Barking up the right tree: comparative use of arboreal and terrestrial artificial refuges to survey reptiles in temperate eucalypt woodlands
Damian R. Michael A B C * , Daniel Florance A * , Mason Crane A , Wade Blanchard A and David B. Lindenmayer A BA Fenner School of Environment and Society, The Australian National University, Canberra, ACT 2601, Australia.
B National Environmental Science Program, Threatened Species Recovery Hub, The Australian National University, Canberra, ACT 2601, Australia.
C Corresponding author. Email: damian.michael@anu.edu.au
Wildlife Research 45(2) 185-192 https://doi.org/10.1071/WR17117
Submitted: 22 August 2017 Accepted: 26 February 2018 Published: 24 April 2018
Abstract
Context: Artificial refuges (cover boards) are a popular method to survey and monitor herpetofauna worldwide. However, one limitation of using artificial refuges in terrestrial environments is the low detection rates of arboreal species. Furthermore, destructive search techniques can damage critical microhabitat such as exfoliating rock or flaking bark of mature trees.
Aim: We tested a non-destructive, passive method of sampling arboreal reptiles in fragmented agricultural landscapes in south-eastern Australia.
Methods: We installed 84 artificial bark refuges consisting of strips of non-toxic, closed-cell foam attached to eucalypt trees in 13 patches of remnant vegetation. We used Bayesian statistics to compare differences in detection rates among artificial bark refuges, terrestrial artificial refuges and active searches of natural habitat over a 4-year period.
Key results: Active searches combined with terrestrial artificial refuges detected the highest number of reptile species, including several cryptic fossorial species. Artificial bark refuges detected, on average, 132 times more individuals of the arboreal southern marbled gecko, Christinus marmoratus, than did terrestrial refuges. Gecko abundance patterns were related to tree characteristics such as tree size, bark thickness and stand basal area, as well as survey year.
Conclusions: Traditional survey methods such as terrestrial cover boards, in combination with active searches of natural habitat, may significantly underestimate counts for arboreal gecko species.
Implications: Artificial bark refuges provide a cost-effective, non-destructive and durable method for surveying and monitoring arboreal reptiles in woodland environments over short to medium time frames. Foil-backed, closed-cell foam has broad application for use in spatial capture–recapture studies and long-term monitoring of arboreal reptiles. This method also may be effective for procuring records of threatened arboreal geckos or as a solution for providing temporary habitat in ecological restoration projects.
Additional keywords: arboreal reptiles, artificial cover boards, environmental-impact assessments, habitat restoration, survey method.
References
Adams, C. E. (2016). ‘Urban Wildlife Management.’ (CRC press, Taylor & Francis Group: Boca Raton, FL.)Ballouard, J.-M., Caron, S., Lafon, T., Servant, L., Devaux, B., and Bonnet, X. (2013). Fibrocement slabs as useful tools to monitor juvenile reptiles: a study in a tortoise species. Amphibia–Reptilia 34, 1–10.
| Fibrocement slabs as useful tools to monitor juvenile reptiles: a study in a tortoise species.Crossref | GoogleScholarGoogle Scholar |
Bell, T. P. (2009). A novel technique for monitoring highly cryptic lizard species in forests. Herpetological Conservation and Biology 4, 415–425.
Bowie, M. H., Hodge, S., Banks, J. C., and Vink, C. J. (2006). An appraisal of simple tree-mounted shelters for non-lethal monitoring of weta (Orthoptera: Anostostomatidae and Rhaphidophoridae) in New Zealand nature reserves. Journal of Insect Conservation 10, 261–268.
| An appraisal of simple tree-mounted shelters for non-lethal monitoring of weta (Orthoptera: Anostostomatidae and Rhaphidophoridae) in New Zealand nature reserves.Crossref | GoogleScholarGoogle Scholar |
Buerkner, P.-C. (2016). ‘brms: an R Package for Bayesian Multilevel Models using Stan.’ Available at https://cran.r-project.org/web/packages/brms/vignettes/brms.pdf [verified 15 August 2017]
Carpenter, B., Gelman, A., Hoffman, M. D., Lee, D., Ben Goodrich, M. B., Brubaker, M., Guo, J., Li, P., and Riddell, A. (2017). Stan: a probabilistic programming language. Journal of Statistical Software 76, .
| Stan: a probabilistic programming language.Crossref | GoogleScholarGoogle Scholar |
Cunningham, R. B. (2016). Design and analysis of quasi-experiments in landscape ecology: responses of fauna to landscape vegetation transformation in South-Eastern NSW. Ph.D. Thesis, The Australian National University, Canberra.
Cunningham, R. B., Lindenmayer, D. B., Crane, M., Michael, D., and MacGregor, C. (2007). Reptile and arboreal marsupial response to replanted vegetation in agricultural landscapes. Ecological Applications 17, 609–619.
| Reptile and arboreal marsupial response to replanted vegetation in agricultural landscapes.Crossref | GoogleScholarGoogle Scholar |
Engeman, R. M. (2005). Indexing principles and a widely applicable paradigm for indexing animal populations. Wildlife Research 32, 203–210.
| Indexing principles and a widely applicable paradigm for indexing animal populations.Crossref | GoogleScholarGoogle Scholar |
Fryxell, J. M., Sinclair, A. R., and Caughley, G. (2014). ‘Wildlife Ecology, Conservation and Management.’ (John Wiley & Sons: Chichester, UK)
Garden, J. G., McAlpine, C. A., Possingham, H. P., and Jones, D. N. (2007). Using multiple survey methods to detect terrestrial reptiles and mammals: what are the most successful and cost-efficient combinations? Wildlife Research 34, 218–227.
| Using multiple survey methods to detect terrestrial reptiles and mammals: what are the most successful and cost-efficient combinations?Crossref | GoogleScholarGoogle Scholar |
Gelman, A., Jakulin, A., Pittau, M. G., and Su, Y.-S. (2008). A weakly informative default prior distribution for logistic and other regression models. The Annals of Applied Statistics 2, 1360–1383.
| A weakly informative default prior distribution for logistic and other regression models.Crossref | GoogleScholarGoogle Scholar |
Gelman, A., Hwang, J., and Vehtari, A. (2014). Understanding predictive information criteria for Bayesian models. Statistics and Computing 24, 997–1016.
| Understanding predictive information criteria for Bayesian models.Crossref | GoogleScholarGoogle Scholar |
Grant, B. W., Tucker, A. D., Lovich, J. E., Mills, A. M., Dixon, P. M., and Gibbons, J. W. (1992). The use of coverboards in estimating patterns of reptile and amphibian biodiversity. In ‘Wildlife 2001: Populations’. (Ed. D. R. McCullough and R. H. Barrett.) pp. 379-403. (Elsevier Science Publishers LTD: Essex, UK)
Halliday, W. D., and Blouin-Demers, G. (2015). Efficacy of coverboards for sampling small northern snakes. Herpetology Notes 8, 309–314.
Hampton, P. (2007). A comparison of the success of artificial cover types for capturing amphibians and reptiles. Amphibia-Reptilia 28, 433–437.
| A comparison of the success of artificial cover types for capturing amphibians and reptiles.Crossref | GoogleScholarGoogle Scholar |
Hesed, K. M. (2012). Uncovering salamander ecology: a review of coverboard design. Journal of Herpetology 46, 442–450.
| Uncovering salamander ecology: a review of coverboard design.Crossref | GoogleScholarGoogle Scholar |
Hobbs, R. J., and Yates, C. J. (2000). ‘Temperate Eucalypt Woodlands in Australia: Biology, Conservation, Management and Restoration.’ (Surrey Beatty: Sydney.)
Hodge, S., Vink, C. J., Banks, J. C., and Bowie, M. H. (2007). The use of tree-mounted artificial shelters to investigate arboreal spider communities in New Zealand nature reserves. The Journal of Arachnology 35, 129–136.
| The use of tree-mounted artificial shelters to investigate arboreal spider communities in New Zealand nature reserves.Crossref | GoogleScholarGoogle Scholar |
Hoehn, M., Sarre, S., and Henle, K. (2007). The tales of two geckos: does dispersal prevent extinction in recently fragmented populations? Molecular Ecology 16, 3299–3312.
| The tales of two geckos: does dispersal prevent extinction in recently fragmented populations?Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD2svntVGmsg%3D%3D&md5=96dbabb242bb72a91d8ab7c636344285CAS |
Howland, B. W., Stojanovic, D., Gordon, I. J., Fletcher, D., Snape, M., Stirnemann, I. A., and Lindenmayer, D. B. (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.
| Habitat preference of the striped legless lizard: implications of grazing by native herbivores and livestock for conservation of grassland biota.Crossref | GoogleScholarGoogle Scholar |
Huey, R. B., Peterson, C. R., Arnold, S. J., and Porter, W. P. (1989). Hot rocks and not‐so‐hot rocks: retreat‐site selection by garter snakes and its thermal consequences. Ecology 70, 931–944.
| Hot rocks and not‐so‐hot rocks: retreat‐site selection by garter snakes and its thermal consequences.Crossref | GoogleScholarGoogle Scholar |
Ikin, K., Mortelliti, A., Stein, J., Michael, D., Crane, M., Okada, S., Wood, J., and Lindenmayer, D. (2015). Woodland habitat structures are affected by both agricultural land management and abiotic conditions. Landscape Ecology 30, 1387–1403.
| Woodland habitat structures are affected by both agricultural land management and abiotic conditions.Crossref | GoogleScholarGoogle Scholar |
Joppa, L. N., Williams, C. K., Temple, S. A., and Casper, G. S. (2009). Environmental factors affecting sampling success of artificial cover objects. Herpetological Conservation and Biology 5, 143–148.
Kay, G. M., Michael, D. R., Crane, M., Okada, S., MacGregor, C., Florance, D., Trengove, D., McBurney, L., Blair, D., and Lindenmayer, D. B. (2013). A list of reptiles and amphibians from box gum grassy woodlands in south-eastern Australia. Check List 9, 476–481.
| A list of reptiles and amphibians from box gum grassy woodlands in south-eastern Australia.Crossref | GoogleScholarGoogle Scholar |
Kay, G. M., Driscoll, D. A., Lindenmayer, D. B., Pulsford, S. A., and Mortelliti, A. (2016). Pasture height and crop direction influence reptile movement in an agricultural matrix. Agriculture, Ecosystems & Environment 235, 164–171.
| Pasture height and crop direction influence reptile movement in an agricultural matrix.Crossref | GoogleScholarGoogle Scholar |
Kearney, M. (2002). Hot rocks and much-too-hot rocks: seasonal patterns of retreat-site selection by a nocturnal ectotherm. Journal of Thermal Biology 27, 205–218.
| Hot rocks and much-too-hot rocks: seasonal patterns of retreat-site selection by a nocturnal ectotherm.Crossref | GoogleScholarGoogle Scholar |
Kearney, M., and Predavec, M. (2000). Do nocturnal ectotherms thermoregulate? A study of the temperate gecko Christinus marmoratus. Ecology 81, 2984–2996.
| Do nocturnal ectotherms thermoregulate? A study of the temperate gecko Christinus marmoratus.Crossref | GoogleScholarGoogle Scholar |
Keith, D. A., and Wales, N. S. (2004). ‘Ocean Shores to Desert Dunes: The Native Vegetation of New South Wales and the ACT.’ (Department of Environment and Conservation: Hurstville, NSW.)
Lettink, M. (2007). Comparison of two techniques for capturing geckos in rocky habitat. Herpetological Review 38, 415–418.
Lindenmayer, D. B., Gibbons, P., Bourke, M., Burgman, M., Dickman, C. R., Ferrier, S., Fitzsimons, J., Freudenberger, D., Garnett, S. T., and Groves, C. (2012a). Improving biodiversity monitoring. Austral Ecology 37, 285–294.
| Improving biodiversity monitoring.Crossref | GoogleScholarGoogle Scholar |
Lindenmayer, D. B., Zammit, C., Attwood, S. J., Burns, E., Shepherd, C. L., Kay, G., and Wood, J. (2012b). A novel and cost-effective monitoring approach for outcomes in an Australian biodiversity conservation incentive program. PLoS One 7, e50872.
| A novel and cost-effective monitoring approach for outcomes in an Australian biodiversity conservation incentive program.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhvV2js7jE&md5=4a1399a316b683ff76d065276986b43bCAS |
Lindenmayer, D. B., Michael, D. R., Crane, M., Barton, P., Ikin, K., and Okada, S. (2016). ‘Wildlife Conservation in Farm Landscapes.’ (CSIRO Publishing: Melbourne.)
Michael, D. R., Lunt, I. D., and Robinson, W. A. (2004). Enhancing fauna habitat in grazed native grasslands and woodlands: use of artificially placed log refuges by fauna. Wildlife Research 31, 65–71.
| Enhancing fauna habitat in grazed native grasslands and woodlands: use of artificially placed log refuges by fauna.Crossref | GoogleScholarGoogle Scholar |
Michael, D. R., Cunningham, R. B., Donnelly, C. F., and Lindenmayer, D. B. (2012). Comparative use of active searches and artificial refuges to survey reptiles in temperate eucalypt woodlands. Wildlife Research 39, 149–162.
| Comparative use of active searches and artificial refuges to survey reptiles in temperate eucalypt woodlands.Crossref | GoogleScholarGoogle Scholar |
Michael, D. R., Wood, J. T., Crane, M., Montague-Drake, R., and Lindenmayer, D. B. (2014). How effective are agri-environment schemes for protecting and improving herpetofaunal diversity in Australian endangered woodland ecosystems? Journal of Applied Ecology 51, 494–504.
| How effective are agri-environment schemes for protecting and improving herpetofaunal diversity in Australian endangered woodland ecosystems?Crossref | GoogleScholarGoogle Scholar |
Michael, D. R., Kay, G. M., Crane, M., Florance, D., MacGregor, C., Okada, S., McBurney, L., Blair, D., and Lindenmayer, D. B. (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.
| Ecological niche breadth and microhabitat guild structure in temperate Australian reptiles: implications for natural resource management in endangered grassy woodland ecosystems.Crossref | GoogleScholarGoogle Scholar |
Michael, D. R., Ikin, K., Crane, M., Okada, S., and Lindenmayer, D. B. (2017). Scale‐dependent occupancy patterns in reptiles across topographically different landscapes. Ecography 40, 415–424.
| Scale‐dependent occupancy patterns in reptiles across topographically different landscapes.Crossref | GoogleScholarGoogle Scholar |
Monti, L., Hunter, M., and Witham, J. (2000). An evaluation of the artificial cover object (ACO) method for monitoring populations of the redback salamander Plethodon cinereus. Journal of Herpetology 34, 624–629.
| An evaluation of the artificial cover object (ACO) method for monitoring populations of the redback salamander Plethodon cinereus.Crossref | GoogleScholarGoogle Scholar |
Nordberg, E. J., and Schwarzkopf, L. (2015). Arboreal cover boards: using artificial bark to sample cryptic arboreal lizards. Herpetologica 71, 268–273.
| Arboreal cover boards: using artificial bark to sample cryptic arboreal lizards.Crossref | GoogleScholarGoogle Scholar |
R Core Team (2015). ‘R: a Language and Environment for Statistical Computing.’ (R Foundation for Statistical Computing: Vienna.) Available at https://www.R-project.org/ [verified 15 August 2017].
Ribeiro-Júnior, M. A., Gardner, T. A., and Ávila-Pires, T. C. (2008). Evaluating the effectiveness of herpetofaunal sampling techniques across a gradient of habitat change in a tropical forest landscape. Journal of Herpetology 42, 733–749.
| Evaluating the effectiveness of herpetofaunal sampling techniques across a gradient of habitat change in a tropical forest landscape.Crossref | GoogleScholarGoogle Scholar |
Sutherland, C., Muñoz, D. J., Miller, D. A., and Grant, E. H. C. (2016). Spatial capture–recapture: a promising method for analyzing data collected using artificial cover objects. Herpetologica 72, 6–12.
| Spatial capture–recapture: a promising method for analyzing data collected using artificial cover objects.Crossref | GoogleScholarGoogle Scholar |
Thierry, A., Lettink, M., Besson, A. A., and Cree, A. (2009). Thermal properties of artificial refuges and their implications for retreat-site selection in lizards. Applied Herpetology 6, 307–326.
| Thermal properties of artificial refuges and their implications for retreat-site selection in lizards.Crossref | GoogleScholarGoogle Scholar |
Thompson, M. J. (2006). The use of artificial refuges to census populations of the ‘threatened’striped legless lizard, Delma impar in Western Victoria. Unpublished Honours thesis, Department of Zoology, La Trobe University, Melbourne.
Thompson, W. (2013). ‘Sampling Rare or Elusive Species: Concepts, Designs, and Techniques for Estimating Population Parameters.’ (Island Press: Washington, DC.)
Vehtari, A., Gelman, A., and Gabry, J. (2015). ‘Efficient Implementation of Leave-one-out Cross-validation and WAIC for Evaluating Fitted Bayesian Models.’ arXiv preprint arXiv:1507.04544. Available at https://github.com/jgabry/loo.
Watanabe, S. (2010). Asymptotic equivalence of Bayes cross validation and widely applicable information criterion in singular learning theory. Journal of Machine Learning Research 11, 3571–3594.
Webb, J. K., and Shine, R. (1998). Using thermal ecology to predict retreat-site selection by an endangered snake species. Biological Conservation 86, 233–242.
Willson, J. D., and Gibbons, J. W. (2010). Drift fences, coverboards, and other traps. In ‘Amphibian Ecology and Conservation: a Handbook of Techniques’. (Ed. C. K. Dodd.) pp. 229-245. (Oxford University Press: New York.)