Habitat loss and degradation reduce the abundance of the glossy grass skink, Pseudemoia rawlinsoni

Jules E. Farquhar; Lucy Wotherspoon; Hilary Porter; David G. Chapple

doi:10.1071/WR23102

RESEARCH ARTICLE (Open Access)

Next Contents Vol 51(3)

Habitat loss and degradation reduce the abundance of the glossy grass skink, Pseudemoia rawlinsoni

Jules E. Farquhar

^A ^# ^* , Lucy Wotherspoon ^A ^# , Hilary Porter ^A ^# and David G. Chapple

^A

+ Author Affiliations

- Author Affiliations

^A School of Biological Sciences, Monash University, Clayton, Vic., Australia. Email: lucy.wotherspoon@gmail.com, hilarykporter@gmail.com, david.chapple@monash.edu

^* Correspondence to: jules.farquhar@monash.edu

^# These authors contributed equally to this paper

Handling Editor: Adam Stow

Wildlife Research 51, WR23102 https://doi.org/10.1071/WR23102

Submitted: 14 August 2023 Accepted: 23 February 2024 Published: 15 March 2024

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

Abstract

Context

Habitat loss and degradation are major drivers of biodiversity loss worldwide. In particular, wetland environments are being removed and degraded faster than any other terrestrial habitat on earth. The loss and degradation of wetlands has been particularly pronounced in south-eastern Australia.

Aims

Here we investigated the impact of habitat loss and degradation on the Data Deficient glossy grass skink (Pseudemoia rawlinsoni), a species that predominantly favours wetland vegetation in south-eastern Australia.

Methods

We established artificial cover-object (roofing tiles) survey grids in paired remnant and disturbed sites at six locations across Victoria, Australia, and surveyed for skinks between November 2021 and April 2022.

Key results

Sites at which glossy grass skinks occur are characterised by tall dense vegetation, with a high cover of matted biomass. Thermal profiles within these complex vegetation structures remain much cooler during hot days, and warmer during cold nights, than external temperatures. Nearby disturbed sites (i.e. grazed or mowed areas within dispersal distance of remnant sites) are generally devoid of skinks, have very low and structurally simple (open) vegetation, and have thermal regimes that offer lizards no respite from high summer temperatures. We found that roofing tiles are an effective way to survey for glossy grass skinks; even on cool cloudy days, the temperature of tiles, and the lizards sheltering beneath them, are often much higher than ambient temperatures.

Conclusions

These findings implicate habitat loss and degradation as having a substantial negative impact on glossy grass skink presence and abundance; skinks largely avoid disturbed areas, even at sites immediately adjacent to remnant habitat. This may be driven not simply by the removal of tall and dense vegetation structures, but the consequent loss of the optimal thermal buffer afforded by such structures.

Implications

Our study emphasises the threat that habitat loss and degradation pose to wetland species in Australia, and throughout the world.

Keywords: agriculture, artificial cover object, Data Deficient, habitat loss, lizard, reptile, thermal biology, threatened, vegetation structure, wetland.

References

Abom R, Vogler W, Schwarzkopf L (2015) Mechanisms of the impact of a weed (grader grass, Themeda quadrivalvis) on reptile assemblage structure in a tropical savannah. Biological Conservation 191, 75-82.
| Crossref | Google Scholar |

Ackley JW, Wu J, Angilletta MJ, Jr., Myint SW, Sullivan B (2015) Rich lizards: how affluence and land cover influence the diversity and abundance of desert reptiles persisting in an urban landscape. Biological Conservation 182, 87-92.
| Crossref | Google Scholar |

Andersson M, Krockenberger A, Schwarzkopf L (2010) Experimental manipulation reveals the importance of refuge habitat temperature selected by lizards. Austral Ecology 35, 294-299.
| Crossref | Google Scholar |

Bates D, Mächler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. Journal of Statistical Software 67, 1-48.
| Crossref | Google Scholar |

Bell KJ, Doherty TS, Driscoll DA (2021) 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 |

Boon PI, Allen T, Carr G, Frood D, Harty C, McMahon A, Mathews S, Rosengren N, Sinclair S, White M, Yugovic J (2015) Coastal wetlands of Victoria, south-eastern Australia: providing the inventory and condition information needed for their effective management and conservation. Aquatic Conservation: Marine and Freshwater Ecosystems 25, 454-479.
| Crossref | Google Scholar |

Bradshaw CJA (2012) Little left to lose: deforestation and forest degradation in Australia since European colonization. Journal of Plant Ecology 5, 109-120.
| Crossref | Google Scholar |

Böhm M, Collen B, Baillie JEM, et al. (2013) The conservation status of the world’s reptiles. Biological Conservation 157, 372-385.
| Crossref | Google Scholar |

Caetano GHdO, Chapple DG, Grenyer R, Raz T, Rosenblatt J, Tingley R, Böhm M, Meiri S, Roll U (2022) Automated assessment reveals that the extinction risk of reptiles is widely underestimated across space and phylogeny. PLoS Biology 20, e3001544.
| Crossref | Google Scholar |

Ceballos G, Ehrlich PR, Barnosky AD, García A, Pringle RM, Palmer TM (2015) Accelerated modern human–induced species losses: entering the sixth mass extinction. Science Advances 1, e1400253.
| Crossref | Google Scholar | PubMed |

Ceballos G, Ehrlich PR, Dirzo R (2017) Biological annihilation via the ongoing sixth mass extinction signaled by vertebrate population losses and declines. Proceedings of the National Academy of Sciences of the United States of America 114, E6089-E6096.
| Crossref | Google Scholar | PubMed |

Ceballos G, Ehrlich PR, Raven PH (2020) Vertebrates on the brink as indicators of biological annihilation and the sixth mass extinction. Proceedings of the National Academy of Sciences of the United States of America 117, 13596-13602.
| Crossref | Google Scholar | PubMed |

Chapple DG, Roll U, Böhm M, Aguilar R, Amey AP, Austin CC, Baling M, Barley AJ, Bates MF, Bauer AM, Blackburn DG, Bowles P, Brown RM, Chandramouli SR, Chirio L, Cogger H, Colli GR, Conradie W, Couper PJ, Cowan MA, Craig MD, Das I, Datta-Roy A, Dickman CR, Ellis RJ, Fenner AL, Ford S, Ganesh SR, Gardner MG, Geissler P, Gillespie GR, Glaw F, Greenlees MJ, Griffith OW, Grismer LL, Haines ML, Harris DJ, Hedges SB, Hitchmough RA, Hoskin CJ, Hutchinson MN, Ineich I, Janssen J, Johnston GR, Karin BR, Keogh JS, Kraus F, LeBreton M, Lymberakis P, Masroor R, McDonald PJ, Mecke S, Melville J, Melzer S, Michael DR, Miralles A, Mitchell NJ, Nelson NJ, Nguyen TQ, de Campos Nogueira C, Ota H, Pafilis P, Pauwels OSG, Perera A, Pincheira-Donoso D, Reed RN, Ribeiro-Júnior MA, Riley JL, Rocha S, Rutherford PL, Sadlier RA, Shacham B, Shea GM, Shine R, Slavenko A, Stow A, Sumner J, Tallowin OJS, Teale R, Torres-Carvajal O, Trape J-F, Uetz P, Ukuwela KDB, Valentine L, Van Dyke JU, van Winkel D, Vasconcelos R, Vences M, Wagner P, Wapstra E, While GM, Whiting MJ, Whittington CM, Wilson S, Ziegler T, Tingley R, Meiri S (2021) Conservation status of the world’s skinks (Scincidae): taxonomic and geographic patterns in extinction risk. Biological Conservation 257, 109101.
| Crossref | Google Scholar |

Clemann N (2015) Cold-blooded indifference: a case study of the worsening status of threatened reptiles from Victoria, Australia. Pacific Conservation Biology 21, 15-26.
| Crossref | Google Scholar |

Cornelis J, von Takach B, Cooper CE, Vos J, Bateman PW, Lettoof DC (2023) Quantifying the impacts of an invasive weed on habitat quality and prey availability for tiger snakes (Notechis scutatus) in urban wetlands. Wetlands Ecology and Management 31, 715-732.
| Crossref | Google Scholar |

Davis MA, Chew MK, Hobbs RJ, Lugo AE, Ewel JJ, Vermeij GJ, Brown JH, Rosenzweig ML, Gardener MR, Carroll SP, Thompson K, Pickett STA, Stromberg JC, Tredici PD, Suding KN, Ehrenfeld JG, Philip Grime J, Mascaro J, Briggs JC (2011) Don’t judge species on their origins. Nature 474, 153-154.
| Crossref | Google Scholar | PubMed |

Department of Environment, Land, Water and Planning (2022) Flora and Fauna Quarantee Act 1988 – threatened list. September 2022. The State of Victoria Department of Environment, Land, Water and Planning. Available at https://www.environment.vic.gov.au/__data/assets/pdf_file/0031/536089/FFG-Threatened-List-September-2022.pdf [accessed 13 March 2023]

Dirzo R, Young HS, Galetti M, Ceballos G, Isaac NJB, Collen B (2014) Defaunation in the Anthropocene. Science 345, 401-406.
| Crossref | Google Scholar | PubMed |

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 |

Dorrough J, Ash JE (1999) Using past and present habitat to predict the current distribution and abundance of a rare cryptic lizard, Delma impar (Pygopodidae). Australian Journal of Ecology 24, 614-624.
| Crossref | Google Scholar |

Dubey S, Shine R (2010) Restricted dispersal and genetic diversity in populations of an endangered montane lizard (Eulamprus leuraensis, Scincidae). Molecular Ecology 19, 886-897.
| Crossref | Google Scholar | PubMed |

Enge KM (2001) The pitfalls of pitfall traps. Journal of Herpetology 35, 467-478.
| Crossref | Google Scholar |

Farquhar JE, Carlesso A, Pili A, Gale N, Chapple DG (2023) Capturing uncatalogued distribution records to improve conservation assessments of data-deficient species: a case study using the glossy grass skink. Animal Conservation 27, 124-137.
| Crossref | Google Scholar |

Garcia RA, Clusella-Trullas S (2019) Thermal landscape change as a driver of ectotherm responses to plant invasions. Proceedings of the Royal Society B: Biological Sciences 286, 20191020.
| Crossref | Google Scholar |

Garden JG, Mcalpine CA, Possingham HP, Jones DN (2007) Habitat structure is more important than vegetation composition for local-level management of native terrestrial reptile and small mammal species living in urban remnants: a case study from Brisbane, Australia. Austral Ecology 32, 669-685.
| Crossref | Google Scholar | PubMed |

Geyle HM, Tingley R, Amey AP, Cogger H, Couper PJ, Cowan M, Craig MD, Doughty P, Driscoll DA, Ellis RJ, Emery J-P, Fenner A, Gardner MG, Garnett ST, Gillespie GR, Greenlees MJ, Hoskin CJ, Keogh JS, Lloyd R, Melville J, McDonald PJ, Michael DR, Mitchell NJ, Sanderson C, Shea GM, Sumner J, Wapstra E, Woinarski JCZ, Chapple DG (2021) Reptiles on the brink: identifying the Australian terrestrial snake and lizard species most at risk of extinction. Pacific Conservation Biology 27, 3-12.
| Crossref | Google Scholar |

Gibbons JW, Scott DE, Ryan TJ, Buhlmann KA, Tuberville TD, Metts BS, Greene JL, Mills T, Leiden Y, Poppy S, Winne CT (2000) The global decline of reptiles, déjà vu amphibians. BioScience 50, 653-666.
| Crossref | Google Scholar |

Gillespie G, Clemann N, Hutchinson M, Michael D, Melville J, Robertson P, Chapple DG (2018) Pseudemoia rawlinsoni, The IUCN Red List of Threatened Species 2018: e.T109480985A109480994. Available at https://dx.doi.org/10.2305/IUCN.UK.2018-1.RLTS.T109480985A109480994.en [accessed 4 August 2023]

Gorissen S, Greenlees M, Shine R (2017) A skink out of water: impacts of anthropogenic disturbance on an endangered reptile in Australian highland swamps. Oryx 51, 610-618.
| Crossref | Google Scholar |

Herrero-Borgoñón JJ, Cristóbal JC, Crespo B. M (1995) Pennisetum clandestinum Hochst. ex Chiov. (Poaceae), an African grass in Europe. Israel Journal of Plant Sciences 43, 159-162.
| Crossref | Google Scholar |

Hoare JM, O’Donnell CFJ, Westbrooke I, Hodapp D, Lettink M (2009) Optimising the sampling of skinks using artificial retreats based on weather conditions and time of day. Applied Herpetology 6, 379-390.
| Crossref | Google Scholar |

Hogue AS, Breon K (2022) The greatest threats to species. Conservation Science and Practice 4, e12670.
| Crossref | Google Scholar |

House SM, Spellerberg IF (1983) Ecology and conservation of the sand lizard (Lacerta agilis L.) habitat in southern England. Journal of Applied Ecology 20, 417-437.
| Crossref | Google Scholar |

Howland BWA, Stojanovic D, Gordon IJ, Fletcher D, Snape M, Stirnemann IA, Lindenmayer DB (2016) Habitat preference of the striped legless lizard: implications of grazing by native herbivores and livestock for conservation of grassland biota. Austral Ecology 41, 455-464.
| Crossref | Google Scholar |

Huey RB, Peterson CR, Arnold SJ, Porter WP (1989) Hot rocks and not-so-hot rocks: retreat-site selection by garter snakes and its thermal consequences. Ecology 70, 931-944.
| Crossref | Google Scholar |

Huey RB, Losos JB, Moritz C (2010) Are lizards toast? Science 328, 832-833.
| Crossref | Google Scholar | PubMed |

Humphrey JE, Robert KA, Leonard SWJ (2017) Elliott traps found to be ineffective for the survey of swamp skink (Lissolepis coventryi): a cautionary tale of outdated survey guidelines. Wildlife Research 44, 514-522.
| Crossref | Google Scholar |

Hutchinson MN, Donnellan SC (1988) A new species of scincid lizard related to Leiolopisma entrecasteauxii, from southeastern Australia. Royal Society of South Australia 112, 143-151.
| Google Scholar |

Jackson DA (1993) Stopping rules in principal components analysis: a comparison of heuristical and statistical approaches. Ecology 74, 2204-2214.
| Crossref | Google Scholar |

Joppa LN, Williams CK, Temple SA, Casper GS (2009) Environmental factors affecting sampling success of artificial cover objects. Herpetological Conservation and Biology 5, 143-148.
| Google Scholar |

Kearney M, Shine R, Porter WP (2009) The potential for behavioral thermoregulation to buffer ‘cold-blooded’ animals against climate warming. Proceedings of the National Academy of Sciences 106, 3835-3840.
| Crossref | Google Scholar |

Lambin EF, Geist HJ (Eds) (2006) ‘Land-use and land-cover change.’ (Springer: Berlin, Germany). doi:10.1007/3-540-32202-7_1

Lampert A, Hastings A, Grosholz ED, Jardine SL, Sanchirico JN (2014) Optimal approaches for balancing invasive species eradication and endangered species management. Science 344, 1028-1031.
| Crossref | Google Scholar | PubMed |

Lindenmayer DB, Wood J, MacGregor C, Hobbs RJ, Catford JA (2017) Non-target impacts of weed control on birds, mammals, and reptiles. Ecosphere 8, e01804.
| Crossref | Google Scholar |

Lê S, Josse J, Husson F (2008) FactoMineR: an R package for multivariate analysis. Journal of Statistical Software 25, 1-18.
| Crossref | Google Scholar |

Martin LJ, Murray BR (2011) A predictive framework and review of the ecological impacts of exotic plant invasions on reptiles and amphibians. Biological Reviews 86, 407-419.
| Crossref | Google Scholar | PubMed |

Meiri S, Chapple DG, Tolley KA, Mitchell N, Laniado T, Cox N, Bowles P, Young BE, Caetano G, Geschke J, Böhm M, Roll U (2023) Done but not dusted: reflections on the first global reptile assessment and priorities for the second. Biological Conservation 278, 109879.
| Crossref | Google Scholar |

Michael DR, Cunningham RB, Lindenmayer DB (2011) Regrowth and revegetation in temperate Australia presents a conservation challenge for reptile fauna in agricultural landscapes. Biological Conservation 144, 407-415.
| Crossref | Google Scholar |

Mizsei E, Fejes Z, Malatinszky Á, Lengyel S, Vadász C (2020) Reptile responses to vegetation structure in a grassland restored for an endangered snake. Community Ecology 21, 203-212.
| Crossref | Google Scholar |

Moore D, Stow A, Kearney MR (2018) Under the weather? The direct effects of climate warming on a threatened desert lizard are mediated by their activity phase and burrow system. Journal of Animal Ecology 87, 660-671.
| Crossref | Google Scholar | PubMed |

Morton SR, James CD (1988) The diversity and abundance of lizards in arid Australia: a new hypothesis. The American Naturalist 132, 237-256.
| Crossref | Google Scholar |

Nugent DT, Baker-Gabb DJ, Green P, Ostendorf B, Dawlings F, Clarke RH, Morgan JW (2022) Multi-scale habitat selection by a cryptic, critically endangered grassland bird – the Plains-wanderer (Pedionomus torquatus): implications for habitat management and conservation. Austral Ecology 47, 698-712.
| Crossref | Google Scholar |

Olsson M, Shine R (2003) Female-biased natal and breeding dispersal in an alpine lizard, Niveoscincus microlepidotus. Biological Journal of the Linnean Society 79, 277-283.
| Crossref | Google Scholar |

Pimm SL, Jenkins CN, Abell R, Brooks TM, Gittleman JL, Joppa LN, Raven PH, Roberts CM, Sexton JO (2014) The biodiversity of species and their rates of extinction, distribution, and protection. Science 344, 1246752.
| Crossref | Google Scholar |

Pyne S (1997) ‘World fire: the culture of fire on earth.’ (University of Washington Press: Seattle, WA, USA)

R Core Team (2021) ‘R: a language and environment for statistical computing.’ (R Foundation for Statistical Computing: Vienna, Austria)

Ritchie EG, Bradshaw CJA, Dickman CR, Hobbs R, Johnson CN, Johnston EL, Laurance WF, Lindenmayer D, McCarthy MA, Nimmo DG, Possingham HH, Pressey RL, Watson DM, Woinarski J (2013) Continental-scale governance and the hastening of loss of Australia’s biodiversity. Conservation Biology 27, 1133-1135.
| Crossref | Google Scholar | PubMed |

Saleeba K, Phillips BL, O’Shea M, Kearney MR (2020) Using biophysical models to improve survey efficiency for cryptic ectotherms. The Journal of Wildlife Management 84, 1185-1195.
| Crossref | Google Scholar |

Sato CF, Wood JT, Schroder M, Green K, Michael DR, Lindenmayer DB (2014a) The impacts of ski resorts on reptiles: a natural experiment. Animal Conservation 17, 313-322.
| Crossref | Google Scholar |

Sato CF, Wood JT, Schroder M, Green K, Osborne WS, Michael DR, Lindenmayer DB (2014b) An experiment to test key hypotheses of the drivers of reptile distribution in subalpine ski resorts. Journal of Applied Ecology 51, 13-22.
| Crossref | Google Scholar |

Senior AF, Clemann N, Gardner MG, Harrisson KA, While GM, Chapple DG (2022) Genetic structure, diversity and distribution of a threatened lizard affected by widespread habitat fragmentation. Conservation Genetics 23, 151-165.
| Crossref | Google Scholar |

Sewell D, Guillera-Arroita G, Griffiths RA, Beebee TJC (2012) When is a species declining? Optimizing survey effort to detect population changes in reptiles. PLoS ONE 7, e43387.
| Crossref | Google Scholar | PubMed |

Sinclair S, Boon P (2012) Changes in the area of coastal marsh in Victoria since the mid 19th century. Cunninghamia 12, 153-176.
| Google Scholar |

Smith BD (1995) ‘The emergence of agriculture, Scientific American Library.’ (W.H. Freeman & Co.: New York, NY, USA)

Steffen W, Crutzen PJ, McNeill JR (2007) The Anthropocene: are humans now overwhelming the great forces of nature? AMBIO: A Journal of the Human Environment 36, 614-621.
| Crossref | Google Scholar | PubMed |

Todd BD, Andrews KM (2008) Response of a reptile guild to forest harvesting. Conservation Biology 22, 753-761.
| Crossref | Google Scholar | PubMed |

Tooth S, McCarthy TS (2007) Wetlands in drylands: geomorphological and sedimentological characteristics, with emphasis on examples from southern Africa. Progress in Physical Geography: Earth and Environment 31, 3-41.
| Crossref | Google Scholar |

United Nations (2022) World population prospects 2022. United Nations, Department of Economic and Social Affairs, Population Division. Available at https://population.un.org/wpp/Graphs/Probabilistic/POP/TOT/900 [accessed 3 August 2023]

Valentine LE, Roberts B, Schwarzkopf L (2007) Mechanisms driving avoidance of non-native plants by lizards. Journal of Applied Ecology 44, 228-237.
| Crossref | Google Scholar |

Victorian Environmental Assessment Council (2011) Remnant native vegetation investigation – final report. Available at https://www.veac.vic.gov.au/investigations-assessments/previous-investigations/investigation/remnant-native-vegetation-investigation-veac-2011 [accessed 3 August 2023]

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

Wong DT, Gruber B, Sarre SD, Osborne WS (2021) Agricultural modification to vegetation drives presence and abundance of a threatened fossorial legless lizard. Austral Ecology 46, 437-448.
| Google Scholar |

Yugovic J (2011) Ecology of the Kooweerup Swamp and associated grasslands. Proceedings of the Royal Society of Victoria 123, 172-188.
| Google Scholar |