View - Kowalewski, M. - Virginia Tech

VERMEIJ—EVOLUTION IN THE CONSUMER AGEdistribution if encounters with prey are lethal or ifprey respond by cowering in refuges.I have shown elsewhere (Vermeij, 1982a) thatunsuccessful predation is an extremely commonphenomenon. Few predators, no matter howsophisticated their technology, are 100% successfulin killing the prey they encounter, capture, orsubdue. Only sophisticated predators like rats, cats,mongoose, and humans that colonize island biotaswhose members had no previous evolutionaryexperience with enemies of comparably highperformance are capable of wiping out entire preyspecies. In all other cases, one or another stage inthe predator’s attack is marked by a high failurerate, and most prey species can persist in refuges,habitats or periods of time in which predators areinactive or absent. Failure rates of more than 90%have been recorded for some raptors (predatorybirds), seastars, and crabs (Dayton et al., 1977;Rudebeck, 1950–1951; Vermeij, 1982b).Unsuccessful predation is essential toantipredatory adaptation. If all attacks weresuccessful, then any prey living long enough toreproduce would have had no encounters withpredators, and therefore could not be adapted tothose predators. Failure provides an opportunityevolutionarily to “learn.” Every instance of failureby the predator “tests” some aspect of a preyindividual’s chemistry, behavior, or morphology.The phase of a predator’s attack with the highestpredator failure rate will be the phase to which theprey is best adapted. For example, crabs mayrecognize and capture most potential prey, but oftenhave low success rates during the subjugationphase. Molluscan adaptation against crabs istherefore concentrated on aspects that conferresistance to breakage or forced entry of the shell.On the other hand, many gastropods and bivalveshave well-developed escape responses to relativelyslow-moving predators such as seastars andgastropods. Here, adaptation may thus beconcentrated in the capture phase.On long time scales appropriate to the fossilrecord, predators have two principal effects. Thefirst is that, as major agents of selection, theyinfluence their victims’ phenotypes. If prey andpredator co-occur and encounter each other, theprey must be adapted to the predator, and alladaptations with respect to such functions asfeeding and mating must be consistent withadaptations to enemies, including predators.Second, prey species that are highly vulnerable tosuccessful attack by predators during all phases ofthe attack are confined to times and places whereencounters with predators are rare, fecundity of preycompensates for losses due to predation, or predatorsare constrained physically in feeding. Environmentswith reduced predation intensities often harborspecies with reduced metabolic capacities enforcedby such limiting factors as low temperatures, lowoxygen levels, low food supplies, high resistance tolocomotion (as in sediments), and high risks topredators. Examples of such refuges today includethe deep sea, caves, the upper intertidal zone, deeplayers of sediment, polar regions, and the bodies ofwell-defended host organisms (Vermeij, 1987).Predation does, of course, occur in theseenvironments, but it does so either at a low rate orduring very restricted times, or both. Predators thusexercise pervasive top-down control over manyspecies, whether this be expressed evolutionarilyor in terms of activity and distribution.A striking, and hitherto undocumented, patterndemonstrates the primary evolutionary influenceof predators over other species. In terms of absoluteperformance, predators of mobile prey haveachieved levels of sophistication beyond those ofanimals with other feeding habits. Organs of visionare best developed among highly active predatorsincluding cephalopods, many trilobites, spiders,decapod and stomatopod crustaceans, beetles andbugs and other insects, fish, and tetrapods. Thesense of hearing is extraordinarily developed innight-hunting owls and bats as well as amongraptors. Distance chemoreception among aquaticinvertebrates is largely confined to predatorygroups in gastropods and sea stars. Most gastropodsthat filter particles, graze algae or detritus, orconsume stationary animal prey sample incomingwater from all around, but they evidently cannotdetect food or enemies chemically at a distance.This capability is reserved for members of the clade377