Estimating biodiversity changes in the Camargue wetlands: An expert knowledge approach

Autoři: Sara Fraixedas aff001;  Thomas Galewski aff001;  Sofia Ribeiro-Lopes aff001;  Jonathan Loh aff002;  Jacques Blondel aff003;  Hugo Fontès aff001;  Patrick Grillas aff001;  Philippe Lambret aff001;  Delphine Nicolas aff001;  Anthony Olivier aff001;  Ilse R. Geijzendorffer aff001
Působiště autorů: Tour du Valat, Research Institute for the conservation of Mediterranean Wetlands, Le Sambuc, Arles, France aff001;  School of Anthropology and Conservation, University of Kent, Canterbury, United Kingdom aff002;  Centre for Functional and Evolutionary Ecology–French National Centre for Scientific Research (CEFE-CNRS), UMR 5175, Montpellier, France aff003;  French Odonatological Society (SfO), Bois d'Arcy, France aff004
Vyšlo v časopise: PLoS ONE 14(10)
Kategorie: Research Article
doi: 10.1371/journal.pone.0224235


Mediterranean wetlands are critical strongholds for biodiversity and the provision of ecosystem functions and services; yet, they are being severely degraded by a number of socio-economic drivers and pressures, including climate change. Moreover, we still lack comprehensive understanding of the extent to which biodiversity loss in Mediterranean wetlands will accelerate change in ecosystem processes. Here, we evaluate how changes in biodiversity can alter the ecosystem of the Camargue (southern France). We collected data on species presence/absence, trends and abundance over a 40-year period by combining observations from the scholarly literature with insights derived from expert knowledge. In total, we gathered more than 1500 estimates of presence/absence, over 1400 estimates of species abundance, and about 1400 estimates of species trends for eight taxonomic groups, i.e. amphibians, reptiles, breeding birds, fish, mammals, dragonflies (odonates), orthopterans and vascular plants. Furthermore, we used information on recently arrived species and invasive species to identify compositional changes across multiple taxa. Complementing targeted literature searches with expert knowledge allowed filling important gaps regarding the status and trends of biodiversity in the Camargue. Species trend data revealed sharp population declines in amphibians, odonates and orthopterans, while birds and plants experienced an average increase in abundance between the 1970s and the 2010s. The general increasing trends of novel and invasive species is suggested as an explanation for the changing abundance of birds and plants. While the observed declines in certain taxa reflect the relative failure of the protection measures established in the Camargue, the increasing exposure to novel and invasive species reveal major changes in the community structure of the different taxonomic groups. This study is the first attempt to assess changes in biodiversity in the Camargue using an expert knowledge approach, and can help manage the uncertainties and complexities associated with rapid social-ecological change in other Mediterranean wetlands.

Klíčová slova:

Amphibians – Biodiversity – Birds – Invasive species – Mammals – Species diversity – Taxonomy – Wetlands


1. Malcolm JR, Liu C, Neilson RP, Hansen L, Hannah L. Global warming and extinctions of endemic species from biodiversity hotspots. Conserv Biol. 2006; 20(2): 538–548. 16903114

2. Cuttelod A, García N, Abdul Malak D, Temple H, Katariya V. The Mediterranean: a biodiversity hotspot under threat. In: Vié J-C, Hilton-Taylor C, Stuart SN, editors. The 2008 Review of The IUCN Red List of Threatened Species. Gland: IUCN; 2008. pp. 1–13.

3. Blondel J, Aronson J, Bodiou J-Y, Boeuf G. The Mediterranean Region: Biodiversity in Space and Time. 2nd ed. Oxford and New York: Oxford University Press; 2010.

4. MWO2. Mediterranean Wetlands Outlook 2. Solutions for Sustainable Mediterranean Wetlands. Tour du Valat; 2018.

5. Green AJ, El Hamzaoui M, El Agbani MA, Franchimont J. The conservation status of Moroccan wetlands with particular reference to waterbirds and to changes since 1978. Biol Conserv. 2002; 104: 71–82.

6. Underwood EC, Viers JH, Klausmeyer KR, Cox RL, Shaw MR. Threats and biodiversity in the mediterranean biome. Divers Distrib. 2009; 15: 188–197.

7. Galewski T, Collen B, McRae L, Loh J, Grillas P, Gauthier-Clerc M, et al. Long-term trends in the abundance of Mediterranean wetland vertebrates: From global recovery to localized declines. Biol Conserv. 2011; 144: 1392–1399.

8. Galewski T, Devictor V. When common birds became rare: Historical records shed light on long-term responses of bird communities to global change in the largest wetland of France. PLoS One. 2016; 11(11): e0165542. doi: 10.1371/journal.pone.0165542 27832127

9. Mathevet R. Camargue incertaine: sciences, usages et natures. 1st ed. Paris: Buchet-Chastel; 2004.

10. Mathevet R, Peluso NL, Couespel A, Robbins P. Using historical political ecology to understand the present: water, reeds, and biodiversity in the Camargue Biosphere Reserve, southern France. Ecol Soc. 2015; 20(4): 17.

11. Vilà M, Espinar JL, Hejda M, Hulme PE, Jarošik V, Maron JL, et al. Ecological impacts of invasive alien plants: a meta-analysis of their effects on species, communities and ecosystems. Ecol Lett. 2011; 14: 702–708. doi: 10.1111/j.1461-0248.2011.01628.x 21592274

12. Oliver TH, Isaac NJB, August TA, Woodcock BA, Roy DB, Bullock JM. Declining resilience of ecosystem functions under biodiversity loss. Nat Commun. 2015; 6: 10122. doi: 10.1038/ncomms10122 26646209

13. Laverty C, Green KD, Dick JTA, Barrios-O’Neill D, Mensink PJ, Médoc V, et al. Assessing the ecological impacts of invasive species based on their functional responses and abundances. Biol Invasions. 2017; 19: 1653–1665.

14. Rodríguez-Pérez H, Hilaire S, Mesléard F. Temporary pond ecosystem functioning shifts mediated by the exotic red swamp crayfish (Procambarus clarkii): a mesocosm study. Hydrobiologia. 2016; 767: 333–345.

15. Anadón JD, Giménez A, Ballestar R, Pérez I. Evaluation of local ecological knowledge as a method for collecting extensive data on animal abundance. Conserv Biol. 2009; 23: 617–625. doi: 10.1111/j.1523-1739.2008.01145.x 19183211

16. O’Donnell KP, Pajaro MG, Vincent ACJ. How does the accuracy of fisher knowledge affect seahorse conservation status? Anim Conserv. 2010; 13: 526–533.

17. Alkemade R, van Oorschot M, Miles L, Nellemann C, Bakkenes M, ten Brink B. GLOBIO3: A framework to investigate options for reducing global terrestrial biodiversity loss. Ecosystems. 2009; 12: 374–390.

18. Janse JH, Kuiper JJ, Weijters MJ, Westerbeek EP, Jeuken MHJL, Bakkenes M, et al. GLOBIO-Aquatic, a global model of human impact on the biodiversity of inland aquatic ecosystems. Environ Sci Policy. 2015; 48: 99–114.

19. Newbold T, Hudson LN, Hill SLL, Contu S, Lysenko I, Senior RA, et al. Global effects of land use on local terrestrial biodiversity. Nature. 2015; 520: 45–50. doi: 10.1038/nature14324 25832402

20. Newbold T, Hudson LN, Arnell AP, Contu S, De Palma A, Ferrier S, et al. Has land use pushed terrestrial biodiversity beyond the planetary boundary? A global assessment. Science. 2016; 353(6296): 288–291. doi: 10.1126/science.aaf2201 27418509

21. Scholes RJ, Biggs R. A biodiversity intactness index. Nature. 2005; 434: 45–49. doi: 10.1038/nature03289 15744293

22. Bonebrake TC, Christensen J, Boggs CL, Ehrlich PR. Population decline assessment, historical baselines, and conservation. Conserv Lett. 2010; 3: 371–378.

23. Adams-Hosking C, McBride MF, Baxter G, Burgman M, de Villiers D, Kavanagh R, et al. Use of expert knowledge to elicit population trends for the koala (Phascolarctos cinereus). Divers Distrib. 2016; 22: 249–262.

24. Fraixedas S, Lindén A, Meller K, Lindström Å, Keišs O, Kålås JA, et al. Substantial decline of Northern European peatland bird populations: Consequences of drainage. Biol Conserv. 2017; 214: 223–232.

25. Ludwig D, Mangel M, Haddad B. Ecology, conservation, and public policy. Annu Rev Ecol Evol Syst. 2001; 32: 481–517.

26. Kuhnert PM. Four case studies in using expert opinion to inform priors. Environmetrics. 2011; 22: 662–674.

27. Drew CA, Perera AH. Expert knowledge as a basis for landscape ecological predictive models. In: Drew CA, Wiersma Y, Huettmann F, editors. Predictive Species and Habitat Modeling in Landscape Ecology. New York: Springer; 2011. pp. 229–248.

28. McBride MF, Garnett ST, Szabo JK, et al. Structured elicitation of expert judgments for threatened species assessment: a case study on a continental scale using email. Methods Ecol Evol. 2012; 3: 906–920.

29. Kuhnert PM, Martin TG, Griffiths SP. A guide to eliciting and using expert knowledge in Bayesian ecological models. Ecol Lett. 2010; 13: 900–914. doi: 10.1111/j.1461-0248.2010.01477.x 20497209

30. Martin TG, Burgman MA, Fidler F, Kuhnert PM, Low-Choy S, McBride M, et al. Eliciting expert knowledge in conservation science. Conserv Biol. 2012; 26(1): 29–38. doi: 10.1111/j.1523-1739.2011.01806.x 22280323

31. Perennou C. La Camargue au fil du temps. Evolutions récentes et perspectives. Tour du Valat; 2009.

32. Ramsar. The Annotated Ramsar List of Wetlands of International Importance: France [Internet]. 2012. Available from:

33. Ernoul L, Mathevet R, Beck N, Legeay L. Community-based conservation in action: what does it really imply in terms of investment? Conserv Soc. 2009; 7(3): 205–212.

34. Wasserman S, Pattison P, Steinley D. Social network analysis. In: Everett B, Howell D, editors. Encyclopedia of Statistics in the Behavioral Science. New York: Wiley; 2005. pp. 1866–1871.

35. Hillebrand H, Blasius B, Borer ET, Chase JM, Downing JA, Eriksson BK, et al. Biodiversity change is uncoupled from species richness trends: Consequences for conservation and monitoring. J Appl Ecol. 2018; 55: 169–184.

36. Valéry L, Fritz H, Lefeuvre J-C, Simberloff D. In search of a real definition of the biological invasion phenomenon itself. Biol Invasions. 2008; 10: 1345–1351.

37. Carboneras C, Genovesi P, Vilà M, Blackburn TM, Carrete M, Clavero M, et al. A prioritised list of invasive alien species to assist the effective implementation of EU legislation. J Appl Ecol. 2018; 55: 539–547.

38. Rosecchi E, Poizat G, Crivelli AJ. Introductions de poissons d’eau douce et d’écrevisses en Camargue: historique, origines et modifications des peuplements. Bull Fr Pêche Piscic. 1997; 344/345: 221–232.

39. Terrin E, Diadema K, Fort N. Stratégie régionale relative aux espèces végétales exotiques envahissantes en Provence-Alpes-Côte d’Azur. Direction Régionale de l'Environnement, de l'Aménagement et du Logement PACA, Région PACA, Conservatoire botanique national alpin & Conservatoire botanique national méditerranéen de Porquerolles; 2014.

40. Burnham KP, Anderson DR. Model selection and multimodel inference. 2nd ed. New York: Springer; 2002.

41. Booth G, Niccolucci M, Schuster E. Identifying proxy sets in multiple linear regression: an aid to better coefficient interpretation. 1st ed. Ogden: U.S. Department of Agriculture, Forest Service, Intermountain Research Station; 1994.

42. R Development Core Team. R: A language and environment for statistical computing. The R Foundation for Statistical Computing; 2013.

43. Tamisier A, Dehorter O. Camargue canards et foulques: Fonctionnement et devenir d'un prestigieux quartier d'hiver. Centre Ornithologique du Gard; 1999.

44. Tamisier A, Grillas P. A review of habitat changes in the Camargue: an assessment of the effects of the loss of biological diversity on the wintering waterfowl community. Biol Conserv. 1994; 70: 39–47.

45. Waterkeyn A, Grillas P, Vanschoenwinkel B, Brendonck L. Invertebrate community patterns in Mediterranean temporary wetlands along hydroperiod and salinity gradients. Freshw Biol. 2008; 53: 1808–1822.

46. Jakob C, Poulin B. Indirect effects of mosquito control using Bti on dragonflies and damselflies (Odonata) in the Camargue. Insect Conserv Diver. 2016; 9: 161–169.

47. Mesléard F, Gauthier-Clerc M, Lambret P. Impact of the insecticide Alphacypermetrine and herbicide Oxadiazon, used singly or in combination, on the most abundant frog in French rice fields, Pelophylax perezi. Aquat Toxicol. 2016; 176: 24–29. doi: 10.1016/j.aquatox.2016.04.004 27107241

48. Riservato E, Boudot J-P, Ferreira S, Jović M, Kalkman VJ, Schneider W, et al. The status and distribution of dragonflies of the Mediterranean Basin. Gland and Malaga: IUCN; 2009.

49. Kalkman VJ, Boudot J-P, Bernard R, Conze KJ, De Knijf G, Dyatlova E, et al. European Red List of Dragonflies. Publications Office of the European Union; 2010.

50. Miller AK, Miller PL, Siva-Jothy MT. Pre-copulatory guarding and other aspects of the reproductive behaviour in Sympetrum depressiusculum (Sélys) in rice fields in southern France (Odonata, Libellulidae). Odonatologica. 1984; 13: 407–414.

51. Siesa ME, Padoa-Schioppa E, Ott J, De Bernardi F, Ficetola GF. Assessing the consequences of biological invasions on species with complex life cycles: Impact of the alien crayfish Procambarus clarkii on Odonata. Ecol Indic. 2014; 46: 70–77.

52. Rodríguez-Pérez H, Cayuela H, Hilaire S, Olivier A, Mesléard F. Is the exotic red swamp crayfish (Procambarus clarkii) a current threat for the Mediterranean tree frog (Hyla meridionalis) in the Camargue (southern France)? Hydrobiologia. 2014; 723: 145–156.

53. Bundschuh R, Schmitz J, Bundschuh M, Brühl CA. Does insecticide drift adversely affect grasshoppers (Orthoptera: Saltatoria) in field margins? A case study combining laboratory acute toxicity testing with field monitoring data. Environ Toxicol Chem. 2012; 31: 1874–1879. doi: 10.1002/etc.1895 22619160

54. Olivier A, Lutz M, Thibault M, Joris A. Une nouvelle espèce de mammifères en Camargue: La martre des pins Martes martes. Arvicola. 2007; 18(1): 9–10.

55. Olivier A, Suet M, Mondain-Monval J-Y. Confirmation de l’implantation de la Martre des pins Martes martes (Linnaeus, 1758) en Camargue. Nature de Provence. 2017a; 1–5. Available from:

56. Poitevin F, Olivier A, Bayle P, Scher O. Mammifères de Camargue. 1st ed. Castelnau-le-Lez: Regard du Vivant & Parc Naturel Régional de Camargue; 2010.

57. Poitevin F, Olivier A. mammifères Les. In: Blondel J, Barruol G, Vianet R, editors. L’Encyclopédie de la Camargue. Paris: Buchet-Chastel; 2013. pp. 71–72.

58. Massez G, Mondain-Monval J-Y, Olivier A, Pineau O, Tetrel C, Vandewalle P. Le Lapin de garenne (Oryctolagus cuniculus) en Camargue: évolution des populations depuis 20 ans et conséquences biologiques. 35ème colloque francophone de Mammalogie; 2012.

59. Olivier A, Smith H, Santos R, Tatin L, Espuno N, Arnal V, et al. Utilisation de chiens pour détecter la présence du Lézard ocellé (Timon lepidus). 45ème congrès de la Société Herpétologique de France; 2017b.

60. Graitson E, Barbraud C, Bonnet X. Catastrophic impact of wild boars: insufficient hunting pressure pushes snakes to the brink. Anim Conserv. 2018; 22(2): 165–176.

61. Aznar J-C, Dervieux A, Grillas P. Association between aquatic vegetation and landscape indicators of human pressure. Wetlands. 2003; 23(1): 149–160.

62. Grillas P. Bilan des actions de gestion de Ludwigia grandiflora et L. peploides (jussies) dans les espaces protégés du Languedoc-Roussillon. In: Muller S, editor. Plantes Invasives en France: Etat des connaissances et propositions d’actions. Paris: Publications scientifiques du MNHN; 2004. vol. 62, pp. 148–152.

63. Marnotte P, Carrara A, Dominati E, Girardot F. Plantes des rizières de Camargue. Cirad, CFR & Camargue Natural Regional Park; 2006.

64. Mesléard F, Yavercovski N, Lefebvre G, Willm L, Bonis A. High stocking density controls Phillyrea angustifolia in Mediterranean grasslands. Environ Manage. 2017; 59(3): 455–463. doi: 10.1007/s00267-016-0808-x 28078388

65. Gaget E, Galewski T, Jiguet F, Le Viol I. Waterbird communities adjust to climate warming according to conservation policy and species protection status. Biol Conserv. 2018; 227: 205–212.

66. Tourenq C, Bennetts RE, Sadoul N, Mesléard F, Kayser Y, Hafner H. Long-term population and colony patterns of four species of tree-nesting herons in the Camargue, South France. Waterbirds. 2000; 23(2): 236–245.

67. Isenmann P. L’évolution de l’avifaune nicheuse de Camargue au cours du XXe siècle. Alauda. 2012; 80: 241–266.

68. Poulin B, Lefebvre G, Crivelli AJ. The invasive red swamp crayfish as a predictor of Eurasian bittern density in the Camargue, France. J Zool. 2007; 273: 98–105.

69. Vačkář D, ten Brink B, Loh J, Baillie JEM, Reyers B. Review of multispecies indices for monitoring human impacts on biodiversity. Ecol Indic. 2012; 17: 58–67.

70. Sardet E, Defaut B. Les Orthoptères menacés en France. Liste rouge nationale et listes rouges par domaines biogéographiques. Matériaux Orthoptériques et Entomocénotiques. 2004; 9: 125–137.

71. Arnaud-Fassetta G. River channel changes in the Rhone Delta (France) since the end of the Little Ice Age: geomorphological adjustment to hydroclimatic change and natural resource management. Catena. 2003; 51: 141–172.

72. Olivier J-M, Carrel G, Lamouroux N, Dole-Olivier M-J, Malard F, Bravard J-P, et al. The Rhône River Basin. In: Tockner K, Uehlinger U, Robinson CT, editors. Rivers of Europe. London: Academic Press; 2009. pp. 247–295.

73. Galewski T. Towards an observatory of Mediterranean wetlands: Evolution of biodiversity from 1970 to the present. Tour du Valat; 2008.

74. Galewski T, Dragonne C. Indice Région Vivante: Comment évolue la biodiversité en Provence-Alpes-Côte d’Azur? Observatoire Régional de la Biodiversité Provence-Alpes-Côte d’Azur; 2018.

Článek vyšel v časopise


2019 Číslo 10