Associative nitrogen fixation, C4photosynthesis, and the evolution of spittlebugs (Hemiptera: Cercopidae) as major pests of neotropical sugarcane and forage grasses

Abstract

AbstractNeotropical grass-feeding spittlebugs of several genera are important pests of pasture grasses from the southeastern USA to northern Argentina, and of sugarcane from southern Mexico to southern Brazil, causing estimated reductions of up to 70% in yield and estimated monetary losses of US $840–2100 million annually. With few exceptions, the species badly damaged by these spittlebugs are introduced C4grasses that exhibit associative nitrogen fixation. This study synthesizes evidence that the pest status of many tropical and subtropical grass-feeding spittlebugs is linked to associative N-fixation in their C4hosts. Recognition that associative N-fixation is a major factor in spittlebug host preferences should deepen understanding of spittlebug agricultural ecology and facilitate efforts to combat spittlebug pests. In particular, spittlebugs should be susceptible to manipulation of xylem transport solutes. However, reduction of nitrate fertilizer rates, increase in ammonium fertilizer rates, or enhancement of associative N-fixation as a consequence of genetic engineering could make hosts more susceptible to spittlebug attack. Because of their predilection for C4grasses, spittlebugs present a clear counterexample to the hypothesis that herbivores prefer C3plants to C4plants. Finally, it appears that declines in atmospheric carbon dioxide levels during recent geological history promoted the proliferation of C4grasses. This, compounded by human agricultural activities, has driven an ecological and evolutionary radiation of grass-feeding spittlebugs that presents continuing opportunities for the evolution of spittlebug pests.