Defaunated and invaded insular tropical rainforests will not recover alone: Recruitment limitation factors disentangled by hierarchical models of spontaneous and assisted regeneration

Most tropical forests are now severely degraded and their ability to recover is highly dependent on frugivores which ensure seed dispersal for most woody plants. The global collapse of large vertebrates therefore raises major concerns about tropical forest succession, but few field studies have been conducted to disentangle recruitment limitations during disrupted succession.This study took place on Reunion (Mascarenes) where all large native frugivores have been extinct since human colonisation in 1665 and where multiple invasions threaten native ecosystems. We set up 20 experimental blocks on a lava flow dated back to 1800, in plant-impoverished post-defaunation vegetation bordered by old-growth forests. We assessed fecundity, seed dispersal and seedling recruitment of the complete fleshy-fruited plant community and used Bayesian analyses to disentangle the impact of multiple factors on these key processes. In the same blocks, we sowed four native trees assumed to be disperserless to test their capacity to establish, controlling for two additional post-dispersal limitations (seed predation and competition with invasive plants).On the flow, small-seeded native plants were fairly dispersed but did not recruit, probably due to strong competition with invasive plants; the few native species that recruited somehow were mostly medium-seeded plants that were still dispersed; large-seeded plants were absent from seed rain (which shows that invasive frugivores did not replace extinct ones) and subsequently from spontaneous recruitment. Instead, some alien plants, notably the tiny-seeded highly dispersed Clidemia hirta and the medium-seeded Psidium cattleianum largely dominated seedling recruitment. Native plants recruited better at the forest margin, including some large-seeded species nearby mother trees.Sown large-seeded species were able to emerge and survive in all plots whatever the treatment, which demonstrates that dispersal loss was the primary cause of regeneration failure on the flow.Synthesis. The strong modulation of the establishment capacity of native plants by seed mass shows that invasive plants win by forfeit of large-seeded plants after native frugivores loss. Our study emphasises the fundamental role of dispersal loss and competition with invasive plants in the disruption of ecological succession, as well as the urgency of restoring seed dispersal and strengthening biosecurity regulations. La plupart des forets tropicales sont aujourd'hui gravement degradees et leur capacite a se reconstruire apres perturbation depend fortement des frugivores qui assurent la dispersion des graines. L'effondrement global des grands vertebres souleve donc des inquietudes majeures pour la la succession ecologique en foret tropicale, mais peu d'etudes de terrain ont ete menees pour demeler les limitations du recrutement dans ce contexte.Cette etude se deroule a la Reunion (archipel des Mascareignes) ou tous les grands frugivores indigenes ont disparu depuis la colonisation humaine en 1665 et ou de multiples invasions menacent les ecosystemes indigenes. Nous installons 20 blocs experimentaux sur une coulee de lave datant de 1800, dans une vegetation post-defaunation tres appauvrie et flanquee de forets anciennes. Nous evaluons la fecondite, la dispersion des graines et le recrutement des plantules pour l'ensemble des plantes a fruits charnus, et nous utilisons des analyses bayesiennes pour demeler l'impact de multiples facteurs sur ces trois processus cles. Dans les memes blocs, nous semons quatre arbres indigenes supposes sans disperseur afin de tester leur capacite a s'etablir, en controlant deux limitations post-dispersion supplementaires (predation des graines et competition avec les plantes envahissantes).Sur la coulee de 1800, les plantes indigenes a petites graines sont relativement bien dispersees mais ne peuvent recruter spontanement, probablement en raison d'une forte competition avec les plantes envahissantes; les quelques especes indigenes capables de recruter sont principalement des plantes a graines moyennes qui sont encore dispersees; les plantes a grosses graines sont absentes de la pluie de graines (ce qui montre aussi que les frugivores introduits n'ont pas fonctionnellement remplace les especes eteintes) et par consequent du recrutement spontane. A l'oppose, certaines plantes exotiques dominent tres largement le recrutement, notamment l'espece a petites graines Clidemia hirta qui archi-domine la dispersion et l'espece a graines moyennes Psidium cattleianum. Les plantes indigenes recrutent davantage a la limite de la foret ancienne, y compris certaines especes a grosses graines a proximite des semenciers.Les especes a grosses graines semees sont capables de lever et survivre dans tous les blocs, quel que soit le traitement, ce qui demontre que la perte de la dispersion est la cause principale de leur absence sur les coulees historiques du Piton de la Fournaise.Synthese. La forte modulation de la capacite d'etablissement des plantes indigenes par la masse de graine montre que les plantes envahissantes gagnent par forfait des plantes indigenes a grosses graines. Notre etude souligne le role fondamental de la perte de la dispersion depuis l'extinction des frugivores indigenes et de la competition avec les plantes envahissantes dans l'alteration de la succession ecologique, ainsi que l'urgence de restaurer la dispersion des graines et de renforcer les reglementations en matiere de biosecurite. We combine observational and experimental approaches to disentangle recruitment limitation factors during primary succession on Reunion. We show on a typical historical lava flow that small-seeded native plants that are still dispersed cannot establish due to strong post-dispersal limitations and that native large-seeded plants cannot establish due to frugivore loss. Direct sowing of native plants with higher competitive ability offers promising prospects for future ecological restoration programmes.image

Automated summary

Based on field surveys and experiments conducted on Reunion Island, this study found that the regeneration of native plants is limited by seed dispersal and competition with invasive plants. The findings emphasize the importance of seed dispersal and competition with invasive plants in ecological succession, as well as the urgent need to restore seed dispersal and strengthen biosecurity regulations.