CASCADE EFFECTS AMONG 4 TROPHIC LEVELS - BIRD PREDATION ON GALLS AFFECTS DENSITY-DEPENDENT PARASITISM

Effects of herbivore density on parasitization, bird predation, and interference between parasitoids and predators were tested using midge gall clusters of Giraudiella inclusa (Diptera, Cecidomyiidae) from Phragmites habitats. Winter predation of Blue Tits (Parus caeruleus) did not simply cause an additional mortality of midge larvae, but affected both midge and parasitoid species. Fifty-six percent of galls were parasitized, so that the average of 70% gall predation resulted in only 30% additional midge mortality. Out of the eight frequent parasitoid species, two showed positive density-dependent responses, two showed negative density-dependent responses, and four showed density-independent responses. However, in aggregate, percent parasitism was density independent. Birds preferentially pecked open large gall clusters and thereby caused a particularly high mortality of parasitoid species concentrated in large clusters. Selection pressure by birds against parasitoids with density-dependent responses suppressed the parasitoids' presumed ability to regulate host populations and probably altered parasitoid coexistence. Host plant characteristics affected distribution and abundance of galls, and also the subsequent pattern of parasitization and the percentage of bird predation. Such four-trophic-level cascade effects can be complex: shoot damage by stem-boring caterpillars induced side shoots, thereby increasing gall abundance and facilitating the inverse density-dependent endoparasitoid Aprostocetus gratus, since (1) gall clusters of side shoots were very small (enhancing percent parasitism), and (2) these small gall clusters were little preyed upon by birds.