Abstract
The success of translocation programmes is reflected by the ability of translocated individuals to survive and reproduce in their new environment. However, it has previously been reported that translocated individuals have lower demographic performance than their wild-born conspecifics, due to management and individual factors (such as release conditions or age). Here, we study six breeding parameters in free-ranging females of the North African Houbara bustard (Chlamydotis undulata undulata) and compare these parameters between captive-bred released (n = 204) and wild-born (n = 101) birds, considering the age of individuals and the period of release (autumn versus spring). Our results indicate that (1) captive-bred released females successfully breed in the wild; (2) for three out of the six breeding parameters studied, released females show lower performances than wild-born females; but, (3) Although we observed consistently reduced breeding performances in 1 year old females relative to older females, we did not uncover any interaction between age and the origin of females, suggesting that the impairment of breeding parameters in released females is long lasting; and, (4) interestingly, this impairment of breeding parameters depends on the period of release, with lower breeding performances for spring releases compared to autumn releases. Overall, our study highlights the capacity of captive-bred females to reproduce in the wild, contributing to the dynamics of the population beyond their individual history. Our results also uncover complex variations of breeding parameters in translocated birds, but suggest that these differences can be minimized through an appropriate translocation strategy.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Amundsen T, Stokland JN (1990) Egg size and parental quality influence nestling growth in the shag. Auk 107:410–413
Araki H, Cooper B, Blouin MS (2007) Genetic effects of captive breeding cause a rapid, cumulative fitness decline in the wild. Science 318:100–103
Armstrong DP, Ewen JG (2001) Assessing the value of follow-up translocations: a case study using New Zealand robins. Biol Conserv 101:239–247. https://doi.org/10.1016/S0006-3207(01)00071-4
Armstrong DP, Seddon PJ (2008) Directions in reintroduction biology. Trends Ecol Evol 23:20–25. https://doi.org/10.1016/j.tree.2007.10.003
Armstrong DP, Le Coeur C, Thorne JM, Panfylova J, Lovegrove TG, Frost PGH, Ewen JG (2017) Using Bayesian mark-recapture modelling to quantify the strength and duration of post-release effects in reintroduced populations. Biol Conserv 215:39–45. https://doi.org/10.1016/j.biocon.2017.08.033
Azar JF, Rautureau P, Lawrence M, Calabuig G, Hingrat Y (2016) Survival of reintroduced Asian houbara in United Arab Emirates’ reserves. J Wildl Manag 80:1031–1039. https://doi.org/10.1002/jwmg.21085
Bacon L (2017) Etude des paramètres de reproduction et de la dynamique d’une population renforcée d’outardes Houbara nord-africaines (Chlamydotis undulata undulata) au Maroc. Thèse, Muséum National d’Histoire Naturelle, p 192
Bacon L, Hingrat Y, Robert A (2017a) Evidence of reproductive senescence of released individuals in a reinforced bird population. Biol Conserv 215:288–295. https://doi.org/10.1016/j.biocon.2017.08.023
Bacon L, Hingrat Y, Jiguet F, Monnet AC, Sarrazin F, Robert A (2017b) Habitat suitability and demography, a time dependent relationship. Ecol Evol 7(7):2214–2222
Barbanera F, Pergams ORW, Guerrini M, Forcina G, Panayides P, Dini F (2010) Genetic consequences of intensive management in game birds. Biol Conserv 143:1259–1268. https://doi.org/10.1016/j.biocon.2010.02.035
Barron DG, Brawn JD, Weatherhead PJ (2010) Meta-analysis of transmitter effects on avian behaviour and ecology. Methods Ecol Evol 1:180–187. https://doi.org/10.1111/j.2041-210X.2010.00013.x
Barton K (2015) MuMIn: multi-model inference. R package version 1 (9), 13
Bates D, Martin M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48. https://doi.org/10.18637/jss.v067.i01
Benchari A, El Aich A, Mahyou H, Baghdad M, Bendaou M (2014) Analyse de l’évolution du système pastoral du Maroc oriental. Revue d’élevage et de médecine vétérinaire des pays tropicaux 67(4):151–162
Bertolero A, Oro D (2009) Conservation diagnosis of reintroducing Mediterranean pond turtles: what is wrong? Anim Conserv 12:581–591. https://doi.org/10.1111/j.1469-1795.2009.00284.x
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. https://doi.org/10.1111/j.1469-1795.2007.00121.x
Blomqvist D, Johansson OC, Götmark F (1997) Parental quality and egg size affect chick survival in a precocial bird, the lapwing Vanellus vanellus. Oecologia 110:18–24. https://doi.org/10.1007/s004420050128
Boulanouar B, Paquay R (1994) L’élevage du mouton et ses systèmes de prodution au Maroc. Institut National de la Recherche Agronomique – Royaume du Maroc.
Bourass K, Hingrat Y (2015) Diet of released captive-bred North-African houbara bustards. Eur J Wildl Res 61:563–574. https://doi.org/10.1007/s10344-015-0930-8
Bourass K, Zaime A, Qninba A, Benhoussa A, Rguibi H, Hingrat Y (2012) Evolution saisonnière du régime alimentaire de l’Outarde houbara nord-africain, Chlamydotis undulata. Bull l’Instut Sci Rabat 34:29–43
Brown JL, Collopy MW, Gott EJ, Juergens PW, Montoya AB, Hunt WG (2006) Wild-reared aplomado falcons survive and recruit at higher rates than hacked falcons in a common environment. Biol Conserv 131:453–458. https://doi.org/10.1016/j.biocon.2006.02.021
Buner F, Schaub M (2008) How do different releasing techniques affect the survival of reintroduced grey partridges Perdix perdix? Wildl Biol 14:26–35. https://doi.org/10.2981/0909-6396(2008)14%5b26:HDDRTA%5d2.0.CO;2
Buner FD, Browne SJ, Aebischer NJ (2011) Experimental assessment of release methods for the re-establishment of a red-listed galliform, the grey partridge (Perdix perdix). Biol Conserv 144:593–601. https://doi.org/10.1016/j.biocon.2010.10.017
Burnham KP, Anderson DE (2002) Model selection and multimodel inference—a practical information-theoric approach, 2nd edn. Springer, New York
Cam E, Aubry LM, Authier M (2016) The conundrum of heterogeneities in life history studies. Trends Ecol Evol 31:872–886. https://doi.org/10.1016/j.tree.2016.08.002
Casas F, Benítez-López A, García JT, Martín CA, Viñuela J, Mougeot F (2015) Assessing the short-term effects of capture, handling and tagging of sandgrouse. Ibis 157:115–124. https://doi.org/10.1111/ibi.12222
Champagnon J, Guillemain M, Elmberg J, Massez G, Cavallo F, Gauthier-Clerc M (2012) Low survival after release into the wild: assessing “the burden of captivity” on Mallard physiology and behaviour. Eur J Wildl Res 58:255–267. https://doi.org/10.1007/s10344-011-0573-3
Chargé R, Saint Jalme M, Lacroix F, Cadet A, Sorci G (2010) Male health status, signalled by courtship display, reveals ejaculate quality and hatching success in a lekking species. J Anim Ecol 79:843–850. https://doi.org/10.1111/j.1365-2656.2010.01696.x
Chargé R, Sorci G, Saint Jalme M, Lesobre L, Hingrat Y, Lacroix F, Teplitsky C (2014) Does recognized genetic management in supportive breeding prevent genetic changes in life-history traits? Evol Appl 7:521–532. https://doi.org/10.1111/eva.12150
Christensen RHB (2015) Ordinal—regression models for ordinal data. R package version 2015, 6–28
Converse SJ, Moore CT, Armstrong DP (2013) Demographics of reintroduced populations: estimation, modelling, and decision analysis. J Wildl Manag 77:1081–1093. https://doi.org/10.1002/jwmg.590
Curio E (1983) Why young birds reproduce less well? Ibis 125:400–404. https://doi.org/10.1111/j.1474-919X.1983.tb03130.x
Development Core Team R (2017) R: a language and environment for statistical computing. R Found Stat Comput, Vienna, Austria
Dickens MJ, Delehanty DJ, Michael Romero L (2010) Stress: an inevitable component of animal translocation. Biol Conserv 143:1329–1341. https://doi.org/10.1016/j.biocon.2010.02.032
Ewen JG, Armstrong DP, Parker KA, Seddon PJ (2012) Reintroduction biology: integrating science and management. Wiley-Blackwell, Hoboken
Fischer J, Lindenmayer DB (2000) An assessment of the published results of animal relocations. Biol Conserv 96:1–11. https://doi.org/10.1016/S0006-3207(00)00048-3
Frankham R (2008) Genetic adaptation to captivity in species conservation programs. Mol Ecol 17:325–333. https://doi.org/10.1111/j.1365-294X.2007.03399.x
Galbraith H (1988) Effects of egg size and composition on the size, quality and survival of lapwing Vanellus vanellus chicks. J Zool 214:383–398. https://doi.org/10.1111/j.1469-7998.1988.tb03747.x
Gaucher P (1995) Breeding biology of the houbara bustard Chlamydotis undulata in Algeria. Alauda 63:291–298
Gelman A (2008) Scaling regression inputs by dividing by two standard deviations. Stat Med 27:2865–2873
Goriup PD (1997) The world status of the houbara bustard Chlamydotis undulata. Bird Conserv Int 7:373–397
Grant TA, Shaffer TL (2012) Time-specific patterns of nest survival for ducks and passerines breeding in North Dakota. Auk 129:1–10
Hardouin LA, Nevoux M, Robert A, Gimenez O, Lacroix F, Hingrat Y (2012) Determinants and costs of natal dispersal in a lekking species. Oikos 121:804–812. https://doi.org/10.1111/j.1600-0706.2012.20313.x
Hardouin LA, Robert A, Nevoux M, Gimenez O, Lacroix F, Hingrat Y (2014) Meteorological conditions influence short-term survival and dispersal in a reinforced bird population. J Appl Ecol 51:1494–1503. https://doi.org/10.1111/1365-2664.12302
Hardouin LA, Hingrat Y, Nevoux M, Lacroix F, Robert A (2015a) Survival and movement of translocated houbara bustards in a mixed conservation area. Anim Conserv 18(5):461–470
Hardouin LA, Legagneux P, Hingrat Y, Robert A (2015b) Sex-specific dispersal responses to inbreeding and kinship. Anim Behav 105:1–10. https://doi.org/10.1016/j.anbehav.2015.04.002
Herzog M (2009) Nestsurvival. R package that performs logistic exposure nest survival analyses
Hill D, Robertson P (1988) Breeding success of wild and hand-reared ring-necked pheasants. J Wildl Manag 52:446–450. https://doi.org/10.2307/3801588
Hoyt D (1979) Practical methods of estimating volume and fresh weight of birg eggs. Auk 96:73–77
Huff DD, Miller LM, Chizinski CJ, Vondracek B (2011) Mixed-source reintroductions lead to outbreeding depression in second-generation descendents of a native North American fish. Mol Ecol 20:4246–4258. https://doi.org/10.1111/j.1365-294X.2011.05271.x
IUCN/SSC (2013) Guidelines for reintroductions and other conservation translocations. Version 1.0. Gland, Switzerland. http://www.issg.org/pdf/publications/RSG_ISSG-Reintroduction-Guidelines-2013.pdf
Koshkin M, Burnside RJ, Packman CE, Collar NJ, Dolman PM (2016) Effects of habitat and livestock on nest productivity of the Asian houbara Chlamydotis macqueenii in Bukhara Province, Uzbekistan. Eur J Wildl Res 62:447–459. https://doi.org/10.1007/s10344-016-1018-9
Lacroix F, Seabury J, Al Bowardi M, Renaud J (2003) The Emirates Center for Wildlife Propagation: comprehensive strategy to secure self-sustaining wild populations of houbara bustard (Chlamydotis undulata undulata) in Eastern Morocco. Houbara News 5:60–62
Le Cuziat J, Lacroix F, Roche P, Vidal E, Médail F, Orhant N, Béranger PM (2005) Landscape and human influences on the distribution of the endangered North African houbara bustard (Chlamydotis undulata undulata) in Eastern Morocco. Animal Conserv 8:143–152. https://doi.org/10.1017/S1367943005001903
Le Gouar P, Robert A, Choisy J-P, Henriquet S, Lecuyer P, Tessier C, Sarrazin F (2008) Roles of survival and dispersal in reintroduction success of griffon vulture (Gyps fulvus). Ecol Appl 18:859–872. https://doi.org/10.1890/07-0854.1
Le Maho Y, Whittington JD, Hanuise N, Pereira L, Boureau M, Brucker M, Chatelain N, Courtecuisse J, Crenner F, Friess B, Grosbellet E, Kernaléguen L, Olivier F, Saraux C, Vetter N, Viblanc VA, Thierry B, Tremblay P, Groscolas R, Le Bohec C (2014) Rovers minimize human disturbance in research on wild animals. Nat Methods 11:1242–1244. https://doi.org/10.1038/nmeth.3173
Lesobre L, Lacroix F, Caizergues A, Hingrat Y, Chalah T, Jalme MS (2010) Conservation genetics of Houbara Bustard (Chlamydotis undulata undulata): population structure and its implications for the reinforcement of wild populations. Conserv Genet 11:1489–1497. https://doi.org/10.1007/s10592-009-9979-9
Mabee TJ (1997) Using eggshell evidence to determine nest fate of shorebirds. Wilson Bull 109:307–313. https://doi.org/10.1111/j.1557-9263.2006.00037.x
Manolis JC, Andersen DE, Cuthbert FJ (2000) Uncertain nest fates in songbird studies and variation in mayfield estimation. Auk 117:615–626. https://doi.org/10.1642/0004-8038(2000)117%5b0615:UNFISS%5d2.0.CO;2
Martin TE (1995) Avian life history evolution in relation to nest sites, nest predation, and food. Ecol Monogr 65:101–127. https://doi.org/10.2307/2937160
Mauck RA, Huntington CE, Doherty PF Jr (2012) Experience versus effort: what explains dynamic heterogeneity with respect to age? Oikos 121:1379–1390. https://doi.org/10.1111/j.1600-0706.2012.20271.x
Mayfield HF (1975) Suggestions for calculating nest success. Wilson Bull 87:456–466. https://doi.org/10.2307/4160682
Mihoub J-B, Robert A, Gouar PL, Sarrazin F (2011) Post-release dispersal in animal translocations: social attraction and the “vacuum effect”. PLoS ONE 6:e27453. https://doi.org/10.1371/journal.pone.0027453
Monnet A-C, Hingrat Y, Jiguet F (2015) The realized niche of captive-hatched Houbara Bustards translocated in Morocco meets expectations from the wild. Biol Conserv 186:241–250. https://doi.org/10.1016/j.biocon.2015.03.013
Montalvo AM, Ellstrand NC (2001) Nonlocal transplantation and outbreeding depression in the subshrub Lotus scoparius (Fabaceae). Am J Bot 88:258–269
Morales MB, Alonso JC, Alonso J (2002) Annual productivity and individual female reproductive success in a Great Bustard Otis tarda population. Ibis 144:293–300. https://doi.org/10.1046/j.1474-919X.2002.00042.x
Nussey DH, Kruuk LEB, Donald A, Fowlie M, Clutton-Brock TH (2006) The rate of senescence in maternal performance increases with early-life fecundity in red deer. Ecol Lett 9:1342–1350. https://doi.org/10.1111/j.1461-0248.2006.00989.x
Pérez JA, Sánchez-García C, Díez C, Bartolomé DJ, Alonso ME, Gaudioso VR (2015) Are parent-reared red-legged partridges (Alectoris rufa) better candidates for re-establishment purposes? Poult Sci 94:2330–2338. https://doi.org/10.3382/ps/pev210
Ponjoan A, Bota G, De La Morena ELG, Morales MB, Wolff A, Marco I, Mañosa S (2008) Adverse effects of capture and handling little bustard. J Wildl Manag 72:315–319. https://doi.org/10.2193/2006-443
Robert A (2009) Captive breeding genetics and reintroduction success. Biol Conserv 142:2915–2922. https://doi.org/10.1016/j.biocon.2009.07.016
Robert A, Couvet D, Sarrazin F (2007) Integration of demography and genetics in population restorations. Ecoscience 14:463–471. https://doi.org/10.2980/1195-6860(2007)14%5b463:IODAGI%5d2.0.CO;2
Robert A, Colas B, Guigon I, Kerbiriou C, Mihoub J-B, Saint-Jalme M, Sarrazin F (2015a) Defining reintroduction success using IUCN criteria for threatened species: a demographic assessment. Anim Conserv 18:397–406. https://doi.org/10.1111/acv.12188
Robert A, Bolton M, Jiguet F, Bried J (2015b) The survival–reproduction association becomes stronger when conditions are good. Proc R Soc B 282:20151529. https://doi.org/10.1098/rspb.2015.1529
Roche EA, Cuthbert FJ, Arnold TW (2008) Relative fitness of wild and captive-reared piping plovers: does egg salvage contribute to recovery of the endangered Great Lakes population? Biol Conserv 141:3079–3088. https://doi.org/10.1016/j.biocon.2008.09.014
Saint Jalme M, Van Heezik Y (1996) Propagation of the houbara bustard. Paul Keegan, London
Sánchez-García C, Alonso ME, Pérez JA, Rodríguez PL, Gaudioso VR (2011) Comparing fostering success between wild-caught and game farm bred captive red-legged partridges (Alectoris rufa, L.). Appl Anim Behav Sci 133:70–77. https://doi.org/10.1016/j.applanim.2011.04.012
Sarrazin F, Bagnolini C, Pinna JL, Danchin E, Clobert J (1994) High survival estimates of griffon vultures (Gyps fulvus fulvus) in a reintroduced population. Auk 111:853–862. https://doi.org/10.2307/4088817
Sarrazin F, Bagnolinp C, Pinna JL, Danchin E (1996) Breeding biology during establishment of a reintroduced Griffon Vulture Gyps fulvus population. Ibis 138:315–325. https://doi.org/10.1111/j.1474-919X.1996.tb04344.x
Shaffer TL (2004) A unified approach to analyzing nest success. Auk 121:526–540
Sutherland WJ, Armstrong D, Butchart SHM, Earnhardt JM, Ewen J, Jamieson I, Jones CG, Lee R, Newbery P, Nichols JD, Parker KA, Sarrazin F, Seddon PJ, Shah N, Tatayah V (2010) Standards for documenting and monitoring bird reintroduction projects. Conserv Lett 3:229–235. https://doi.org/10.1111/j.1755-263X.2010.00113.x
Tavecchia G, Viedma C, Martínez-Abraín A, Bartolomé M-A, Gómez JA, Oro D (2009) Maximizing re-introduction success: assessing the immediate cost of release in a threatened waterfowl. Biol Conserv 142:3005–3012. https://doi.org/10.1016/j.biocon.2009.07.035
van de Pol M, Verhulst S (2006) Age- dependent traits: a new statistical model to separate within- and between- individual effects. Am Nat 167:766–773. https://doi.org/10.1086/503331
Williams TD (1994) Intraspecific variation in egg size and egg composition in birds: effects on offspring fitness. Biol Rev Camb Philos Soc 69:35–59
Zuur AF, Ieno EN, Walker N, Saveliev AA, Smith GM (2009) Mixed effects models and extensions in ecology with R, statistics for biology and health. Springer, New York. https://doi.org/10.1007/978-0-387-87458-6
Acknowledgements
This study was funded by the Emirates Center for Wildlife Propagation (ECWP), a project of the International Fund for Houbara Conservation (IFHC). We are grateful to H.H. Sheikh Mohammed bin Zayed Al Nahyan, Crown Prince of Abu Dhabi and Chairman of the IFHC and H.E. Mohammed Al Bowardi, Deputy Chairman of IFHC, for their support. This study was conducted under the guidance of Reneco International Wildlife Consultants LLC., a consulting company managing ECWP. We are thankful to Dr. F. Lacroix, managing director, and G. Leveque, project director, for their supervision. We sincerely thank all ECWP staff from the Ecology division who participated in data collection. We are thankful to Pascale Reding and Grégoire Liénart for producing our study area map. We are grateful to Doug Armstrong and two anonymous reviewers for their helpful and constructive comments on the manuscript, as well as to Dr Thomas Martin for improving the English text.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by Jan C Habel.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Bacon, L., Robert, A. & Hingrat, Y. Long lasting breeding performance differences between wild-born and released females in a reinforced North African Houbara bustard (Chlamydotis undulata undulata) population: a matter of release strategy. Biodivers Conserv 28, 553–570 (2019). https://doi.org/10.1007/s10531-018-1651-6
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10531-018-1651-6