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Modern, skeleton-breaking predators, particularly teleosts, neoselachian sharks and rays, and decapod crustaceans, began to diversify in nearshore environments during the Jurassic Period Fig. Radiations of these durophagous taxa were accompanied by, and are thought to have stimulated, the evolution of architectural defenses in gastropods, bivalves, cephalopods, crinoids, and other marine invertebrates during the Mesozoic and Cenozoic Vermeij, , ; Meyer and Macurda, ; Aronson, a ; Harper, The macroevolutionary adaptations of gastropod shells to increasing predation pressure included increased spination, ribbing, and other defensive sculpture, decreased width and increased dentition of the aperture, and tighter coiling Vermeij, , Similar changes in the morphology of gastropod shells have occurred with increasing predation on smaller temporal scales Seeley, ; West et al.

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Increased expressions of antipredatory morphology in gastropods are also associated with spatial gradients in shell-breaking predation on a variety of scales e. Vermeij argued that the frequency of sublethal shell damage repaired cracks in a gastropod population should be positively related to the survival value of that population's morphological defenses: increased sublethal damage should imply decreased lethal predation. In agreement with this prediction, shell repair in gastropods generally increased in frequency beginning in the Jurassic Vermeij et al.

Nevertheless, interpreting the frequency of shell repair can be problematic. If only a few shells in a population display sublethal damage, then either the attack rate is high and most attacks are lethal, or both the lethal and sublethal attack rates are extremely low Schoener, A second assertion about sublethal damage is that by recording the frequency of sublethal encounters, such injuries provide an index of the selection pressure for antipredatory features Vermeij, Sih contested this claim, arguing that frequent encounters between predators and prey are not necessary to select strongly for the evolution of antipredatory traits in prey.

Thus, the significance of sublethal damage to gastropods is not entirely clear. Unlike the situation with gastropods, sublethal damage is relatively easy to interpret in ophiuroids and crinoids. This is because predators generally attack the arms of these echinoderms before attacking the centrally-located viscera Meyer, ; references in Aronson, , ; Nichols, The proportion of individuals regenerating one or more arms in a population is an indicator of the frequency of predator-prey encounters and, hence, the frequency of lethal predation in living and fossil ophiuroids and crinoids Meyer, ; Aronson, b ; Oji and Okamoto, Frequencies of sublethal arm injury were higher in living populations of tropical ophiuroids than in an ecologically comparable fossil population of confamilial ophiuroids from the Jurassic, a result that supports the idea of a Mesozoic increase in skeleton-breaking predation Aronson, b.

The adaptations of gastropods for drilling molluscan prey also increased during the Mesozoic and Cenozoic Vermeij, As a result, the thickness of prey shells, the frequency of drilled prey, the match between predator and prey sizes, and the localization of drillholes to thin areas of prey shells should have increased through time Kelley and Hansen, , Temporal patterns of drilling predation are complex and noisy, however, and they do not always follow these predictions e.

An added complication is that drilling gastropods are themselves subject to changing levels of durophagy, including both shell-breaking predation and cannibalistic drilling Vermeij et al. Increasing durophagous predation need not result in the increased expression of defensive features in prey.

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A more direct consequence of increased predation, which we have documented for ophiuroids, is a decline in prey abundance. The primary predators of epifaunal ophiuroids living in dense populations are slow-moving invertebrates, including asteroids and polychaetes Fig. On a macroecological scale, the diversification of fast-moving, durophagous predators in the Mesozoic caused a global decline in the occurrence of these dense, low-predation ophiuroid populations Aronson, b , Durophagous predators originated onshore, eliminating epifaunal, suspension-feeding populations from soft-substratum habitats Bottjer and Jablonski, ; Jablonski and Bottjer, , From the Jurassic onward, epifaunal suspension-feeders on soft substrata were replaced by infaunal and more mobile epifaunal suspension-feeders, giving onshore soft-substratum communities their modern, bivalve-dominated ecology Stanley, ; Vermeij, ; Jablonski and Bottjer, ; Bottjer and Ausich, As a broad generalization, predation is lower and community structure is archaic in offshore, deep-water habitats compared to nearshore, shallow-water habitats.

The restriction of dense ophiuroid populations in coastal waters during the Mesozoic is an aspect of the onshore-offshore trend. As another example, stalked crinoids were abundant in shallow water in the Paleozoic and early Mesozoic Meyer and Macurda, ; Oji, ; Bottjer and Jablonski, The unstalked crinoids order Comatulida , which are mobile and thus presumably better able to evade predators, replaced the stalked crinoids in shallow water.

Smith suggested that the onshore-offshore pattern is an artifact of geology rather than a biological effect. There are more Mesozoic onshore and more Cenozoic offshore deposits available for study, potentially biasing the fossil record in the direction of the perceived macroevolutionary trend. Regardless of the distribution of rock outcrops, however, all stalked crinoids and most dense ophiuroid populations now live only in deep, offshore habitats.

Soft sediments in shallow water are now dominated by bivalves, and the skeletonized invertebrates that have been studied are generally better defended against predators than were their ecological equivalents early in the Mesozoic.

Trophic relationships in the Mesozoic evolved within the context of global events. The end-Permian mass extinction opened the way for the diversification of modern predators, perhaps by creating an ecological vacuum of vacant niches Sepkoski, Escalation of predator-prey interactions during the Mesozoic also coincided with increased productivity, which apparently supplied the energy required to drive the acquisition of antipredatory features in prey Rosenzweig and McCord, ; Bambach, ; Vermeij, ; Martin, Evolutionary innovations of predators and prey transcended the end-Cretaceous mass extinction, and escalation continued in the Cenozoic.

Episodes of elevated extinction in the Cenozoic selectively wiped out well-defended prey; this set back escalatory trends, but only temporarily Vermeij, , b ; Jablonski, Temporal trends in durophagy are mirrored by modern biogeographic patterns in that shell-breaking predation increases with decreasing latitude. Defensive features of gastropod shells, including heavy calcification, spines, ribs, tight coiling, narrow apertures, and low spires, increase along the same latitudinal gradient Vermeij, ; Palmer, ; see Leighton [] for a Paleozoic example.

Escalation has occurred to a greater extent in the tropics in part for purely physiological reasons: calcification and enzymatic activity are more rapid and less energetically expensive at higher temperatures Graus, ; Vermeij, As a result, shells are comparatively thick and ornate in the tropics, and thin and plain at temperate and polar latitudes Vermeij, Another reason is that species diversity and the rate of evolution of morphological novelties are greater in the tropics than at higher latitudes Jablonski, ; Rosenzweig, Well-defended mollusks in the tropics are particularly vulnerable to extinction as temperature and productivity decline Vermeij, , but there may be no overall bias toward greater extinction vulnerability near the equator Raup and Jablonski, ; see also Clarke, Although low temperatures depress shell-drilling activity by lowering metabolic rates Kabat, , predation by shell-drilling gastropods is thought to increase with increasing latitude as the shell-breaking activity of the predators of those drillers declines Vermeij et al.

Preliminary observations using scuba in McMurdo Sound suggest that shell-drilling predation is intense in at least some antarctic shallow-water habitats R.

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In this sense the analogy of spatial and temporal gradients in predation is imperfect: shell-drilling increased in the Mesozoic, but apparently it also increases toward the poles. The consumption of macrophytes is as fundamental a force as predation in structuring living, shallow-water benthic communities in the temperate zone and the tropics reviewed in Aronson, Vermeij and Lindberg recently suggested that herbivory, which has evolved many times in many clades, is a derived condition relative to detritivory, microphagy, and predation.

As an example, sea urchins possessing a robust Aristotle's lantern the jaw apparatus are members of the Modern evolutionary fauna Sepkoski, , and these herbivores may have been important in driving the modernization of algal assemblages during the Cenozoic Steneck, Modern macrophyte-herbivore relationships are a product of the Mesozoic marine revolution, and like predator-prey relationships they were probably driven by increased productivity in the Mesozoic.

In contrast, herbivory was apparently of minor importance during the Paleozoic Vermeij and Lindberg, Cooling in the late Eocene was thus the beginning of a long-term shift from the cool-temperate climate of the Eocene to the glaciated, polar climate found in Antarctica today Lear et al.

Climatic changes in Antarctica and elsewhere during the late Eocene may have been related to extraterrestrial impacts, but causal connections have not yet been clarified Clymer et al.


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Climatic cooling directly or indirectly reduced predation pressure, causing a fundamental shift in the structure of benthic communities in Antarctica. Most of what we know about this critical time in the history of the antarctic benthos comes from studies of the La Meseta Formation at Seymour Island, off the Antarctic Peninsula. The La Meseta Formation, a marine deposit composed of siliciclastic sediments, forms a large plateau on the northern portion of the island Fig.

The sediments are locally fossiliferous, constituting the most abundant source of Cenozoic marine fossils in Antarctica. The La Meseta Formation was deposited in a complex of nearshore, shallow-water settings Sadler, A high diversity of marine fossils throughout the formation and the absence of any clear indicators of fluvial deposition or subaerial exposure indicate fully marine conditions, possibly at the mouth or immediately seaward of a bay-like or estuary-like basin see Elliott and Trautman, ; Marcellari, ; Sadler, Porebski , interpreted the La Meseta as representing a series of three cycles of sedimentary deposition.

The three stacked, sequence-stratigraphic units were produced by episodes of faulting, subsidence, and infilling. Temporal correlation of the La Meseta Formation to regions outside Antarctica has proven problematic. The precise ages of the individual sedimentary units are not required for the present discussion, but it is critical that the depositional interval represent a time span that is sufficient to reflect climatically mediated ecological change.

The La Meseta appears to span an interval as long as late early Eocene to early Oligocene, although the formation may only include the middle and late Eocene Wrenn and Hart, ; Fordyce, ; Cocozza and Clarke, ; Gazdzicki et al.

Berggren et al. The important point is that the La Meseta Formation records the marine faunas that lived in shallow-water habitats off the Antarctic Peninsula during a period of abrupt cooling and expansion of ice sheets in the late Eocene or possibly early Oligocene, around 35 million years ago Gazdzicki et al. During this time, a series of minor, climatically driven extinction events occurred around the world Prothero , Beginning in the late Eocene, declining temperatures accompanied by reduced shelf area due to glaciation altered the geographic and bathymetric ranges of a variety of antarctic taxa Zinsmeister and Feldmann, ; Clarke and Crame, ; Meyer and Oji, ; Blake and Aronson, The effects of changing climate on fish and crabs are of particular interest because of their importance as predators in benthic communities.

Isolated teleost bones are scattered throughout the La Meseta Formation but not in sufficient numbers to determine temporal patterns of abundance and diversity. Crabs are found throughout, but shark remains are concentrated in the lower earlier units Feldmann and Wilson, ; Long, The distribution of batoids through La Meseta time is not known, as skate teeth have been found at only one site, midway up the formation Long, The early Tertiary teleost fauna probably went extinct in Antarctica sometime around the Eocene-Oligocene transition, and the current, endemic fauna of notothenioids and liparids radiated some time later Eastman and Clarke, Likewise, crabs and sharks disappeared from Antarctica in association with late Eocene and subsequent cooling trends Dayton et al.

At least one species of crab, however, survived into the early Miocene Feldmann and Crame, Crabs and sharks are now absent from shallow benthic communities in Antarctica, and teleosts and rajids are minor players in terms of durophagous predation. These faunal changes are correlated with declining temperatures. Since global cooling by itself was probably not sufficient to cause widespread extinction Clarke, , and since durophagous predation remains strong in the Arctic Dayton, , the causal connections in Antarctica must be complex and indirect.

Whatever the causes, the loss of skeleton-breaking predators in the late Eocene disrupted trophic linkages in shallow-water habitats, with profound and lasting consequences for community structure. During expeditions to Seymour Island in the austral summers of and , we found dense, monospecific concentrations of hundreds to thousands of ophiuroids and tens to hundreds of crinoids in the La Meseta Formation Aronson et al.

We located six assemblages of the ophiuroid Ophiura hendleri Blake and Aronson order Ophiurida and four assemblages of the crinoid Metacrinus fossilis Rasmussen order Isocrinida. The good state of preservation of the fossils, their concentration within single horizons, the lack of bioturbation, and other sedimentological evidence indicate that the animals were buried rapidly and preserved in place, and not transported significant distances. These autochthonous fossil assemblages represent localized, short-lived populations.

All of the assemblages were found close to the central plateau Fig. Their placement puts them close to the end of La Meseta time, when crabs and sharks had essentially disappeared and when teleosts may already have been in decline as well.


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Brett et al. Such variations affect the likelihood that echinoderm assemblages will be subject to rapid burial and autochthonous preservation. Sedimentation may have been more rapid near the top of the uppermost sequence-stratigraphic unit of the La Meseta Formation than further down in that unit, and the result would have been a sedimentological bias favoring the preservation of ophiuroid and crinoid assemblages near the top. This possibility could account for the vertical distribution of dense assemblages within the uppermost sequence-stratigraphic unit.

It does not, however, explain why no dense assemblages were found anywhere within the lower two units. Those lower units would have shown the same bias toward preservation of echinoderms during the phases of their cycles in which sedimentation was rapid. An ecological explanation is more likely, particularly in light of our inferences about predation pressure. Waves and turbulence in stably stratified flows: based on the proceedeings of a conference on waves and turbulence in stably stratified flows, organized by the Institute of Mathematics and its Applications and held at the University of Leeds in December.

Climatic changes on a yearly to millennial basis - Proceedings of the second Nordic symposium on climatic changes and related problems, Stockholm, Sweden, May , Jean Charcot.

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Ozone depletion, greenhouse gases, and climate change - Proceedings of a joint symposium by the Board on Atmospheric Sciences and Climate and the Committee on Global Change. Dynamics, transport and photochemistry in the middle atmosphere of the southern hemisphere - Proceedings of the NATO advanced research workshop on dynamics, transport and photochemistry in the middle atmosphere of the southern hemisphere, San Francisco. The changing atmosphere: report on the Dahlem workshop on the changing atmosphere, Berlin , November British Antarctic Terra Nova expedition metereology, Vol.

The Arctic and environmental change - Papers presented at the Royal Society discussion meeting on the Arctic environmental change held on October Climate change impacts, adaptations and mitigation of climate change: scientific and technical analyses. International conference on the role of the Polar regions in global change, Vol.