiciops gliroides in rural Chiloe Island, Chile. J Mammal 93:134–148
Chanchani P, Noon BR, Bailey L, Warrier RA (2016) Conserving tigers in working landscapes. Conserv Biol 30(3):649–660
Conde DA, Colchero F, Zarza H, Christensen NL Jr, Sexton JO, Manterola C, Chávez C, Rivera A, Azuara D, Ceballos G (2010) Sex matters: modeling male and female habitat differences for jaguar conservation. Biol Conserv 143(9):1980–1988
Crooks KR (2002) Relative sensitivities of mammalian carnivores to habitat fragmentation. Conserv Biol 16:488–502
Crooks KR, Burdett CL, Theobald DM, Rondinini C, Boitani L (2011) Global patterns of fragmentation and connectivity of mammalian carnivore habitat. Philos Trans R Soc Lond B 366:2642–2651
Cubaynes S, Pradel R, Choquet R, Duchamp C, Gaillard J-M, Lebreton J-D, Marboutin E, Miquel C, Reboulet Marie-Anne, Poillot C, Taberlet P, Gimenez O (2010) Importance of accounting for detection heterogeneity when estimating abundance: the case of French wolves. Conserv Biol 24(2):621–626
Davis ML, Kelly MJ, Stauffer DF (2011) Carnivore co-existence and habitat use in the Mountain Pine Ridge Forest Reserve, Belize. Anim Conserv 14(1):56–65
Donoso DS, Grez AA, Simonetti JA (2004) Effects of forest fragmentation on the granivory of differently sized seeds. Biol Conserv 115(1):63–70
Edwards S, Gange AC, Wiesel I (2016) An oasis in the desert: the potential of water sources as camera trap sites in arid environments for surveying a carnivore guild. J Arid Environ 124:304–309
Elgueta EI, Valenzuela J, Rau JR (2007) New insights into the prey spectrum of Darwin′s fox (Pseudalopex fulvipes Martin, 1837) on Chiloé island, Chile. Mamm Biol - Zeitschrift für Säugetierkd 72:179–185
Fahrig L (2003) Effects of habitat fragmentation on biodiversity. Annu Rev Ecol Evol Syst 34:487–515
Farias AA, Jaksic FM (2011) Low functional richness and redundancy of a predator assemblage in native forest fragments of Chiloe island, Chile. J Anim Ecol 80:809–817
Foster RJ, Harmsen BJ, Doncaster CP (2010) Habitat use by sympatric jaguars and pumas across a gradient of human disturbance in Belize. Biotropica 42(6):724–731
Gálvez N, Hernández F, Laker J, Gilabert H, Petitpas R, Bonacic C, Gimona A, Hester A, Macdonald D (2013) Forest cover outside protected areas plays an important role in the conservation of the Vulnerable guiña Leopardus guigna. Oryx 47:251–258
Gannon WL, Sikes RS (2007) Guidelines of the American Society of mammalogists for the use of wild mammals in research. J Mammal 88(3):809–823
Gehring TM, Swihart RK (2003) Body size, niche breadth, and ecologically scaled responses to habitat fragmentation: mammalian predators in an agricultural landscape. Biol Conserv 109(2):283–295
Gelman A, Hill J (2006) Data analysis using regression and multilevel/hierarchical models. Cambridge University Press, Cambridge
Gillies CS, Hebblewhite M, Nielsen SE, Krawchuk MA, Aldridge L, Frair JL, Saher DJ, Stevens CE, Jerde CL (2006) Application of random effects to the study of resource selection by animals. J Anim Ecol 75:887–898
Grassel SM, Rachlow JL, Williams CJ (2015) Spatial interactions between sympatric carnivores: asymmetric avoidance of an intraguild predator. Ecol Evol 5(14):2762–2773
Hall B (2016) LaplacesDemon: Complete environment for Bayesian inference Bayesian-Inference.com. R package version 16.0.1. Retrieved from https://web.archive.org/web/20150206004624/http://www.bayesian-inference.com/software
Hansen MC, Potapov PV, Moore R, Hancher M, Turubanova SA, Tyukavina A, Thau D, Stehman SV, Goetz SJ, Loveland TR, Kommareddy A, Egorov A, Chini L, Justice CO, Townshend JRG (2013) High-resolution global maps of 21st-century forest cover change. Science 342:850–853
Hidalgo-Hermoso E, Cabello J, Vega C, Kroeger-Gómez H, Moreira-Arce D, Napolitano C, Navarro C, Sacristán I, Cevidanes A, Di Cataldo S, Dubovi EJ, Mathieu-Benson C, Millán J (2020) An eight-year survey for canine distemper virus indicates lack of exposure in the endangered Darwin’s fox (Lycalopex fulvipes). J Wildl Dis 56(2):482–485
Holland JD, Bert DG, Fahrig L (2004) Determining the spatial scale of species’ response to habitat. Bioscience 54:227
Hooten MB, Hobbs NT (2015) A guide to Bayesian model selection for ecologists. Ecol Monogr 85(1):3–28
Jiménez JE (2007) Ecology of a coastal population of the critically endangered Darwin’s fox (Pseudalopex fulvipes) on Chiloé island, southern Chile. J Zool 271:63–77
Jiménez JE, Marquet PA, Medel R, Jaksić FM (1990) Comparative ecology of Darwin’s Fox (Pseudalopex fulvipes) in mainland and insland settings of southern Chile. Rev Chil Hist Nat 63:177–186
Jonsen ID, Myers RA, Flemming JM (2003) Meta-analysis of animal movement using state-space models. Ecology 84:3055–3063
Kelt DA (2000) Small mammal communities in rainforest fragments in central southern Chile. Biol Conserv 92(3):345–358
Kéry M, Schaub M (2011) Bayesian population analysis using WinBUGS: a hierarchical perspective. Academic Press, Cambridge. https://doi.org/10.1016/C2010-0-68368-4
Kéry M, Gardner B, Stoeckle T, Weber D, Royle JA (2011) Use of spatial capture-recapture modeling and DNA data to estimate densities of elusive animals. Conserv Biol 25(2):356–364
Landa A, Strand O, Linnell JD, Skogland T (1998) Home-range sizes and altitude selection for arctic foxes and wolverines in an alpine environment. Can J Zool 76(3):448–457
Langrock R, King R, Matthiopoulos J, Thomas L, Fortin D, Morales JM (2012) Flexible and practical modeling of animal telemetry data: hidden Markov models and extensions. Ecology 93(11):2336–2342
Lantschner MV, Rusch V, Hayes JP (2012) Habitat use by carnivores at different spatial scales in a plantation forest landscape in Patagonia, Argentina. For Ecol Manage 269:271–278
Lean C, Sterelny K (2016) Ecological hierarchy and biodiversity. The Routledge handbook of biodiversity. Routledge, London
Leclerc M, Vander Wal E, Zedrosser A, Swenson JE, Kindberg J, Pelletier F (2016) Quantifying consistent individual differences in habitat selection. Oecologia 180(3):697–705
Lewis JS, Bailey LL, VandeWoude S, Crooks KR (2015) Interspecific interactions between wild felids vary across scales and levels of urbanization. Ecol Evol 5(24):5946–5961
Link WA (2003) Nonidentifiability of population size from capture-recapture data with heterogeneous detection probabilities. Biometrics 59(4):1123–1130
Long RA, Donovan TM, MacKay P, Zielinski WJ, Buzas JS (2011) Predicting carnivore occurrence with noninvasive surveys and occupancy modeling. Landsc Ecol 26(3):327–340
Loyola RD, De Oliveira G, Diniz-Filho JAF, Lewinsohn TM (2008) Conservation of neotropical carnivores under different prioritization scenarios: mapping species traits to minimize conservation conflicts. Divers Distrib 14:949–960
Lyra-Jorge MC, Ribeiro MC, Ciocheti G, Tambosi LR, Pivello VR (2010) Influence of multi-scale landscape structure on the occurrence of carnivorous mammals in a human-modified savanna, Brazil. Eur J Wildl Res 56(3):359–368
MacKenzie DI, Nichols JD, Lachman GB, Droege S, Andrew Royle J, Langtimm CA (2002) Estimating site occupancy rates when detection probabilities are less than one. Ecology 83(8):2248–2255
Mangas JG, Lozano J, Cabezas-Díaz S, Virgós E (2008) The priority value of scrubland habitats for carnivore conservation in Mediterranean ecosystems. Biodivers Conserv 17(1):43–51
Martin AE, Fahrig L (2012) Measuring and selecting scales of effect for landscape predictors in species-habitat models. Ecol Appl 22:2277–2292
McDonald L (2004) Sampling rare populations. In: Thompson W (ed) Sampling rare or elusive species: concepts, designs, and techniques for estimating population parameters. Island Press, Washington, D.C., pp 11–42
McGarigal K, Marks BJ (1995) FRAGSTATS: spatial pattern analysis program for quantifying landscape structure. Gen. Tech. Rep. PNW-GTR-351. US Department of Agriculture, Forest Service, Pacific Northwest Research Station, Portland, OR, p 122. https://doi.org/10.2737/PNW-GTR-351
Moreira-Arce D, Vergara PM, Boutin S (2015a) Diurnal human activity and introduced species affect occurrence of carnivores in a human-dominated landscape. PLoS ONE 10:e0137854
Moreira-Arce D, Vergara PM, Boutin S, Simonetti JA, Briceño C, Acosta-Jamett G (2015b) Native forest replacement by exotic plantations triggers changes in prey selection of mesocarnivores. Biol Conserv 192:258–267
Moreira-Arce D, Vergara PM, Boutin S, Carrasco G, Briones R, Soto GE, Jimenez JE (2016) Mesocarnivores respond to fine-grain habitat structure in a mosaic landscape comprised by commercial forest plantations in southern Chile. For Ecol Manag 369:135–143
Mortelliti A, Boitani L (2008) Interaction of food resources and landscape structure in determining the probability of patch use by carnivores in fragmented landscapes. Landsc Ecol 23:285–298
Nichols JD, Bailey LL, O’Connell AF Jr, Talancy NW, Campbell Grant EH, Gilbert AT, Annand EM, Husband TP, Hines JE (2008) Multi-scale occupancy estimation and modelling using multiple detection methods. J Appl Ecol 45(5):1321–1329
Oehler JD, Litvaitis JA (1996) The role of spatial scale in understanding responses of medium-sized carnivores to forest fragmentation. Can J Zool 74:2070–2079
Pickett STA, Kolasa J, Armesto JJ, Collins SL (1989) The ecological concept of disturbance and its expression at various hierarchical levels. Oikos. https://doi.org/10.2307/3565258
Queen JP, Quinn GP, Keough MJ (2002) Experimental design and data analysis for biologists. Cambridge University Press, Cambridge
Ratti JT, Reese KP (1988) Preliminary test of the ecological trap hypothesis. J Wildl Manage 52:484–491
Ripple WJ, Estes JA, Beschta RL, Wilmers CC, Ritchie EG, Hebblewhite M, Berger J, Elmhagen B, Letnic M, Nelson MP, Schmitz OJ, Smith DW, Arian DW, Wirsinget AJ (2014) Status and ecological effects of the world’s largest carnivores. Science 343:1241484
Rovero F, Marshall AR (2009) Camera trapping photographic rate as an index of density in forest ungulates. J App Ecol 46(5):1011–1017
Royle JA, Dorazio RM (2008) Hierarchical modeling and inference in ecology: the analysis of data from populations, metapopulations and communities. Elsevier, London
Šálek M, Kreisinger J, Sedláček F, Albrecht T (2010) Do prey densities determine preferences of mammalian predators for habitat edges in an agricultural landscape? Landsc Urban Plan 98(2):86–91
Santos MJ, Matos HM, Palomares F, Santos-Reis M (2011) Factors affecting mammalian carnivore use of riparian ecosystems in Mediterranean climates. J Mammal 92(5):1060–1069
Schooley RL (2006) Spatial Heterogeneity and chracteristics scales of species-habitat relationships. Bioscience 56:533–537
Schooley RL, Branch LC (2007) Spatial heterogeneity in habitat quality and cross-scale interactions in metapopulations. Ecosystems 10:846–853
Sergio F, Caro T, Brown D, Clucas B, Hunter J, Ketchum J, McHugh K, Hiraldo F (2008) Top predators as conservation tools: ecological rationale, assumptions, and efficacy. Annu Rev Ecol Evol Syst 39:1–19
Silva-Rodríguez EA, Ortega-Solís GR, Jiménez JE (2010) Conservation and ecological implications of the use of space by chilla foxes and free-ranging dogs in a human-dominated landscape in southern Chile. Austral Ecol 35(7):765–777
Silva-Rodríguez EA, Farias AA, Moreira-Arce D, Cabello J, Hidalgo-Hermoso E, Lucherini M, Jiménez J (2016). Lycalopex fulvipes. (errata version published in 2016) The IUCN Red List of Threatened Species 2016. https://doi.org/10.2305/IUCN.UK.2016-1.RLTS.T41586A85370871.en
Silva-Rodríguez E, Ovando E, González D, Zambrano B, Sepúlveda MA, Svensson G, Cárdenas R, Contreras P, Farías A (2018) Large-scale assessment of the presence of Darwin’s fox across its newly discovered range. Mamm Biol 92:45–53
Smith JNM, Hellmann JJ (2002) Population persistence in fragmented landscapes. Trends Ecol Evol 17:397–399
Smith-Ramirez C, Celis-Diez JL, von Jenstchyk E, Jimenez JE, Armesto JJ (2010) Habitat use of remnant forest habitats by the threatened arboreal marsupial Dromiciops gliroides (Microbiotheria) in a rural landscape of southern Chile. Wildl Res 37(3):249–254
Sollmann R, Furtado MM, Gardner B, Hofer H, Jácomo AT, Tôrres NM, Silveira L (2011) Improving density estimates for elusive carnivores: accounting for sex-specific detection and movements using spatial capture–recapture models for jaguars in central Brazil. Biol Conserv 144(3):1017–1024
Soranno PA, Cheruvelil KS, Bissell EG, Bremigan MT, Downing JA, Fergus CE et al (2014) Cross-scale interactions: quantifying multi-scaled cause–effect relationships in macrosystems. Front Ecol Environ 12(1):65–73
Spiegelhalter D, Thomas A, Best N, Lunn D (2003). WinBUGS user manual. Version 1.4, MRC. Biostatistics Unit, Institute of Public health and Department of Epidemiology and Public Health, Imperial College School of medicine, UK. http://mrc-bsu.cam.ac.uk/bugs. Accessed 15 June 2019
Sturtz S, Ligges U, Gelman AE (2005) R2WinBUGS: a package for running WinBUGS from R
Valdez J, Klop-Toker K, Stockwell MP, ClulowS CJ, Mahony MJ (2016) Microhabitat selection varies by sex and age class in the endangered green and golden bell frog Litoria aurea. Aust Zool 38(2):223–234
Veblen TT, Schlegel F, Oltremari J (1983) Temperate broad-leaved evergreen forests of South America. Temperate broad-leaved evergreen forests. Elsevier, Amsterdam, pp 5–31
Vergara PM, Armesto JJ (2009) Responses of Chilean forest birds to anthropogenic habitat fragmentation across spatial scales. Landsc Ecol 24(1):25–38
Virgós E (2001) Relative value of riparian woodlands in landscapes with different forest cover for medium-sized Iberian carnivores. Biodivers Conserv 10(7):1039–1049
Virgós E, Tellería JL, Santos T (2002) A comparison on the response to forest fragmentation by medium-sized Iberian carnivores in central Spain. Biodivers Conserv 11:1063–1079
Wagner T, Fergus CE, Stow CA, Cheruvelil KS, Soranno PA (2016) The statistical power to detect cross-scale interactions at macroscales. Ecosphere 7(7):e01417
Walton Z, Samelius G, Odden M, Willebrand T (2017) Variation in home range size of red foxes Vulpes vulpes along a gradient of productivity and human landscape alteration. PLoS ONE 12(4):e0175291
Watanabe S (2010) Asymptotic equivalence of Bayes cross validation and widely applicable information criterion in singular learning theory. J Mach Learn Res 11:3571–3594
Willson MF, Armesto JJ (1995) The natural history of Chiloe: on Darwin’s trail. Rev Chil Hist Nat 69:149–161
Willson MF, De Santo TL, Sabag C, Armesto JJ (1994) Avian communities of fragmented south-temperate rainforests in Chile. Conserv Biol 8(2):508–520
Acknowledgements
We are grateful to several volunteers from Chiloé Silvestre NGO who participated in the trapping surveys across Chiloé Island. D. Moreira-Arce and P. Vergara were supported by CONICYT/ANID Fondecyt No 11181180 and CONICYT/ANID Fondecyt No 1180978, and 021875VE-POSTDOC DICYT (USACH). Additional support was provided by Fundación Buin Zoo.
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JC, DMA, CPH and KN conceived and designed the study. JC, DMA and EHH collected the data. DMA, PV, LM, CPH, AA analysed the data. DMA and PV drafted the manuscript with significant input and critical revisions from KN and AA.
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Moreira-Arce, D., Cabello, J., Meneses, L.O. et al. Scale-dependent habitat use from an individual-based perspective: the case of the endangered Darwin’s fox living in heterogeneous forest landscapes. Landscape Ecol 36, 513–526 (2021). https://doi.org/10.1007/s10980-020-01171-w
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DOI: https://doi.org/10.1007/s10980-020-01171-w