Proc. Natl. Acad. Sci. USA Vol. 95, pp. 9396–9401, August 1998 Evolution Oxygen and evolutionary patterns in the sea: Onshoreyoffshore trends and recent recruitment of deep-sea faunas DAVID K. JACOBS*† AND DAVID R. LINDBERG‡ *Department of Biology, University of California, Los Angeles, CA 90095-1606; and ‡Department of Integrative Biology and Museum of Paleontology, University of California, Berkeley, CA 94720-4780 Communicated by Stephen M. Stanley, The Johns Hopkins University, Baltimore, MD, June 1, 1998 (received for review April 15, 1997) ABSTRACT Over the last 15 years a striking pattern of In this paper we argue (i) that a component of the post- diversification has been documented in the fossil record of Paleozoic onshoreyoffshore evolutionary pattern (3–7) re- benthic marine invertebrates. Higher taxa (orders) tend to sulted from the preferential influence of anoxicydysoxic bot- originate onshore, diversify offshore, and retreat into deep- tom conditions (aydbc) on offshore faunas; (ii) that aydbc were water environments. Previous studies attribute this macro- prevalent in the offshore in the Mesozoic before the Late evolutionary pattern to a variety of causes, foremost among Cretaceous and declined thereafter; and (iii) as a consequence them the role of nearshore disturbance in providing oppor- of this quantitative change in aydbc over time, the influence of tunities for the evolution of novel forms accorded ordinal aydbc on evolutionary patterns can be subjected to a simple rank. Our analysis of the post-Paleozoic record of ordinal first statistical test using the data of Jablonski and Bottjer (6). This appearances indicates that the onshore preference of ordinal statistical argument is a first-order analysis at a coarse scale of origination occurred only in the Mesozoic prior to the Turo- temporal resolution. More refined studies may be possible with nian stage of the Cretaceous, a period characterized by the assembly of additional data. y relatively frequent anoxic dysoxic bottom conditions in y deeper marine environments. Later, in the Cretaceous and Anoxia Dysoxia and the Fossil Record Cenozoic, ordinal origination of benthic organisms did not y occur exclusively, or even preferentially, in onshore environ- A variety of factors expanded the influence of a dbc in ments. This change in environmental pattern of ordinal offshore sedimentary environments in the Mesozoic beyond those observed in the Cenozoic. Anoxia is associated with origination roughly correlates with Late Cretaceous: (i) de- transgression (11). First-order sea level rose from the Permoy cline in anoxiaydysoxia in offshore benthic environments; (ii) Triassic to the Cenomanian increasing the proportion of extinction of faunas associated with dysoxic conditions; (iii) transgressive and highstand facies in this part of the record. increase in bioturbation with the expansion of deep burrowing Tectonic factors in the Mesozoic generated a suite of intracra- iv forms into offshore environments; and ( ) offshore expansion tonic and oceanic basins with limited deep-water connection to of bryozoan diversity. We also advance a separate argument y the open ocean and frequent anoxic conditions (11). These that the Cenomanian Turonian and latest Paleocene global basins include rift related features, such as the North Sea in events eliminated much of the deep-water benthos. This Europe, and foreland basins, such as the Western Interior requires a more recent origin of modern vent and deep-sea Seaway of North America. Furthermore, in the Mesozoic, large faunas, from shallower water refugia, than the Paleozoic or portions of the Atlantic and Tethys had limited deep-water early Mesozoic origin of these faunas suggested by other connection to other ocean basins. Much of the Mesozoic fossil workers. record derives from such basinal or adjacent settings. Greenhouse conditions in the Mesozoic also greatly en- An onshore to offshore evolutionary pattern is evident in hanced aydbc and its biotic impact. Isotopic data suggest that benthic marine invertebrate clades of the Paleozoic (1, 2) and Mesozoic bottom waters were on the order of 10–15°C warmer post-Paleozoic (3–7) age. Ordinal rank taxa are observed to than mid and bottom waters today (12). As a consequence of originate onshore, diversify offshore, and eventually relinquish the reduced solubility of gases in water with increasing tem- nearshore habitat. This pattern has been attributed to a perature, this temperature difference would reduce the oxygen number of factors (5), the most clearly articulated of which carrying capacity of bottom water by 15–20%. More impor- invokes higher disturbance in shallow marine environments as tantly, increased bacterial metabolic rates result in a twofold a mechanism that eliminates niche incumbents, permitting the increase in oxygen uptake of sediment for each 5°C increase in evolution of novel attributes subsequently recognized as new, temperature, resulting in a four- to eightfold higher oxygen ordinal rank, higher taxa (8). Expansion across the shelf to demand at the sediment–water interface under greenhouse deeper offshore habitats then accompanies diversification of conditions (13). Furthermore, metabolic oxygen requirements ' the clade (3–6). Explanations advanced for the subsequent of benthic animals would also rise by twofold for a 10°C offshore retreat of taxonomic groups include the evolution of increase in temperature (14). Thus, given a similar temporal sequence of organic carbon inputs, first principles support new predators (9) and more effective competitors (10) in the y nearshore environment. Thus, the nearshore is thought of as more intense and more volatile fluctuation in a dbc under a source of evolutionary novelty resulting from disturbance, Mesozoic greenhouse conditions, and indicate that biotic and subsidiary aspects of the pattern, such as offshore retreat, responses to similar reductions in oxygen would have been are thought of as responses to ecological interaction associated greater. In addition, the reduced temperature gradient in the Mesozoic seas implies a much reduced density difference with the appearance of evolutionary novelty in the nearshore. between surface and bottom waters. In this context, upwelling The publication costs of this article were defrayed in part by page charge Abbreviations: aydbc, anoxicydysoxic bottom condition; CenyTur, payment. This article must therefore be hereby marked ‘‘advertisement’’ in CenomanianyTuronian. accordance with 18 U.S.C. §1734 solely to indicate this fact. †To whom reprint requests should be addressed at: Department of © 1998 by The National Academy of Sciences 0027-8424y98y959396-6$2.00y0 Biology, 621 Circle Drive South, University of California, Los PNAS is available online at www.pnas.org. Angeles, CA 90095-1606. e-mail: [email protected]. 9396 Downloaded by guest on September 25, 2021 Evolution: Jacobs and Lindberg Proc. Natl. Acad. Sci. USA 95 (1998) 9397 and consequent surface water productivity and organic carbon as well as in the Triassic (22, 23). Additional significant events delivery to the bottom could be generated from much weaker of regional extent are evident in the upper Jurassic (24). thermohaline and dynamic forcing than are required in the Subsidiary peaks in anoxia of more modest geographic scale modern ocean (15). precede and succeed anoxic events of global scale (18). Mesozoic marine rocks record aydbc on a wide range of From the Aptian through the Cenomanian stages of the y temporal and spatial scales from global events to laterally Cretaceous deep-sea drill cores document anoxic dysoxic extensive alternating carbon-rich and bioturbated beds indic- conditions that fluctuated in intensity, but were substantial in ative of fluctuating oxygenation of the sediment–water inter- the deeper portions of the Atlantic basin (25). Thus, the global face. The largest scale global and regional events are summa- anoxic events of the mid-Cretaceous can be viewed as lateral rized in Fig. 1. Anoxic events of global extent have been expansions into shallower water environments of more con- tinuous basinal aydbc. Similarly, in anoxic events of regional documented for the Permo-Triassic, Toarcian (18), Lower scale, such as the late Jurassic (Kimmeridge) of Europe, Aptian (19), Lower and Upper Albian, and Cenomaniany y reduced oxygen conditions expanded outwards from graben or Turonian (Cen Tur) (20). Supporting evidence includes or- other basinal settings in shelves or epieric seas (24). Thus, ganic carbon preservation in stratigraphic sections and deep- Mesozoic anoxiaydysoxia tended to influence outer shelf, sea drill cores distributed around the world, as well as global slope, and basinal habitats more frequently, and for longer shifts in carbon isotopes thought to reflect the rate of organic durations, than the major regional and global episodes re- carbon burial (20). Isotopic shifts suggest additional large corded across the shelves (11, 24, 25) (Fig. 1). These offshore events in the Valanginian stage (21) of the Lower Cretaceous, facies are the deepest water environments regularly sampled in the post-Paleozoic fossil record. Deep bathyal and abyssal sediments are not exposed on land, except in the most tec- tonically active settings, limiting sampling of these offshore paleoenvironments to deep-sea drill core, which does not generally recover macrofossils. Carbon-rich deposits were widespread in epieric seas in the Coniacian and Santonian (23). However, these later Creta- ceous aydbc are not