Persistent predator–prey dynamics revealed by mass extinction

Abstract

Predator-prey interactions are thought by many researchers to define both modern ecosystems and past macroevolutionary events. In modern ecosystems, experimental removal or addition of taxa is often used to determine trophic relationships and predator identity. Both characteristics are notoriously difficult to infer in the fossil record, where evidence of predation is usually limited to damage from failed attacks, individual stomach contents, onesided escalation, or modern analogs. As a result, the role of predation in macroevolution is often dismissed in favor of competition and abiotic factors. Here we show that the end-Devonian Hangenberg event (359 Mya) was a natural experiment in which vertebrate predators were both removed and added to an otherwise stable prey fauna, revealing specific and persistent trophic interactions. Despite apparently favorable environmental conditions, crinoids diversified only after removal of their vertebrate consumers, exhibiting predatory release on a geological time scale. In contrast, later Mississippian (359-318 Mya) camerate crinoids declined precipitously in the face of increasing predation pressure from new durophagous fishes. Camerate failure is linked to the retention of obsolete defenses or "legacy adaptations" that prevented coevolutionary escalation. Our results suggest that major crinoid evolutionary phenomena, including rapid diversification, faunal turnover, and species selection, might be linked to vertebrate predation. Thus, interactions observed in small ecosystems, such as Lotka-Volterra cycles and trophic cascades, could operate at geologic time scales and higher taxonomic ranks. Both trophic knock-on effects and retention of obsolete traits might be common in the aftermath of predator extinction.Carboniferous | durophagy | biodiversity | paleontology | macroecology

Predator-induced macroevolutionary trends in Mesozoic crinoids

“…However, our data, as well as those for several other groups (13,37,38), indicate that such interactions can have consequences, directly or indirectly, at higher taxonomic levels. Most compelling are cases of increasing incidence of taxa with well-developed antipredatory defenses, and it has been suggested that taxa possessing such traits may be more prone to speciation (38).…”

Evolution of long-toothed fishes and the changing nature of fish–benthos interactions on coral reefs

“…In many cases, changes in fish morphology and the appearance of new higher taxonomic groups mark major shifts in the nature of fish-benthos interactions 14,19,20 . However, on modern reefs, and in aquatic systems in general, herbivory and other biotic interactions are characterized by considerable complexity 16,21 .…”

Cyst size trends in the genus Leiosphaeridia across the Mulde (lower Silurian) biogeochemical event

“…Therefore, this indirectly shows that top-down trophic controls (i.e., predation) could be an important factor in macroevolution and long-term changes in phenotype distributions (Stanley 2008, Sallan et al 2011, Voje et al 2015. In this way the association of the higher values of á with 4 th order highstands of the sea level is an indirect effect of higher diversities of potential consumers of leiospheres (in this case graptolites), with the high sea level conditions.…”

“…An increase in the diversity and productivity of prey could occur during the aftermath of an extinction event when the prey experiences relief from the negative effects of predation (Solé et al 2010), but eventually the long-term diversification of predators during the recovery phase following extinction (Sallan et al 2011) or delayed dispersal after immediate rediversification will down-regulate the prey to the presumed equilibrium values. Therefore, this indirectly shows that top-down trophic controls (i.e., predation) could be an important factor in macroevolution and long-term changes in phenotype distributions (Stanley 2008, Sallan et al 2011, Voje et al 2015.…”