Compensatory recruitment allows amphibian population persistence in anthropogenic habitats

Author:

Cayuela Hugo12,Monod-Broca Benjamin3ORCID,Lemaître Jean-François1ORCID,Besnard Aurélien4,Gippet Jérôme M. W.2ORCID,Schmidt Benedikt R.56ORCID,Romano Antonio78,Hertach Thomas910ORCID,Angelini Claudio11,Canessa Stefano12,Rosa Giacomo13,Vignoli Leonardo14ORCID,Venchi Alberto14,Carafa Marco15,Giachi Filippo16,Tiberi Andrea17,Hantzschmann Alena M.18,Sinsch Ulrich18ORCID,Tournier Emilie19,Bonnaire Eric20,Gollmann Günter21ORCID,Gollmann Birgit22,Spitzen-van der Sluijs Annemarieke2324,Buschmann Holger25ORCID,Kinet Thierry26ORCID,Laudelout Arnaud26ORCID,Fonters Remi27,Bunz Yoann28,Corail Marc28,Biancardi Carlo29ORCID,Di Cerbo Anna R.30,Langlois Dominique31,Thirion Jean-Marc32,Bernard Laurent33,Boussiquault Elodie34,Doré Florian35,Leclerc Titouan36ORCID,Enderlin Nadine36ORCID,Laurenceau Florian37,Morin Lucy38,Skrzyniarz Mégane39,Barrioz Mickael39,Morizet Yohan40,Cruickshank Sam S.541ORCID,Pichenot Julian42,Maletzky Andreas43,Delsinne Thibaut44ORCID,Henseler Dominik45,Aumaître Damien46,Gailledrat Miguel47,Moquet Julien48,Veen Robert49,Krijnen Peter50,Rivière Laurent51,Trenti Matteo8ORCID,Endrizzi Sonia8ORCID,Pedrini Paolo8ORCID,Biaggini Marta52ORCID,Vanni Stefano52ORCID,Dudgeon David53ORCID,Gaillard Jean-Michel1ORCID,Léna Jean-Paul3

Affiliation:

1. University of Lyon, Université Claude Bernard Lyon 1, CNRS, UMR 5558, Laboratoire de Biométrie et Biologie Evolutive, F-769622 Villeurbanne, France

2. Department of Ecology and Evolution, University of Lausanne, 1015 Lausanne, Switzerland

3. University of Lyon, Université Claude Bernard Lyon 1, CNRS, ENTPE, UMR 5023 LEHNA, F-69622 Villeurbanne, France

4. CEFE, University of Montpellier, CNRS, EPHE-PSL University, IRD, Montpellier 34090, France

5. Department of Evolutionary Biology and Environmental Studies, University of Zurich, 8057 Zürich, Switzerland

6. Info Fauna Karch, 2000 Neuchâtel, Switzerland

7. Institute of Bioeconomy (IBE)—Italian National Research Council (CNR), Roma 00185, Italy

8. Conservation Biology Area, Vertebrate Zoology Division, Museo delle Scienze di Trento (MUSE), Trento 38122, Italy

9. Swiss Federal Institute for Forest, Snow and Landscape Research WSL, 8903 Birmensdorf, Switzerland

10. Natural History Museum of Bern, 3005 Bern, Switzerland

11. Salamandrina Sezzese Search Society, 04018 Sezze, Italy

12. Conservation Biology, Institute for Ecology and Evolution, University of Bern, 3012 Bern, Switzerland

13. Dipartimento di Scienze della Terra, dell’Ambiente e della Vita, Università di Genova, 16132 Genoa, Italy

14. Dipartimento di Scienze, Università Roma Tre, 00146 Rome, Italy

15. Majella National Park, Via Badia 28 - Sulmona (AQ) 67039, Italy

16. Via del Cerreto 8, 56041 Castelnuovo v. Cecina (PI), Italy

17. Via C. Pisacane 13, 00012 Guidonia (Roma), Italy

18. Institute of Integrated Natural Sciences, University of Koblenz-Landau, 56070 Koblenz, Germany

19. NARIES Association, Biodiversity Conservation Unit, Geneva 1225, Switzerland

20. Office National des Forêts (ONF), Agence de Meurthe-et-Moselle, 54052 Nancy, France

21. Department of Evolutionary Biology, University of Vienna, 1030 Vienna, Austria

22. Department of Functional and Evolutionary Ecology, University of Vienna, 1030 Vienna, Austria

23. Reptile, Amphibian and Fish Conservation the Netherlands, 6501 BK Nijmegen, The Netherlands

24. Institute for Water and Wetland Research, Animal Ecology and Physiology, Radboud University, 6525 AJ Nijmegen, The Netherlands

25. NABU (Nature and Biodiversity Conservation Union) of Lower Saxony, 30167 Hannover, Germany

26. Natagora, 5000 Namur, Belgium

27. LPO Isère, 38000 Grenoble, France

28. Parc National des Écrins, Domaine de Charance, 05000 Gap, France

29. Department of Biological Sciences, Universidad de la República, Paysandú 60000, Uruguay

30. Centro Studi Faunistica dei Vertebrati, Società Italiana di Scienze Naturali, Museo di Storia Naturale, 20121 Milan, Italy

31. Conservatoire D'espaces Naturels de Franche-Comté, Réserve Naturelle Nationale du Ravin de Valbois, 25330 Cléron, France

32. Objectifs Biodiversité, 17250 Pont-l’Abbé-d’Arnoult, France

33. SMAT du Haut-Allier, 43300 Langeac, France

34. Charente Nature, Impasse Lautrette, 16000 Angoulême, France

35. Deux-Sèvres Nature Environnement, 79000 Niort, France

36. Pays de Montbéliard Agglomération, 25200 Montbéliard, France

37. Perche Nature, Maison Consigny, 41170 Mondoubleau, France

38. Communauté d'Agglomération Seine-Eure, 27400 Louviers, France

39. URCPIE de Normandie, 14000 Caen, France

40. Indre Nature, 36000 Châteauroux, France

41. Swiss National Park, Chasté Planta-Wildenberg, 7530 Zernez, Switzerland

42. CERFE, Centre de Recherche et Formation en Eco-Éthologie, 08240 Boult-Aux-Bois, France

43. Department of Environment and Biodiversity, University of Salzburg, Salzburg 5020, Austria

44. Société d’Histoire Naturelle Alcide-d’Orbigny, F-63170 Aubière, France

45. Naturlehrgebiet Buchwald, 6218 Ettiswil, Switzerland

46. Conservatoire D'espaces Naturels de Lorraine, 57400 Sarrebourg, France

47. Vienne Nature, 86 240 Fontaine-le-Comte, France

48. Lpo Sarthe, Maison de l'eau, 72000 Le Mans, France

49. Natuurcentrum TIGOULEIX, 23260 Saint-Agnant-près-Crocq, France

50. FLOT Biology, Fontys University, Tilburg 5022, The Netherlands

51. Office National des Forêts (ONF), 28 Av. d'Auvergne, 23000 Guéret, France

52. Museo di Storia Naturale dell’Università degli Studi di Firenze, “La Specola”, 50125 Florence, Italy

53. Division of Ecology and Biodiversity, School of Biological Sciences, The University of Hong Kong, Hong Kong SAR 999077

Abstract

Habitat anthropization is a major driver of global biodiversity decline. Although most species are negatively affected, some benefit from anthropogenic habitat modifications by showing intriguing life-history responses. For instance, increased recruitment through higher allocation to reproduction or improved performance during early-life stages could compensate for reduced adult survival, corresponding to “compensatory recruitment”. To date, evidence of compensatory recruitment in response to habitat modification is restricted to plants, limiting understanding of its importance as a response to global change. We used the yellow-bellied toad ( Bombina variegata ), an amphibian occupying a broad range of natural and anthropogenic habitats, as a model species to test for and to quantify compensatory recruitment. Using an exceptional capture–recapture dataset composed of 21,714 individuals from 67 populations across Europe, we showed that adult survival was lower, lifespan was shorter, and actuarial senescence was higher in anthropogenic habitats, especially those affected by intense human activities. Increased recruitment in anthropogenic habitats fully offset reductions in adult survival, with the consequence that population growth rate in both habitat types was similar. Our findings indicate that compensatory recruitment allows toad populations to remain viable in human-dominated habitats and might facilitate the persistence of other animal populations in such environments.

Publisher

Proceedings of the National Academy of Sciences

Subject

Multidisciplinary

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