Compensatory recruitment allows amphibian population persistence in anthropogenic habitats

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.

Keywords: amphibians; global change; recruitment; senescence; survival.

Fig. 1.

(A) Map showing the 67 western European populations of B. variegata monitored using capture–recapture methods. The distributional range of this species according to IUCN data (24) is displayed, although a few of the study populations occurred outside this range. (B and C) Examples of natural habitats: natural pond created by landslides (B) and rocky pools on riverbanks (C). (D–F) Examples of anthropogenic habitats: ruts in a logged forest (D), drinking trough in farmland (E), and puddles in a quarry (F).

Fig. 2.

(A–G) Demographic parameters of 67 B. variegata in natural and anthropogenic (“Anthrop”) habitats (farmland, quarry, and logged forest combined) in western Europe: annual survival probability (A), lifespan (i.e., the age at which 90% of the individuals alive after the first overwintering were dead) (B), senescence rate (i.e., the increase in mortality with age) (C), annual recruitment (D), survival elasticity (E), generation time ($T_b$, in years) (F), population growth rate (λ) (G), and net reproductive rate (R₀) (H). The plots were produced from raw demographic estimates. F statistics and P values are from metaregression models where demographic variables were log transformed and where survival and recruitment probabilities were on the logit scale. The models also accounted for differences in variance between anthropogenic and natural habitats (SI Appendix).

Fig. 3.

(A–F) Demographic rates of 21 B. variegata populations in anthropogenic habitats where human activities (quarrying and logging) were attenuated (“Atten”, 10 populations) or intense (“Intens”, 10 populations): annual survival probability (A), annual recruitment probability (B), survival elasticity (C), generation time ($T_b$, in years) (D), population growth rate (λ) (E), net reproductive rate (R₀) (F), and senescence rate (G). Sites with attenuated activities correspond to protected areas (i.e., protected forests and abandoned quarries in nature reserves), whereas sites with intense activities designate areas where logging and quarrying operations continued unabated outside protected zones (e.g., forests managed for timber production and active quarries). The plots were produced from raw demographic estimates. F statistics and P values are from metaregression models, where demographic variables were log transformed and where survival and recruitment probabilities were on the logit scale (SI Appendix).