Historical vertebrate herbivory drives ontogenetic shifts in plant defense across oceanic islands

Abstract

Islands with contrasting herbivore histories provide a natural framework to investigate the evolution of plant defenses. Theory predicts that on islands with historically intense vertebrate herbivory, juveniles maintain strong defenses while adults may reduce them once out of reach, whereas islands lacking vertebrate browsers show minimal ontogenetic differences and generally lower defenses. Alternatively, when extinct herbivores were particularly large, selection might also favor stronger adult defenses. Despite these theoretical expectations, empirical tests across multiple island systems remain scarce. In this study, we quantified leaf physical, chemical, and nutritional traits related to resistance and palatability in juvenile and adult individuals of 60 woody plant species across 33 families from six archipelagos: three with extinct large herbivores (New Zealand, New Caledonia, Mauritius) and three without vertebrate browsers (the Canary Islands, Azores, Channel Islands of California). We found that species from islands with historical herbivory exhibited overall lower defenses, with trait expression strongly shaped by ontogeny. Adults displayed higher phenolic concentrations and lower nutrient content than juveniles, reducing leaf palatability. By contrast, species from islands lacking herbivores showed no ontogenetic variation. These results reveal the lasting evolutionary legacy of extinct herbivores and show how herbivore history and ontogeny shape island plant defenses.