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Ecology, management and conservation in natural and modified habitats
RESEARCH ARTICLE (Open Access)

Decline in semi-arid reptile occurrence following habitat loss and fragmentation

R. E. L. Simpson https://orcid.org/0009-0001-7815-7695 A B * , D. G. Nimmo A B , L. J. Wright A B , S. Wassens A B and D. R. Michael https://orcid.org/0000-0003-3980-9723 B
+ Author Affiliations
- Author Affiliations

A School for Agricultural, Environmental and Veterinary Sciences, Charles Sturt University, Wagga Wagga, NSW 2650, Australia.

B Gulbali Institute for Agriculture, Water and Environment, Charles Sturt University, Albury, NSW 2640, Australia.

* Correspondence to: bec.simpson@yahoo.com

Handling Editor: Janet Gardner

Wildlife Research 51, WR23034 https://doi.org/10.1071/WR23034
Submitted: 19 March 2023  Accepted: 6 July 2023  Published: 24 July 2023

© 2024 The Author(s) (or their employer(s)). Published by CSIRO Publishing. This is an open access article distributed under the Creative Commons Attribution 4.0 International License (CC BY)

Abstract

Context

Habitat loss and fragmentation are leading causes of biodiversity decline worldwide. In Australia, woodland habitat has been extensively cleared and fragmented yet there has been limited research on the effects of habitat loss and fragmentation on semi-arid reptiles, impeding conservation planning and recovery efforts.

Aims

We aimed to investigate factors influencing the distribution and occurrence of habitat specialist and generalist reptile species on a large agricultural holding in south-eastern Australia that has experienced habitat loss and fragmentation.

Methods

Reptiles were surveyed using pitfall and funnel traps and active searches across 20 sites stratified by land use and vegetation type. Twelve sites were established in remnant woodland patches embedded within an agricultural matrix and eight sites were established in a private conservation reserve on the same property. Generalised linear models were used to explore relationships between the occurrence of eight reptile species and predictor variables describing site, landscape and vegetation variables.

Key results

Of the 31 reptile species that were detected, eight were modelled. The results revealed that four specialist species, the eastern mallee dragon (Ctenophorus spinodomus), nobbi dragon (Diporiphora nobbi), barred wedge-snouted ctenotus (Ctenotus schomburgkii) and shrubland pale-flecked morethia (Morethia obscura), were closely associated with the conservation reserve, and that the southern spinifex ctenotus (Ctenotus atlas) had a strong association with spinifex (Triodia scariosa) dominated vegetation community.

Conclusions

Reptile habitat specialists are particularly sensitive to habitat loss and fragmentation and are at a higher risk of local extinction compared with habitat generalists. Reptile occurrence was reduced in remnant woodland patches, but remnant patches also supported a suite of habitat generalists.

Implications

A suite of semi-arid reptile species are sensitive to the effects of habitat loss and fragmentation and are susceptible to localised extinction. However, the presence of habitat generalists within woodland remnants highlights the value of retaining representative habitat patches in agricultural landscapes. Conservation of semi-arid woodland reptiles will depend on the retention of large tracts of protected vegetation across a broad range of soil types to maintain habitat heterogeneity and reptile diversity.

Keywords: agricultural intensification, generalist, habitat fragmentation, habitat relationships, landscape modification, mallee, reptile occurrence, semi-arid woodland, specialist.

References

Atlas of Living Australia (ALA) (2023) Atlas of Living Australia. Available at https://www.ala.org.au/ [Accessed 15 February 2023]

Baumgardt JA, Morrison ML, Brennan LA, Thornley M, Campbell TA (2021) Variation in herpetofauna detection probabilities: implications for study design. Environmental Monitoring and Assessment 193, 658.
| Crossref | Google Scholar | PubMed |

Bell KJ, Doherty TS, Driscoll DA (2021a) Predators, prey or temperature? Mechanisms driving niche use of a foundation plant species by specialist lizards. Proceedings of the Royal Society B: Biological Sciences 288, 20202633.
| Crossref | Google Scholar |

Bell K, Driscoll DA, Patykowski J, Doherty TS (2021b) Abundance, condition and size of a foundation species vary with altered soil conditions, remnant type and potential competitors. Ecosystems 24, 1516-1530.
| Crossref | Google Scholar |

BOM (2022) Climate statistics for Australian locations. Available at http://www.bom.gov.au/ [Accessed 9 June 2022]

Burnham KP, Anderson DR (2002) ‘Model selection and multimodel inference: a practical information-theoretic approach.’ 2nd edn. (Springer: New York, USA)

Clarke MF, Kelly LT, Avitabile SC, Benshemesh J, Callister KE, Driscoll DA, Ewin P, Giljohann K, Haslem A, Kenny SA, Leonard S, Ritchie EG, Nimmo DG, Schedvin N, Schneider K, Watson SJ, Westbrooke M, White M, Wouters MA, Bennett AF (2021) Fire and its interactions with other drivers shape a distinctive, semi-arid ‘mallee’ ecosystem. Frontiers in Ecology and Evolution 9, 647557.
| Crossref | Google Scholar |

Cox N, Young BE, Bowles P, Fernandez M, Marin J, Rapacciuolo G, Böhm M, Brooks TM, Hedges SB, Hilton-Taylor C, Hoffmann M, Jenkins RKB, Tognelli MF, Alexander GJ, Allison A, Ananjeva NB, Auliya M, Avila LJ, Chapple DG, Cisneros-Heredia DF, Cogger HG, Colli GR, de Silva A, Eisemberg CC, Els J, Fong G. A, Grant TD, Hitchmough RA, Iskandar DT, Kidera N, Martins M, Meiri S, Mitchell NJ, Molur S, Nogueira CdC, Ortiz JC, Penner J, Rhodin AGJ, Rivas GA, Rödel M-O, Roll U, Sanders KL, Santos-Barrera G, Shea GM, Spawls S, Stuart BL, Tolley KA, Trape J-F, Vidal MA, Wagner P, Wallace BP, Xie Y (2022) A global reptile assessment highlights shared conservation needs of tetrapods. Nature 605, 285-290.
| Crossref | Google Scholar |

Devictor V, Julliard R, Jiguet F (2008) Distribution of specialist and generalist species along spatial gradients of habitat disturbance and fragmentation. Oikos 117, 507-514.
| Crossref | Google Scholar |

Doherty TS, Balouch S, Bell K, Burns TJ, Feldman A, Fist C, Garvey TF, Jessop TS, Meiri S, Driscoll DA (2020) Reptile responses to anthropogenic habitat modification: a global meta-analysis. Global Ecology and Biogeography 29, 1265-1279.
| Crossref | Google Scholar |

Driscoll DA (2004) Extinction and outbreaks accompany fragmentation of a reptile community. Ecological Applications 14, 220-240.
| Crossref | Google Scholar |

Driscoll DA, Hardy CM (2005) Dispersal and phylogeography of the agamid lizard Amphibolurus nobbi in fragmented and continuous habitat. Molecular Ecology 14, 1613-1629.
| Crossref | Google Scholar | PubMed |

Driscoll DA, Banks SC, Barton PS, Lindenmayer DB, Smith AL (2013) Conceptual domain of the matrix in fragmented landscapes. Trends in Ecology & Evolution 28, 605-613.
| Crossref | Google Scholar | PubMed |

Dundas SJ, Ruthrof KX, Hardy GESJ, Fleming PA (2021) Some like it hot: drought-induced forest die-off influences reptile assemblages. Acta Oecologica 111, 103714.
| Crossref | Google Scholar |

Fahrig L (2003) Effects of habitat fragmentation on biodiversity. Annual Review of Ecology, Evolution, and Systematics 34, 487-515.
| Crossref | Google Scholar |

Fischer J, Fazey I, Briese R, Lindenmayer DB (2005) Making the matrix matter: challenges in Australian grazing landscapes. Biodiversity & Conservation 14, 561-578.
| Crossref | Google Scholar |

Fiske I, Chandler R (2011) unmarked: an R package for fitting hierarchical models of wildlife occurrence and abundance. Journal of Statistical Software 43, 1-23.
| Crossref | Google Scholar |

Franklin JF, Lindenmayer DB (2009) Importance of matrix habitats in maintaining biological diversity. Proceedings of the National Academy of Sciences of the United States of America 106, 349-350.
| Crossref | Google Scholar |

Garnett ST, Hayward-Brown BK, Kopf RK, Woinarski JCZ, Cameron KA, Chapple DG, Copley P, Fisher A, Gillespie G, Latch P, Legge S, Lintermans M, Moorrees A, Page M, Renwick J, Birrell J, Kelly D, Geyle HM (2022) Australia’s most imperilled vertebrates. Biological Conservation 270, 109561.
| Crossref | Google Scholar |

Gibbs JP (2001) Demography versus habitat fragmentation as determinants of genetic variation in wild populations. Biological Conservation 100, 15-20.
| Crossref | Google Scholar |

Greer A (2022) Encyclopedia of Australian reptiles. Version 1, April 2022. Available at https://www.researchgate.net [Accessed 21 July 2022]

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 D-X, Townshend JR (2015) Habitat fragmentation and its lasting impact on Earth’s ecosystems. Science Advances 1, e1500052.
| Crossref | Google Scholar | PubMed |

Hansen NA, Sato CF, Michael DR, Lindenmayer DB, Driscoll DA (2019) Predation risk for reptiles is highest at remnant edges in agricultural landscapes. Journal of Applied Ecology 56, 31-43.
| Crossref | Google Scholar |

Hansen NA, Driscoll DA, Michael DR, Lindenmayer DB (2020) Movement patterns of an arboreal gecko in fragmented agricultural landscapes reveal matrix avoidance. Animal Conservation 23, 48-59.
| Crossref | Google Scholar |

Hartig F (2022) DHARMa: residual diagnostics for hierarchical (multi-level/mixed) regression models. R package version 0.4.6. Available at https://CRAN.R-project.org/package=DHARMa

Henle K (1989) Ecological segregation in a subterranean reptile assemblage in arid Australia. Amphibia-Reptilia 10, 277-295.
| Crossref | Google Scholar |

IUCN (2022) The IUCN red list of threatened species. Available at https://www.iucnredlist.org [Accessed 28 June 2022]

Jellinek S, Parris KM, McCarthy MA, Wintle BA, Driscoll DA (2014) Reptiles in restored agricultural landscapes: the value of linear strips, patches and habitat condition. Animal Conservation 17, 544-554.
| Crossref | Google Scholar |

Jules ES, Shahani P (2003) A broader ecological context to habitat fragmentation: why matrix habitat is more important than we thought. Journal of Vegetation Science 14, 459-464.
| Crossref | Google Scholar |

Kay GM, Driscoll DA, Lindenmayer DB, Pulsford SA, Mortelliti A (2016) Pasture height and crop direction influence reptile movement in an agricultural matrix. Agriculture, Ecosystems & Environment 235, 164-171.
| Crossref | Google Scholar |

Keinath DA, Doak DF, Hodges KE, Prugh LR, Fagan W, Sekercioglu CH, Buchart SHM, Kauffman M (2017) A global analysis of traits predicting species sensitivity to habitat fragmentation. Global Ecology and Biogeography 26, 115-127.
| Crossref | Google Scholar |

Kéry M (2002) Inferring the absence of a species: a case study of snakes. The Journal of Wildlife Management 66, 330-338.
| Crossref | Google Scholar |

Kosmidis I (2021) brglm: bias reduction in binomial-rsponse generalized linear models. R package version 0.7.2. Available at https://CRAN.R-project.org/package=brglm

Levy E, Kennington JW, Tomkins JL, Lebas NR (2010) Land clearing reduces gene flow in the granite outcrop-dwelling lizard, Ctenophorus ornatus. Molecular Ecology 19, 4192-4203.
| Crossref | Google Scholar | PubMed |

Lüdecke D (2018) ggeffects: tidy data frames of marginal effects from regression models. Journal of Open Source Software 3, 772.
| Crossref | Google Scholar |

MacKenzie DI, Nichols JD, Lachman GB, Droege S, Andrew Royle J, Langtimm CA (2002) Estimating site occupancy rates when detection probabilities are less than one. Ecology 83, 2248-2255.
| Crossref | Google Scholar |

MacKenzie DI, Nichols JD, Seamans ME, Gutiérrez RJ (2009) Modeling species occurrence dynamics with multiple states and imperfect detection. Ecology 90, 823-835.
| Crossref | Google Scholar | PubMed |

Matthews TJ, Cottee-Jones HE, Whittaker RJ (2014) Habitat fragmentation and the species–area relationship: a focus on total species richness obscures the impact of habitat loss on habitat specialists. Diversity and Distributions 20, 1136-1146.
| Crossref | Google Scholar |

Maxwell SL, Fuller RA, Brooks TM, Watson JEM (2016) Biodiversity: the ravages of guns, nets and bulldozers. Nature 536, 143-145.
| Crossref | Google Scholar | PubMed |

Mazerolle MJ (2020) AICcmodavg: model selection and multimodel inference based on (Q)AIC(c) (version 2.3.1). Available at https://cran.r-project.org/package=AICcmodavg [Accessed 27 June 2022]

Meiri S, Chapple DG (2016) Biases in the current knowledge of threat status in lizards, and bridging the ‘assessment gap’. Biological Conservation 204, 6-15.
| Crossref | Google Scholar |

Menkhorst PW, Bennett AF (1990) Vertebrate fauna of mallee vegetation in southern Australia. In ‘The mallee lands: a conservation perspective: proceedings of the National Mallee Conference, Adelaide, April, 1989’. (Eds JC Noble, PJ Joss, GK Jones) pp. 39–53. (CSIRO Publishing: East Melbourne, Victoria)

Michael DR, Cunningham RB, Lindenmayer DB (2008) A forgotten habitat? Granite inselbergs conserve reptile diversity in fragmented agricultural landscapes. Journal of Applied Ecology 45, 1742-1752.
| Crossref | Google Scholar |

Michael DR, Kay GM, Crane M, Florance D, MacGregor C, Okada S, McBurney L, Blair D, Lindenmayer DB (2015) Ecological niche breadth and microhabitat guild structure in temperate Australian reptiles: implications for natural resource management in endangered grassy woodland ecosystems. Austral Ecology 40, 651-660.
| Crossref | Google Scholar |

Michael DR, Wood JT, O’Loughlin T, Lindenmayer DB (2016) Influence of land sharing and land sparing strategies on patterns of vegetation and terrestrial vertebrate richness and occurrence in Australian endangered eucalypt woodlands. Agriculture, Ecosystems & Environment 227, 24-32.
| Crossref | Google Scholar |

Mulhall SJ, Sitters H, Di Stefano J (2022) Vegetation cover and configuration drive reptile species distributions in a fragmented landscape. Wildlife Research
| Crossref | Google Scholar |

Munguia-Vega A, Rodriguez-Estrella R, Shaw WW, Culver M (2013) Localized extinction of an arboreal desert lizard caused by habitat fragmentation. Biological Conservation 157, 11-20.
| Crossref | Google Scholar |

Neilly H, Ward M, Cale P (2021) Converting rangelands to reserves: small mammal and reptile responses 24 years after domestic livestock grazing removal. Austral Ecology 46, 1112-1124.
| Crossref | Google Scholar |

Nimmo DG, Kelly LT, Spence-Bailey LM, Watson SJ, Haslem A, White JG, Clarke MF, Bennett AF (2012) Predicting the century-long post-fire responses of reptiles. Global Ecology and Biogeography 21, 1062-1073.
| Crossref | Google Scholar |

Nimmo DG, Kelly LT, Spence-Bailey LM, Watson SJ, Taylor RS, Clarke MF, Bennett AF (2013) Fire mosaics and reptile conservation in a fire-prone region. Conservation Biology 27, 345-353.
| Crossref | Google Scholar | PubMed |

Nimmo DG, Kelly LT, Farnsworth LM, Watson SJ, Bennett AF (2014) Why do some species have geographically varying responses to fire history? Ecography 37, 805-813.
| Crossref | Google Scholar |

OEH (2022) Vegetation Keith class NSW Office of Environment and Heritage. Available at https://www.environment.nsw.gov.au [Accessed 25 July 2022]

Pulsford SA, Lindenmayer DB, Driscoll DA (2017) Reptiles and frogs conform to multiple conceptual landscape models in an agricultural landscape. Diversity and Distributions 23, 1408-1422.
| Crossref | Google Scholar |

R Core Team (2022) R Studio: integrated development environment for R. Available at http://www.rstudio.com/ [Accessed 18 July 2022]

Ricketts TH (2001) The matrix matters: effective isolation in fragmented landscapes. The American Naturalist 158, 87-99.
| Crossref | Google Scholar | PubMed |

Sadlier RA, Colgan DJ, Beatson CA, Cogger HG (2019) Ctenophorus spinodomus sp. nov., a new species of dragon lizard (Squamata: Agamidae) from Triodia Mallee habitat of southeast Australia. Records of the Australian Museum 71, 199-215.
| Crossref | Google Scholar |

Sass S (2006) The reptile fauna of Nombinnie Nature Reserve and State Conservation Area, western New South Wales. Australian Zoologist 33, 511-518.
| Crossref | Google Scholar |

Slatyer C, Rosauer D, Lemckert F (2007) An assessment of endemism and species richness patterns in the Australian Anura. Journal of Biogeography 34, 583-596.
| Crossref | Google Scholar |

Smith AL, Gardner MG, Bull CM, Driscoll DA (2011) Primers for novel microsatellite markers in “fire-specialist” lizards (Amphibolurus norrisi, Ctenotus atlas and Nephrurus stellatus) and their performance across multiple populations. Conservation Genetics Resources 3, 345-350.
| Crossref | Google Scholar |

Tan WC, Herrel A, Rödder D (2023) A global analysis of habitat fragmentation research in reptiles and amphibians: what have we done so far? Biodiversity and Conservation 32, 439-468.
| Crossref | Google Scholar |

Thompson GG, Thompson SA (2007) Usefulness of funnel traps in catching small reptiles and mammals, with comments on the effectiveness of the alternatives. Wildlife Research 34, 491-497.
| Crossref | Google Scholar |

Thompson ME, Nowakowski AJ, Donnelly MA (2016) The importance of defining focal assemblages when evaluating amphibian and reptile responses to land use. Conservation Biology 30, 249-258.
| Crossref | Google Scholar | PubMed |

Tingley R, Meiri S, Chapple DG (2016) Addressing knowledge gaps in reptile conservation. Biological Conservation 204, 1-5.
| Crossref | Google Scholar |

Tingley R, Macdonald SL, Mitchell NJ, Woinarski JCZ, Meiri S, Bowles P, Cox NA, Shea GM, Böhm M, Chanson J, Tognelli MF, Harris J, Walke C, Harrison N, Victor S, Woods C, Amey AP, Bamford M, Catt G, Clemann N, Couper PJ, Cogger H, Cowan M, Craig MD, Dickman CR, Doughty P, Ellis R, Fenner A, Ford S, Gaikhorst G, Gillespie GR, Greenlees MJ, Hobson R, Hoskin CJ, How R, Hutchinson MN, Lloyd R, McDonald P, Melville J, Michael DR, Moritz C, Oliver PM, Peterson G, Robertson P, Sanderson C, Somaweera R, Teale R, Valentine L, Vanderduys E, Venz M, Wapstra E, Wilson S, Chapple DG (2019) Geographic and taxonomic patterns of extinction risk in Australian squamates. Biological Conservation 238, 108203.
| Crossref | Google Scholar |

Triska MD, Craig MD, Stokes VL, Pech RP, Hobbs RJ (2016) The relative influence of in situ and neighborhood factors on reptile recolonization in post-mining restoration sites. Restoration Ecology 24, 517-527.
| Crossref | Google Scholar |

Triska MD, Craig MD, Stokes VL, Pech RP, Hobbs RJ (2017) Conserving reptiles within a multiple-use landscape: determining habitat affiliations of reptile communities in the northern jarrah forest of south-western Australia. Australian Journal of Zoology 65, 21.
| Crossref | Google Scholar |

Uetz P, Freed P, Aguilar R, Hošek J (2022) The reptile database. Available at http://www.reptile-database.org [Accessed 11 August 2022]

Verdon SJ, Watson SJ, Nimmo DG, Clarke MF (2020) Are all fauna associated with the same structural features of the foundation species Triodia scariosa? Austral Ecology 45, 773-787.
| Crossref | Google Scholar |

Watson DM, Watson MJ (2015) Wildlife restoration: mainstreaming translocations to keep common species common. Biological Conservation 191, 830-838.
| Crossref | Google Scholar |

Wickham H (2016) ‘ggplot2: elegant graphics for data analysis.’ 2nd edn. (Springer: New York, USA)

Wilson S, Swan G (2021) ‘A complete guide to reptiles of Australia.’ 6th edn. (Reed New Holland: Sydney, NSW, Australia)

Yan Y, Jarvie S, Liu Q, Zhang Q (2022) Effects of fragmentation on grassland plant diversity depend on the habitat specialization of species. Biological Conservation 275, 109773.
| Crossref | Google Scholar |

Youngentob KN, Wood JT, Lindenmayer DB (2013) The response of arboreal marsupials to landscape context over time: a large-scale fragmentation study revisited. Journal of Biogeography 40, 2082-2093.
| Crossref | Google Scholar |