Collapse of dispersal trait diversity across a long‐term chronosequence reveals a strong negative impact of frugivore extinctions on forest resilience

Understanding how seed dispersal disruption may alter plant community diversity and dynamics over a large temporal scale remains a challenge. Here, we use a long‐term chronosequence to compare changes in the richness and composition of different dispersal trait assemblages in communities established before and after human colonization in the Mascarene archipelago. Our study was located on Réunion on the slopes of the Piton de la Fournaise which is one of the most active volcanoes worldwide. We analysed 151 vegetation surveys on lava flows dated between 1401 AD and 1956 AD and in tropical rainforests established on older substrata. We defined five classes of substratum age, according to the well‐known chronology of native frugivore defaunation: ‘old substrata’ and [1401, 1665[ when frugivores were abundant and diverse before permanent human settlement; [1665, 1800[ when large‐bodied frugivore populations were strongly reduced; [1800, 1900[ when large‐bodied frugivores went extinct and small‐bodied frugivores were still abundant; [1900, 1956] decline in the populations of small‐bodied frugivores. Based on dispersal traits, we categorized 146 native woody species as anemochorous, small fleshy‐fruited or large fleshy‐fruited, i.e. plant of which fruit could not theoretically be dispersed by extant frugivores. Changes in dispersal trait diversity strongly correlated with the chronology of defaunation. Species‐rich communities settled before human colonization was strongly dominated by fleshy‐fruited species. Large fleshy‐fruited plants in the oldest communities settled after human colonization declined markedly and almost disappeared after 1800. The richness of small fleshy‐fruited plants decreased less rapidly across the chronosequence, with medium levels on [1665, 1800[ and [1800, 1900[ lava flows and low levels on [1900, 1956] lava flows. Conversely, the richness of anemochorous plants remained unchanged. Communities settled before human colonization had a similar composition. Fleshy‐fruited assemblages showed strong species loss across the chronosequence, while anemochorous assemblages showed strong species turnover, which was probably due to lower dispersal limitation. Synthesis. Our results provide the first insights into the tremendous impact that frugivore extinction has on plant colonization dynamics over 300 years. The dramatic loss of fleshy‐fruited plant diversity on historical lava flows highlights the irreplaceable dispersal role played by frugivores, especially large‐bodied species. The conservation of plant–animal mutualistic interactions is invaluable and refaunation efforts need to be undertaken in areas where frugivores have been extirpated.