Conservation Genetics

, Volume 20, Issue 5, pp 1163–1174 | Cite as

Integrating measures of long-distance dispersal into vertebrate conservation planning: scaling relationships and parentage-based dispersal analysis in the koala

  • Janette A. NormanEmail author
  • Stephen S. Phillips
  • Caroline J. Blackmore
  • Ross Goldingay
  • Les Christidis
Research Article


Improved knowledge of dispersal parameters across multiple populations is essential for the effective management of species exposed to ongoing threats from habitat loss, fragmentation and climate change. Currently, management decisions are based on incomplete or insufficient knowledge of key dispersal parameters, especially long-distance dispersal, and its role in maintaining metapopulation connectivity, facilitating range shifts under climate change, or enabling the colonization of new habitats. Using a combination of microsatellite-based population genetic analyses, scaling relationships and parentage-based dispersal analysis we investigated levels and patterns of long-distance dispersal in the koala. Using home range size as a scalar predicted spatial variation in maximum dispersal distance amongst regional populations (range 13.4–43.4 km), while parentage-based dispersal analysis showed that long-distance dispersal (> 11.2 km) accounted for 16.7–18.5% of movements in a focal population. Common movement patterns were discerned, despite varying levels of imprecision and bias, that suggest an important role for long-distance dispersal in maintaining metapopulation connectivity. Our results suggest that implementation of a systematic approach to the estimation of dispersal across multiple populations would benefit koala conservation and management. This will require the use of both empirical and simulation studies to quantify and minimize sources of imprecision and bias that can occur including those related to incomplete sampling, the presence of fine-scale spatial genetic structure and areas of localized inbreeding. As limitations associated with partial sampling are likely to remain an inherent feature of large-scale dispersal studies, a large number of loci should be assayed.


Dispersal Scaling relationships Parentage analysis Metapopulation connectivity Koala 



This study benefited enormously from input provided by members of the Australian Wildlife Genomics Group (L. Neaves, M. Eldridge and R. Johnson), the New South Wales Koala Expert Advisory Committee, C. Moritz and W. Sherwin for which we are grateful. They offered differing perspectives and approaches for the estimation of dispersal parameters from molecular data that led us to consider more carefully the limitations and benefits of parentage-based dispersal analysis and whether it would be feasible to implement a systematic approach to the estimation of dispersal parameters to support conservation management of this vulnerable species. We gratefully acknowledge the assistance provided by L. Vass and volunteers of Friends of the Koala Inc. who undertook opportunistic collection of koala tissue samples and provided access to collection and translocation data for these animals. This study was supported by a Southern Cross University Research Seed Grant 2016 to RG and JAN and funding from New South Wales Roads and Maritime Services to Ecosure Pty Ltd as part of a research consultancy to LC, RG and SP.

Compliance with ethical standards

Human participants and animal consent

Animal capture and sampling procedures were performed under scientific license S12578 issued to SP by the NSW Office of Environment & Heritage, and an Animal Research Authority and associated Animal Care and Ethics Approval issued by the NSW Department of Primary Industries. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. SP is Managing Director of Biolink Ecological Consultants. This does not alter the authors’ adherence to data sharing policies.

Supplementary material

10592_2019_1203_MOESM1_ESM.xlsx (37 kb)
Supplementary material 1 (XLSX 37 kb)
10592_2019_1203_MOESM2_ESM.xlsx (25 kb)
Supplementary material 2 (XLSX 25 kb)
10592_2019_1203_MOESM3_ESM.docx (42 kb)
Supplementary material 3 (DOCX 42 kb)
10592_2019_1203_MOESM4_ESM.docx (19 kb)
Supplementary material 4 (DOCX 18 kb)
10592_2019_1203_MOESM5_ESM.docx (96 kb)
Supplementary material 5 (DOCX 105 kb)
10592_2019_1203_MOESM6_ESM.xlsx (12 kb)
Supplementary material 6 (XLSX 11 kb)
10592_2019_1203_MOESM7_ESM.xlsx (15 kb)
Supplementary material 7 (XLSX 14 kb)


  1. Adams-Hosking C, Grantham HS, Rhodes JR, McAlpine C, Moss PT (2011) Modelling climate-change-induced shifts in the distribution of the koala. Wildl Res 38:122–130CrossRefGoogle Scholar
  2. Anderson AD, Weir BS (2007) A maximum-likelihood method for the estimation of pairwise relatedness in structured populations. Genetics 176(1):421–440CrossRefGoogle Scholar
  3. Arora N, Van Noordwijk MA, Ackermann C, Willems EP, Nater A, Greminger M, Nietlisbach P, Dunkel LP, Utami Atmoko SS, Pamungkas J, Perwitasari-Farajallah D, Van Schaik CP, Krutzen M (2012) Parentage-based pedigree reconstruction reveals female matrilineal clusters and male-biased dispersal in nongregarious Asian great apes, the Bornean orang-utans (Pongo pygmaeus). Mol Ecol 21:3352–3362CrossRefGoogle Scholar
  4. Ashton KG, Tracy MC, de Queiroz A (2000) Is Bergmann’s rule vaid for mammals? Am Nat 156:390–415CrossRefGoogle Scholar
  5. Augustine D (1998) Modelling Chlamydia-koala interactions: coexistence, population dynamics and conservation implications. J Appl Ecol 35:261–272CrossRefGoogle Scholar
  6. Baguette M, Van Dyck H (2007) Landscape connectivity and animal behavior: functional grain as a key determinant for dispersal. Landsc Ecol 22:1117–1129CrossRefGoogle Scholar
  7. Banks SC, Skerratt LF, Taylor AC (2002) Female dispersal and relatedness structure in common wombats (Vombatus ursinus). J Zool 256:389–399CrossRefGoogle Scholar
  8. Baudinette RV (1978) Scaling of heart rate during locomotion in mammals. J Comp Physiol B 127:337–342CrossRefGoogle Scholar
  9. Bode M, Williamson D, Harrison H, Outram N, Jones GP (2017) Estimating dispersal kernels using genetic parentage data. Methods Ecol Evol 00:1–12Google Scholar
  10. Bowler DE, Benton TG (2005) Causes and consequences of animal dispersal strategies: relating individual behaviour to spatial dynamics. Biol Rev 80:205–225CrossRefGoogle Scholar
  11. Bowman J, Jaeger JAG, Fahrig L (2002) Dispersal distance of mammals is proportional to home range size. Ecology 83:2049–2055CrossRefGoogle Scholar
  12. Broquet T, Petit EJ (2009) Molecular estimation of dispersal for ecology and population genetics. Annu Rev Ecol Evol Syst 40:193–216CrossRefGoogle Scholar
  13. Cain ML, Milligan BG, Strand AE (2000) Long-distance seed dispersal in plant populations. Am J Bot 87:1217–1227CrossRefGoogle Scholar
  14. Clobert J, Danchin E, Dhondt AA, Nichols JD (2001) Dispersal. Oxford University Press, OxfordGoogle Scholar
  15. Cotto O, Olivieri I, Ronce O (2013) Optimal life-history schedule in a metapopulation with juvenile dispersal. J Evolut Biol 26:944–954CrossRefGoogle Scholar
  16. Cristescu R, Cahill V, Sherwin WB, Handasyde K, Carlyon K, Whisson D, Herbert CA, Carlsson BLJ, Wilton AN, Cooper DW (2009) Inbreeding and testicular abnormalities in a bottlenecked population of koalas (Phascolarctos cinereus). Wildl Res 36:299–308CrossRefGoogle Scholar
  17. Cristescu R, Ellis W, de Villiers D, Lee K, Woosnam-Merchez O, Frere C, Banks PB, Dique D, Hodgkison S, Carrick H, Carter D, Smith P, Carrick, F (2011) North Stradbroke Island: an island ark for Queensland's koala population? Proc Royal Soc Qld 117:309–334Google Scholar
  18. Davies N, Gramotnev G, Seabrook L, Bradley A, Baxter G, Rhodes J, Lunney D, McAlpine C (2013) Movement patterns of an arboreal marsupial at the edge of its range: a case study of the koala. Mov Ecol 1:8CrossRefGoogle Scholar
  19. Dawson TJ, Needham AD (1981) Cardiovascular characteristics of two resting marsupials: an insight into the cardio-respiratory allometry of marsupials. J Comp Physiol 145:95–100CrossRefGoogle Scholar
  20. Degabriele R, Dawson TJ (1979) Metabolism and heat balance in an arboreal marsupial, the koala (Phascolarctos cinereus). J Comp Physiol B 134:293–301CrossRefGoogle Scholar
  21. Dennison S, Frankham GJ, Neaves LE, Flanagan C, FitzGibbon S, Eldridge MDB, Johnson RN (2017) Population genetics of the koala (Phascolarctos cinereus) in north-eastern New South Wales and south-eastern Queensland. Aust J Zool 64:402–412CrossRefGoogle Scholar
  22. D’Eon R, Serrouya R (2005) Mule deer seasonal movements and multiscale resource selection using global positioning system radiotelemetry. J Mammal 86:736–744CrossRefGoogle Scholar
  23. Dique DS, Thompson J, Preece HJ, de Villiers DL, Carrick FN (2003) Dispersal patterns in a regional koala population in south-east Queensland. Wildl Res 30:281–290CrossRefGoogle Scholar
  24. Dudaniec RY, Rhodes JR, Worthington Wilmer J, Lyons M, Lee KE, McAlpine CA, Carrick FN (2013) Using multilevel models to identify drivers of landscape-genetic structure among management areas. Mol Ecol 22:3752–3765CrossRefGoogle Scholar
  25. Eberhard IH (1972) Ecology of the koala, Phascolarctos cinereus (Goldfuss) on the Flinders Chase. University of Adelaide, Kangaroo IslandGoogle Scholar
  26. Ellis WAH, Bercovitch FB (2011) Body size and sexual selection in the koala. Behav Ecol Sociobiol 65:1229–1235CrossRefGoogle Scholar
  27. Ellis WA, Hale PT, Carrick F (2002) Breeding dynamics of koalas in open woodlands. Wildl Res 29:19–25CrossRefGoogle Scholar
  28. Ellis WAH, Melzer A, Bercovitch FB (2009) Spatiotemporal dynamics of habitat use by koalas: the checkerboard model. Behav Ecol Sociobiology 63(8):1181–1188CrossRefGoogle Scholar
  29. Gall BC (1980) Aspects of the Ecology of the Koala, Phascolarctos cinereus (Goldfuss), in Tucki Tucki Nature Reserve, New South Wales. Wildl Res 7:167–176CrossRefGoogle Scholar
  30. Goldingay R, Dobner B (2014) Home range areas of koalas in an urban area of north-east New South Wales. Aust Mammal 36:74–80CrossRefGoogle Scholar
  31. Gordon G, McGreevy DG, Lawrie BC (1990) Koala population turnover and male social organisation. In: Lee AK, Handasyde KA, Sanson GD (eds) Biology of the koala. Surrey Beatty and Sons, Chipping Norton, pp 189–192Google Scholar
  32. Greenwood PJ, Harvey PH (1982) The natal and breeding dispersal of birds. Annu Rev Ecol Syst 13:1–21CrossRefGoogle Scholar
  33. Harrison HB, Saenz-Agudelo P, Planes S, Jones GP, Berumen ML (2013) Relative accuracy of three common methods of parentage analysis in natural populations. Mol Ecol 22:1158–1170CrossRefGoogle Scholar
  34. Hillman SS, Drewes RC, Hedrick MS, Hancock TV (2014) Physiological vagility and its relationship to dispersal and neutral genetic heterogeneity in vertebrates. J Exp Biol 217:3356–3364CrossRefGoogle Scholar
  35. Houlden BA, England P, Sherwin WB (1996) Paternity exclusion in koalas using hypervariable microsatellites. J Heredity 87:149–152CrossRefGoogle Scholar
  36. Jones AG, Arden WR (2003) Methods of parentage analysis in natural populations. Mol Ecol 12:2511–2523CrossRefGoogle Scholar
  37. Jones AG, Small CM, Paczolt KA, Ratterman NL (2010) A practical guide to methods of parentage analysis. Mol Ecol 10:6–30CrossRefGoogle Scholar
  38. Kalinowski ST, Wagner AP, Taper ML (2006) ml-relate: a computer program for maximum likelihood estimation of relatedness and relationship. Mol Ecol Notes 6:576–579CrossRefGoogle Scholar
  39. Kavanagh RP, Stanton MA, Brassil TE (2007) Koalas continue to occupy their previous home-ranges after selective logging in Callitris-Eucalyptus forest. Wildl Res 34(2):94CrossRefGoogle Scholar
  40. King W, Garant D, Festa-Bianchet M (2015) Mother-offspring distances reflect sex differences in fine-scale genetic structure of eastern grey kangaroos. Ecol Evol 5:2084–2094CrossRefGoogle Scholar
  41. Kjeldsen SR, Zenger KR, Leigh K, Ellis W, Tobey J, Phalen D, Melzer A, FitzGibbon S, Raadsma HW (2016) Genome-wide SNP loci reveal novel insights into koala (Phascolarctos cinereus) population variability across its range. Conserv Genet 17:337–353CrossRefGoogle Scholar
  42. Klein EK, Lavigne C, Gouyon P (2006) Mixing of propagules from discrete sources at long distance: comparing a dispersal tail to an exponential. BMC Ecol 6:3CrossRefGoogle Scholar
  43. Koenig WD, Van Vuren D, Hooge PN (1996) Detectability, philopatry, and the distribution of dispersal distances in vertebrates. Trends Ecol Evol 11:514–517CrossRefGoogle Scholar
  44. Kopps AM, Kang J, Sherwin WB, Palsbøll PJ (2015) How well do molecular and pedigree relatedness correspond in populations with diverse mating systems, and various types and quantities of molecular and demographic data? G3: Genes. Genomes Genet 5:1815–1826Google Scholar
  45. Kormann U, Gugerli F, Ray N, Excoffier L, Bollmann K (2012) Parsimony-based pedigree analysis and individual-based landscape genetics suggest topography to restrict dispersal and connectivity in the endangered capercaillie. Biol Cons 152:241–252CrossRefGoogle Scholar
  46. Lassau S, Ryan B, Close R, Moon C, Geraghty P, Coyle A, Pile J (2008) Home ranges and mortality of a roadside Koala Phascolarctos cinereus population at Bonville, New South Wales. Aust Zool 34:127–136Google Scholar
  47. Lee KE, William E, Carrick F, Corley S, Johnston S, Baverstock PR, Nock C, Rowe K, Seddon J (2013) Anthropogenic changes to the landscape resulted in colonization of koalas in north-east New SouthWales, Australia. Aust Ecol 38:355–363CrossRefGoogle Scholar
  48. Lowe WH (2009) What drives long-distance dispersal? A test of theoretical predictions. Ecology 90:1456–1462CrossRefGoogle Scholar
  49. Matthews A, Lunney D, Gresser S, Waitz M (2016) Movement patterns of koalas in remnant forest after fire. Aust Mammal 38:91–104CrossRefGoogle Scholar
  50. McAlpine C, Lunney D, Melzer A, Menkhorst P, Phillips S, Phalen D, Ellis W, Foley W, Baxter G, de Villier D, Kavanagh R, Adams-Hosking C, Todd C, Whisson D, Molsher R, Walter M, Lawler I, Close R (2015) Conserving koalas: a review of the contrasting regional trends, outlooks and policy challenges. Biol Cons 192:226–236CrossRefGoogle Scholar
  51. Melero Y, Oliver MK, Lambin X (2017) Relationship type affects the reliability of dispersal distance estimated using pedigree inferences in partially sampled populations: a case study involving invasive American mink in Scotland. Mol Ecol 26:4059–4071CrossRefGoogle Scholar
  52. Melzer A (1995) Aspects of the ecology of the koala, Phascolarctos cinereus (Goldfuss, 1817), in the sub-humid woodlands of central Queensland. PhD Thesis, School of Biological Sciences, The University of QueenslandGoogle Scholar
  53. Melzer A, Ellis W, Gordon G, Tucker G, Kindness R, Carrick F (2011) Unusual patterns of tooth wear among koalas Phascolarctos cinereus from St Bees Island, Queensland, require re-evaluation of criteria for aging koalas by tooth-wear class. Aust Zool 35:550–554CrossRefGoogle Scholar
  54. Milligan BG (2003) Maximum-likelihood estimation of relatedness. Genetics 163:1153–1167Google Scholar
  55. Moore JA, Draheim HM, Etter D, Winterstein S, Scribner KT (2014) Application of large-scale parentage analysis for investigating natal dispersal in highly vagile vertebrates: a case study of american black bears (Ursus americanus). PLoS ONE 9:e91168CrossRefGoogle Scholar
  56. Nathan R (2001) The challenges of studying dispersal. Trends Ecol Evol 16:481–483CrossRefGoogle Scholar
  57. Nathan R (2005) Long-distance dispersal research: building a network of yellow brick roads. Divers Distrib 11:125–130CrossRefGoogle Scholar
  58. Nathan R, Perry G, Cronin JT, Strand AE, Cain ML (2003) Methods for estimating long-distance dispersal. Oikos 103(2):261–273CrossRefGoogle Scholar
  59. Nathan R, Klein E, Robledo-Anuncio JJ, Revilla E (2012) Dispersal kernels: review. In: Clobert J, Baguette M, Benton TG, Bullock JM (eds) Dispersal ecology and evolution. Oxford University Press, Oxford, pp 186–210CrossRefGoogle Scholar
  60. NSWNPWS (2002) Tuckean Nature Reserve Plan of Management. New South Wales National Parks and Wildlife Service, Sydney, p 16Google Scholar
  61. Paradis E, Baillie SR, Sutherland WJ, Gregory RD (1998) Patterns of natal and breeding dispersal in birds. J Anim Ecol 67:518–536CrossRefGoogle Scholar
  62. Parkes T, Delaney M, Dunphy M, Woodford R, Bower H, Bower S, Bailey D, Joseph R, Nagle J, Roberts T, Lymburner S (2012) Big Scrub: a cleared landscape in transition back to forest? In: McDonald T, editor. Ecological Society of Australia, Ecological Management and Restoration. pp 212–223Google Scholar
  63. Peakall R, Smouse PE (2006) GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295CrossRefGoogle Scholar
  64. Peakall R, Smouse PE (2012) GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research-an update. Bioinformatics 28:2537–2539CrossRefGoogle Scholar
  65. Phillips SS (2000) Population trends and the koala conservation debate. Conserv Biol 14:650–659CrossRefGoogle Scholar
  66. Phillips S, Chang M (2013) Koala habitat and population assessment: Ballina Shire Council LGA. Final Report to Ballina Shire Council. Biolink Ecological Consultants, UkiGoogle Scholar
  67. Pulliam HR (1988) Sources, sinks, and population regulation. Am Nat 132:652–661CrossRefGoogle Scholar
  68. Ramsay S (1999) The ecology and dispersal patterns of juvenile koalas, Phascolarctos cinereus, in fragmented habitat. Ph.D. Thesis, University of SydneyGoogle Scholar
  69. Robinson AC (1978) The Koala in South Australia. In: The Koala. Proceedings of the Taronga Symposium on Koala Biology, Management and Medicine. Bergin TJ, editor. Zoological Parks Board of New South Wales, Sydney. pp 132–143Google Scholar
  70. Ruiz-Rodriguez CT, Ishida Y, Greenwood AD, Roca AL (2014) Development of 14 microsatellite markers in the Queensland koala (Phascolarctos cinereus adustus) using next generation sequencing technology. Conserv Genet Resour 6:429–431CrossRefGoogle Scholar
  71. Santini L, Di Marco M, Visconti P, Baisero D, Boitani L, Rondinini C (2013) Ecological correlates of dispersal distance in terrestrial mammals. Hystrix Italian J Mammal 24:181–186Google Scholar
  72. Smith AG, McAlpine CA, Rhodes JR, Lunney D, Seabrook L, Baxter G (2013) Out on a limb: habitat use of a specialist folivore, the koala, at the edge of its range in a modified semi-arid landscape. Landscape Ecol 28:415–426CrossRefGoogle Scholar
  73. Spong G, Creel S (2001) Deriving dispersal distances from genetic data. Proc R Soc Lond Ser B Biol Sci 268:2571–2574CrossRefGoogle Scholar
  74. Sutherland GD, Harestad AS, Price K, Lertzman KP (2000) Scaling of natal dispersal distances in terrestrial birds and mammals. Conserv Ecol 16Google Scholar
  75. Telfer S, Piertney SB, Dallas JF, Stewart WA, Marshall F, Gow JL, Lambin X (2003) Parentage assignment detects frequent and large-scale dispersal in water voles. Mol Ecol 12:1939–1949CrossRefGoogle Scholar
  76. Thompson J (2006) The comparative ecology and population dynamics of koalas in the Koala Coast region of south-east Queensland. Ph.D. Thesis, University of Queensland, BrisbaneGoogle Scholar
  77. Trakhtenbrot A, Nathan R, Perry G, Richardson DM (2005) The importance of long-distance dispersal in biodiversity conservation. Divers Distrib 11:173–181CrossRefGoogle Scholar
  78. Truvé J, Lemel J (2003) Timing and distance of natal dispersal for wild boar Sus scrofa in Sweden. Wildl Biol 9:51–57CrossRefGoogle Scholar
  79. van Beest FM, Rivrud IM, Loe LE, Milner JM, Mysterud A (2011) What determines variation in home range size across spatiotemporal scales in a large browsing herbivore? Anim Ecol 80:771–785CrossRefGoogle Scholar
  80. Walton Z, Samelius G, Odden M, Willebrand T (2003) Long-distance dispersal in red foxes Vulpes vulpes revealed by GPS tracking. Eur J Wildl Res 64:64CrossRefGoogle Scholar
  81. West GB, Brown JH (2004) Life’s universal scaling laws. Phys Today 57:36–42CrossRefGoogle Scholar
  82. Whisson DA, Holland GJ, Carlyon K (2012) Translocation of overabundant species: implications for translocated individuals. J Wildl Manag 76:1661–1669CrossRefGoogle Scholar
  83. White NA (1999) Ecology of the koala (Phascolarctos cinereus) in rural south-east Queensland. Australia. Wildl Res 26(6):731CrossRefGoogle Scholar
  84. Whitmee S, Orme CDL (2013) Predicting dispersal distance in mammals: a trait-based approach. J Anim Ecol 82:211–221CrossRefGoogle Scholar
  85. Wikelski M, Kays WR, Kasdin NJ, Thorup K, Smith JA, Swenson GWJ (2007) Going wild: what a global small-animal tracking system could do for experimental biologists. J Exp Biol 210:181–186CrossRefGoogle Scholar
  86. Yang D, Song Y, Ma J, Li P, Zhang H, Price MRS, Li C, Jiang Z (2016) Stepping-stones and dispersal flow: establishment of a meta-population of Milu (Elaphurus davidianus) through natural re-wilding. Sci Rep 6:27297CrossRefGoogle Scholar
  87. Yom-Tov Y, Nix H (1986) Climatological correlates for body size of five species of Australian mammals. Biol J Lin Soc 29:245–262CrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  1. 1.National Marine Science Centre, Southern Cross UniversityCoffs HarbourAustralia
  2. 2.School of Graduate StudiesSouthern Cross UniversityEast LismoreAustralia
  3. 3.Biolink Ecological ConsultantsUkiAustralia
  4. 4.School of Environment, Science and EngineeringSouthern Cross UniversityEast LismoreAustralia
  5. 5.School of BiosciencesUniversity of MelbourneParkvilleAustralia

Personalised recommendations