Skip to main content
SpringerLink
Log in

Excellent performances of dogs to detect cryptic tortoises in Mediterranean scrublands

Biodiversity and Conservation volume 28, pages 4027–4045 (2019)Cite this article

Abstract

Mediterranean ecosystems are severely impacted by urbanization, habitat clearing, fires and landscape fragmentation; conservation actions are urgently needed. The protection status of a given area depends notably on the presence and detection rate of protected species. Further, habitat restoration, conservation translocations, or population reinforcement require precise information on the distribution of individuals. Thus, the success of important conservation measures relies on the capacity to locate individuals. Thanks to their sense of smell combined with high learning abilities, dogs have been used to track a wide range of biological targets. They generally surpass humans to detect cryptic species. In this study, we aimed at testing their detection performances with Hermann’s tortoises. This secretive reptile provides a typical case of threatened Mediterranean species where protection actions are hampered by low detection rates; especially because low population densities increase the risk of false negative results during surveys. The ability to detect and save individuals, for example before destructive land-work, might be crucial. We evaluated the detection ability of dogs to find tortoises with two experiments. First, field trials showed that relative detection rate was three times higher in dogs compared to well-trained humans. Then, and more importantly, the absolute detection rate of dogs to find radio tracked tortoises was excellent: after two trials, dogs rapidly located all the experimental tortoises dissimulated along different field transects. Overall, dogs were very efficient in finding tortoises, especially well-hidden individuals. More generally, the immense potential of trained dogs should be extended to improve the techniques to detect and protect Mediterranean reptiles.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

39,95 €

Price includes VAT (Netherlands)

Fig. 1
Fig. 2
Fig. 3
Fig. 4

References

  • Arsovski D, Tomović L, Golubović A, Nikolić S, Sterijovski B, Ajtić R, Ballouard JM, Bonnet X (2018) When carapace governs size: variation among age classes and individuals in a free-ranging ectotherm with delayed maturity. Oecologia 186(4):953–963

    PubMed  Google Scholar 

  • Badiane A, Matos C, Santos X (2017) Uncovering environmental, land-use and fire effects on the distribution of a low-dispersal species, the Hermann’s tortoise Testudo hermanni. Amphibia-Reptilia 38(1):67–77

    Google Scholar 

  • Ballouard J-M, Caron S, Lafon T, Servant L, Devaux B, Bonnet X (2013) Fibrocement slabs as useful tools to monitor juvenile reptiles: a study in a tortoise species. Amphibia-Reptilia 34(1):1–10

    Google Scholar 

  • Ballouard J-M, Bonnet X, Gravier C, Ausanneau M, Caron S (2016) Artificial water ponds and camera trapping of tortoises, and other vertebrates, in a dry Mediterranean landscape. Wildlife R 43(7):533–543

    Google Scholar 

  • Bates D, Maechler M, Bolker BS, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67(1):1–48

    Google Scholar 

  • Benhamou S (2004) How to reliably estimate the tortuosity of an animal’s path: straightness, sinuosity, or fractal dimension? J Theor Biol 229(2):209–220

    PubMed  Google Scholar 

  • Bertolero A, Cheylan M, Hailey A, Livoreil B, Willemsen RE (2011) Testudo hermanni (Gmelin 1789)—Hermann’s tortoise. Conservation biology of freshwater turtles and tortoises: a compilation project of the IUCN/SSC Tortoise and Freshwater Turtle Specialist Group. Chelonian Research Monographs 5:059

    Google Scholar 

  • Boers K, Leister K, Byrd J, Band M, Phillips CA, Allende MC (2017) Capture effort, rate, demographics, and potential for disease transmission in wild eastern box turtles (Terrapene Carolina carolina) captured through canine directed searches. Herpetol Rev 48(2):300–304

    Google Scholar 

  • Bonnet X, Golubović A, Arsovski D, Đorđević S, Ballouard J-M, Sterijovski B, Ajtić R, Barbraud D, Tomović L (2016) A prison effect in a wild population: a scarcity of females induces homosexual behaviors in males. Behav Ecol 27(4):1206–1215

    Google Scholar 

  • Cablk ME, Heaton JS (2006) Accuracy and reliability of dogs in surveying for desert tortoise (Gopherus agassizii). Ecol Appl 16(5):1926–1935

    PubMed  Google Scholar 

  • Cablk ME, Sagebiel JC, Heaton JS, Valentin C (2008) Olfaction-based detection distance: a quantitative analysis of how far away dogs recognize tortoise odor and follow it to source. Sensors 8(4):2208–2222

    PubMed  Google Scholar 

  • Celse J, Roux A, Guyon B, Catard A, Caron S, Ballouard J-M, Cheylan M, Bosc V, Daniel G (2018) Second Plans national d’actions en faveur de la Tortue d’Hermann 2018–2027. Ministère de la Transition Ecologique et Solidaire, Paris La défense

    Google Scholar 

  • Chelazzi G, Francisci F (1979) Movement patterns and homing behaviour of Testudo hermanni Gmelin (Reptilia Testudinidae). Monit Zool Ital 13:105–127

    Google Scholar 

  • Couturier T, Cheylan M, Guérett E, Besnard A (2011) Impacts of a wildfire on the mortality rate and small-scale movements of a Hermann’s tortoise Testudo hermanni hermanni population in south eastern France. Amphibia-Reptilia 32(4):541–545

    Google Scholar 

  • Couturier T, Cheylan M, Bertolero A, Astruc G, Besnard A (2013) Estimating abundance and population trends when detection is low and highly variable: a comparison of three methods for the Hermann’s tortoise. J Wildlife Manage 77(3):454–462

    Google Scholar 

  • Couturier T, Besnard A, Bertolero A, Bosc V, Astruc G, Cheylan M (2014) Factors determining the abundance and occurrence of Hermann’s tortoise Testudo hermanni in France and Spain: fire regime and landscape changes as the main drivers. Biol Conserv 170:177–187

    Google Scholar 

  • Craven BA, Paterson EG, Settles GS (2009) The fluid dynamics of canine olfaction: unique nasal airflow patterns as an explanation of macrosmia. J R Soc Interface. https://doi.org/10.1098/rsif20090490

    Article  PubMed  PubMed Central  Google Scholar 

  • Cristescu RH, Foley E, Markula A, Jackson G, Jones D, Frère C (2015) Accuracy and efficiency of detection dogs: a powerful new tool for koala conservation and management. Sci Rep 5:8349

    PubMed  PubMed Central  Google Scholar 

  • Fahrig L, Merriam G (1994) Conservation of fragmented populations. Conserv Biol 8(1):50–59

    Google Scholar 

  • Fraser JL, Thompson GG, Moro D (2003) Adequacy of terrestrial fauna surveys for the preparation of Environmental Impact Assessments in the mining industry of Western Australia. Ecol Manag Restor 4(3):187–192

    Google Scholar 

  • Freilich JE, LaRue EL (1998) Importance of observer experience in finding desert tortoises. J Wildlife Manage 62(2):590–596

    Google Scholar 

  • Gagno S, Jardé N, Marchis N, Ballouard J-M (2013) Pressions anthropiques subies par les chéloniens dans le Var, Testudo hermanni (Gmelin, 1789) et Emys orbicularis (Linnaeus, 1758): premier retour d’un centre de soins de la faune sauvage. Bul Société Herp de France 145:157–168

    Google Scholar 

  • Germano JM, Field KJ, Griffiths RA, Clulow S, Foster J, Harding G, Swaisgood RR (2015) Mitigation-driven translocations: are we moving wildlife in the right direction? Front Ecol Enviro 13(2):100–105

    Google Scholar 

  • Glen A, Veltman CJ (2018) Search strategies for conservation detection dogs. Wildlife Biol. https://doi.org/10.2981/wlb-00393

    Article  Google Scholar 

  • González-Varo JP, Arroyo J, Aparicio A (2009) Effects of fragmentation on pollinator assemblage, pollen limitation and seed production of Mediterranean myrtle (Myrtus communis). Biol Conserv 142(5):1058–1065

    Google Scholar 

  • Gsell A, de Monchy IJ, Brunton D (2010) The success of using trained dogs to locate sparse rodents in pest-free sanctuaries. Wildlife R 37(1):39–46

    Google Scholar 

  • Hailey A (1989) How far do animals move? Routine movements in a tortoise. Can J Zool 67(1):208–215

    Google Scholar 

  • Heaton JS, Cablk ME, Nussear KE, Esque TC, Medica PA, Sagebiel JC, Francis SS (2008) Comparison of effects of humans versus wildlife-detector dogs. South West Nat 53(4):472–479

    Google Scholar 

  • Hofmeyr MD, Henen BT (2016) Terrestrial turtles and tortoises. In: Dodd CK Jr (ed) Reptile ecology and conservation. A handbook of techniques. Oxford University Press, New York

    Google Scholar 

  • Hudson V (2013) Fynbos Forum. In: Smith D (ed) The development of a conservation detection dog team as an additional tool to survey geometric tortoises. Kirtsenbosch, Cape Town, pp 175–194

    Google Scholar 

  • Hurt A, Smith DA (2009) Conservation dogs. In: Smith D (ed) Canine ergonomics: the science of working dogs. CRC Press, Boca Raton, pp 175–194

    Google Scholar 

  • IUCN, MNHN, SHF (2015) La liste rouge des espèces menace´es en France-Reptiles et Amphibiens de France métropolitaine. France, Paris

    Google Scholar 

  • Kapfer JM, Munoz DJ, Tomasek T (2012) Use of wildlife detector dogs to study Eastern Box Turtle (Terrapene Carolina carolina) populations. Herpetol Conserv Biol 7(2):169–175

    Google Scholar 

  • Lagarde F, Louzizi T, Slimani T, El Mouden H, Kaddour KB, Moulherat S, Bonnet X (2012) Bushes protect tortoises from lethal overheating in arid areas of Morocco. Environ Conserv J 39(2):172–182

    Google Scholar 

  • Lecq S, Ballouard J-M, Caron S, Livoreil B, Seynaeve V, Matthieu LA, Bonnet X (2014) Body condition and habitat use by Hermann’s tortoises in burnt and intact habitats. Conserv Physiol. https://doi.org/10.1093/conphys/cou019

    Article  PubMed  PubMed Central  Google Scholar 

  • Leigh KA, Dominick M (2015) An assessment of the effects of habitat structure on the scat finding performance of a wildlife detection dog. Methods Ecol Evol 6(7):745–752

    Google Scholar 

  • Lepeigneul O, Ballouard J-M, Bonnet X, Beck E, Barbier M, Ekori A, Buisson E, Caron S (2014) Immediate response to translocation without acclimation from captivity to the wild in Hermann’s tortoise. Eur J Wildlife Res 60(6):897–907

    Google Scholar 

  • Livoreil B (2009) Distribution of the endangered Hermann’s tortoise Testudo hermanni hermanni in Var, France, and recommendations for its conservation. Oryx 43(02):299–305

    Google Scholar 

  • Loehr VJ (2017) Unexpected decline in a population of speckled tortoises. J Wildlife Manage 81(3):470–476

    Google Scholar 

  • Lovich JE, Ennen JR, Agha M, Gibbons JW (2018) Where have all the turtles gone, and why does it matter? Bioscience 68(10):771–781

    Google Scholar 

  • Luiselli L, Capula M, Burke RL, Rugiero L, Capizzi D (2014) Sighting frequency decreases over two decades in three populations of Testudo hermanni from central Italy. Biodiv Cons 23(12):3091–3100

    Google Scholar 

  • MacKenzie DI (2005) What are the issues with presence–absence data for wildlife managers? J Wildl Manage 69:849–860

    Google Scholar 

  • Marchal S, Bregeras O, Puaux D, Gervais R, Ferry B (2016) Rigorous training of dogs leads to high accuracy in human scent matching-to-sample performance. PLoS ONE 11(2):e0146963

    PubMed  PubMed Central  Google Scholar 

  • Matthews A, Lunney D, Gresser S, Maitz W (2016) Movement patterns of koalas in remnant forest after fire. Aust Mammal 38(1):91–104

    Google Scholar 

  • Mc Cormack (2010) Training detection dogs for research and conservation of tortoises and freshwater turtle in Southeast Asia. Turtle Surv Alliance Mag 22:70–72

    Google Scholar 

  • Mc Culloch M, Jezierski T, Broffman M, Hubbard A, Turner K, Janecki T (2006) Diagnostic accuracy of canine scent detection in early-and late-stage lung and breast cancers. Integr Cancer Ther 5(1):30–39

    Google Scholar 

  • Meyer CF, Kalko EK, Kerth G (2009) Small-scale fragmentation effects on local genetic diversity in two Phyllostomid bats with different dispersal abilities in Panama. Biotropica 41(1):95–102

    Google Scholar 

  • Moulherat S, Delmas V, Slimani T, Louzizi T, Lagarde F, Bonnet X (2014) How far can a tortoise walk in open habitat before overheating? Implications for conservation. J Nat Conserv 22(2):186–192

    Google Scholar 

  • Nielsen TP, Jackson G, Bull CM (2016) A nose for lizards; can a detection dog locate the endangered pygmy bluetongue lizard (Tiliqua adelaidensis)? Trans R Soc S Aust 140(2):234–243

    Google Scholar 

  • Nussear KE, Esque TC, Heaton JS, Cablk ME, Drake KK, Valentin C, Yee JL, Medica PA (2008) Are wildlife detector dogs or people better at finding desert tortoises (Gopherus Agassizii)? Herp Cons Bio 3(1):103–115

    Google Scholar 

  • Orkin JD, Yang Y, Yang C, Douglas WY, Jiang X (2016) Cost-effective scat-detection dogs: unleashing a powerful new tool for international mammalian conservation biology. Sci Rep 6:34758

    PubMed  PubMed Central  CAS  Google Scholar 

  • Pfiester M, Koehler PG, Pereira RM (2008) Ability of bed bug-detecting canines to locate live bed bugs and viable bed bug eggs. J Econ Entomol 101(4):1389–1396

    PubMed  Google Scholar 

  • Pille F, Caron S, Bonnet X, Deleuze S, Busson D, Etien T, Girard F, Ballouard J-M (2018) Settlement pattern of tortoises translocated into the wild: a key to evaluate population reinforcement success. Biodiv Conserv 27(2):437–457

    Google Scholar 

  • Platt SG, Ko WK, Khaing LL, Myo KM, Sw T, Lwin T, Rainwater TR (2003) Population status and conservation of the critically endangered Burmese star tortoise Geochelone platynota in central Myanmar. Oryx 37(04):464–471

    Google Scholar 

  • Quétier F, Lavorel S (2011) Assessing ecological equivalence in biodiversity offset schemes: key issues and solutions. Biol Conserv 144(12):2991–2999

    Google Scholar 

  • R Core Team (2016) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. https://www.R-project.org/

  • Reed SE, Bidlack AL, Hur A, Getz WM (2011) Detection distance and environmental factors in conservation detection dog surveys. J Wildlife Manage 75(1):243–251

    Google Scholar 

  • Rhodin AG, Stanford CB, van Dijk PP, Eisemberg C, Luiselli L, Mittermeie et al (2018) Global conservation status of turtles and tortoises (Order Testudines). Chelonian Conserv Bio 17(2):135–161

    Google Scholar 

  • Roberge JM, Angelstam PER (2004) Usefulness of the umbrella species concept as a conservation tool. Conserv Biol 18(1):76–85

    Google Scholar 

  • Salvati L, Sateriano A, Bajocco S (2013) To grow or to sprawl? Land Cover Relationships in a Mediterranean City Region and implications for land use management. Cities 30:113–121

    Google Scholar 

  • Santos T, Tellería JL, Virgós E (1999) Dispersal of Spanish juniper Juniperus thurifera by birds and mammals in a fragmented landscape. Ecography 22(2):193–204

    Google Scholar 

  • Savidge JA, Stanford JW, Reed RN, Haddock GR, Adams AY (2011) Canine detection of free-ranging brown treesnakes on Guam. N Z J Ecol 35(2):174–181

    Google Scholar 

  • Seddon PJ, Griffiths CJ, Soorae S, Armstrong DP (2014) Reversing defaunation: restoring species in a changing world. Science 345(6195):406–412

    PubMed  CAS  Google Scholar 

  • Smith DA, Ralls KA, Hurt B, Adams M, Parker B, Davenport MC, Smith JE, Maldonado (2003) Detection and accuracy rates of dogs trained to find scats of San Joaquin Kit Foxes (Vulpes macrotismutica). Anim Conser 6:339–346

    Google Scholar 

  • Stevenson DJ, Ravenscroft KR, Zappalorti RT, Ravenscroft MD, Weigley SW, Jenkins CL (2010) Using a wildlife detector dog for locating eastern indigo snakes (Drymarchon couperi). Herp Review 41(4):437–442

    Google Scholar 

  • Terhune TM, Sisson DC, PalmeWE Faircloth BC, Stribling HL, Carroll JP (2010) Translocation to a fragmented landscape: survival, movement, and site fidelity of northern bobwhites. Ecol Appl 20(4):1040–1052

    PubMed  Google Scholar 

  • Woollett DAS, Hurt A, Richards NL (2013) The current and future roles of free-ranging detection dogs in conservation efforts. In: Gomper M (ed) Free-ranging dogs and wildlife conservation, p 239

    Google Scholar 

  • Zylstra ER, Steidl RJ, Swann DE (2010) Evaluating survey methods for monitoring a rare vertebrate, the Sonoran desert tortoise. J Wildlife Manag 74(6):1311–1318

    Google Scholar 

Download references

Acknowledgments

We thank the CEN PACA, CAVEM and Conseil General 83 for their collaboration and providing accessibility to the study sites. We warmly thank the human prospectors notably Geoffrey Gillet, Vincent Danias, Nicolas, Delphine Buisson and Thibaut Lafon. We thank Fabien Pille and Laura Andreo for his help to perform analyses and cartography. This study conducted under the permits 83-2012/08 and 83-2012/09 issued by prefectural authorities and DDTM.

Author information

Authors and Affiliations

  1. CRCC Centre for Research and Conservation of Chelonians, SOPTOM, Var, Gonfaron, France

    Ballouard Jean-Marie & Caron Sébastien

  2. TestuDOg, 193 Chemin de Peyblou, Callas, France

    Gayraud Raphael

  3. CAVEM, Communauté d’agglomération Var Estérel Méditerranée, Saint-Raphael, France

    Rozec Fabien

  4. CNRS, UM, SupAgro, IRD, INRA, UMR 5175 CEFE, EPHE, PSL Research University, 34293, Montpellier, France

    Besnard Aurélien

  5. Laboratoire Ecologie et Biologie des Interactions, UMR CNRS 7267, Equipe ‘Ecologie, Evolution, Symbiose’, Université de Poitiers, Poitiers, France

    Bech Nicolas

  6. CEBC, UMR-7372, CNRS-Université de La Rochelle, La Rochelle, France

    Bonnet Xavier

Authors
  1. Ballouard Jean-Marie
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Gayraud Raphael
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Rozec Fabien
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Besnard Aurélien
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Caron Sébastien
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Bech Nicolas
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Bonnet Xavier
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Ballouard Jean-Marie.

Additional information

Communicated by Dirk Sven Schmeller.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and Permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Jean-Marie, B., Raphael, G., Fabien, R. et al. Excellent performances of dogs to detect cryptic tortoises in Mediterranean scrublands. Biodivers Conserv 28, 4027–4045 (2019). https://doi.org/10.1007/s10531-019-01863-z

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10531-019-01863-z

Keywords

  • Detection effectiveness
  • Hermann tortoise
  • Land management
  • Reptiles
  • Wildlife detection

Search

Navigation