Downsized mutualisms: Consequences of seed dispersers’ body-size reduction for early plant recruitment

Extinction-driven, body-size reduction of seed dispersers (i.e. an ecological downsizing resulting from severe defaunation) can entail the loss of unique ecological functions, and impair plant regeneration. However, the manner in which the downsizing of mutualistic animals affects seed dispersal and plant recruitment remains understudied. Here, we took advantage of a natural experiment in the Canarian archipelago to document the consequences of lizards body-size reduction (Gallotia, Lacertidae) on the recruitment of Neochamaelea pulverulenta (Rutaceae), which relies exclusively on these frugivores for seed dispersal. Subsequent to the arrival of humans (ca. 2000–2500 yr BP), the extinction of large-bodied lizards generated a gradient of increasing defaunation on the three islands inhabited by this plant. We hypothesized a significant reduction, and eventually collapse, of early seedling recruitment mirroring the defaunation intensity of the frugivores. We sampled 42 populations spanning the whole geographic range of the plant to examine the quantitative (age structure pattern) and qualitative components (proportion of seedlings growing outside the canopy, number of seedlings established outside the canopy relative to the number of adults – effective recruitment rate, and seedling vigour) of plant regeneration. Our results show that the age structure patterns did not differ among the three contrasted insular scenarios. However, we found significant reductions in seedling recruitment outside the canopy, effective recruitment rate, and delayed negative effects on seedling vigour in populations hosting small- to medium-sized lizard species. Thus, extirpation of large seed-dispersers did not cause substantial reductions in quantitative components of seed dispersal, but determined declines in qualitative aspects impairing dispersal effectiveness. Our study highlights the importance of examining all components of the dispersal and recruitment process to properly document the regeneration outcomes of plants in defaunated, downsized ecological scenarios.