Steven M. Stanley

A double mass extinction at the end of the paleozoic era.

Three tests based on fossil data indicate that high rates of extinction recorded in the penultimate (Guadalupian) stage of the Paleozoic era are not artifacts of a poor fossil record. Instead, they represent an abrupt mass extinction that was one of the largest to occur in the past half billion years. The final mass extinction of the era, which took place about 5 million years after the Guadalupian event, remains the most severe biotic crisis of all time. Taxonomic losses in the Late Permian were partitioned among the two crises and the intervening interval, however, and the terminal Permian crisis eliminated only about 80 percent of marine species, not 95 or 96 percent as earlier estimates have suggested.

Anatomy of a regional mass extinction; Plio-Pleistocene decimation of the western Atlantic bivalve fauna

The Early Pliocene marine faunas of the southeastern United States were distinct from those of the Bahamas and Caribbean, apparently being separatedfrom them by a zone of cool upwelling. Study of the fates of 361 Early Pliocene bivalve species reveals that a regional mass extinction occurred in the Eastern United States beginning in Late Pliocene time, when continental glaciers expanded, and continued into Early Pleistocene time, eliminating perhaps as many as 65% of the Early Pliocene species. Several patterns suggest that refrigeration during intervals of glacial expansion was the primary cause. The 57 bivalve species that have survivedfrom the tropical zone of Florida all range into nontropical zones today: the mass extinction operated as a thermal filter, eliminating all purely tropical species. Endemic Early Pliocene species experienced especially low survivorship (15%7o) and most of the casualities of these stenothermal forms came early, in Late Pliocene time. A larger percentage of eurythermal Early Pliocene species survived; and most of those that did not, died out relatively late, during cold Early Pleistocene glacial intervals when even Florida became nontropical. Several observations oppose the hypothesis that Pleistocene regressions would have caused heavy extinction even in the absence of refrigeration. Among these are (1) the fact that in the Eastern Pacific Pleistocene extinction was weak even for species endemic to the temperate-warm temperate shelf, which was areally smaller than the shelf of the southeastern United States, and (2) the fact that even Western Atlantic species that were small, abundant, and adapted to muddy conditions suffered heavy losses.

Rates of evolution

For some higher taxa, species can be identified in the fossil record with a high degree of reliability. The great geological durations of species indicate that phyletic evolution is normally so slow that little change occurs within a lineage during 10 5 –10 7 generations. Failure to recognize sibling species in the fossil record has no bearing on this conclusion because they embody virtually no morphological change. Although slowness is the rule, we have no more precise assessment of morphological rates of phyletic evolution for any major taxon. Morphological data that have been assembled to assess rates of phyletic evolution have been meager, unrepresentative, and predominantly reflective of nothing more than body size. Net selection pressures within long segments of phylogeny—even ones that embrace large amounts of evolution—are infinitesimal and seemingly unsustainable against random fluctuations. This suggests that natural selection operates in a highly episodic fashion. Rates of adaptive radiation and extinction at the species level can be estimated for many taxa and, from them, rates of speciation in adaptive radiation. Species selection should universally tend to increase rate of speciation and decrease rate of extinction, yet these rates are positively correlated in the animal world, apparently because they are linked by common controls: both rate of speciation and rate of extinction seem to increase with level of stereotypical behavior and to decrease with dispersal ability. Only a few “supertaxa” have been able to combine high rates of speciation with moderate rates of extinction.

Population size, extinction, and speciation: the fission effect in Neogene Bivalvia

The extinction of a species represents reduction of both geographic range and population size to zero. Most workers have focused on geographic range as a variable strongly affecting the vulnerability of established species to extinction, but Lyellian percentages for Neogene bivalve faunas of California and Japan suggest that population size is a more important variable along continental shelves. The data employed to reach this conclusion are Lyellian percentages for latest Pliocene (-2 ma old) bivalve faunas of California and Japan (N = 245 species). These regions did not suffer heavy extinction during the recent Ice Age, and for each region the Lyellian percentage is 70%-7 1%. Discrepancies in population size appear to explain the following differences in survivorship to the Recent (Lyellian percentage) for three pairs of subgroups: (1) burrowing nonsiphonate species (42%) versus burrowing siphonate species (84%), which suffer less heavy predation; (2) burrowing nonsiphonate species of small size (73%) versus burrowing nonsiphonate species of large body size (96%); (3) Pectinacea (30%) versus other epifauna (71%), which suffer less heavy predation. During the Mesozoic Era, when predation was less effective in benthic settings, mean species duration for the Pectinacea was much greater (- 20 ma). Along the west coast of North and Central America, mean geographic range is greater for siphonate species of large body size than for siphonate species of small body size and greater still for pectinacean species. These ranges are inversely related to mean species longevity for the three groups, which indicates that geographic range is not of first-order importance in influencing species longevity. Species with non- planktotrophic development neither exhibit narrow geographic ranges along the west coast of North and Central America nor have experienced high rates of extinction in California and Japan. Rates of extinction are so high for Neogene pectinaceans and nonsiphonate burrowers that without enjoying high rates of speciation these groups could not exist at the diversities they have maintained during the Neogene Period. They are apparently speciating rapidly because of thefission efect: the relatively frequent generation of new species from populations that are fragmented by heavy predation. Thus, ironically, there may be a tendency for high rates of speciation to be approximately offset by high rates of extinction. Only if mean population size for species in a particular group becomes extremely small is it likely to result in a high rate of extinction and a low rate of speciation-and hence a dramatic decline of the group. The fission effect may contribute to the general correlation in the animal world between rate of speciation and rate of extinction.

An Analysis of the History of Marine Animal Diversity

Abstract According to when they attained high diversity, major taxa of marine animals have been clustered into three groups, the Cambrian, Paleozoic, and Modern Faunas. Because the Cambrian Fauna was a relatively minor component of the total fauna after mid-Ordovician time, the Phanerozoic history of marine animal diversity is largely a matter of the fates of the Paleozoic and Modern Faunas. The fact that most late Cenozoic genera belong to taxa that have been radiating for tens of millions of years indicates that the post-Paleozoic increase in diversity indicated by fossil data is real, rather than an artifact of improvement of the fossil record toward the present. Assuming that ecological crowding produced the so-called Paleozoic plateau for family diversity, various workers have used the logistic equation of ecology to model marine animal diversification as damped exponential increase. Several lines of evidence indicate that this procedure is inappropriate. A plot of the diversity of marine animal genera through time provides better resolution than the plot for families and has a more jagged appearance. Generic diversity generally increased rapidly during the Paleozoic, except when set back by pulses of mass extinction. In fact, an analysis of the history of the Paleozoic Fauna during the Paleozoic Era reveals no general correlation between rate of increase for this fauna and total marine animal diversity. Furthermore, realistically scaled logistic simulations do not mimic the empirical pattern. In addition, it is difficult to imagine how some fixed limit for diversity could have persisted throughout the Paleozoic Era, when the ecological structure of the marine ecosystem was constantly changing. More fundamentally, the basic idea that competition can set a limit for marine animal diversity is incompatible with basic tenets of marine ecology: predation, disturbance, and vagaries of recruitment determine local population sizes for most marine species. Sparseness of predators probably played a larger role than weak competition in elevating rates of diversification during the initial (Ordovician) radiation of marine animals and during recoveries from mass extinctions. A plot of diversification against total diversity for these intervals yields a band of points above the one representing background intervals, and yet this band also displays no significant trend (if the two earliest intervals of the initial Ordovician are excluded as times of exceptional evolutionary innovation). Thus, a distinctive structure characterized the marine ecosystem during intervals of evolutionary radiation—one in which rates of diversification were exceptionally high and yet increases in diversity did not depress rates of diversification. Particular marine taxa exhibit background rates of origination and extinction that rank similarly when compared with those of other taxa. Rates are correlated in this way because certain heritable traits influence probability of speciation and probability of extinction in similar ways. Background rates of origination and extinction were depressed during the late Paleozoic ice age for all major marine invertebrate taxa, but remained correlated. Also, taxa with relatively high background rates of extinction experienced exceptionally heavy losses during biotic crises because background rates of extinction were intensified in a multiplicative manner; decimation of a large group of taxa of this kind in the two Permian mass extinctions established their collective identity as the Paleozoic Fauna. Characteristic rates of origination and extinction for major taxa persisted from Paleozoic into post-Paleozoic time. Because of the causal linkage between rates of origination and extinction, pulses of extinction tended to drag down overall rates of origination as well as overall rates of extinction by preferentially eliminating higher taxa having relatively high background rates of extinction. This extinction/origination ratchet depressed turnover rates for the residual Paleozoic Fauna during the Mesozoic Era. A decline of this faunas extinction rate to approximately that of the Modern Fauna accounts for the nearly equal fractional losses experienced by the two faunas in the terminal Cretaceous mass extinction. Viewed arithmetically, the fossil record indicates slow diversification for the Modern Fauna during Paleozoic time, followed by much more rapid expansion during Mesozoic and Cenozoic time. When viewed more appropriately as depicting geometric—or exponential—increase, however, the empirical pattern exhibits no fundamental secular change: the background rate of increase for the Modern Fauna—the fauna that dominated post-Paleozoic marine diversity—simply persisted, reflecting the intrinsic origination and extinction rates of constituent taxa. Persistence of this overall background rate supports other evidence that the empirical record of diversification for marine animal life since Paleozoic time represents actual exponential increase. This enduring rate makes it unnecessary to invoke environmental change to explain the post-Paleozoic increase of marine diversity. Because of the resilience of intrinsic rates, an empirically based simulation that entails intervals of exponential increase for the Paleozoic and Modern Faunas, punctuated by mass extinctions, yields a pattern that is remarkably similar to the empirical pattern. It follows that marine animal genera and species will continue to diversify exponentially long into the future, barring disruption of the marine ecosystem by human-induced or natural environmental changes.

Low-magnesium calcite produced by coralline algae in seawater of Late Cretaceous composition

Shifts in the Mg/Ca ratio of seawater driven by changes in midocean ridge spreading rates have produced oscillations in the mineralogy of nonskeletal carbonate precipitates from seawater on time scales of 108 years. Since Cambrian time, skeletal mineralogies of anatomically simple organisms functioning as major reef builders or producers of shallow marine limestones have generally corresponded in mineral composition to nonskeletal precipitates. Here we report on experiments showing that the ambient Mg/Ca ratio actually governs the skeletal mineralogy of some simple organisms. In modern seas, coralline algae produce skeletons of high-Mg calcite (>4 mol % MgCO3). We grew three species of these algae in artificial seawaters having three different Mg/Ca ratios. All of the species incorporated amounts of Mg into their skeletons in proportion to the ambient Mg/Ca ratio, mimicking the pattern for nonskeletal precipitation. Thus, the algae calcified as if they were simply inducing precipitation from seawater through their consumption of CO2 for photosynthesis; presumably organic templates specify the calcite crystal structure of their skeletons. In artificial seawater with the low Mg/Ca ratio of Late Cretaceous seas, the algae in our experiments produced low-Mg calcite (<4 mol % MgCO3), the carbonate mineral formed by nonskeletal precipitation in those ancient seas. Our results suggest that many taxa that produce high-Mg calcite today produced low-Mg calcite in Late Cretaceous seas.

Temperature and biotic crises in the marine realm

Climatic change has been a prominent cause of marine mass extinction, but areal restriction of seafloor during global regression has not. Late Eocene and Pliocene-Pleistocene cooling, for example, caused major extinctions, but profound global Oligocene and Pleistocene regressions had little or no direct effect on benthic diversity. Recurrent themes of pre-Cenozoic marine crises suggest that global temperature change also served as a major, and perhaps dominant, agent of extinction in these events: (1) Mass extinctions have frequently been concentrated in the tropics, which seem to have become a refrigerated trap from which there has been no escape; biotas previously occupying high latitudes have shifted equatorward, to replace disappearing tropical biotas. (2) Some crises were not instantaneous but followed protracted and pulsatile temporal patterns, as would be predicted for complex, global climatic crises. (3) Several mass extinctions coincided with recognized intervals of climatic cooling.

Predation defeats competition on the seafloor

… the snail, whose tender horns being hit Shrinks backward in his shelly cave with pain, And there, all smothered up, in shade doth sit, Long after fearing to creep forth again. … — William Shakespeare, Venus and Adonis (1593) For many decades, ecology textbooks presented classical competition theory without reservation. The central principle here is that two species sharing an essential resource that is in limited supply cannot coexist for long because the competitively superior species will eliminate the other one. The implication is that ecological communities should be characterized by division of resources among species, or niche partitioning. Thus, it is understandable that many paleontologists have continued to invoke concepts of competitive exclusion and niche partitioning in their studies of ancient guilds and communities. By now, however, there is a large body of neontological literature demonstrating that interspecific competition and resource partitioning play only a minor role in many ecological communities— especially benthic marine communities, which are the primary focus of the following discussion. Predation and physical disturbance inflict so much damage on biotas of the seafloor that populations of one species seldom monopolize a potentially limiting resource, except sporadically and locally. As a result, it is uncommon for any species to drive another to extinction through competitive exclusion—or even to force another species to drastically change its exploitation of any environmental resource throughout its geographic range. Furthermore, what particular species or group of species occupies a particular microhabitat is often simply a matter of time of arrival. The present contribution follows a memoir (Stanley 2007) showing that the taxonomic diversification of the large groups of marine taxa that Sepkoski (1981) identified as the Paleozoic and Modern faunas has entailed intervals of unbridled exponential increase separated by episodic mass extinctions. On this largest biotic scale, it is evident …

Climatic cooling and mass extinction of Paleozoic reef communities

A variety ofpatterns suggest that climatic cooling was the primary cause of the extinction of organic reef communities late in the Ordovician, Devonian, and Permian periods. Other potential agents exhibit serious deficiencies. Anoxic conditions, for example, cannot spread to surface waters. Eustatic sea-level lowering occurred during only two of the extinction intervals, and at other times during the Phanerozoic, lowering of sea level failed to produce mass extinction. Furthermore, sea-level drops precipitate an increase in the areas around volcanic islands available for reef growth. No iridium anomaly that might have resulted from a bolide impact has been found for any of the three Paleozoic crisis intervals, and each of these intervals spanned several million years. Patterns consistent with the idea that climatic cooling caused heavy extinction of Paleozoic reef communities are the following: 1) Non-tropical marine taxa suffered less severe extinction than tropical groups, presumably because many of their species were able to migrate equatorward. 2) During the protracted Ordovician and Permian crises, biogeographic provinces contracted toward the equator. 3) For each crisis, a disproportionately large percentage of surviving taxa were cosmopolitan in distribution. 4) In the aftermath of each event, carbonate production was reduced. 5) Reef-building was suppressed for several million years after each crisis, even though potential reef-builders survived. 6) Each mass extinction approximately coincided with the initiation of a glacial interval in a polar region.

Scleractinian corals produce calcite, and grow more slowly, in artificial Cretaceous seawater

The mineralogies of most biotic and abiotic carbonates have alternated in synchroneity between the calcite (hexagonal) and aragonite (orthorhombic) polymorphs of CaCO3 throughout the Phanerozoic Eon. These intervals of calcite and aragonite production, or calcite seas and aragonite seas, are thought to be caused primarily by secular variation in the molar magnesium/calcium ratio of seawater (mMg/Ca . 2 5 aragonite 1 high-Mg calcite; mMg/Ca , 2 5 low-Mg calcite), a ratio that has oscillated between 1.0 and 5.2 throughout the Phanerozoic. In laboratory experiments, we show that three species of scleractinian corals, which produce aragonite in modern seawater and which have flourished as important reef builders primarily during aragonite seas of the past, began producing calcite in artificial seawater with an ambient mMg/Ca ratio below that of modern seawater (5.2). The corals produced progressively higher percentages of calcite and calcified at lower rates with further reduction of the ambient mMg/Ca ratio. In artificial seawater of imputed Late Cretaceous composition (mMg/Ca 5 1.0), which favors the precipitation of the calcite polymorph, scleractinian corals produced skeletons containing .30% low-Mg calcite (skeletal mMg/Ca , 0.04). These results indicate that the skeletal mineral used by scleractinian corals is partially determined by seawater chemistry. Furthermore, slow calcification rates, resulting from the production of largely aragonitic skeletons in chemically unfavorable seawater (mMg/Ca , 2), probably contributed to the scleractinians’ diminished reef-building role in the calcite seas of Late Cretaceous and early Cenozoic time.