Is there a lizard down that spider burrow? Microhabitat influences spider burrow occupancy by the endangered pygmy bluetongue
Kimberley H. Michael A * , Ryan Baring A and Michael G. Gardner AA
Abstract
Reptiles partition their activity among their microhabitats for thermoregulatory, predatory, and refuge opportunities. We investigated whether a habitat specialist, the endangered pygmy bluetongue (Tiliqua adelaidensis), preferentially occupied vacant spider burrows in specific microhabitats in agricultural grasslands.
We investigated whether (1) microhabitat availability influenced associations of lizards occupying burrows among four populations, (2) lizard microhabitat preferences varied over time and, (3) whether a correlation was present between lizard body condition and the occupancy of spider burrows in specific microhabitats.
We assessed the microhabitat surrounding pygmy bluetongue-occupied spider burrows and unoccupied burrows that fit the criteria to be potentially suitable for pygmy bluetongue occupancy among four populations over two field seasons. We used the presence or absence of a lizard within a spider burrow to generate models to assess the probability of lizard occupancy to test whether pygmy bluetongues exhibited microhabitat preferences when occupying a spider burrow.
We found that pygmy bluetongues were strongly positively associated with burrows on an angle and were negatively associated with burrows surrounded by bare ground, rock, lichen, and that were further from vegetation. Microhabitat preferences varied among populations and time, which may have been influenced by habitat availability at each site and season. We also found that pygmy bluetongue body condition was positively associated with greater rock cover; however, rock availability did not exceed 10% cover, which suggests that it may have been an incidental association owing to the low sample size of caught lizards or was affected by above-average rainfall.
Microhabitat preferences exhibited by habitat specialists such as the pygmy bluetongue may differ when inhabiting locations that differ in their availability of high-quality habitat.
Our results have implications for selecting appropriate microhabitats when installing artificial burrows for lizards at future translocation sites and land-management implications to ensure landscape heterogeneity of benefit for successful conservation.
Keywords: burrow, conservation, landscape heterogeneity, microhabitat preference, microhabitat use, reptile, Scincidae, Tiliqua adelaidensis.
References
Baling M, Stuart-Fox D, Brunton DH, Dale J (2016) Habitat suitability for conservation translocation: the importance of considering camouflage in cryptic species. Biological Conservation 203, 298-305.
| Crossref | Google Scholar |
Berger-Tal O, Blumstein DT, Swaisgood RR (2020) Conservation translocations: a review of common difficulties and promising directions. Animal Conservation 23(2), 121-131.
| Crossref | Google Scholar |
Blázquez MC, Rodríguez-Estrella R (2007) Microhabitat selection in diet and trophic ecology of a spiny-tailed iguana Ctenosaura hemilopha. Biotropica 39(4), 496-501.
| Crossref | Google Scholar |
Bradley HS, Craig MD, Cross AT, Tomlinson S, Bamford MJ, Bateman PW (2022) Revealing microhabitat requirements of an endangered specialist lizard with LiDAR. Scientific Reports 12(1), 5193.
| Crossref | Google Scholar | PubMed |
Bromham L, Cardillo M, Bennett AF, Elgar MA (1999) Effects of stock grazing on the ground invertebrate fauna of woodland remnants. Australian Journal of Ecology 24(3), 199-207.
| Crossref | Google Scholar |
Bull CM, Godfrey SS, Ebrahimi M, Fenner AL (2015) Long and short term residence in refuge burrows by endangered pygmy bluetongue lizards. Amphibia-Reptilia 36(2), 119-124.
| Crossref | Google Scholar |
Bureau of Meteorology (2008) Drought statement – Issued 6th August 2008. Available at http://www.bom.gov.au/announcements/media_releases/climate/drought/20080806.shtml [accessed 19 October 2023]
Bureau of Meteorology (2023) Rainfall deficiencies and water availability – Issued 6th October 2023. Available at http://www.bom.gov.au/climate/drought/archive/20231006.archive.shtml [accessed 19 October 2023]
Clayton J, Bull CM (2015) The impact of sheep grazing on burrows for pygmy bluetongue lizards and on burrow digging spiders. Journal of Zoology 297(1), 44-53.
| Crossref | Google Scholar |
Clayton J, Bull M (2016) The impact of sheep grazing on the depth of spider burrows and of burrows selected by the pygmy bluetongue lizard (Tiliqua adelaidensis). Wildlife Research 43(8), 691-703.
| Crossref | Google Scholar |
Clayton J, Gardner MG, Fenner AL, Bull M (2020) Co-occupancy of spider-engineered burrows within a grassland community changes temporally. Austral Ecology 45(4), 454-459.
| Crossref | Google Scholar |
Cox RM, Calsbeek R (2015) Survival of the fattest? Indices of body condition do not predict viability in the brown anole (Anolis sagrei). Functional Ecology 29(3), 404-413.
| Crossref | Google Scholar |
Damgaard CF, Irvine KM (2019) Using the beta distribution to analyse plant cover data. Journal of Ecology 107, 2747-2759.
| Crossref | Google Scholar |
Davis KL, Silverman ED, Sussman AL, Wilson RR, Zipkin EF (2022) Errors in aerial survey count data: identifying pitfalls and solutions. Ecology and Evolution 12, e8733.
| Crossref | Google Scholar | PubMed |
Decker O, Eldridge DJ, Gibb H (2019) Restoration potential of threatened ecosystem engineers increases with aridity: broad scale effects on soil nutrients and function. Ecography 42(8), 1370-1382.
| Crossref | Google Scholar |
Delean S, Bull CM, Brook BW, Heard LMB, Fordham DA (2013) Using plant distributions to predict the current and future range of a rare lizard. Diversity and Distributions 19(9), 1125-1137.
| Crossref | Google Scholar |
Dengler J, Dembicz I (2023) Should we estimate plant cover in percent or on ordinal scales? Vegetation Classification and Survey 4, 131-138.
| Crossref | Google Scholar |
Donovan M, Monaghan R (2021) Impacts of grazing on ground cover, soil physical properties and soil loss via surface erosion: a novel geospatial modelling approach. Journal of Environmental Management 287, 112206.
| Crossref | Google Scholar |
Doucette LI, Duncan RP, Osborne WS, Evans M, Georges A, Gruber B, Sarre SD (2023) Climate warming drives a temperate-zone lizard to its upper thermal limits, restricting activity, and increasing energetic costs. Scientific Reports 13, 9603.
| Crossref | Google Scholar | PubMed |
Ebrahimi M, Schofield JA, Bull CM (2012) Getting your feet wet: responses of the endangered pygmy bluetongue lizard (Tiliqua adelaidensis) to rain induced burrow flooding. Herpetology Notes 5, 297-301.
| Google Scholar |
Eldridge DJ, James AI (2009) Soil-disturbance by native animals plays a critical role in maintaining healthy Australian landscapes. Ecological Management & Restoration 10, S27-S34.
| Crossref | Google Scholar |
Fellows HL, Fenner AL, Bull CM (2009) Spiders provide important resources for an endangered lizard. Journal of Zoology 279(2), 156-163.
| Crossref | Google Scholar |
Fenner AL, Bull CM (2007) Short-term impact of grassland fire on the endangered pygmy bluetongue lizard. Journal of Zoology 272(4), 444-450.
| Crossref | Google Scholar |
Fenner AL, Schofield J, Smith AL, Bull CM (2008) Observations of snake predation on the pygmy bluetongue lizard, Tiliqua adelaidensis. Herpetofauna 38, 105-109.
| Google Scholar |
Fordham DA, Watts MJ, Delean S, Brook BW, Heard LMB, Bull CM (2012) Managed relocation as an adaptation strategy for mitigating climate change threats to the persistence of an endangered lizard. Global Change Biology 18(9), 2743-2755.
| Crossref | Google Scholar | PubMed |
Gaudenti N, Nix E, Maier P, Westphal MF, Taylor EN (2021) Habitat heterogeneity affects the thermal ecology of an endangered lizard. Ecology and Evolution 11(21), 14843-14856.
| Crossref | Google Scholar | PubMed |
Gedeon CI, Boross G, Németh A, Altbäcker V (2012) Release site manipulation to favour European ground squirrel Spermophilus citellus translocations: translocation and habitat manipulation. Wildlife Biology 18(1), 97-104.
| Crossref | Google Scholar |
Gimmel A, Öfner S, Liesegang A (2021) Body condition scoring (BCS) in corn snakes (Pantherophis guttatus) and comparison to pre-existing body condition index (BCI) for snakes. Journal of Animal Physiology and Animal Nutrition 105(S2), 24-28.
| Crossref | Google Scholar |
Hacking J, Abom R, Schwarzkopf L (2014) Why do lizards avoid weeds? Biological Invasions 16(4), 935-947.
| Crossref | Google Scholar |
Hodgson MJ, Ritchie D (2023) Strange bedfellows: mammal burrow disturbances may provide thermoregulatory microsites for fossorial reptiles in densely vegetated dunes. Austral Ecology 48, 1473-1478.
| Crossref | Google Scholar |
Howison RA, Olff H, van de Koppel J, Smit C (2017) Biotically driven vegetation mosaics in grazing ecosystems: the battle between bioturbation and biocompaction. Ecological Monographs 87(3), 363-378.
| Crossref | Google Scholar |
Howland B, Stojanovic D, Gordon IJ, Manning AD, Fletcher D, Lindenmayer DB (2014) Eaten out of house and home: impacts of grazing on ground-dwelling reptiles in Australian grasslands and grassy woodlands. PLoS ONE 9(12), e105966.
| Crossref | Google Scholar | PubMed |
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: habitat preferences of a threatened reptile. Austral Ecology 41(4), 455-464.
| Crossref | Google Scholar |
Hutchinson MN, Milne T, Croft T (1994) Redescription and ecological notes on the pygmy bluetongue, Tiliqua adelaidensis (Squamata: Scincidae). Transactions of the Royal Society of South Australia 118, 217-226.
| Google Scholar |
Jones CG, Lawton JH, Shachak M (1994) Organisms as ecosystem engineers. Oikos 69(3), 373-386.
| Crossref | Google Scholar |
Kerr GD, Bull CM (2004) Microhabitat use by the scincid lizard tiliqua rugosa: exploiting natural temperature gradients beneath plant canopies. Journal of Herpetology 38(4), 536-545.
| Crossref | Google Scholar |
Kovács D, Kiss I (2016) Microhabitat use of different age groups of snake-eyed skink and eastern green lizard. Amphibia-Reptilia 37(2), 191-198.
| Crossref | Google Scholar |
Marshall KLA, Philpot KE, Stevens M (2016) Microhabitat choice in island lizards enhances camouflage against avian predators. Scientific Reports 6(1), 19815.
| Crossref | Google Scholar |
Michael KH, Gardner MG (2023) Hold your breath: observations of the endangered pygmy bluetongue (Tiliqua adelaidensis) submerged in flooded burrows. Austral Ecology 48(6), 1200-1204.
| Crossref | Google Scholar |
Michael DR, Cunningham RB, Lindenmayer DB (2010a) Microhabitat relationships among five lizard species associated with granite outcrops in fragmented agricultural landscapes of south-eastern Australia. Austral Ecology 35(2), 214-225.
| Crossref | Google Scholar |
Michael DR, Cunningham RB, Lindenmayer DB (2010b) The social elite: habitat heterogeneity, complexity and quality in granite inselbergs influence patterns of aggregation in Egernia striolata (Lygosominae: Scincidae). Austral Ecology 35(8), 862-870.
| Crossref | Google Scholar |
Michael KH, Leonard SWJ, Decker O, Verdon SJ, Gibb H (2022) Testing the effects of ecologically extinct mammals on vegetation in arid Australia: a long-term experimental approach. Austral Ecology 47(2), 226-238.
| Crossref | Google Scholar |
Milne T, Bull CM (2000) Burrow choice by individuals of different sizes in the endangered pygmy blue tongue lizard Tiliqua adelaidensis. Biological Conservation 95(3), 295-301.
| Crossref | Google Scholar |
Milne T, Bull CM, Hutchinson MN (2003) Use of burrows by the endangered pygmy blue-tongue lizard, Tiliqua adelaidensis (Scincidae). Wildlife Research 30(5), 523-528.
| Crossref | Google Scholar |
Mulhall SJ, Di Stefano J, Dorph A, Swan M, Sitters H (2024) Do reptile responses to habitat structure and time since fire depend on landscape structure? Forest Ecology and Management 553, 121564.
| Crossref | Google Scholar |
Naeth MA, Bailey AW, Pluth DJ, Chanasyk DS, Hardin RT (1991) Grazing impacts on litter and soil organic matter in mixed prairie and fescue grassland ecosystems of Alberta. Journal of Range Management 44, 7-12.
| Crossref | Google Scholar |
Nafus MG, Yackel Adams AA, Boback SM, Siers SR, Reed RN (2020) Behavior, size, and body condition predict susceptibility to management and reflect post-treatment frequency shifts in an invasive snake. Global Ecology and Conservation 21, e00834.
| Crossref | Google Scholar |
Neilly H, O’Reagain P, Vanderwal J, Schwarzkopf L (2018) Profitable and sustainable cattle grazing strategies support reptiles in tropical savanna rangeland. Rangeland Ecology & Management 71(2), 205-212.
| Crossref | Google Scholar |
Pettigrew M, Bull CM (2011) The impact of heavy grazing on burrow choice in the pygmy bluetongue lizard, Tiliqua adelaidensis. Wildlife Research 38(4), 299-306.
| Crossref | Google Scholar |
Pettigrew M, Bull CM (2012) The response of pygmy bluetongue lizards to simulated grazing in the field during three drought years. Wildlife Research 39(6), 540-545.
| Crossref | Google Scholar |
Pizzuto TA, Finlayson GR, Crowther MS, Dickman CR (2007) Microhabitat use by the brush-tailed bettong (Bettongia penicillata) and burrowing bettong (B. lesueur) in semiarid New South Wales: implications for reintroduction programs. Wildlife Research 34, 271-279.
| Crossref | Google Scholar |
Porensky LM, McGee R, Pellatz DW (2020) Long-term grazing removal increased invasion and reduced native plant abundance and diversity in a sagebrush grassland. Global Ecology and Conservation 24, e01267.
| Crossref | Google Scholar |
Prugh LR, Brashares JS (2012) Partitioning the effects of an ecosystem engineer: kangaroo rats control community structure via multiple pathways: partitioning effects of engineers. Journal of Animal Ecology 81(3), 667-678.
| Crossref | Google Scholar | PubMed |
R Core Team (2023) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Available at https://www.R-project.org/
Raymond CM, Spoehr J (2013) The acceptability of climate change in agricultural communities: comparing responses across variability and change. Journal of Environmental Management 115, 69-77.
| Crossref | Google Scholar | PubMed |
Read JL (2002) Experimental trial of Australian arid zone reptiles as early warning indicators of overgrazing by cattle: arid zone reptiles as indicators of overgrazing. Austral Ecology 27(1), 55-66.
| Crossref | Google Scholar |
Richards SA (2005) Testing ecological theory using the information-theoretic approach: examples and cautionary results. Ecology 86(10), 2805-2814.
| Crossref | Google Scholar |
Ridley JCH, Schlesinger CA (2023) Activity of tjakura (great desert skinks) at burrows in relation to plant cover and predators. Ecology and Evolution 13, e10391.
| Crossref | Google Scholar | PubMed |
Roznik EA, Johnson SA (2009) Burrow use and survival of newly metamorphosed gopher frogs (Rana capito). Journal of Herpetology 43(3), 431-437.
| Crossref | Google Scholar |
Schofield JA, Fenner AL, Pelgrim K, Bull CM (2012) Male-biased movement in pygmy bluetongue lizards: implications for conservation. Wildlife Research 39(8), 677-684.
| Crossref | Google Scholar |
Shamiminoori L, Fenner AL, Bull CM (2014) Weight watching in burrows: variation in body condition in pygmy bluetongue lizards. Australian Journal of Zoology 62(4), 284-293.
| Crossref | Google Scholar |
Souter NJ, Michael Bull C, Hutchinson MN (2004) Adding burrows to enhance a population of the endangered pygmy blue tongue lizard, Tiliqua adelaidensis. Biological Conservation 116(3), 403-408.
| Crossref | Google Scholar |
Souter NJ, Bull CM, Lethbridge MR, Hutchinson MN (2007) Habitat requirements of the endangered pygmy bluetongue lizard, Tiliqua adelaidensis. Biological Conservation 135(1), 33-45.
| Crossref | Google Scholar |
Spiegel O, Leu ST, Sih A, Godfrey SS, Bull CM (2015) When the going gets tough: behavioural type-dependent space use in the sleepy lizard changes as the season dries. Proceedings of the Royal Society B: Biological Sciences 282, 20151768.
| Crossref | Google Scholar |
Staver AC, Wigley-Coetsee C, Botha J (2019) Grazer movements exacerbate grass declines during drought in an African savanna. Journal of Ecology 107, 1482-1491.
| Crossref | Google Scholar |
Stevens TA, Evans MC, Osborne WS, Sarre SD (2010) Home ranges of, and habitat use by, the grassland earless dragon (Tympanocryptis pinguicolla) in remnant native grasslands near Canberra. Australian Journal of Zoology 58(2), 76-84.
| Crossref | Google Scholar |
Toft CA (1985) Resource partitioning in amphibians and reptiles. Copeia 1985(1), 1-21.
| Crossref | Google Scholar |
Verdon SJ, Gibb H, Leonard SWJ (2016) Net effects of soil disturbance and herbivory on vegetation by a re-established digging mammal assemblage in arid zone Australia. Journal of Arid Environments 133, 29-36.
| Crossref | Google Scholar |
Vieira EM, Iob G, Briani DC, Palma ART (2005) Microhabitat selection and daily movements of two rodents (Necromys lasiurus and Oryzomys scotti) in Brazilian Cerrado, as revealed by a spool-and-line device. Mammalian Biology 70(6), 359-365.
| Crossref | Google Scholar |
Zipkin EF, Leirness JB, Kinlan BP, O’Connell AF, Silverman ED (2014) Fitting statistical distributions to sea duck count data: implications for survey design and abundance estimation. Statistical Methodology 17, 67-81.
| Crossref | Google Scholar |