View - Kowalewski, M. - Virginia Tech

VERMEIJ—EVOLUTION IN THE CONSUMER AGEEVOLUTION IN THE CONSUMER AGE:PREDATORS AND THE HISTORY OF LIFEGEERAT J. VERMEIJDepartment of Geology, University of California at Davis, One Shields Avenue, Davis, California 95616 USAABSTRACT—Three properties of predation make this form of consumption an important agency of evolution:universality (all species have predators), high frequency (encounters of prey with predators test both parties often),and imperfection (many predatory attacks fail, enabling antipredatory selection to take place). On long time scales,predators have two principal effects: they influence their victims’ phenotypes, and prey species that are highlyvulnerable to all phases of predatory attacks are evolutionarily restricted to environments where predators arerarely encountered. Although predator and prey can affect each other’s behavior and morphology on timescalescommensurate with individual lifespans, predators have the evolutionary upper hand over the long run, especiallyin the expression of sensory capacities, locomotor performance, and the application of force. Only in passive defenses(armor, toxicity, large body size) does escalation favor the prey. In a review of methods for inferring predation in thegeological past, I argue against the use of whole assemblages, which combine species of contrasting adaptive type.Instead, I strongly favor species-level and clade-level approaches (including examples of clade replacement) inwhich comparisons among places and among time intervals are made within the same adaptive types and the samephysical environments. The available evidence, much of which comes from studies of shell drilling and shell breakage,points to temporal increases in both predator power and prey defenses. Escalation between species and their enemies,including predators, has proceeded episodically against a backdrop of generally increasing productivity andincreasing top-down evolutionary control by high-energy predators during the Phanerozoic, the consumer age.INTRODUCTIONCONSUMPTION OF ONE organism byanother is a universal phenomenon in all livingecosystems. Herbivory (eating plants), predation(a large animal or sometimes a plant consumingpart or the whole of another animal), and parasitism(a small animal, fungus, microbe, or plant drawingnutrients from another organism) are differentmanifestations of this phenomenon. Consumptionis itself a special case of competition for food, orchemical energy. Competition in this broadest senseis the central process common to all economicsystems, and has been with us since the origin oflife. Consumption is a derived form of competition.Parasitism could be a very ancient form ofconsumption, whereas herbivory and predationhave become prominent only during the last 600to 700 million years, the interval encompassing thelatest Proterozoic to the Recent, a phase inecological history we may call the consumer age.These forms of consumption have played animportant role in evolution. They represent a typeof top-down evolutionary control that hasprofoundly affected the phenotypes anddistribution of all species, a control that has likelyintensified through time.In this chapter, I first summarize whyconsumption in general, and predation inparticular, should have such a far-reachinginfluence on evolution and in the history of life.Second, I review and evaluate the kinds ofevidence that are available about predation in thefossil record. Third, I discuss briefly the temporaltrends in predation and what these trends implyabout the history of ecosystems and theirconstituent species. Along the way, I suggestavenues for further research, concentratingespecially on better temporal resolution ofevolutionarily important predation-relatedinnovations and on temporal studies of lineagesand clades in physically similar habitats.375