Herbivore-mediated ecological costs of reproduction shape the life history of a desert cactus

Plant reproduction can be costly in terms of survival, growth, and future fecundity. Long-standing life history theory posits that reproductive strategies – when to reproduce and how much to invest in each reproductive event – are shaped by trade-offs between current and future fitness that result from these direct, demographic costs. Additionally, allocation to reproduction may incur indirect, ecological costs if it increases susceptibility to herbivores. Yet, ecological costs of reproduction have received little empirical attention and remain poorly integrated into life history theory. Here, we provide evidence for herbivore-mediated ecological costs of reproduction and show that these costs influence life history strategies. Field experiments with an iteroparous Chihuahuan desert cactus (Opuntia imbricata) indicated that greater reproductive effort (proportion of available meristems allocated to reproduction) led to greater attack by a specialist insect herbivore (Narnia pallidicornis) and that insect damage caused the abortion of initiated flower buds. We constructed an optimality model of size-dependent reproductive effort and compared predictions when ecological costs were included in the model versus predictions based solely on direct costs. The two sets of predictions were markedly different: inclusion of ecological costs shifted the optimal strategy toward flowering at smaller size and a more gradual increase in reproductive effort with size. Independent empirical data on size-dependent reproductive effort showed a good match with optimality predictions when ecological costs were included in the model, but were poorly described by the model when these costs were ignored. The results suggest that feedbacks between plant reproduction and herbivore damage have played an important role in shaping contemporary reproductive strategies.