Abstract
Dispersal is a critical biological process that contributes to the persistence of species in complex and dynamic landscapes. However, little is known about the ability of different types of data to reveal how species interact with landscape patterns during dispersal. Further, application of process-based, landscape-scale models able to capture the influence of land use and climate change are limited by this lack of dispersal knowledge. Here we highlight a method for building such models when dispersal parameters are unknown, but information on the mating system and survival are available. We applied a common statistical framework, rooted in information theory, to contrast the ability of abundance, movement, and genetic data to estimate dispersal parameters for endangered Red-cockaded woodpecker (RCW), using an individual-based, spatially-explicit population model. Dispersal was modeled as a multifaceted process in which foray distance, long-distance dispersal, competition for mates, and landscape permeability were treated as uncertain. We found that movement data are three-times more powerful than abundance data collected at the same spatial and temporal scales. However, habitat occupancy data collected over much a shorter time scale but at regional spatial scales were very effective for estimating dispersal. We also found that one-year of abundance data provided a similar reduction in uncertainty as genetic differences among breeding groups estimated using a 24-year pedigree. Substituting population genetic data for movement and abundance data often led to the same parameter values, but not always. Our study highlights important differences in the information content of data commonly collected in the field.



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References
Anderson C, Epperson BK, Fortin MJ, Holderegger R, James P, Rosenberg MS, Scribner K, Spear S (2010) Considering spatial and temporal scale in landscape-genetic studies of gene flow. Mol Ecol 19:3565–3575
Balkenhol N, Gugerli F, Cushman SA, Waits LP, Coulon A, Arntzen JW, Holderegger R, Wagner HH (2009) Identifying future research needs in landscape genetics: where to from here? Landscape Ecol 24:455–463
Bruggeman DJ, Wiegand T, Fernandez N (2010) The relative effects of habitat loss and fragmentation on population genetic structure of the Red-cockaded Woodpecker (Picoides borealis). Mol Ecol 19:3679–3691
Clobert J, Danchin E, Dhondt AA, Nichols JD (eds) (2001) Dispersal. Oxford University Press, USA
Cooper CB, Daniels SJ, Walters JR (2008) Can we improve estimates of juvenile dispersal and survival. Ecology 89:3349–3361
Csillery K, Blum MGB, Gaggiotti OE, Francois O (2010) Approximate Bayesian computation (ABC) in practice. Trends Ecol Evol 25:410–418
Cushman SA, Landguth EL (2010) Spurious correlations and inference in landscape genetics. Mol Ecol 19:3592–3602
Cushman SA, Lewis JS (2010) Movement behavior explains genetic differentiation in American black bears. Landscape Ecol 25:1613–1625
Cushman SA, McKelvey KS, Hayden J, Schwartz MK (2006) Gene flow in complex landscapes: testing multiple hypotheses with causal modeling. Am Nat 168:486–499
Epperson BK (2004) Multilocus estimation of genetic structure within populations. Theor Popul Biol 65:227–237
Epperson BK, Mcrae BH, Scribner K, Cushman SA, Rosenberg MS, Fortin M-J, James PMA, Murphy M, Manel S, Legendre P, Dale MRT (2010) Utility of computer simulations in landscape genetics. Mol Ecol 19:3549–3564
Fike JA, Athrey G, Bowman R, Leberg PL, Rhodes OE (2009) Development of twenty-five polymorphic microsatellite markers for the endangered red-cockaded woodpecker (Picoides borealis). Conserv Gen 10:1021–1023
Finnegan LA, Wilson PJ, Price GN, Lowe SJ, Patterson BR, Fortin M-J, Murray DL (2011) the complimentary role of genetic and ecological data in understanding population structure: a case study using moose (Alces alces). Eur J Wildl Res 58:415–423
Grimm V, Revilla E, Berger U, Jeltsch F, Mooij WM, Railsback SF, Thuke HH, Weiner J, Wiegand T, DeAngelis DL (2005) Pattern-oriented modeling of agent-based complex systems: lessons from ecology. Science 310:987–991
Grimm V, Berger U, DeAngelis DL, Polhill JG, Giske J, Railsback SF (2010) The ODD protocol: a review and first update. Ecol Mod 221:2760–2768
Hartig F, Calabrese JM, Reineking B, Wiegand T, Huth A (2011) Statistical inference for stochastic simulation models—theory and application. Ecol Lett 14:816–827
Hutchison DW, Templeton AR (1999) Correlation of pairwise genetic and geographic distance measures: inferring the relative influences of gene flow and drift on the distribution of genetic variability. Evolution 53:1898–1914
Jaquiéry J, Broquet T, Hirzel AH, Yearsley J, Perrin N (2011) Inferring landscape effects on dispersal from genetic distances: how far can we go? Mol Ecol 20:692–705
Kesler DC, Walters JR, Kappes JJ (2010) Social influences on dispersal and the fat-tailed dispersal distribution in red-cockaded woodpeckers. Behav Ecol 21:1337–1343
Keyghobadi N (2007) The genetic implications of habitat fragmentation for animals. Can J Zool 85:1049–1064
Landguth EL, Cushman SA, Schwartz MK, McKelvey KS, Murphy M, Luikart G (2010) Quantifying the lag time to detect barriers in landscape genetics. Mol Ecol 19:4179–4191
Landguth EL, Fedy BC, Oyler-McCance S, Garey AL, Emel SL, Mumma M, Wagner HH, Fortin MJ, Cushman SA (2012) Effects of sample size, number of markers, and allelic richness on the detection of spatial genetic pattern. Mol Ecol Res 12:276–284
Letcher BH, Priddy JA, Walters JR, Crowder LB (1998) An individual-based, spatially-explicit simulation model of the population dynamics of the endangered red-cockaded woodpecker, Picoides borealis. Biol Conserv 86:1–14
Lloyd MW, Campbell L, Neel MC (2013) The power to detect recent fragmentation events using genetic differentiation methods. PLoS ONE 8(5):e63981
Lowe WH, Allendorf FW (2010) What can genetics tell us about population connectivity? Mol Ecol 19:3038–3051
Martınez I, Wiegand T, Camarero JJ, Batllori E, Gutiérrez E (2011) Disentangling the formation of contrasting tree-line physiognomies combining model selection and Bayesian parameterization for simulation models. Am Nat 177:E136–E152
McRae BH (2006) Isolation by resistance. Evolution 60(8):1551–1561
Nathan R, Perry G, Cronin JT, Strand AE, Cain ML (2003) Methods for estimating long-distance dispersal. Oikos 103:261–273
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 USA 105:19052–19059
Nei M (1973) Analysis of gene diversity in subdivided populations. Proc Natl Acad Sci USA 70:3321–3323
Nei M (1986) Definition and estimation of fixation indices. Evolution 40:643–645
Palmer M, Swan C, Nelson K, Silver P, Alvestad R (2000) Streambed landscapes: evidence that stream invertebrates respond to the type and spatial arrangement of patches. Landscape Ecol 15:563–576
Reding DM, Cushman SA, Gosselink TE, Clark WR (2013) Linking movement behavior and fine-scale genetic structure to model landscape connectivity for bobcats (Lynx rufus). Landscape Ecol 28:471–486
Revilla E, Wiegand T, Palomares F, Ferreras P, Delibes M (2004) Effects of matrix heterogeneity on animal dispersal: from individual behavior to metapopulation-level parameters. Am Nat 164:E130–E153
Rosenberg MS, Anderson CD (2008) PASSaGE: pattern analysis, spatial statistics and geographic exegesis. Version 2. Methods Ecol Evol 2:229–232
Rousset F (1997) Genetic differentiation and estimation of gene flow from F-statistics under isolation by distance. Genetics 145:1219–1228
Scribner KT, Blanchong JA, Bruggeman DJ, Epperson BK, Lee C-Y, Pan Y-W, Shorey RI, Prince HH, Winterstein SR, Luukkonen DR (2005) Geographical genetics: conceptual foundations and empirical applications of spatial genetic data in wildlife management. J Wildl Manage 69:1434–1453
Sork VL, Waits L (2010) Contributions of landscape genetics—approaches, insights, and future potential. Mol Ecol 19:3489–3495
Spear SF, Balkenhol N, Fortin MJ, McRae BH, Scribner K (2010) Use of resistance surfaces for landscape genetic studies: considerations for parameterization and analysis. Mol Ecol 19:3576–3591
Walters JR, Doerr PD, Carter JH III (1988) The cooperative breeding system of the red-cockaded woodpecker. Ethology 78:275–305
Watts PC, Rousset F, Saccheri IJ, Leblois R, Kemp SJ, Thompson DJ (2007) Compatible genetic and ecological estimates of dispersal rates in insect (Coenagrion mercurial: Odonata: Zygoptera) populations: analysis of ‘neighbourhood size’ using a more precise estimator. Mol Ecol 16:737–751
Whitlock MC, McCauley DE (1999) Indirect measures of gene flow and migration: FST ≠ 1/(4NM + 1). Heredity 82:117–125
Wiegand T, Jeltsch F, Hanski I, Grimm V (2003) Using pattern-oriented modeling for revealing hidden information: a key for reconciling ecological theory and application. Oikos 100:209–222
Wiegand T, Revilla E, Knauer F (2004) Dealing with uncertainty in spatially explicit population models. Biodivers Conserv 13:53–78
Wood SN (2010) Statistical inference for noisy nonlinear ecological dynamic systems. Nature 466:1102–1104
Wright S (1951) The genetical structure of populations. Ann Eugen 15:323–354
Acknowledgments
We are indebted to Marine Corps Base Camp Lejeune (W. Rogers, C. Ten Brink, G. Haught, and S. Cohen), Croatan National Forest (R. Powell, L. Thornhill, and G. Kauffman), Holly Shelter State Game Lands (T. Hughes, K Shugart, and D. Allen), and Steve Simon for help with data. We also thank K. Convery for collecting field data at Holly Shelter and I. Martinez for discussions and help with code. We thank four anonymous reviewers who contributed greatly to the presentation of this work. This research was supported by SERDP RC-1656. T. W. was supported by the ERC advanced grant 233066.
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Bruggeman, D.J., Wiegand, T., Walters, J.R. et al. Contrasting the ability of data to make inferences regarding dispersal: case study of the Red-cockaded woodpecker (Picoides borealis). Landscape Ecol 29, 639–653 (2014). https://doi.org/10.1007/s10980-014-0011-5
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DOI: https://doi.org/10.1007/s10980-014-0011-5


