Predicting burrowing owl flight trajectories in urban environments
Tóm tắt
It is important to understand how animals respond to changes in landscape structure, especially when considering habitat alteration and urbanization. Using the burrowing owl (Athene cunicularia) as an ecological model we tested two hypotheses: (1) the landscape of urban areas influences trajectories of the burrowing owl, which responds changing its displacement patterns, and (2) models incorporating species-specific traits, such as stochasticity and landscape perception, better predict flight trajectories than least-cost path models. Thirty owls were captured at the Brasília International Airport, fitted with VHF transmitters, and released in random locations within 30 km of the airport. We generated a habitat suitability map for use as a resistance raster to model flight trajectories: one model was based on the least-cost path, and four models included stochasticity and variations of the owls’ landscape perception and dependency on natural ecosystems. Observed trajectories were compared with those predicted by models using the following metrics extracted from the trajectories: mean habitat suitability values, sinuosity, and length. The best generalized linear models were selected using the Akaike information criterion. The owls dispersed through areas with a lower cost than expected by chance (z = 104.65, p < 0.05). More complex models performed better than the least-cost path model for suitability (r2 = 0.18, p > 0.05), sinuosity (r2 = 0.03, p > 0.05), and length (r2 = 0.37, p > 0.05). Our results demonstrate that landscape information influences flight trajectories, and models incorporating landscape perception and stochasticity better predict burrowing owl flight trajectories.
Tài liệu tham khảo
Adriaensen F, Chardon JP, De Blust G, Swinnen E, Villalba S, Gulinck H, Matthysen E (2003) The application of “least-cost” modelling as a functional landscape model. Landsc Urban Plan 64:233–247. https://doi.org/10.1016/S0169-2046(02)00242-6
Anon (2019) Cities Alliance. Available at https://www.citiesalliance.org. Accessed in November, 2020
Anselin L (1995) Local indicators of spatial analysis–LISA. Geogr Anal 27(2):93–115
Ayram CAC, Mendoza ME, Etter A, Salicrup DRP (2016) Habitat connectivity in biodiversity conservation: a review of recent studies and applications. Prog Phys Geogr 40(1):7–37. https://doi.org/10.1177/0309133315598713
Baladrón AV, Isacch JP, Cavalli M, Bó MS (2016) Habitat selection by burrowing owls Athene cunicularia in the pampas of argentina: a multiple-scale assessment. Acta Ornithologica 51(2):137–150. https://doi.org/10.3161/00016454AO2016.51.2.001
Barton K (2018) MuMIn: multi-model inference. R Package Version 1(40):4
Battley PF, Warnock N, Tibbitts TL, Gill RE, Piersma T, Hassell CJ, Douglas DC, Mulcahy DM, Gartrell BD, Schuckard R, Melville DS, Riegen AC (2012) Contrasting extreme long-distance migration patterns in bar-tailed godwits Limosa lapponica. J Avian Biol 43:21–32. https://doi.org/10.1111/j.1600-048X.2011.05473.x
Bauer S, Hoye BJ (2014) Migratory animals couple biodiversity and ecosystem functioning worldwide. Science 344(1242552–1):8. https://doi.org/10.1126/science.1242552
Beier P, Majka DR, Spencer WD (2008) Forks in the road: choices in procedures for designing wildland linkages. Conserv Biol 22(4):836–851. https://doi.org/10.1111/j.1523-1739.2008.00942.x
Bovet P, Benhamou S (1988) Spatial analysis of animals’ movements using a correlated random walk model. J Theor Biol 131(4):419–433. https://doi.org/10.1016/S0022-5193(88)80038-9
Brandell EE, Fountain-Jones NM, Gilbertson MLJ, Cross PC, Hudson PJ, Smith DW, Stahler DR, Packer C, Craft ME (2021) Group density, disease, and season shape territory size and overlap of social carnivores. J Anim Ecol 00:1–15. https://doi.org/10.1111/1365-2656.13294
Bunn AG, Urban DL, Keitt TH (2000) Landscape connectivity: a conservation application of graph theory. J Environ Manage 59:265–278. https://doi.org/10.1006/jema.2000.0373
Burnham KP, Anderson DR (2002) Model selection and multimodel inference : a practical information-theoretic approach. Springer-Verlag, New York
Burnham KP, Anderson DR (2016) Model selection and multimodel inference: a practical information-theoretic approach. https://doi.org/10.1016/j.ecolmodel.2003.11.004
Candia-Gallardo C, Awade M, Boscolo D, Bugoni L (2010) Rastreamento de aves através de telemetria por rádio e satélite. In: Books T (ed) Ornitologia e Conservação, Ciência aplicada, técnica de pesquisa e levantamento. Rio de Janeiro, pp 1–516
Castellón TD, Sieving KE (2006) An experimental test of permeability and corridor use by an endemic understory bird. Conserv Biol 20(1):135–145. https://doi.org/10.1111/j.1523-1739.2006.00332.x
Cavalli M, Baladrón AV, Isacch JP, Amico VD, Bó MS (2018) Leukocyte profiles and body condition of free-living burrowing Owls (Athene cunicularia) from rural and urban areas in the Argentinean Pampas. Revista Brasileira De Ornitologia 26(1):45–51
CDB (2012) Cities and biodiversity outlook: a global assessment of the links between urbanization, biodiversity, and ecosystem services. Convention on Biological Diversity – CDB. Available at https://www.cbd.int/doc/health/cbo-action-policy-en.pdf. Accessed in April, 2020
Chardon JP, Adriaensen F, Matthysen E (2003) Incorporating landscape elements into a connectivity measure: a case study for the speckled wood butterfly (Pararge aegeria L.). Landscape Ecol 18:561–573. https://doi.org/10.1023/A:1026062530600
Chetkiewicz C, Boyce MS (2009) Use of resource selection functions to identify conservation corridors. J Appl Ecol 46:1036–1047. https://doi.org/10.1111/j.1365-2664,2009.01686.X
Cooke SJ, Hinch SG, Wikelski M, Andrews RD, Kuchel LJ, Wolcott TG, Butler PJ (2004) Biotelemetry: a mechanistic approach to ecology. Trends Ecol Evol 19(6):334–343. https://doi.org/10.1016/j.tree.2004.04.003
Cushman SA, Mckelvey KS, Hayden J, Schwartz MK (2006) Gene flow in complex landscapes: testing multiple hypotheses with causal modeling. Am Nat 168(4):486–499
Demsar U, Slingsby A, Weibel R (2018) Introduction to the special section on visual movement analytics. Inf vis 18(1):133–137. https://doi.org/10.1521/ijct.2009.2.2.105
Dickson BG, Albano CM, Anantharaman R, Beier P, Fargione J, Graves TA, Gray ME, Hall KR, Lawler JJ, Leonard PB, Littlefield CE, McClure ML, Novembre J, Schloss CA, Schumaker NH, Shah VB, Theobald DM (2018) Circuit-theory applications to connectivity science and conservation. Conserv Biol. https://doi.org/10.1111/cobi.13230
Driezen K, Adriaensen F, Rondinini C, Doncaster CP, Matthysen E (2007) Evaluating least-cost model predictions with empirical dispersal data: A case-study using radiotracking data of hedgehogs (Erinaceus europaeus). Ecol Model 209:314–322. https://doi.org/10.1016/j.ecolmodel.2007.07.002
Eiten G (1972) The Cerrado vegetation of Brazil. Bot Rev 38(2):201–341
Etten JV (2017) R Package gdistance: Distances and Routes on Geographical Grids. J Stat Softw 76(13):1–21. https://doi.org/10.18637/jss.v076.i13
Fahrig L (2007) Non-optimal animal movement in human-altered landscapes. Funct Ecol 21(6):1003–1015. https://doi.org/10.1111/j.1365-2435.2007.01326.x
Ferreras P (2001) Landscape structure and asymmetrical inter-patch connectivity in a metapopulation of the endangered Iberian lynx. Biol Cons 100:125–136
Foster E, Love J, Rader R, Reid N, Dillon M, Drielsma MJ (2016) Planning for metapopulation persistence using a multiple-component, cross-scale model of connectivity. Biol Cons 195:177–186. https://doi.org/10.1016/j.biocon.2015.12.034
Franco FF, Marçal-Junior O (2018) Influence of urbanization on the distribution and defense strategies of the burrowing owl Athene cunicularia in the city of Uberlândia, southeastern Brazil. Revista Brasileira De Ornitologia 26(1):1–8
Gervais JA, Rosenberg DK, Anthony RG (2003) Space use and pesticide exposure risk of male burrowing owls in an agricultural landscape. J Wildl Manag 67(1):155–164. https://doi.org/10.2307/3803071
Gillies CS, Beyer HL, Clair CC (2011) Fine-scale movement decisions of tropical forest birds in a fragmented landscape. Ecol Appl 21(3):944–954
Gillies CS, Clair CC (2008) Riparian corridors enhance movement of a forest specialist bird in fragmented tropical forest. PNAS 105(50):19774–19779
Gittleman JL, Kot M (1990) Adaptation: statistics and a null model for estimating phylogenetic efects. Syst Zool 39(3):227–241
Godet L, Harmange C, Marquet M, Joyeux E, Fournier J (2017) Differences in home-range sizes of a bird species in its original, refuge and substitution habitats: challenges to conservation in anthropogenic habitats. Biodivers Conserv 27:719–732
Green GA, Anthony RG (1989) Nesting success and habitat relationships of burrowing owls in the Columbia Basin, Oregon. Condor 91(2):347. https://doi.org/10.2307/1368313
Grueber CE, Nakagawa S, Laws RJ, Jamieson IG (2011) Multimodel inference in ecology and evolution: challenges and solutions. J Evol Biol 24:699–711. https://doi.org/10.1111/j.1420-9101.2010.02210.x
Gu Z, Pan S, Lin Z, Hu L, Dai X, Chang J, Xue Y, Su H, Long J, Sun M, Ganusevich S, Sokolov V, Sokolov A, Pokrovsky I, Ji F, Bruford MW, Dixon A, Zhan X (2021) Climate-driven flyway changes and memory-based long-distance migration. Nature 591:259–264. https://doi.org/10.1038/s41586-021-03265-0
Haddad NM, Brudvig LA, Clobert J, Davies KF, Gonzalez A, Holt RD, Lovejoy TE, Sexton JO, Austin MP, Collins CD, Cook WM, Damschen EI, Ewers RM, Foster BL, Jenkins CN, King AJ, Laurance WF, Levey DJ, Margules CR, Melbourne BA, Nicholls AO, Orrock JL, Song DX, Townshend JR (2015) Habitat fragmentation and its lasting impact on Earth’s ecosystems. Sci Adv 1(2):e1500052. https://doi.org/10.1126/sciadv.1500052
Hansbauer M, Storch I, Pimentel R, Metzger J (2008) Comparative range use by three Atlantic Forest understorey bird species in relation to forest fragmentation. J Trop Ecol 24(3):291–299. https://doi.org/10.1017/S0266467408005002
Hansen R, Olafsson AS, van der Jagt APN, Rall E, Pauleit S (2019) Planning multifunctional green infrastructure for compact cities: What is the state of practice? Ecol Ind 96:99–110
Hargrove WW, Hoffman FM, Efroymson RA (2004) A practical map-analysis tool for detecting potential dispersal corridors. Landscape Ecol 20(4):361–373. https://doi.org/10.1007/s10980-004-3162-y
Haug EA, Oliphant LW (1990) Movements, activity patterns, and habitat use of burrowing owls is Saskatchewan. J Wildl Manag 54(1):27–35
Hijmans RJ (2017) raster: Geographic Data Analysis and Modeling. R package version 2.6–7
Holyoak M, Casagrandi R, Nathan R, Revilla E, Spiegel O (2008) Trends and missing parts in the study of movement ecology. PNAS 105(49):19060–19065. https://doi.org/10.1073/pnas.0800483105
IBGE (2020) Instituto Brasileiro de Geografia e Estatística – IBGE – www.ibge.gov.br. Accessed in April, 2020
Kays R, Crofoot MC, Jetz W, Wikelski M (2015) Terrestrial animal tracking as an eye on life and planet. Science 348(6240):1222–1232. https://doi.org/10.1126/science.aaa2478
Knaapen JP, Scheffer M, Harms B (1992) Estimating habitat isolation in landscape planning. Landsc Urban Plan 23:1–16
Koen EL, Bowman J, Garroway CJ, Mills SC, Wilson PJ (2012a) Landscape resistance and American marten gene flow. Landscape Ecol 27(1):29–43. https://doi.org/10.1007/s10980-011-9675-2
Koen EL, Bowman J, Walpole AA (2012b) The effect of cost surface parameterization on landscape resistance estimates. Mol Ecol Resour 12(4):686–696. https://doi.org/10.1111/j.1755-0998.2012.03123.x
Lincer JL, Clark RJ, Fleming TL, Sieradzki A (2018) A review of burrowing owl (Athene cunicularia) literature using bibliometric comparisons: topical bibliographies and online databases. J Raptor Res 52(2):207–224. https://doi.org/10.3356/JRR-17-04.1
Liu Z, Huang Q, Tang G (2020) Identification of urban flight corridors for migratory birds in the coastal regions of Shenzhen city based on three- dimensional landscapes. Landsc Ecol. https://doi.org/10.1007/s10980-020-01032-6
Luna A, Palma A, Sanz-Aguilar A, Tella JL, Carrete M (2019) Personality-dependent breeding dispersal in rural but not urban burrwoing owls. Sci Rep 9:2886. https://doi.org/10.1038/s41598-019-39251-w
Mclean DJ, Skowron Volponi MA (2018) trajr: an R package for characterisation of animal trajectories. Ethology. https://doi.org/10.1111/eth.12739
McLean DJ (2018) trajr: Animal Trajectory Analysis. R package version 1.0.0. https://CRAN.R-project.org/package=trajr
McRae BH (2006) Isolation by resistance. Evolution 60(8):1551–1561. https://doi.org/10.1554/05-321.1
Mitchell AM, Wellicome TI, Brodie D, Cheng KM (2011) Captive-reared burrowing owls show higher site-affinity, survival, and reproductive performance when reintroduced using a soft-release. Biol Conserv 144(5):1382–1391. https://doi.org/10.1016/j.biocon.2010.12.019
Motta-Junior JC, Braga ACR (2012) Estado del conocimiento sobre la ecología y biología de búhos en Brasil. Ornitol Neotrop 23:227–234
Moulton CE, Brady RS, Belthoff JR (2004) Territory defense of nesting burrowing owls: responses to simulated conspecific intrusion. J Field Ornithol 75(3):288–295. https://doi.org/10.1648/0273-8570(2004)075
Nathan R, Getz WM, Revilla E, Holyoak M, Kadmon R, Saltz D, Smouse PE (2008) A movement ecology paradigm for unifying organismal movement research. PNAS 105(49):19052–19059. https://doi.org/10.1073/pnas.0800375105
Nowakowski AJ, Otero Jiménez B, Allen M, Diaz-Escobar M, Donnelly MA (2013) Landscape resistance to movement of the poison frog, Oophaga pumilio, in the lowlands of northeastern Costa Rica. Anim Conserv 16(2):188–197. https://doi.org/10.1111/j.1469-1795.2012.00585.x
O’Brien D, Manseau M, Fall A, Fortin MJ (2006) Testing the importance of spatial configuration of winter habitat for woodland caribou: an application of graph theory. Biologia Da Conservação I30:70–83. https://doi.org/10.1016/j.biocon.2005.12.014
Olazabal M, Ruiz De Gopegui M (2021) Adaptation planning in large cities is unlikely to be effective. Landsc Urban Plan 206:103974
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(1):32–42. https://doi.org/10.1111/1365-2656.12386
Paradis E, Schliep K (2018) ape 5.0: an environment for modern phylogenetics and evolutionary analyses in R. Bioinformatics
Pinto N, Keitt TH (2009) Beyond the least-cost path: evaluating corridor redundancy using a graph-theoretic approach. Landscape Ecol 24(2):253–266. https://doi.org/10.1007/s10980-008-9303-y
Poulin RG, Todd LD, Haug EA, Millsap BA, Martell MS (2020) Burrowing Owl (Athene cunicularia). In: Birds of the World (Poole AF, Editor). Cornell Lab of Ornithology, Ithaca, NY, USA. https://doi.org/10.2173/bow.burowl.01
Proft KM, Jones ME, Johnson CN, Burridge CP (2018) Making the connection: expanding the role of restoration genetics in restoring and evaluating connectivity. Restor Ecol 26(3):411–418. https://doi.org/10.1111/rec.12692
R Core Team (2018) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Vienna, Austria
Rabosky ARD, Cox CL, Rabosky DL, Title PO, Holmes IA, Feldman A, McGuire JA (2016) Coral snakes predict the evolution of mimicry across New World snakes. Nat Commun 7:11484
Rayfield B, Fortin MJ, Fall A (2010) The sensitivity of least-cost habitat graphs to relative cost surface values. Landscape Ecol 25(4):519–532. https://doi.org/10.1007/s10980-009-9436-7
Rebolo-Ifrán N, Carrete M, Sanz-Aguilar A, Rodriguez-Martinez S, Cabezas S, Marchant TA, Bortolotti GR, Tella JL (2015) Links between fear of humans, stress and survival support a non-random distribution of birds among urban and rural habitats. Sci Rep 5(5):13723. https://doi.org/10.1038/srep13723
Revilla E, Wiegand T, Palomares F, Ferreras P, Revilla E, Delibes M (2004) Effects of heterogeneity on animal dispersal: from individual behavior to metapopulation-level parameters. Am Nat 164(5):130–153
Ribeiro JW, Silveira dos Santos J, Dodonov P, Martello F, Brandão Niebuhr B, Ribeiro MC (2017) LandScape Corridors (lSCorridors): a new software package for modelling ecological corridors based on landscape patterns and species requirements. Methods Ecol Evol 8(11):1425–1432. https://doi.org/10.1111/2041-210X.12750
Ribeiro, JF, Walter, BMT (1998) Fitofisionomias do bioma Cerrado. In Cerrado: ambiente e flora (pp. 89–166). Embrapa Cerrados
Rosenberg DK, Haley KL (2004) The ecology of burrowing owls in the agroecosystem of the Imperial Valley, California. Stud Avian Biol 27(27):120–135
Sawyer SC, Epps CW, Brashares JS (2011) Placing linkages among fragmented habitats: do least-cost models reflect how animals use landscapes? J Appl Ecol 48(3):668–678. https://doi.org/10.1111/j.1365-2664.2011.01970.x
Shimazaki A, Yamaura Y, Senzaki M, Yabuhara Y, Akasaka T, Nakamura F (2016) Urban permeability for birds: an approach combining mobbing-call experiments and circuit theory. Urban for Urban Green 19:167–175. https://doi.org/10.1016/j.ufug.2016.06.024
Sick H (1997) Ornitologia Brasileira. Nova Guanabara, Rio de Janeiro, RJ
Sutcliffe OL, Bakkestuen V, Fry G, Stabbetorp OE (2003) Modelling the benefits of farmland restoration: methodology and application to butterfly movement. Landsc Urban Plan 63:15–31
Thompson PL, Rayfield B, Gonzalez A (2017) Loss of habitat and connectivity erodes species diversity, ecosystem functioning, and stability in metacommunity networks. Ecography 40(1):98–108. https://doi.org/10.1111/ecog.02558
Trénel P, Hansen MM, Normand S, Borchsenius F (2008) Landscape genetics, historical isolation and cross-andean gene flow in the wax palm, Ceroxylon echinulatum (Arecaceae). Mol Ecol 17:3528–3540. https://doi.org/10.1111/j.1365-294X.2008.03853.x
UN (2019) World Population Prospects. Available at https://population.un.org/wpp/Publications/. Accessed in April, 2020
Valdez-Gómez AHE, Holroyd GL, Trefry HE, Contreras-balderas AJ (2018) Home ranges, habitats, and roosts of wintering burrowing owls in agricultural landscapes in Central Mexico. J Raptor Res 52(2):178–190
Verbeylen G, Bruyn L, Adriaensen F, Matthysen E (2003) Does resistance influence Red squirrel (Sciurus vulgaris L. 1758) distribution in an urban landscape? Landscape Ecol 18:791–805
Wang YH, Yang KC, Bridgman CL, Lin LK (2008) Habitat suitability modelling to correlate gene flow with landscape connectivity. Landscape Ecol 23(8):989–1000. https://doi.org/10.1007/s10980-008-9262-3
Ye X, Skidmore AK, Wang T (2014) Joint effects of habitat heterogeneity and species’ life-history traits on population dynamics in spatially structured landscapes. PLoS One 9(9):1–10. https://doi.org/10.1371/journal.pone.0107742
York AM, Shrestha M, Boone CG, Zhang S, Harrington JA, Prebyl TJ, Swann A, Agar M, Antolin MF, Nolen B, Wright JB, Skaggs R (2011) Land fragmentation under rapid urbanization: A cross-site analysis of Southwestern cities. Urban Ecosyst 14(3):429–455. https://doi.org/10.1007/s11252-011-0157-8