View - Kowalewski, M. - Virginia Tech

LABANDEIRA—PREDATORS, PARASITOIDS, AND PARASITESversions of carnivory—though there is a smallliterature on the more poorly known associationsof marine invertebrate parasites. By contrast,research on the history of terrestrial invertebratecarnivory has been dominated by studies ofparasitoids and parasites, and far fewer of predators,particularly during the past 40 years (Askew, 1979;Price, 1980; Godfray, 1994; Schmid-Hempel, 1998).The work on parasites and especially parasitoids hasbeen a primary source of data for ecological theoriesof community structure, particularly valuable forstudies of tritrophic interactions (Abrahamson andWeis, 1997), for instance, and for food-web analyses(Godfray et al., 1999). In fact, many investigationscenter around whether the parasitic habit promotesdiversification (Wiegmann et al., 1993; Cronin andAbrahamson, 2001), and if individual phylogeniesof hosts and their parasites reflect coevolvedassociations (Lyal, 1987; Kim, 1988; Hafner andNadler, 1988). Recent biological work and the fossilhistory of parasitoids and parasites supports theconclusion that more accommodationistmechanisms, typified by the coexistence of host andconsumer, characterize the post-Triassic history ofcarnivory in freshwater and terrestrial ecosystems.What was trophic structure like beforeparasites and parasitoids?—There is no directfossil evidence for insect parasitism orparasitoidism on arthropods in continentalecosystems before the Early Jurassic. Evidencefrom the phylogenetic relationships of noninsectanparasites and parasitoids would strongly supportthe presence during this interval of freshwater orterrestrial members of the phyla Acanthocephala,Platyhelminthes, Annelida, Nematoda,Nematomorpha, and Pentastoma, whose hostspresumably were vertebrates, arachnids, or insects.The absence of direct evidence for parasitic insectsis countered by phylogenetic relationshipsindicating that some of these life-habits originatedduring the Permian to Late Jurassic (Waage, 1979),in, for example, the Phthiraptera (Kim, 1988),Siphonaptera (Traub and Starcke, 1980), andStrepsiptera (Kinzelbach and Pohl, 1994). Theseorders could have existed for all that time as ghostlineages alongside their earlier occurring, freelivingsister groups, but this is unlikely. In otherclades dominated by parasitoids, which have aconsiderably better fossil record than parasites, therecord reveals explosive diversification for theHymenoptera and to a lesser extent the Dipteraduring the Middle Jurassic to mid-Cretaceous. Thuscontinental invertebrate carnivory from the latestSilurian to Early Jurassic can be characterized asentirely or near-entirely predaceous in nature. Thefossil record indicates that predators were the soleor overwhelmingly dominant carnivores during theearliest Pennsylvanian to the mid-Cretaceous, asevidenced by the dominance of Odonatoptera,some protorthopteran lineages, Titanoptera,gerromorph Hemiptera, Raphidioptera,Megaloptera, Planipennia, and caraboid andstaphylinoid Coleoptera (Fig. 4). The presence ofonly predator guilds of carnivores in continentalecosystems must have had a profound effect onthe regulation of herbivorous and otherheterotrophic organisms (see Eggleton andBelshaw, 1992), particularly since considerableevidence shows that modern trophic webs arestrongly regulated by parasites and parasitoids(DeAngelis, 1992; Godfray et al., 1999).Accordingly, in a world without these two keycarnivore guilds, one would expect simpler foodwebs with linear trophic pathways (Dunne et al.,2002), and the absence of lineages with typicaldefensive strategies to ward off parasites andparasitoids, such as small size, concealment,exoskeletal or other types of mechanical isolation,and behaviors to reduce the risk of attack such asparental or group care and protection. The latterwould include the caste-based, regulated societiesseen today in social insects—and this may explainthe rise of sociality in termites, ants, wasps, andbees (Wilson, 1992) during the Mesozoicdiversification of parasitoids.Is there trophic-level selectivity at massextinctions?—Among terrestrial carnivorousinvertebrates, insects have the best fossil record.The insect fossil record is characterized by twoimportant extinction events. The first is deducedfrom the geochronologic distributions of order-rankclades. This was a catastrophic extinction at the237