Dragon detectives: citizen science confirms photo-ID as an effective tool for monitoring an endangered reptile
John Gould
A B * , Chad Beranek A B C and George Madani A B
A Conservation Science Research Group, School of Environmental and Life Sciences, University of Newcastle, Callaghan, NSW, Australia.
B Grassland Earless Dragon Alliance, Cooma, NSW, Australia.
C FAUNA Research Alliance, Kahibah, NSW, Australia.
Abstract
Among amphibians and reptiles, traditional methods of capture–mark–recapture (CMR) have relied on artificial marking techniques (in particular, toe clipping), which has raised concerns because it may impact climbing ability, survival, and behaviour. A potential alternative involves the exploitation of natural biometric identifiers that are already present, including scale configuration or colour patterns. These natural markers can be applied in photo-based CMR, which has several advantages over artificial markers, including reduced costs, the reduction of harm or stress, and the potential for public participation in conservation and research.
Our aim was to test the feasibility of applying citizen science in the manual visual identification of the endangered Monaro grassland earless dragon (Tympanocryptis osbornei) using dorsal pattern as a natural marker.
We collected photographs of dorsal patterns of wild T. osbornei individuals using a smartphone device under field conditions. We subsequently recruited participants anonymously from the public using social media to complete an online survey, in which they were asked to correctly match these field-captured images of individuals from small image pools, mimicking the process of detecting recapture events.
Participants were able to successfully detect recapture events from small image pools based solely on a comparison of dorsal patterns. High consensus was reached on all matches included in the online survey, with the majority vote among participants representing the correct matching of individuals on all occasions.
Our results indicate that there is sufficient intra-specific variability and temporal stability in dorsal patterning for it to be used as a reliable natural marker for identifying T. osbornei at the individual level.
Our findings suggest that photo-CMR could be applied to other agamids with similar dorsal patterns, making it a potentially valuable tool and an alternative to artificial marking for monitoring wild populations of Australian lizards in the future.
Keywords: Agamidae, biometrics, capture–mark–recapture, citizen science, Monaro grassland earless dragon, population estimates, reptile, skin features, Tympanocryptis.
References
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 |
Bauwens D, Claus K, Mergeay J (2018) Genotyping validates photo-identification by the head scale pattern in a large population of the European adder (Vipera berus). Ecology and Evolution 8, 2985-2992.
| Crossref | Google Scholar |
Beekmans BWPM, Whitehead H, Huele R, Steiner L, Steenbeek AG (2005) Comparison of two computer-assisted photo-identification methods applied to sperm whales (Physeter macrocephalus). Aquatic Mammals 31, 243-247.
| Crossref | Google Scholar |
Bendik NF, Morrison TA, Gluesenkamp AG, Sanders MS, O’Donnell LJ (2013) Computer-assisted photo identification outperforms visible implant elastomers in an endangered salamander, Eurycea tonkawae. PLoS ONE 8, e59424.
| Crossref | Google Scholar |
Bloch N, Irschick DJ (2005) Toe-clipping dramatically reduces clinging performance in a pad-bearing lizard (Anolis carolinensis). Journal of Herpetology 39, 288-293.
| Crossref | Google Scholar |
Börger L (2016) EDITORIAL: Stuck in motion? Reconnecting questions and tools in movement ecology. Journal of Animal Ecology 85, 5-10.
| Crossref | Google Scholar |
Cadena V, Rankin K, Smith KR, Endler JA, Stuart-Fox D (2018) Temperature-induced colour change varies seasonally in bearded dragon lizards. Biological Journal of the Linnean Society 123, 422-430.
| Crossref | Google Scholar |
Carlström D, Edelstam C (1946) Methods of marking reptiles for identification after recapture. Nature 158, 748-749.
| Crossref | Google Scholar |
Carretero MA, Ajtíc R, Tomović L, Crnobrnja-Isailovic J (2008) Evidence for post-natal instability of head scalation in the meadow viper (Vipera ursinii) – patterns and taxonomic implications. Amphibia-Reptilia 29, 61-70.
| Crossref | Google Scholar |
Castro ALF, Rosa RS (2005) Use of natural marks on population estimates of the nurse shark, Ginglymostoma cirratum, at Atol das Rocas Biological Reserve, Brazil. Environmental Biology of Fishes 72, 213-221.
| Crossref | Google Scholar |
Castrucci AMD, Sherbrooke WC, Zucker N (1997) Regulation of physiological color change in dorsal skin of male tree lizards Urosaurus ornatus. Herpetologica 53, 405-410.
| Google Scholar |
Dickinson JL, Zuckerberg B, Bonter DN (2010) Citizen science as an ecological research tool: challenges and benefits. Annual Review of Ecology, Evolution, and Systematics 41, 149-172.
| Crossref | Google Scholar |
Dimond WJ, Osborne WS, Evans MC, Gruber B, Sarre SD (2012) Back to the brink: population decline of the endangered grassland earless dragon (Tympanocryptis pinguicolla) following its rediscovery. Herpetological Conservation and Biology 7, 132-149.
| Google Scholar |
Gamble L, Ravela S, McGarigal K (2008) Multi-scale features for identifying individuals in large biological databases: an application of pattern recognition technology to the marbled salamander Ambystoma opacum. Journal of Applied Ecology 45, 170-180.
| Crossref | Google Scholar |
Gardiner RZ, Doran E, Strickland K, Carpenter-Bundhoo L, Frère C (2014) A face in the crowd: a non-invasive and cost effective photo-identification methodology to understand the fine scale movement of eastern water dragons. PLoS ONE 9, e96992.
| Crossref | Google Scholar |
Gibbons WJ, Andrews KM (2004) Pit tagging: simple technology at its best. Bioscience 54, 447-454.
| Crossref | Google Scholar |
Gollan J, de Bruyn LL, Reid N, Wilkie L (2012) Can volunteers collect data that are comparable to professional scientists? A study of variables used in monitoring the outcomes of ecosystem rehabilitation. Environmental Management 50, 969-978.
| Crossref | Google Scholar |
Gould J, Callen A, Maynard C, Knibb G, Mcgregor J, Gill L, Sanders S, Davies B, Schmahl K, Donelly R, Turner A, Mchenry C (2021a) Standing out in a crowd: intraspecific variability in dorsal patterning allows for photo-identification of a threatened anuran. Austral Ecology 46, 1383-1391.
| Crossref | Google Scholar |
Gould J, Clulow J, Clulow S (2021b) Using citizen science in the photo-identification of adult individuals of an amphibian based on two facial skin features. PeerJ 9, e11190.
| Crossref | Google Scholar |
Gould J, Taylor J, Davies B, Donelly R, Schmahl K, Bugir CK, Beranek CT, McGregor J, Mahony SV, Seeto R, Upton R, McHenry C, Callen A (2023) Tadpole fingerprinting: using tail venation patterns to photo-identify tadpole individuals of a threatened frog. Austral Ecology 48, 585-599.
| Crossref | Google Scholar |
Guimaraes M, Corrêa DT, Filho SS, Oliveira TAL, Doherty PF, Jr, Sawaya RJ (2014) One step forward: contrasting the effects of toe clipping and pit tagging on frog survival and recapture probability. Ecology and Evolution 4, 1480-1490.
| Crossref | Google Scholar |
Hoefer S, Rotger A, Mills S, Robinson NJ (2021) Semi-automated photo-identification of Bahamian racers (Cubophis vudii vudii). Acta Herpetologica 16, 133-136.
| Crossref | Google Scholar |
Hohnen R, Ashby J, Tuft K, McGregor H (2013) Individual identification of northern quolls (Dasyurus hallucatus) using remote cameras. Australian Mammalogy 35, 131-135.
| Crossref | Google Scholar |
Hudson S (1996) Natural toe loss in southeastern Australian skinks: implications for marking lizards by toe-clipping. Journal of Herpetology 30, 106-110.
| Crossref | Google Scholar |
Jones MD, Marshall BM, Smith SN, Christie JT, Waengsothorn S, Artchawakom T, Suwanwaree P, Strine CT (2020) Can post-capture photographic identification as a wildlife marking technique be undermined by observer error? A case study using king cobras in northeast Thailand. PLoS ONE 15, e0242826.
| Crossref | Google Scholar |
Karanth KU, Nichols JD (1998) Estimation of tiger densities in India using photographic captures and recaptures. Ecology 79, 2852-2862.
| Crossref | Google Scholar |
Kenyon N, Phillott AD, Alford RA (2009) Evaluation of the photographic identification method (pim) as a tool to identify adult Litoria genimaculata (anura: Hylidae). Herpetological Conservation and Biology 4, 403-410.
| Google Scholar |
Kühl HS, Burghardt T (2013) Animal biometrics: quantifying and detecting phenotypic appearance. Trends in Ecology & Evolution 28, 432-441.
| Crossref | Google Scholar |
Lenth R, Singmann H, Love J, Buerkner P, Herve M (2018) Package ‘emmeans’. Available at https://cran.r-project.org/web/packages/emmeans/index.html
Madani G, Pietsch R, Beranek CT (2023) Where are my dragons? Replicating refugia to enhance the detection probability of an endangered cryptic reptile. Acta Oecologica 119, 103910.
| Crossref | Google Scholar |
Marshall AD, Pierce SJ (2012) The use and abuse of photographic identification in sharks and rays. Journal of Fish Biology 80, 1361-1379.
| Crossref | Google Scholar |
May RM (2004) Ethics and amphibians. Nature 431, 403.
| Crossref | Google Scholar |
McCarthy MA, Parris KM (2004) Clarifying the effect of toe clipping on frogs with Bayesian statistics. Journal of Applied Ecology 41, 780-786.
| Crossref | Google Scholar |
Melville J, Chaplin K, Hutchinson M, Sumner J, Gruber B, MacDonald AJ, Sarre SD (2019) Taxonomy and conservation of grassland earless dragons: new species and an assessment of the first possible extinction of a reptile on mainland Australia. Royal Society Open Science 6, 190233.
| Crossref | Google Scholar |
Middelburg JJM, Strijbosch H (1988) The reliability of the toe clipping method with the common lizard (Lacerta vivipara). Herpetological Journal 1, 291-293.
| Google Scholar |
O’Shea M (2017) Identification of individual striped legless lizards Delma impar using the dorsal head scale pattern. The Victorian Naturalist 134, 177-186.
| Google Scholar |
Powell RA, Proulx G (2003) Trapping and marking terrestrial mammals for research: integrating ethics, performance criteria, techniques, and common sense. ILAR Journal 44, 259-276.
| Crossref | Google Scholar |
Renet J, Guillaud F, Xeres A, Brichard J, Baudat-Franceschi J, Rosa G (2021) Assessing reliability of pit-tagging in an endangered fossorial toad (Pelobates cultripes) and its effect on individual body mass. Herpetological Conservation and Biology 16, 584-593.
| Google Scholar |
Robbins R, McKone E (2007) No face-like processing for objects-of-expertise in three behavioural tasks. Cognition 103, 34-79.
| Crossref | Google Scholar |
Sacchi R, Scali S, Fasola M, Galeotti P (2007) The numerical encoding of scale morphology highly improves photographic identification in lizards. Acta Herpetologica 2, 27-35.
| Crossref | Google Scholar |
Sacchi R, Scali S, Pellitteri-Rosa D, Pupin F, Gentilli A, Tettamanti S, Cavigioli L, Racina L, Maiocchi V, Galeotti P, Fasola M (2010) Photographic identification in reptiles: a matter of scales. Amphibia-Reptilia 31, 489-502.
| Crossref | Google Scholar |
Schmidt K, Schwarzkopf L (2010) Visible implant elastomer tagging and toe-clipping: effects of marking on locomotor performance of frogs and skinks. The Herpetological Journal 20, 99-105.
| Google Scholar |
Shine C, Shine N, Shine R, Slip D (1988) Use of subcaudal scale anomalies as an aid in recognizing individual snakes. Herpetological Review 19, 79-80.
| Google Scholar |
Smith S, Young T, Skydmore D (2018) Effectiveness of the field identification of individual natterjack toads (Epidalea calamita) using comparisons of dorsal features through citizen science. Herpetological Journal 28, 31-38.
| Google Scholar |
Speed CW, Meekan MG, Bradshaw CJA (2007) Spot the match – wildlife photo-identification using information theory. Frontiers in Zoology 4, 2.
| Crossref | Google Scholar |
Sreekar R, Purushotham CB, Saini K, Rao SN, Pelletier S, Chaplod S (2013) Photographic capture–recapture sampling for assessing populations of the Indian gliding lizard Draco dussumieri. PLoS ONE 8, e55935.
| 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, 76-84.
| Crossref | Google Scholar |
Swanson A, Kosmala M, Lintott C, Packer C (2016) A generalized approach for producing, quantifying, and validating citizen science data from wildlife images. Conservation Biology 30, 520-531.
| Crossref | Google Scholar |
Taggart PL, Morris S, Caraguel CG (2021) The impact of PIT tags on the growth and survival of pythons is insignificant in randomised controlled trial. PeerJ 9, e11531.
| Crossref | Google Scholar |
Tanaka JW, Taylor M (1991) Object categories and expertise: is the basic level in the eye of the beholder? Cognitive Psychology 23, 457-482.
| Crossref | Google Scholar |
Town C, Marshall A, Sethasathien N (2013) Manta matcher: automated photographic identification of manta rays using keypoint features. Ecology and Evolution 3, 1902-1914.
| Crossref | Google Scholar |
Unger SD, Burgmeier NG, Williams RN (2012) Genetic markers reveal high PIT tag retention rates in giant salamanders (Cryptobranchus alleganiensis). Amphibia-Reptilia 33, 313-317.
| Crossref | Google Scholar |
Winne CT, Willson JD, Andrews KM, Reed RN (2006) Efficacy of marking snakes with disposable medical cautery units. Herpetological Review 37, 52-54.
| Google Scholar |
Zemanova MA (2020) Towards more compassionate wildlife research through the 3Rs principles: moving from invasive to non-invasive methods. Wildlife Biology 2020, 1-17.
| Crossref | Google Scholar |
