Skip to main content
SpringerLink
Log in

Settlement pattern of tortoises translocated into the wild: a key to evaluate population reinforcement success

  • Original Paper
  • Published:
Biodiversity and Conservation Aims and scope Submit manuscript

Abstract

A lack of long-term monitoring often impedes the evaluation of translocation used to reinforce populations. Crucial questions regarding the exact timing and place of possible settlement remain unanswered. To examine these issues we radio-tracked during three years 24 tortoises (Testudo hermanni hermanni) released to reinforce a resident population impacted by fire. Individuals from the resident population (N = 20) and from a distant control population (N = 11) were also radio-tracked. More than 11,000 fixes were collected, enabling us to precisely describe movement patterns. Most translocated tortoises first dispersed (> 500 m to > 3000 m away) in a random direction and sometimes crossed unfavorable areas. Later, a marked shift in movement pattern, from a relatively unidirectional course to multidirectional displacements indicated settlement. Movement patterns of translocated and resident individuals became undistinguishable after settlement. Most individuals settled during the first year after release but several settled in the second year. Mean annual survival rate (> 85%) remained within the range of the species but was lower compared to the resident (93%) and control tortoises (100%). Overall, most translocated individuals (~ 63%) settled and adapted well to their novel environment. This result is essential regarding current controversies that are unfounded and that limit conservation translocations. Yet, translocation sites should be large enough and/or surrounded by secondary favorable areas to limit the mortality associated with dispersal in hazardous environments. Large numbers of individuals rescued during urbanization works may easily supply conservation translocations to reinforce fragile populations.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Aragón P, Clobert J, Massot M (2006) Individual dispersal status influences space use of conspecific residents in the common lizard, Lacerta vivipara. Behav Ecol Sociobiol 60:430–438

    Article  Google Scholar 

  • Armstrong DP, Castro I, Alley JC, Feenstra B, Perrott JK (1999) Mortality and behaviour of hihi, an endangered New Zealand honeyeater, in the establishment phase following translocation. Biol Conserv 89:329–339

    Article  Google Scholar 

  • Attum O, Cutshall CD (2015) Movement of translocated turtles according to translocation method and habitat structure. Restor Ecol 23:588–594

    Article  Google Scholar 

  • Attum O, Rabia B (2016) Movement patterns of soft released, translocated Egyptian tortoises. J Arid Environ 134:62–65

    Article  Google Scholar 

  • Attum O, Esawy MM, Farag WE, Gad AE, Baha El Din SM, Kingsbury B (2007) Returning them back to the wild: movement patterns of repatried Egyptian tortoises, Testudo kleinmanni Lortet, 1883 (Sauropsida: Testudinidae). Zool Middle East 41:35–40

    Article  Google Scholar 

  • Attum O, Farag W, Baha El Din SM, Kingsbury B (2010) Retention rate of hard-released translocated Egyptian tortoises Testudo kleinmanni. Endanger Species Res 12:11–15

    Article  Google Scholar 

  • Attum O, Otoum M, Amr Z, Tietjen B (2011) Movement patterns and habitat use of soft-released translocated spur-thighed tortoises, Testudo graeca. Eur J Wildl Res 57:251–258

    Article  Google Scholar 

  • Ayres RM, Nicol MD, Raadik TA (2012) Establishing new populations for fire-affected Barred Galaxias (Galaxias fuscus): site selection, trial translocation and population genetics. Black Saturday Victoria 2009—natural values fire recovery program. Department of Sustainability

  • Baker J, Bain D, Clarke J, French K (2012) Translocation of the eastern bristlebird 2: applying principles to two case studies. Ecol Manag Restor 13:159–165

    Article  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 34:1–10

    Article  Google Scholar 

  • Ballouard J-M, Deleuze S, Caron S (2014). Rapport final E2/C7: evaluation de l’impact des translocations expérimentales. Projet no LIFE 08NAT/F/000475

  • 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. Wildl Res. doi:10.1071/WR16035

    Google Scholar 

  • Bauder JM, Castellano C, Jensen JB, Stevenson DJ, Jenkins CL (2014) Comparison of movements, body weight, and habitat selection between translocated and resident gopher tortoises. J Wildl Manag 78:1444–1455

    Article  Google Scholar 

  • Berry KH (1986) Desert tortoise Gopherus agassizii relocation: implications of social behavior and movements. Herpetologica 42:113–125

    Google Scholar 

  • Bertolero A, Oro D (2009) Conservation diagnosis of reintroducing Mediterranean pond turtles: what is wrong ? Anim Conserv 12:581–591

    Article  Google Scholar 

  • Bertolero A, Oro D, Besnard A (2007) Assessing the efficacy of reintroduction programmes by modelling adult survival: the example of Hermann’s tortoise. Anim Conserv 10:360–368

    Article  Google Scholar 

  • Bertolero A, Cheylan M, Hailey A, Livoreil B, Willemsen R (2011) Testudo hermanni (Gmelin 1789) Hermann’s tortoise. In Rhodin A, Pritchard P, VanDijk P, Saumure R, Buhlmann K, Iverson J, Mittermeier R (eds) Conservation biology of freshwater turtles and tortoises: a compilation project of the IUCN/SSC tortoise and fresh- water turtle specialist group, vol 5, Chelonian Research, pp 1–20

  • Böhm M, Collen B, Baillie JE, Bowles P, Chanson J, Cox N, Rhodin AG et al (2013) The conservation the world’s reptiles. Biol Conserv 157:372–385

    Article  Google Scholar 

  • Bradley DW, Molles LE, Valderrama SV, King S, Waas JR (2012) Factors affecting post-release dispersal, mortality, and territory settlement of endangered kokako translocated from two distinct song neighborhoods. Behav Ecol 24:570–578

    Article  Google Scholar 

  • Bright PW, Morris PA (1994) Animal translocation for conservation: performance of dormice in relation to release methods, origin and season. J Appl Ecol 31:699–708

    Article  Google Scholar 

  • Calvete C, Estrada R (2004) Short-term survival and dispersal of translocated European wild rabbits. Improving the release protocol. Biol Conserv 120:507–516

    Article  Google Scholar 

  • Celse J, Catard A, Caron S, Ballouard J-M, Gagno S, Jardé N, Cheylan M, Astruc G, Croquet V, Bosc M et al (2014) Guide de gestion des populations et des habitats de la Tortue d’Hermann. LIFE 08 NAT/F/000475. ARPE PACA

  • Champagnon J, Elmberg J, Guillemain M, Gauthier-Clerc M, Lebreton J-D (2012) Conspecifics can be aliens too: a review of effects of restocking practices in vertebrates. J Nat Conserv 20:231–241

    Article  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 

  • Christie K, Craig MD, Stokes VL, Hobbs RJ (2011) Movement patterns by Egernia napoleonis following reintroduction into restored jarrah forest. Wildl Res 38:475–481

    Article  Google Scholar 

  • Clarke MF, Schedvin N (1997) An experimental study of the translocation of noisy miners Manoria melanocephala and difficulties associated with dispersal. Biol Conserv 80:161–167

    Article  Google Scholar 

  • Claussen DL, Finkler MS, Smith MM (1997) Thread trailing of turtles: methods for evaluating spatial movements and pathway structure. Can J Zool 76:2120–2128

    Article  Google Scholar 

  • Cook RP (2004) Dispersal, home range establishment, survival, and reproduction of translocated eastern box turtles. Terrapene c. carolina. Appl Herp 1:197–228

    Google Scholar 

  • Couturier T, Cheylan M, Guérette 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 southeastern France. Amphibia-Reptilia 32:541–545

    Article  Google Scholar 

  • Cushman SA (2006) Effects of habitat loss and fragmentation on amphibians: a review and prospectus. Biol Conserv 128:231–240

    Article  Google Scholar 

  • de Milliano J, Di Stefano J, Courtney P, Temple-Smith P, Coulson G (2016) Soft-release versus hard-release for reintroduction of an endangered species: an experimental comparison using eastern barred bandicoots (Perameles gunnii). Wildl Res 43:1–12

    Article  Google Scholar 

  • del Mar Delgado, Penteriani V, Nams VO, Campioni L (2009) Changes of movement patterns from early dispersal to settlement. Behav Ecol Sociobiol 64:35–43

    Article  Google Scholar 

  • Dickens MJ, Delehanty DJ, Romero LM (2010) Stress: an inevitable component of animal translocation. Biol Conserv 143:1329–1341

    Article  Google Scholar 

  • Dodd CK, Seigel RA (1991) Relocation, repatriation, and translocation of amphibians and reptiles: are they conservation strategies that work? Herpetologica 47:336–350

    Google Scholar 

  • Eastridge R, Clark JD (2001) Evaluation of 2 soft-release techniques to reintroduce black bears. Wildl Soc Bull 29:1163–1174

    Google Scholar 

  • Estevez I, Christman MC (2006) Analysis of the movement and use of space of animals in confinement: the effect of sampling effort. Appl Anim Behav Sci 97:221–240

    Article  Google Scholar 

  • Field KJ, Tracy CR, Medica PA, Marlow RW, Corn PS (2007) Return to the wild : Translocation as a tool in conservation of the Desert Tortoise (Gopherus agassizii). Biol Conserv 136:232–245

    Article  Google Scholar 

  • Fischer J, Lindenmayer DB (2000) An assessment of the published results of animal relocations. Biol Conserv 96:1–11

    Article  Google Scholar 

  • Germano JM, Bishop PJ (2009) Suitability of amphibians and reptiles for translocation. Conserv Biol 23:7–15

    Article  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Griffith B, Scott J, Carpenter JW, Reed C (1989) Translocation as a species conservation tool: status and strategy. Science 245:477–480

    Article  CAS  PubMed  Google Scholar 

  • Hambler C (1994) Giant tortoise Geochelone gigantea translocation to Curieuse Island (Seychelles): Success or failure? Biol Conserv 69:293–299

    Article  Google Scholar 

  • Hardman B, Moro D (2006) Optimising reintroduction success by delayed dispersal: is the release protocol important for hare-wallabies? Biol Conserv 128:403–411

    Article  Google Scholar 

  • Hinderle D (2011) Desert Tortoises (Gopherus agassizii) and translocation: homing, hehavior, habitat and shell temperature experiments. Dissertation, San Diego University

  • Hinderle D, Lewison RL, Walde AD, Deutschman D, Boarman WI (2015) The effects of homing and movement behaviors on translocation: Desert tortoises in the western Mojave Desert. J Wildl Manag 79:137–147

    Article  Google Scholar 

  • Huot-Daubremont C, Grenot C (1997) Rythme d’activité de la tortue d’Hermann (Testudo hermanni hermanni) en semi-liberté dans le Massif des Maures (VAR). Rev Ecol Terre Vie 52:331–344

    Google Scholar 

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

  • Kaplan EL, Meier P (1958) Nonparametric estimation from incomplete observations. J Am Stat Assoc 53:457–481

    Article  Google Scholar 

  • King R, Berg C, Hay B (2004) A repatriation study of the eastern massasauga (Sistrurus catenatus catenatus) in Wisconsin. Herpetologica 60:429–437

    Article  Google Scholar 

  • Knox CD, Monks JM (2014) Penning prior to release decreases post-translocation dispersal of jewelled geckos. Anim Conserv 17:18–26

    Article  Google Scholar 

  • Lagarde F, Guillon M, Dubroca L, Bonnet X, Ben Kaddour K, Slimani T, El mouden EH (2008) Slowness and acceleration: a new method to quantify the activity budget of chelonians. Anim Behav 75:319–329

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Lambert M (1984) Threats to Mediterranean (West Palaearctic) tortoises and their effects on wild populations: an overview. Amphibia-Reptilia 5:5–15

    Article  Google Scholar 

  • Le Gouar P, Mihoub J-B, Sarrazin F (2012) Dispersal and habitat selection: behavioural and spatial constraints for animal translocations. In: Ewen JG, Armstrong DP, Parker KA, Seddon PJ (eds) Reintroduction biology: integrating science and management. Blackwell, London, pp 223–256

    Google Scholar 

  • Lecq S, Ballouard J-M, Caron S, Livoreil B, Seynaeve V, Matthieu L-A, Bonnet X (2014) Body condition and habitat use by Hermann’s tortoises in burnt and intact habitats. Conserv Physiol 2:1–10

    Article  Google Scholar 

  • Lennartsson T (2002) Extinction thresholds and disrupted plant—pollinator interactions in fragmented plant populations. Ecology 83:3060–3072

    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 Wildl Res 60:897–907

    Article  Google Scholar 

  • Letty J, Marchandeau S, Aubineau J (2007) Problems encountered by individuals in animal translocations: lessons from field studies. Ecoscience 14:420–431

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Madsen T, Shine R, Olsson M, Wittzell H (1999) Conservation biology: restoration of an inbred adder population. Nature 402:34–35

    Article  CAS  Google Scholar 

  • Manly B, McDonald L, Thomas D, MacDonald T, Erickson W (2002) Resource selection by animals. Statistical design and analysis for field studies. Kluwer Academic Publisher, Dordrecht

    Google Scholar 

  • Micheli G, Caron S, Michel CL, Ballouard J-M (2014) Le comportement anti-prédateur de la tortue d’Hermann, Testudo hermanni hermanni Gmelin, 1789, est-il altéré après un long séjour en semi-captivité ? Bull Soc Herp Fr 152:1–12

    Google Scholar 

  • Moran PAP (1950) A test for the serial independence of residuals. Biometrika 37:178–181

    Article  CAS  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Nafus MG, Esque TC, Averill-Murray RC, Nussear KE, Swaisgood RR (2016) Habitat drives dispersal and survival of translocated juvenile desert tortoises. J Appl Ecol. doi:10.1111/1365-2664.12774

    Google Scholar 

  • Nakagawa S, Cuthill I (2007) Effect size, confidence interval and statistical significance: a practical guide for biologists. Biol Rev 82:591–605

    Article  PubMed  Google Scholar 

  • Nakagawa S, Schielzeth H (2013) A general and simple method for obtaining R2 from generalized linear mixed-effects models. Methods Ecol Evol 4:133–142

    Article  Google Scholar 

  • Nussear KE, Tracy CR, Medica PA, Wilson DS, Marlow RW, Corn PS (2012) Translocation as a conservation tool for Agassiz’s desert tortoises: Survivorship, reproduction, and movements. J Wildl Manag 76:1341–1353

    Article  Google Scholar 

  • Pollock KH, Winterstein SR, Bunck C, Curtis PD (1989a) Survival analysis in telemetry studies: the staggered entry design. J Wildl Manag 53:7–15

    Article  Google Scholar 

  • Pollock KH, Winterstein SR, Conroy MJ (1989b) Estimation and analysis of survival distributions for radio-tagged animals. Biometrics 45:99–109

    Article  Google Scholar 

  • Reinert HK, Rupert RR (1999) Impacts of translocation on behavior and survival of timber rattlesnakes, Crotalus horridus. J Herpetol 33:45–61

    Article  Google Scholar 

  • Rittenhouse CD, Millspaugh JJ, Hubbard MW, Sheriff SL (2007) Movements of translocated and resident three-toed box turtles. J Herpetol 41:115–121

    Article  Google Scholar 

  • Rozylowicz L, Popescu VD (2012) Habitat selection and movement ecology of eastern Hermann’s tortoises in a rural Romanian landscape. Eur J Wildl Res 59:47–55

    Article  Google Scholar 

  • Sæther BE, Ringsby TH, Røskaft E (1996) Life history variation, population processes and priorities in species conservation: towards a reunion of research paradigms. Oikos 77:217–226

    Article  Google Scholar 

  • Seddon PJ, Strauss WM, Innes J (2012) Animal translocations: what are they and why do we do them? In: Ewen JG, Armstrong DP, Parker KA, Seddon PJ (eds) Reintroduction biology: integrating science and management. Blackwell, London, pp 223–256

    Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Spinola RM, Serfass TL, Brooks RP (2008) Survival and post-release movements of river otters translocated to western New York. Northeast Nat 15:13–24

    Article  Google Scholar 

  • Stamps JA, Swaisgood RR (2007) Someplace like home: Experience, habitat selection and conservation biology. Anim Behav Sci 102:392–409

    Article  Google Scholar 

  • Sullivan BK, Kwiatkowski MA, Schuett GW (2004) Translocation of urban Gila Monsers: a problematic conservation tool. Biol Conserv 117:235–242

    Article  Google Scholar 

  • Sullivan BK, Nowak EM, Kwiatkowski MA (2015) Problems with mitigation translocation of herpetofauna. Conserv Biol 29:12–18

    Article  PubMed  Google Scholar 

  • Swingland IR, Stubbs D, Newdick M, Worton B (1986) Movement patterns in Testudo hermanni and implications for management. In Rocek Z (ed) Studies in herpetology. Proc European Herpetological Meeting (3rd Ordinary General Meeting of Societas Europaea Herpetologica) 1985, Prague, pp 573–578

  • Teixeira CP, de Azevedo CS, Mendl M, Cipreste CF, Young RJ (2007) Revisiting translocation and reintroduction programs: the importance of considering stress. Anim Behav 73:1–13

    Article  Google Scholar 

  • Tingley R, Meiri S, Chapple DG (2016) Addressing knowledge gaps in reptile conservation. Biol Conserv 204:1–5

    Article  Google Scholar 

  • Traill LW, Bradshaw CJA, Brook BW (2007) Minimum viable population size: a meta-analysis of 30 years of published estimates. Biol Conserv 139:159–166

    Article  Google Scholar 

  • Tuberville TD, Clark EE, Buhlmann KA, Gibbons JW (2005) Translocation as a conservation tool: site fidelity and movement of repatriated gopher tortoises (Gopherus polyphemus). Anim Conserv 8:349–358

    Article  Google Scholar 

  • Ujvari B, Brown G, Shine R, Madsen T (2015) Floods and famine: climate-induced collapse of a tropical predator-prey community. Funct Ecol 30:453–458

    Article  Google Scholar 

  • Vilardell-Bartino A, Capalleras X, Budó J, Bosch R, Pons P (2015) Knowledge of habitat preferences applied to habitat management: the case of an endangered tortoise population. Amphibia-Reptilia 36:13–25

    Article  Google Scholar 

Download references

Acknowledgements

We thank field assistants, Mathieu Ausanneau, Manon Baptista, Stacy Baugier, Fran De Coster, Edhy Ghetti, Audrey Johany, Julie Jourdan, Laure Servant, Kathy Cano, Olivier Trepos, Sarah Boilet, Solène Briard, Marie Jehanno, Corinne Chaize, Loreline Jean, Camille Gravier, Manon Batista, Marie-Pauline Dessert, Antoine Vignol, Amaury Peyrot, Gaelle Marday, Julie Vingère, Océane Thusy, Céline Luciano, Roxane Bron, Marie Pierrejean, Aurélia Dubois, Baptiste Genolet, Thomas Ferrari, Manon Valat, Cécile Maurand, Clément Blin, Yolan Richard, Quentin Guillaury, Vincent Danias, Lapin Scoupante, and Alexis Veldeman. We thank the CEN PACA and Conseil Général 83 for their collaboration. This study was funded by the Life Program European Project LIFE08NAT/F/000475 and conducted under the permits 83-2012/08 and 83-2012/09 isued by prefectural authorities and DDTM.

Author information

Authors and Affiliations

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

    Fabien Pille, Sébastien Caron, Simon Deleuze, Delphine Busson, Thomas Etien, Florent Girard & Jean-Marie Ballouard

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

    Xavier Bonnet

  3. Syndicat Mixte du Pays de la Vallée de la Dordogne; Service Gestion des Milieux Aquatiques et Prévention des Inondations, Château Neuf, Creysse, France

    Thomas Etien

Authors
  1. Fabien Pille
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Sébastien Caron
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Xavier Bonnet
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Simon Deleuze
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Delphine Busson
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Thomas Etien
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Florent Girard
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Jean-Marie Ballouard
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jean-Marie Ballouard.

Additional information

Communicated by Pedro Aragón.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Pille, F., Caron, S., Bonnet, X. et al. Settlement pattern of tortoises translocated into the wild: a key to evaluate population reinforcement success. Biodivers Conserv 27, 437–457 (2018). https://doi.org/10.1007/s10531-017-1445-2

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10531-017-1445-2

Keywords

Search

Navigation