Skip to main content
Log in

Transition to density dependence in a reintroduced ecosystem engineer

  • Original Paper
  • Published:
Biodiversity and Conservation Aims and scope Submit manuscript

Abstract

When does a reintroduced population of animals become self-regulating? Quantifying this is critical in determining when interventions can be tapered off, or when they may need to be reinstated. We tracked the growth trajectory of a reintroduced population to establish whether it was irruptive and/or had transitioned to self-regulation. In 2012, we reintroduced 32 eastern bettongs (Bettongia gaimardi), a potoroid marsupial from Tasmania, Australia, to a 485 ha exotic predator-proof fenced reserve in the Australian Capital Territory. We established a 92 cage trap monitoring network to track population growth between the Austral Autumn 2014 and Summer 2018. We used capture-recapture models to track changes in the population through time, and modelled ‘bettong weight’, ‘pouch occupancy’ and ‘age of pouch young’ with population variation, to establish potential associations with changes in population size. The estimated population grew from 32 individuals in 2012 to 100 in 2014, 192 in Autumn 2016, and then declined to 151 in Summer 2018. Estimated survival of adults was high—above 92% between most sessions. Adult female weights ranged between 0.485 and 2.428 kg, and adult males between 0.470 and 2.775 kg. Our study showed density dependence was achieved over the 6 year period. Low adult mortality, and variable pouch occupancy related to female weight, suggested that food availability had influenced lactation in females, with flow-on impacts on juvenile survival. Long-term, broad-scale population dynamics were probably driven by a mix of direct (e.g. disease, harvesting for other reintroductions), and indirect (i.e. climate dependent availability of nutritious food) influences on population size.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • ACT Government (2004) Woodlands for Wildlife: ACT Lowland Woodland Conservation Strategy. Action Plan No. 27. Environment ACT, Canberra

  • Armstrong DP, Davidson RS, Perrott JK, Roygard J, Buchanan L (2005) Density-dependent population growth in a reintroduced population of North Island saddlebacks. J Anim Ecol 74:160–170

    Google Scholar 

  • Bateman A, Chambers B, Pacioni C, Rafferty C, Jones K, Bencini R (2017) Application of underpasses to expand nature reserves: responses of a critically endangered marsupial, the woylie, Bettongia penicillata. Hystrix Ital J Mammal 28:194–201

    Google Scholar 

  • Batson W et al (2016a) Re-introduction of eastern bettong to a critically endangered woodland habitat in the Australian Capital Territory, Australia. Glob Re-introduc Perspect 172

  • Batson WG, Gordon IJ, Fletcher DB, Manning AD (2016b) The effect of pre-release captivity on post-release performance in reintroduced eastern bettongs Bettongia gaimardi. Oryx 50:664–673

    Google Scholar 

  • Batson W, Gordon I, Fletcher D, Portas T, Manning A (2017) The effect of pre-release captivity on the stress physiology of a reintroduced population of wild eastern bettongs. J Zool 303:311–319

    Google Scholar 

  • Belaganahalli MN, Mann S, Mann NS, Nomikou K, Pritchard I, Lunt R, Kirkland PD, Attoui H, Brownlie J, Mertens PPC (2012) Full genome sequencing and genetic characterization of Eubenangee viruses identify Pata virus as a distinct species within the genus Orbivirus. PLoS ONE 7:e31911

    PubMed  PubMed Central  CAS  Google Scholar 

  • Bennett VA, Doerr VAJ, Doerr ED, Manning AD, Lindenmayer DB, Yoon H-J (2013) Habitat selection and behaviour of a reintroduced passerine: linking experimental restoration. Behav Habitat Ecol PLoS ONE 8:e54539. https://doi.org/10.1371/journal.pone.0054539

    Article  CAS  Google Scholar 

  • Bonferroni C (1936) Teoria statistica delle classi e calcolo delle probabilita. Pubblicazioni del R Istituto Superiore di Scienze Economiche e Commericiali di Firenze 8:3–62

    Google Scholar 

  • Botero A et al (2013) Trypanosomes genetic diversity, polyparasitism and the population decline of the critically endangered Australian marsupial, the brush tailed bettong or woylie (Bettongia penicillata). Int J Parasitol 2:77–89. https://doi.org/10.1016/j.ijppaw.2013.03.001

    Article  Google Scholar 

  • Burbidge AA, Woinarski JCZ, Johnson CN (2016) Bettongia gaimardi. The IUCN red list of threatened species 2016: e.T2783A21960911

  • Bureau of Meteorology (2018) Climate Data Online, http://www.bom.gov.au/climate/data/index.shtml. Accessed 7 May 2018

  • Burnham KP, Anderson D (2002) Model selection and multimodel inference: a practical information-theoretic approach. Springer, New York

    Google Scholar 

  • Canty A, Ripley B (2014) boot: bootstrap R (S-Plus) functions, R package version 1.3-10 edn

  • Cockburn A (1989) Sex-ratio variation in marsupials. Aust J Zool 37:467–479

    Google Scholar 

  • Davidson AD, Friggens MT, Shoemaker KT, Hayes CL, Erz J, Duran R (2014) Population dynamics of reintroduced Gunnison’s Prairie dogs in the southern portion of their range. J Wildl Manag 78:429–439. https://doi.org/10.1002/jwmg.681

    Article  Google Scholar 

  • Davison AC, Hinkley DV (1997) Bootstrap methods and their applications. Cambridge University Press, Cambridge

    Google Scholar 

  • Department of Arts Heritage and Environment (2006) EPBC Policy Statement 3.5—White Box—Yellow Box—Blakely’s Red Gum Grassy Woodlands and Derived Native Grasslands listing

  • Fischer J, Lindenmayer DB (2000) An assessment of the published results of animal relocations. Biol Conserv 96:1–11

    Google Scholar 

  • Fisher DO (1999) Offspring sex ratio variation in the bridled nailtail wallaby, Onychogalea fraenata. Behav Ecol Sociobiol 45:411–419

    Google Scholar 

  • Flynn TT (1930) The uterine cycle of pregnancy and pseudo-pregnancy as it is in the diprotodont marsupial Bettongia cuniculus

  • Fox J (2003) Effect displays in R for generalised linear models. J Stat Softw 8:1–27

    Google Scholar 

  • Fox J, Hong J (2009) Effect displays in R for multinomial and proportional-odds logit models: extensions to the effects package. J Stat Softw 32:1–24

    Google Scholar 

  • Gillespie LL (1992) Ginninderra, forerunner to Canberra: a history of the Ginninderra district Campbell, ACT

  • Göran H (1994) Long-term population development of a reintroduced beaver (Castor fiber) population in Sweden. Conserv Biol 8:713–717. https://doi.org/10.1046/j.1523-1739.1994.08030713.x

    Article  Google Scholar 

  • Green B, Merchant J, Newgrain K (1988) Milk consumption and energetics of growth in pouch young of the Tammar Wallaby, Macropus-Eugenii. Aust J Zool 36:217–227

    Google Scholar 

  • IUCN/SSC (2013) Guidelines for reintroductions and other conservation translocations. Version 1.0. IUCN Species Survival Commission, Gland, Switzerland

  • Johnson CN (1994) Distribution of feeding-activity of the Tasmanian bettong (Bettongia gaimardi) in relation to vegetation patterns. Wildl Res 21:249–255

    Google Scholar 

  • Johnson CN, Ritchie EG (2002) Adaptive biases in offspring sex ratios established before birth in a marsupial, the common brushtail possum Trichosurus vulpecula. Behav Ecol 13:653–656

    Google Scholar 

  • Kassambara A (2018) ggpubr: ‘ggplot2’ based publication ready plots. R package version 0.2

  • Kendall WL, Nichols JD (2002) Estimating state-transition probabilities for unobservable states using capture–recapture/resighting data. Ecology 83:3276–3284

    Google Scholar 

  • Kendall WL, Pollock KH, Brownie C (1995) A likelihood-based approach to capture-recapture estimation of demographic parameters under the robust design. Biometrics 51:293–308

    PubMed  CAS  Google Scholar 

  • Kendall WL, Nichols JD, Hines JE (1997) Estimating temporary emigration using capture–recapture data with Pollock’s robust design. Ecology 78:563–578

    Google Scholar 

  • Laake J (2013) RMark: an R interface for analysis of capture–recapture data with MARK. AFSC processed report 2013-01 Alaska Fisheries Science Center, National Marine Fisheries Service, NOAA, Seattle, Washington

  • Le Gall-Payne C, Coulson G, Festa-Bianchet M (2015) Supersize me: heavy eastern grey kangaroo mothers have more sons. Behav Ecol Sociobiol 69:795–804

    Google Scholar 

  • Lenth R (2018) Emmeans: estimated marginal means, aka least-squares means R package version 1

  • Manning AD, Wood JT, Cunningham RB, McIntyre S, Shorthouse DJ, Gordon IJ, Lindenmayer DB (2011) Integrating research and restoration: the establishment of a long-term woodland experiment in south-eastern Australia. Aust Zool 35:633–648

    Google Scholar 

  • Manning AD, Eldridge DJ, Jones CG (2015) Ecosystem engineering for multiple ecosystem benefits: policy implications. In: Armstrong DP, Hayward MW, Moro D, Seddon PJ (eds) Advances in Reintroduction Biology of Australian and New Zealand Fauna. CSIRO

  • Mijangos JL, Pacioni C, Spencer P, Craig MD (2015) Contribution of genetics to ecological restoration. Mol Ecol 24:22–37

    PubMed  Google Scholar 

  • Munro NT, McIntyre S, Macdonald B, Cunningham SA, Gordon IJ, Cunningham RB, Manning AD (2019) Returning a lost process by reintroducing a locally extinct digging marsupial. PeerJ 7:e6622

    PubMed  PubMed Central  Google Scholar 

  • Nicholson AJ, Bailey VA (1935) The balance of animal populations—part I. J Zool 105:551–598

    Google Scholar 

  • Pollock KH (1982) A capture-recapture design robust to unequal probability of capture. J Wildl Manag 46:752–757. https://doi.org/10.2307/3808568

    Article  Google Scholar 

  • Portas T et al (2014) Health evaluation of free-ranging eastern bettongs (bettongia gaimardi) during translocation for reintroduction in australia. J Wildl Dis 50:210–223. https://doi.org/10.7589/2013-08-202

    Article  PubMed  CAS  Google Scholar 

  • Portas TJ et al (2016) Beyond morbidity and mortality in reintroduction programmes: changing health parameters in reintroduced eastern bettongs Bettongia gaimardi. Oryx 50:674–683. https://doi.org/10.1017/S0030605315001283

    Article  Google Scholar 

  • Pradel R (1996) Utilization of capture-mark-recapture for the study of recruitment and population growth rate Biometrics 703–709

  • R Core Team (2017) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  • Ripple WJ, Beschta RL (2012) Trophic cascades in yellowstone: the first 15 years after wolf reintroduction. Biol Conserv 145:205–213. https://doi.org/10.1016/j.biocon.2011.11.005

    Article  Google Scholar 

  • Rose RW (1987) Reproductive-biology of the Tasmanian bettong (Bettongia-Gaimardi, Macropodidae). J Zool 212:59–67

    Google Scholar 

  • Rose R (1989) Age estimation of the tasmanian bettong (Bettongia-Gaimardi) (Marsupialia, Potoroidae). Wildl Res 16:251–261

    Google Scholar 

  • Rose RW, Johnson KA (2008) Tasmanian Bettong Bettongia gaimardi. In: Van Dyck S, Strahan R (eds) The mammals of Australia. Reed New Holland, Sydney, pp 287–288

    Google Scholar 

  • Rose R, Morahan T, Mulchay J, Ratkowsky D (2003) Milk composition and growth in wild and captive Tasmanian bettongs, Bettongia gaimardi (Marsupialia). J Comp Physiol B 173:125–133

    PubMed  CAS  Google Scholar 

  • Rose KA, Kirkland PD, Davis RJ, Cooper DW, Blumstein D, Pritchard LI, Newberry KM, Lunt RA (2012) Epizootics of sudden death in tammar wallabies (Macropus eugenii) associated with an orbivirus infection. Aust Vet J 90:505–509

    PubMed  CAS  Google Scholar 

  • Ross CE, Munro NT, Barton PS, Evans MJ, Gillen J, Macdonald BCT, McIntyre S, Cunningham SA, Manning AD (2019) Effects of digging by a native and introduced ecosystem engineer on soil physical and chemical properties in temperate grassy woodland. PeerJ 7:e7506

    PubMed  PubMed Central  Google Scholar 

  • Short J (1998) The extinction of rat-kangaroos (Marsupialia: Potoroidae) in New South Wales. Aust Biol Conserv 86:365–377

    Google Scholar 

  • Shorthouse DJ et al (2012) The ‘making of’ the Mulligans flat—Goorooyarroo experimental restoration project. Ecol Manag Restor 13:112–125

    Google Scholar 

  • Sibly RM, Hone J (2002) Population growth rate and its determinants: an overview. Philos Trans R Soc Lond B 357:1153–1170

    Google Scholar 

  • Sunnucks P, Taylor AC (1997) Sex of pouch young related to maternal weight in Macropus eugenii and M. parma (Marsupialia: Macropodidae). Aust J Zool 45:573–578

    Google Scholar 

  • Svenning J-C et al (2016) Science for a wilder Anthropocene: synthesis and future directions for trophic rewilding research. Proc Natl Acad Sci USA 113:898–906

    PubMed  CAS  Google Scholar 

  • Taylor RJ (1992) Distribution and abundance of fungal sporocarps and diggings of the Tasmanian bettong, Bettongia gaimardi. Aust J Ecol 17:155–160

    Google Scholar 

  • Trivers RL, Willard DE (1973) Natural selection of parental ability to vary the sex ratio of offspring. Science 179:90–92

    PubMed  CAS  Google Scholar 

  • Tukey JW (1949) Comparing individual means in the analysis of variance. Biometrics 5:99–114

    PubMed  CAS  Google Scholar 

  • Veller C, Haig D, Nowak MA (2016) The Trivers-Willard hypothesis: sex ratio or investment? Proc R Soc B 283:20160126

    PubMed  Google Scholar 

  • Verdon-Kidd DC, Kiem AS (2009) Nature and causes of protracted droughts in southeast Australia: comparison between the Federation, WWII, and big dry droughts. Geophys Res Lett 36:LL22707

    Google Scholar 

  • Vernes K, Pope LC (2006) Capture success and population density of the northern bettong Bettongia tropica in northeastern Queensland. Aust Mammal 28:87–92

    Google Scholar 

  • Wauters LA, Somers L, Dhondt A (1997) Settlement behaviour and population dynamics of reintroduced red squirrels Sciurus vulgaris in a park in Antwerp, Belgium. Biol Conserv 82:101–107. https://doi.org/10.1016/S0006-3207(97)00007-4

    Article  Google Scholar 

  • Wayne AF, Maxwell MA, Ward CG, Vellios CV, Wilson IJ, Dawson KE (2013) Woylie conservation and research project: progress report 2010–2013. Department of Parks and Wildlife, Perth

    Google Scholar 

  • Wayne AF, Maxwell MA, Ward CG, Vellios CV, Wilson I, Wayne JC, Williams MR (2015) Sudden and rapid decline of the abundant marsupial Bettongia penicillata in Australia. Oryx 49:175–185

    Google Scholar 

  • White G (2016) MARK, 6.2nd edn. Department of Fish, Wildlife, and Conservation Biology, Colorado State University, Fort Collins

    Google Scholar 

  • Wickham H (2009) ggplot2: elegant graphics for data analysis. Springer, New York

    Google Scholar 

  • Wood SN (2006) Generalized additive models: an introduction with R. Chapman & Hall/CRC, Boca Raton

    Google Scholar 

  • Zuckerman S (1952) The breeding seasons of mammals in captivity. J Zool 122:827–950

    Google Scholar 

Download references

Acknowledgements

The translocation was carried out under license from the Tasmanian Department of Primary Industries, Parks, Water and Environment (DPIPWE) using procedures approved by their associated Ethics Committee (AEC Project 18/2010–2011). We thank DPIPWE for their support. The post-reintroduction procedures were approved by the Australian National University Animal Experimentation Ethics Committee (ethics protocol A2011/017; A2017/33). WB was supported by a Ph.D. scholarship funded through an Australian Research Council Linkage Grant (LP110100126). ADM was supported by an Australian Research Council Future Fellowship (FT100100358) during part of this study. This project was conducted as part of the Mulligans Flat–Goorooyarroo Woodland Experiment. Thanks to all the staff and volunteers that assisted with the bettong trapping. We also thank Ross Cunningham, David Dobroszczyk, Elyce Fraser, Daniel Iglesias, Stuart Jeffress, Chris Johnson, Margaret Kitchin, Ani Kunz, John Lawler, Peter Mills, Nick Mooney, Matthew Pauza, Andrea Reiss, Scott Ryan, David Shorthouse, Georgeanna Story, Jeff Wood, Grant Woodbridge and Tingbao Xu for their assistance during the project.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Adrian D. Manning.

Ethics declarations

Conflict of interest

We declare that there are no conflict of interest.

Additional information

Communicated by Kirsty Park.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Appendix

Appendix

See Figs. 8, 9, 10 and Tables 1, 2, 3 and 4.

Fig. 8
figure 8

Histograms overlaid with density plots of the distribution of the estimated age of pouch young in each primary survey. Histogram bins are 10 days long. Percentage figures (rounded to 2 significant figures) above the bars represent the percentage of the population of pouch young falling within that age group

Fig. 9
figure 9

Histograms overlaid with density plots of the distribution of the estimated age of pouch young in each primary survey. Histogram bins are 55 days long. Percentage figures (rounded to 2 significant figures) above the bars represent the percentage of the population of pouch young falling within that age group

Fig. 10
figure 10

Bettong weight against time with Tukey honesty test of significance. We applied a Bonferroni correction due to multiple comparisons in the same model (p = 0.05/10 sessions; i.e. p = 0.005). Letters above the upper confidence limits denote significant differences between the estimates in each session

Table 1 Bettong trapping sessions and trapping events in each primary trapping session
Table 2 Pradel robust design capture-recapture model selection table using all data combined, regardless of sex
Table 3 Pradel robust design capture-recapture model selection table using group attributes function to assign two groups to the data (female and male)
Table 4 Survival and recruitment estimates using the Pradel robust design model

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Manning, A.D., Evans, M.J., Banks, S.C. et al. Transition to density dependence in a reintroduced ecosystem engineer. Biodivers Conserv 28, 3803–3830 (2019). https://doi.org/10.1007/s10531-019-01852-2

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10531-019-01852-2

Keywords

Navigation