Abstract
Invasive non-native deer can cause negative impacts at ecosystem, community and population levels. Here we aim to determine which characteristics predict success at two stages of the invasion process, establishment and spread, in introduced deer. We collected historical data on the outcomes of introduction events and compiled a dataset of species traits. Characteristics correlated to the success of invasion were identified using linear modelling methods, which control for the non-independence of the introduction events. A phylogenetic tree of the deer was reconstructed using DNA markers in order to control for the effects of common ancestry in species level analyses. At the species level, we found weaning age, age at sexual maturity and native range size are predictive of establishment, whereas weaning body mass is predictive of spread. At the population level we found that establishment success is primarily determined by the number of introduced individuals whereas breadth of habitat and diet determine which of the established populations will spread.
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References
Acevedo P, Ward AI, Real R, Smith GC (2010) Assessing biogeographical relationships of ecologically related species using favourability functions: a case study on British deer. Divers Distrib 16:515–528
Allendorf FW (2003) Introduction: population biology, evolution, and control of invasive species. Conserv Biol 17:24–30
Ball MC, Pither R, Manseau M, Clark J, Petersen SD, Kingston S, Morrill N, Wilson P (2007) Characterization of target nuclear DNA from faeces reduces technical issues associated with the assumptions of low-quality and quantity template. Conserv Genet 8:577–586
Beck B, Walkup K, Rodrigues M, Unwin S, Travis D, Stoinski T (2007) Best practice guidelines for re-introduction of great apes. SSC Primate Specialist Group of the World Conservation Union
Blackburn TM, Duncan RP (2001) Determinants of establishment success in introduced birds. Nature 414:195–197
Bolker BM, Brooks ME, Clark CJ, Geange SW, Poulsen JR, Stevens MHH, White JSS (2009) Generalized linear mixed models: a practical guide for ecology and evolution. Trends Ecol Evol 24:127–135
Bomford M, Darbyshire RO, Randall L (2009) Determinants of establishment success for introduced exotic mammals. Wildl Res 36:192–202
Boyle AE (1996) The Rio convention on biological diversity. In: Bowman M, Redgwell C (eds) International law and the conservation of biological diversity. Kluwer Law International, London, pp 33–49
Chadwick AH, Ratcliffe PR, Abernethy K (1996) Sika deer in Scotland: density, population size, habitat use and fertility—some comparisons with red deer. Scott For 50:8–16
Chapman NG, Claydon K, Claydon M, Forde PG, Harris S (1993) Sympatric populations of muntjac (Muntiacus reevesi) and roe deer (Capreolus capreolus)—a comparative analysis of their ranging behavior, social organization and activity. J Zool 229:623–640
Chapman N, Harris S, Stanford A (1994) Reeves’ Muntjac (Muntiacus reevesi) in Britain: their history, spread, habitat selection, and the role of human intervention in accelerating their dispersal. Mamm Rev 24:113–160
Clout MN, Russell JC (2008) The invasion ecology of mammals: a global perspective. Wildl Res 35:180–184
Cooke A, Farrell L (1998) Chinese water deer. Mammal Society and British Deer Society, London
Cooke AS, Farrell L (2001) Impact of muntjac deer (Muntiacus reevesi) at Monks Wood National Nature Reserve, Cambridgeshire, Eastern England. Forestry 74:241–250
Cooke AS, Lakhani KH (1996) Damage to coppice regrowth by muntjac deer (Muntiacus reevesi) and protecting with electric fencing. Biol Conserv 75:231–238
Cote SD, Rooney TP, Tremblay JP, Dussault C, Waller DM (2004) Ecological impacts of deer overabundance. Ann Rev Ecol Evol Syst 35:113–147
Courchamp F, Chapuis JL, Pascal M (2003) Mammal invaders on islands: impact, control and control impact. Biol Rev 78:347–383
Danilkin A (1996) Behavioural ecology of Siberian and European roe deer. Wildlife ecology and behaviour series, vol 2. Chapman and Hall, London
DEFRA (2004) The sustainable management of wild deer populations in England: an action plan. DEFRA and Foresty Commission, England
Dolman PM, Waber K (2008) Ecosystem and competition impacts of introduced deer. Wildl Res 35:202–214
Duncan RP (2001) High predictability in introduction outcomes and the geographical range size of introduced Australian birds: a role for climate. J Anim Ecol 70:621–623
Ehrlich P (1989) Attributes of invaders and the invading process: vertebrates. Biological invasions: a global perspective. Wiley, New York
Elton CS (1958) The ecology of invasions by animals and plants. University Chicago Press, Chicago
Feldhamer G, Armstrong W (1993) Interspecific competition between four exotic species and native artiodactyls in the United States. In: Transactions of the North American wildlife and natural resources conference, vol 58, pp 468–478
Feldhamer GA, Demarais S (2009) Free ranging and confined sika deer in North America: current status, biology and management. In: McCullough DR, Takatsuki S, Kaji K (eds) Sika deer biology and management of native and introduced populations. Springer, New York, pp 615–642
Forde PG (1989) Comparative ecology of Muntiacus reevesi and roe deer Capreolus capreolus in a commercial coniferous forest. Ph.D. thesis, University of Bristol
Forsyth DM, Duncan RP (2001) Propagule size and the relative success of exotic ungulate and bird introductions to New Zealand. Am Nat 157:583–595
Forsyth DM, Coomes DA, Nugent G, Hall GMJ (2002) Diet and diet preferences of introduced ungulates (Order: Artiodactyla) in New Zealand. NZ J Zool 29:323–343
Forsyth DM, Duncan RP, Bomford M, Moore G (2004) Climatic suitability, life-history traits, introduction effort, and the establishment and spread of introduced mammals in Australia. Conserv Biol 18:557–569
Forsyth DM, Wilmshurst JM, Allen RB, Coomes DA (2010) Impacts of introduced deer and extinct moa on New Zealand ecosystems. NZ J Ecol 34:48–65
Fuller RJ, Gill RMA (2001) Ecological impacts of increasing numbers of deer in British woodland. Forestry 74:193–199
Gilbert C, Ropiquet A, Hassanin A (2006) Mitochondrial and nuclear phylogenies of Cervidae (Mammalia, Ruminantia): systematics, morphology, and biogeography. Mol Phylogen Evol 40:101–117
Gill RMA (1992) A review of damage by mammals in north temperate forests: 1. Deer. Forestry 65:145–169
Gill RMA, Morgan G (2010) The effects of varying deer density on natural regeneration in woodlands in lowland Britain. Forestry 83:53–63
Goodman SJ, Barton NH, Swanson G, Abernethy K, Pemberton JM (1999) Introgression through rare hybridization: a genetic study of a hybrid zone between red and sika deer (genus Cervus) in Argyll, Scotland. Genetics 152:355–371
Hassanin A, Pasquet E, Vigne JD (1998) Molecular systematics of the subfamily Caprinae (Artiodactyla, Bovidae) as determined from cytochrome b sequences. J Mammal Evol 5:217–236
Hemami MR, Watkinson AR, Dolman PM (2004) Habitat selection by sympatric muntjac (Muntiacus reevesi) and roe deer (Capreolus capreolus) in a lowland commercial pine forest. For Ecol Manag 194:49–60
Hemami MR, Watkinson AR, Dolman PM (2005) Population densities and habitat associations of introduced muntjac (Muntiacus reevesi) and native roe deer (Capreolus capreolus) in a lowland pine forest. For Ecol Manag 215:224–238
Hulme PE (2006) Beyond control: wider implications for the management of biological invasions. J Appl Ecol 43:835–847
Jaksic FM, Iriarte JA, Jiménez JE, Martínez DR (2002) Invaders without frontiers: cross-border invasions of exotic mammals. Biol Invasions 4:157–173
Jeschke JM (2008) Across islands and continents, mammals are more successful invaders than birds. Divers Distrib 14:913–916
Jeschke JM, Strayer DL (2006) Determinants of vertebrate invasion success in Europe and North America. Glob Chang Biol 12:1608–1619
Katoh K, Misawa K, Kuma K, Miyata T (2002) MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res 30:3059–3066
Katoh K, Kuma K, Toh H, Miyata T (2005) MAFFT version 5: improvement in accuracy of multiple sequence alignment. Nucleic Acids Res 33:511–518
Keiper RR (1985) Are sika deer responsible for the decline of white-tailed deer on Assateague Island, Maryland? Wildl Soc Bull 13:144–146
Kolar CS, Lodge DM (2001) Progress in invasion biology: predicting invaders. Trends Ecol Evol 16:199–204
Lande R (1993) Risks of population extinction from demographic and environmental stochasticity and random catastrophes. Am Nat 142:911–927
Lever C (1985) Naturalized mammals of the world. Longman, Essex
Lockwood JL, Cassey P, Blackburn T (2005) The role of propagule pressure in explaining species invasions. Trends Ecol Evol 20:223–228
Long JL (2003) Introduced mammals of the world. CSIRO, Victoria
Lowe VPW, Gardiner AS (1975) Hybridization between red deer (Cervus elaphus) and sika deer (Cervus nippon) with particular reference to stocks in NW England. J Zool 177:553–566
Maddison DR, Maddison WP (2001) MacClade 4: analysis of phylogeny and character evolution, 4.02nd edn. Sinauer Associates, Sunderland
Moriarty A (2004) The liberation, distribution, abundance and management of wild deer in Australia. Wildl Res 31:291–299
Nunez MA, Bailey JK, Schweitzer JA (2010) Population, community and ecosystem effects of exotic herbivores: a growing global concern. Biol Invasions 12:297–301
Nylander JAA (2004) MrModeltest v2. Program distributed by the author. Evolutionary Biology Centre, Uppsala University, Sweden
Paradis E, Claude J (2002) Analysis of comparative data using generalized estimating equations. J Theor Biol 218:175–185
Paradis E, Claude J, Strimmer K (2004) APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20:289–290
Pimentel D (2001) Economic and environmental threats of alien plant, animal, and microbe invasions. Agric Ecosyst Environ 84:1–20
Pitra C, Fickel J, Meijaard E, Groves PC (2004) Evolution and phylogeny of old world deer. Mol Phylogen Evol 33:880–895
Pocock RI (1910) On the specialized cutaneous glands of ruminants. Proc Zool Soc 80:840–845
Pollard E, Cooke AS (1994) Impact of muntjac deer (Muntiacus reevesi) on egg-laying sites of the white admiral butterfly (Ladoga camilla) in a Cambridgeshire wood. Biol Conserv 70:189–191
Putman RJ, Moore NP (1998) Impact of deer in lowland Britain on agriculture, forestry and conservation habitats. Mamm Rev 28:141–163
R Development Core Team (2008) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna
Randi E, Mucci N, Pierpaoli M, Douzery E (1998) New phylogenetic perspectives on the Cervidae (Artiodactyla) are provided by the mitochondrial cytochrome b gene. Proc R Soc B 265:793–801
Randi E, Mucci N, Claro-Hergueta F, Bonnet A, Douzery E (2001) A mitochondrial DNA control region phylogeny of the Cervinae: speciation in Cervus and implications for conservation. Anim Conserv 4:1–11
Ratcliffe PR (1987) Distribution and current status of sika deer (Cervus nippon) in Great Britain. Mamm Rev 17:39–58
Reed DH, Frankham R (2003) Correlation between fitness and genetic diversity. Conserv Biol 17:230–237
Rejmanek M, Richardson DM (1996) What attributes make some plant species more invasive? Ecology 77:1655–1661
Relva MA, Nunez MA, Simberloff D (2010) Introduced deer reduce native plant cover and facilitate invasion of non-native tree species: evidence for invasional meltdown. Biol Invasions 12:303–311
Rodriguez-Cabal MA, Barrios-Garcia MN, Simberloff D (2009) Across islands and continents, mammals are more successful invaders than birds (reply). Divers Distrib 15:911–912
Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574
Senn HV, Pemberton JM (2009) Variable extent of hybridization between invasive sika (Cervus nippon) and native red deer (C. elaphus) in a small geographical area. Mol Ecol 18:862–876
Simberloff D (1996) Hybridization between native and introduced wildlife species: importance for conservation. Wildl Biol 33:143–150
Sol D, Duncan RP, Blackburn TM, Cassey P, Lefebvre L (2005) Big brains, enhanced cognition, and response of birds to novel environments. PNAS 102:5460–5465
Sol D, Bacher S, Reader SM, Lefebvre L (2008a) Brain size predicts the success of mammal species introduced into novel environments. In: Symposium of the American Society of Naturalists, Christchurch, New Zealand, pp S63–S71
Sol D, Vila M, Kuhn I (2008b) The comparative analysis of historical alien introductions. Biol Invasions 10:1119–1129
Theodorou K, Couvet D (2006) On the expected relationship between inbreeding, fitness, and extinction. Genet Sel Evol 38:371–387
Walker B, Steffen W (1997) An overview of the implications of global change for natural and managed terrestrial ecosystems. Conserv Ecol 1. http://www.consecol.org/vol1/iss2/art2
Ward AI (2005) Expanding ranges of wild and feral deer in Great Britain. Mamm Rev 35:165–178
White PCL, Ford AES, Clout MN, Engeman RM, Roy S, Saunders G (2008) Alien invasive vertebrates in ecosystems: pattern, process and the social dimension. Wildl Res 35:171–179
Acknowledgments
We thank Rory Putman for his valuable suggestions and comments on the manuscript. Sven Bacher generously provided access to the mammal introduction database, and Simon Reader kindly shared the data on brain masses. We thank William Pearse for his advice on coding in R. Edinburgh and Chester Zoos provided samples for the phylogenetic analysis. Finally, we would like to thank three anonymous reviewers whose comments greatly improved the paper. This study was funded by the Biotechnology and Biological Sciences Research Council, the British Deer Society, the Royal Society and the European Research Council.
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Fautley, R., Coulson, T. & Savolainen, V. A comparative analysis of the factors promoting deer invasion. Biol Invasions 14, 2271–2281 (2012). https://doi.org/10.1007/s10530-012-0228-7
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DOI: https://doi.org/10.1007/s10530-012-0228-7