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Modern and ancient continental shelf anoxia: an overview

R. V. TYSON 1 & T. H. PEARSON 2 1 Newcastle Research Group, Fossil Fuels and Environmental Geochemistry (Postgraduate Institute), Drummond Building, The University, Newcastle upon Tyne, NE1 7RU, UK. 2 Scottish Environmental Advisory Services Limited, c/o Dunstaffnage Marine Research Laboratory, P.O. Box 3, Oban, Argyll, PA34 4AD, UK.

Abstract: The characteristics of mid-latitude shelf seas are primarily controlled by seasonal cyclicity in wind-driven mixing. Seasonal dysoxic-anoxic conditions may occur in summer in salinity-stratified estuarine or pro-delta settings, or more extensively in those open shelf areas where a total depth of ~<60 m and the seasonal thcrmocline result in a bottom water layer ~<10 m thick. When bottom circulation is limited the oxygen stored in this layer may become periodically exhausted if climatic factors extend the stratified period to seven or more months, or if there is additional organic loading (via flagellate blooms and/or pollution). This causes widespread mortalities and a shift to soft-bodied, non-fossilizing benthic faunas. Our review supports seasonal dysoxia-anoxia as being the best model to account for the key characteristics of many ancient epeiric sea black shales. It would appear that the latter rarely represent true continuous anoxia except locally in more- confined deeper sub-basins. We recommend that the following terms should be applied to environments, facies, or oxygenation levels: oxic (8.0-2.0 ml/1 O2), dysoxic (2.0-0.2 ml/1), suboxic (0.2-0.0 ml/1) and anoxic (0.0 ml/I). The corresponding biofacies terms are: aerobic, dysaerobic, quasi- anaerobic (laminated, without macrofauna, but with in situ benthic microfauna) and anaerobic. Hypoxic and normoxic should only be used with regard to the physiological responses of living organisms.

The phenomenon of severe oxygen depletion in groups of scientists, an examination of the rel- continental shelf waters is of great significance evant literature indicates that rather little inter- to both geologists and marine biologists. For change of ideas, perspectives or terminology geologists its importance lies in the face that has hitherto occurred. In this introduction we most, perhaps 80%, of the world's petroleum attempt to integrate these different perspec- has been generated from ancient organic-rich tives, and show how a greater understanding of sediments whose sedimentological, geochemi- modern processes can enhance interpretation cal, and palaeontological characteristics indicate of the geological record, and how that record formation in a regime where oxygen-depleted can aid our analyses of modern anoxic or oxygen-free conditions prevailed at the environments. sediment-water interface. Most of these organic-rich petroleum source rocks are marine and were deposited on the continental shelf or Some fundamental characteristics of the upper slope. For the marine biologist, the in- shelf sea environment creasing frequency of bottom water anoxia in coastal waters and the severity of the resultant During the last twenty years the stimuli of the summer mass mortalities, with its disastrous Deep Sea Drilling Project and the Ocean Drill- commercial consequences for coastal fisheries, ing Project have resulted in a rather oceano- makes the phenomenon of continental shelf graphic perspective on the geological analysis of anoxia an area of urgent research. It is essential anoxic environments. However, the shelves are for the marine biologist to distinguish the rela- very distinct and often rather separate systems, tive importance of natural processes from the influenced by their own internal hydrographic effects of eutrophication caused by pollution, controls, rather than by external oceanographic and to forecast the likely response to global factors (although both are influenced by global warming and the increased urbanization of the climate and sea level). Table I summarizes some world's coastlines. of the key differences between modern conti- Despite the great mutual interest to these two nental shelves and oceans. Modern shelves are

From TYSON, R. V. & PEARSON, T. H. (eds), 1991, Modern and Ancient Continental ShelfAnoxia Geological Society Special Publication No 58, pp 1-24. Downloaded from http://sp.lyellcollection.org/ by guest on September 24, 2021

2 R.V. TYSON & T. H. PEARSON

Table 1. Comparison of modern shelves and oceans (from Tyson, in preparation, based on multiple sources)

Shelf Ocean

Percent of global surface area 4.5% 66.3% Relative marine area 7.6% (~<200 m) 92.4% Average depth ~<133 m 3,730 m Long-term sediment accumulation 10-200 1-4 m/MY Mean TOC (wt%) of sediment 1.02 (0.5-3.0) 0.34 Mean primary productivity 164 57 g/C/m2/yr Global marine productivity 27% (~<200 m) 73% Mean levels of new production 30% (~<50%) 6% Recycling of production ~<50% 80-90% Carbon burial effic!ency (oxic) 8-70% 0.5-5% Preservation of productivity 1-25% 0.4-1.0% Oxygen consumption rate 1-100 0.01-0.1 gM/l Global benthic oxygen consumption 83% (<~200 m) 17% Global sulphate reduction />90% ~<10% Relative global carbon burial 80-90% 10-20% Global benthic biomass 83% 17% Mean thickness of bioturbated layer 20 cm 10 cm Bioturbation coefficients 1-10 0.04-0.05

covered by relatively shallow marginal seas that during settling, and the much higher sediment occur only around the periphery of the conti- accumulation rates, shelf sediments are more nents and are generally only -+70 km wide and organic-rich and more reducing than their less than 130 m deep. However, sea level has oceanic counterparts, leading to a greater burial shown an approximately 400 m range of vari- of the sedimented organic matter (greater car- ation over geological time, and prior to around bon burial efficiency), despite the fact that there 65 million years ago (the beginning of the is greater exploitation by infaunal benthos. Cenozoic area), extensive epeiric seas period- Being shallow, shelf waters are generally ically covered large areas of the continents. It better mixed and are seldom deep enough to be was in these large extensive epeiric seas that beyond the reach of storm mixing (probably oxygen deficient conditions were most severe ~<100 m, and certainly no more than 200 m). and widespread; during the last 90 million years Although tides are locally of great importance, (i.e. since the early Turonian stage of the Late most of the energy for mixing is provided by the Cretaceous) they have occurred only on a much wind, and thus varies seasonally. This regular smaller, localized, and sporadic scale. variation in the extent of wind-driven mixing is From Table 1 we can see that the mean the single most important characteristic of shelf primary productivity of modern shelf waters is seas, as it controls the water column chemistry, over three times greater than the mean for the the hydrodynamic regime, and the dynamics oceans. The difference in productivity between and life histories of both the plankton and adjacent shelves and oceans in fact varies benthos (Tyson 1985). The seasonal stratifi- with latitude between a factor of 5 and 20 cation cycle is a well known and well docu- (Romankevitch 1984). Furthermore, a much mented phenomenon and is described in many higher proportion of shelf productivity rep- oceanography and marine ecology texts (e.g. resents 'new production' that can be exported Thurman & Webber 1984). from the euphotic zone (see Berger et al. 1989). In temperate shallow shelf waters convection This higher productivity reflects the shallower and wind-driven turbulence result in a complete depth and thus the higher proportion of the mixing of the whole water column during the water column that lies within the euphotic zone, winter months. This homogenizes the distri- the greater frequency and extent of mixing in bution of nutrients throughout the water shallow waters (which provides 'new' nutrients column. However, the growth of phytoplankton to the surface layer), and the greater proximity shows an annual minimum because the depth of to riverine sources of nutrients. Because the the wind-mixed surface layer exceeds the depth water column is so shallow, much of the primary of the euphotic zone, and the downward com- production is sedimented to the sea floor where ponent of the turbulent mixing prevents the it supports a much greater benthic biomass. phytoplankton from making effective use of the Because of the higher productivity, lower losses available light and nutrients. Downloaded from http://sp.lyellcollection.org/ by guest on September 24, 2021

MODERN & ANCIENT CONTINENTAL SHELF ANOXIA 3

Turbulent mixing decreases in the spring as water from the upper layers of the bottom mean wind intensity and storm frequency de- water. Along with the reduced levels of grazing, crease, and the greater insolation increases the this nutrient supply may permit a secondary buoyancy of the surface water and progressively autumn bloom while sufficient light is still avail- inhibits the vertical extent of mixing. Once the able (= new production). In low latitudes this whole of the mixed layer lies within the euphotic destratification may lead to the annual peak zone, the rapid growth of large chain-forming in primary production (e.g. Beers & Herman diatoms results in the 'spring bloom' (new pro- 1969). In the late autumn falling temperatures duction, the annual peak in primary pro- reduce the buoyancy of the mixed layer, the ductivity). Losses due to grazing are initially gradient of the thermocline/pyconocline de: insignificant as these diatoms multiply much creases, and turbulence and convective mixing faster than the zooplankton. The rapid phyto- eventually destroy the stratification completely. plankton growth is initially fuelled by the nutri- Winter storms mix the water column to the ents that were mixed into the surface waters bottom (or to the depth of the permanent ther- during the winter. However, as the intensity of mocline in deep water) and consequently to mixing declines further, the resupply of nutri- depths below those light levels critical for ents from deeper water is restricted, pro- efficient photosynthesis. ductivity declines, and the large, non-motile, chain-forming diatoms tend to sink out of the euphotic zone. Nutrient- and silica-limitation, Terminology of oxygen deficient sinking, and increased zooplankton grazing environments pressure lead to the collapse of the spring bloom (usually by May). Geological terminology based on From spring into early summer the increased palaeoecological criteria insolation and declining level of turbulent mix- ing result in progressive heating of the upper There is no universally accepted terminology to water column. This results in the formation and describe oxygen-deficient conditions (see Tyson stabilisation of a strong seasonal thermocline 1987). The terminology most widely used by (generally at about 10-40 m) which stratifies geologists is that of Rhoads & Morse (1971). the water column into three distinct layers: On the basis of the available early 1960s litera- the surface mixed layer, the thermocline- ture on depth-related faunal patterns in the pycnocline, and the bottom water. Tidal circu- modern Black Sea, Gulf of California and lation in shallow areas may also produce a Californian Continental Borderland basins, they benthic mixed layer that may extend upward to deduced that there were three critical ranges of the thermocline or keep the whole water column dissolved oxygen for metazoan organisms: locally mixed. Where tidal mixing is weak, the >1 ml/1, 1.0-0.1 ml/1 and 0.1-0.0 ml/1. These thermocline becomes a persistent feature by divisions they respectively termed aerobic, dys- April, and attains its maximum areal extent by aerobic and azoic. The term 'anaerobic' was the end of May. Vertical exchange of nutrients scarcely used in their paper, although following and oxygen across the thermocline are largely Byers (1977) it largely replaced the use of 'azoic' limited to rates of eddy diffusion, and hence the in the subsequent literature. The biofacies terms mixed layer becomes rapidly nutrient-depleted, were applied to both the oxygen conditions and while the decay of the settling and sedimented the associated biofacies, which were defined on organic matter leads to higher nutrient concen- the basis of faunal diversity, general degree of trations and falling oxygenation in the cooler calcification, size, and trophic groupings of the (winter residual) bottom water. The summer macrofauna, and the occurrence of bio- planktonic biomass is dominated by small phyto- turbation. They noted (partly because of a short- flagellates which concentrate at the thermocline, age of critical data?) that the boundary between exploiting the relative water column stability dysaerobic and anaerobic was transitional over there to optimise utilization of light from above the 0.1-0.3 ml/1 range, and that the calcification and nutrients from below. Summer production trends were general rather than absolute. Note is usually much lower than during the Spring, that the data they used to define their model but in some cases it may represent the annual were taken from environments that are distinctly maximum, as in Chesapeake Bay (Taft et al. different (and certainly more stable) than the 1980). shelf settings in which most ancient 'anoxia' has In the autumn, increased wind-stress during occurred. equinoctial gales leads to greater mixing and More recent biological surveys of modern deepening of the thermocline. This involves the oxygen-deficient environments have led to some turbulent entrainment of relatively nutrient-rich modification of the original Rhoads and Morse Downloaded from http://sp.lyellcollection.org/ by guest on September 24, 2021

4 R.V. TYSON & T. H. PEARSON model (see discussions in Rhoads et al., Savrda environments near the dysaerobic/anaerobic & Bottjer, and Cuomo & Bartholomew, this boundary (0.1-0.2 ml/1 dissolved oxygen) that volume). In particular, the critical oxygen level are characterized by deposition of laminated for the suppression of obvious bioturbation is strata and anomalous occurrences of shelly now widely taken as 0.2 ml/1 rather than 0.1 ml/1 faunas. In these sediments the laminated fabric (based largely on the work of Douglas 1981; implies 'anaerobic conditions' but the presence Soutar et al. 1981; and Thompson et al. 1985). of moderately or strongly calcified epifaunal Note that this revised boundary lies exactly in bivalves indicates higher oxygenation or unusual the middle of Rhoads and Morse's transitional tolerance to such conditions. The 'shelly interval. The occurrence of heavily calcified laminite' of Hallam (1987) and the 'benthic echinoids down to values of 0.3 ml/1 has also re- boundary biofacies' of Sageman (1989) are es- emphasized the non-absolute nature of the cal- sentially equivalent to the 'exaerobic biofacies'. cification trend (Thompson et al. 1985). The We consider that, unlike the Rhoads and Morse real significance of the 1.0 ml/1 boundary has biofacies, this biofacies is not the inevitable also been questioned (Savrda et al. 1984). Dur- result of a specific range of oxygen values, and ing 1983-1988 various geologists modified the that it should not be expressed in these terms. definition of dysaerobic, sometimes in error or We believe it to be primarily related to the with little detailed justification, by using various occurrence of sulphide-oxidising bacterial mats. other oxygen limits including 0.1-0.3 ml/1, 0.1- Although the sediments were completely anoxic 0.5 ml/1, 0.1-2.0 ml/1, 0.2-0.5 ml/1, 0.3- and inaccessible to most infauna (but not necess- 0.7 ml/1 and 0.5-1.0 ml/I. Some workers have arily so to some annelid and nematode worms, also recognized two ('upper and lower' or 'slight c.f. Andersin et al. 1978; Pearson 1987), the and extreme') subdivisions using boundary presence of these mats largely prevents escape values of 0.3 or 0.5 ml/l (see Rhoads et al., this of HzS and may thus have allowed some low- volume). oxygen tolerant epifauna to survive. The long- More significantly, the occurrence of in situ term maintenance of these bacterial mats was benthic microfauna (especially foraminifera) probably dependent on fairly stable dysoxic within 'anaerobic'/azoic biofacies sediments (not anoxic) conditions and a relatively high (e.g. Phleger & Soutar 1973; Bernhard 1986; and stable flux of metabolizable organic matter, Koutsoukos et al. 1990; Van der Zwaan in part explaining why they are currently most & Jorissen, this volume) has emphasized that characteristic of the oxygen minimum zones of macrofaunal evidence alone cannot reliably dis- upwelling regions (see Arntz et al., this volume). tinguish between dysaerobic and truly 'anaer- It must be noted that there are no equivalent obic' conditions (Tyson 1985). Furthermore, bivalve faunas associated with these mats at although it has long been appreciated that areas the present day. Although the etymology of with laminated sediment within oxygen minima 'exaerobic' is questionable, there is no doubt were often not 'azoic', but characterized by that this biofacies is a distinct and important non-fossilizing sedentary tube-building poly- feature in the geological record. chaetes (e.g. Calvert 1964), evidence of poly- chaete activity has now been observed in Geological terminology based on 'anaerobic' biofacies sediments (see Cuomo & geochemical criteria Bartholomew, this volume). Many workers now consider that the definition of the azoic/'anaer- The other terminology in wide use by geologists obic' boundary must be changed, as the original is based on chemical or geochemical criteria. usage patently includes sediments that were not Breck (1974) used chemical oceanographic par- deposited under strictly 'anaerobic' conditions, ameters to define three oxygenation regimes: that is completely free of macro-, meio-, one where oxygen was freely available, one or micro-organisms with obligate aerobic or transitional regime characterised by drastic pE 'microaerophilic' metabolisms dependent upon change and the appearance of NO2 (from ni- the availability of free molecular oxygen. trate reduction), and one characterized by the Koutsoukos et al. (1990) have used the term absence of oxygen and the presence of sulphate 'quasi-anaerobic' for laminated sediments free reduction. These he respectively termed oxic, of benthic macrofauna but containing an in situ suboxic and anoxic. Many subsequent studies benthic microfauna, and this terminology have demonstrated that denitrification, the most has been followed by Savrda & Bottjer (this important suboxic process, occurs at very low volume). ('microaerophilic') oxygen concentrations, Savrda & Bottjer (1987, see also this volume) below about 0.2 ml/1 (e.g. Sugahara et al. introduced the biofacies term 'exaerobic' for 1974; Deuser 1975; Sorokin 1978; Devol 1978; Downloaded from http://sp.lyellcollection.org/ by guest on September 24, 2021

MODERN & ANCIENT CONTINENTAL SHELF ANOXIA 5

Seitzinger 1988; Lipschultz et al. 1990). Unfor- Physiologists have long used the term tunately, a number of authors have corrupted 'hypoxia' ('hypoxic') to describe conditions or the definition of 'suboxic' by using it as equiv- responses produced by stressful levels of oxygen alent to dysaerobic, or as general term for deficiency. We have not been able to trace an oxygen deficiency (but the term is in fact seldom original definition, but the earliest use we could encountered outside the field of sedimentary find of it with respect to the present context is geochemistry where it is applied to a within- that by Davis (1975). Its application to natural sediment early diagenetic regime). The terms oxygen deficient environments began to be oxic and anoxic are very widely employed, but common in the late 1970s, especially by those not always with reference to the conditions at working in the Gulf of Mexico, and it is now in the sediment-water interface, or with strict widespread use by marine biologists and ecol- reference to oxygen levels per se. ogists. Based on laboratory and/or field In his geochemical classification of environ- observations on oxygen stress responses in in- ments Berner (1981) subsequently deliberately vertebrate and fish faunas, hypoxic has been excluded suboxic by defining oxic and anoxic by variously defined as corresponding to dissolved the presence or absence of detectable amounts oxygen levels lower than a range of 3.0-0.2 ml/ of oxygen (>10 _6 M, or about 0.5% satu- 1, with the consensus being in favour of 1.4 ml/l ration), but he also distinguished between (= 2 mg/l or ppm). Although less often sulphidic anoxic and 'post-oxic non-sulphidic used, the complementary term to hypoxic (i.e. anoxic' (the last encompassing a broadly similar > 1.4 ml/1) is 'normoxic' ('normoxia'). diagenetic regime to suboxic). Berner (1981), The term 'hypoxic' has not generally been Berner & Raiswell (1985) and other (mostly used in the geological literature, although in the American) sedimentary geochemists have also last few years the term has begun to appear employed the traditional term 'euxinic' (literally sporadically. Following the meeting on which 'pertaining to the Black Sea' = Pontus Euxinus) this volume is based, several geological con- to distinguish anoxic (sulphidic) water column tributors initially chose to use the term in their environments, and 'semi-euxinic' for environ- papers, but in order to avoid hybrid terminology ments where the water column regularly fluctu- and confusion we took an editorial decision to ates between 'dysaerobic' and 'euxinic'. restrict its use to the biological papers. Many workers have considered it desirable to distinguish between faunal and absolute chemi- Problems cal criteria in defining levels of oxygen, and since about 1984 this has lead to the increasingly There are a number of 'hidden' problems in the common use of the term 'dysoxic' to indicate question of oxygen terminology. In most, and that range of oxygen values associated with particularly older, data sets the dissolved oxygen the dysaerobic biofacies (though this is rarely content of seawater has been determined explicitly stated). by some modification of the Winkler titration method, and this is widely held to be unreliable below values of 0.2 ml/l (e.g. Richards 1975; Biological terminology Soutar et al. 1981). Compared to more accurate Traditional biological usage distinguishes be- colourimetric methods (sensitive down to 0.01- tween 'aerobic' (organisms, environments, and/ 0.02 ml/1) the Winkler method may give values or processes that require, or are characterized 0.1 to 0.15 ml/l too high at such low concen- by, the availability of free molecular oxygen), trations (Deuser 1975; Savrda et al. 1984; and 'anaerobic' (organisms, environments, and/ Kamykowski & Zentara 1990). Consequently, or processes characterized by the absence of use of any boundary values below 0.2 ml/1 may free molecular oxygen). As some organisms are be largely unjustified. able to adapt their metabolisms according to In recent work most oxygen values are the availability of oxygen, a distinction is also generally measured 0.5-1.0 m above the sedi- made between facultative anaerobes which can ment surface (though sometimes 2 m or more). switch from aerobic to anaerobic metabolism, When detailed oxygen versus depth profiles and obligate anaerobes to whom oxygen is toxic have been obtained they have revealed sharp and lethal. Some cyanobacteria and bacteria gradients, e.g. from 3.0 to 0.4 ml/1 between 25 (such as denitrifiers and sulphide-oxidizers) are and 5 cm above the bottom, with the totally also adapted to the very low (suboxic) oxygen anoxic layer being perhaps only a few centi- concentrations that occur in strong gradients of metres thick (JOrgensen 1980). Other studies oxygen consumption and are commonly referred have reported mortalities on the bottom, but to as 'microaerophilic'. no effects in cages raised 40 cm above the Downloaded from http://sp.lyellcollection.org/ by guest on September 24, 2021

6 R.V. TYSON & T. H. PEARSON sediment (Arntz & Rumohr 1986). Oxygen H2S contamination becomes significant there is gradients above the surface of fine-grained typically a strong selection for adult survival sediments are probably normal features (e.g. (e.g. Thurberg & Goodlett 1979; Groenendaal Jones 1982), but above organic-rich sediments, 1980; Shumway et al. 1983). Here we will use and particularly in the presence of bacterial the terms 'euryoxic', and 'stenoxic' to indicate mats, the gradients may be intense (JCrgensen organisms which can tolerate wide (and & Revsbech 1985). Clearly the minimum near- thus lower) and narrow ranges in oxygen bottom oxygen concentrations reported in the respectively. literature do not accurately represent the actual conditions to which the benthos are subjected Proposals in the benthic boundary layer. The surficial 'oxic' zone of sediments occupied Reflecting the mood of the meeting on which by the infaunal benthos is widely held to be this volume is based, we propose the adoption 'oxygenated', but it is often defined only by its of a dual terminology: one set of terms to (brown) colour, and thus the redox couple (Eh) describe the oxygen conditions themselves as which determines the reduction state of iron. they occur at the sediment water interface, and Fine-scale measurements with platinum elec- another set of terms to describe the resulting trode probes indicate that most of the oxic biofacies seen in the sediment record (Table 2). sediment layer of shelf sediments is in fact often Terms describing oxygenation and the related oxygen-free, oxygen rarely penetrating further facies have '-oxic' endings, while those describ- than 5 mm even when the oxic zone is ten times ing the associated biofacies have '-aerobic' end- deeper (S0rensen et al. 1979; Revsbech et al. ings. Clearly the biological normoxic/hypoxic 1980). Although the oxic layer supports an terminology does not conform to this rule. The aerobic biofacies, obligate aerobic (oxygen- term hypoxic is also poorly defined, partly be- requiring) metabolisms can only operate in its cause the critical levels at which hypoxic re- uppermost part and in the immediate vicinity of sponses are observed depend upon the taxa ventilated burrows. There is clearly a termino- involved, and to a certain extent, the environ- logical problem here: the geochemist's 'oxic' ment. We recommend that 'hypoxic' and relates primarily to Eh, while 'aerobic' or 'hypoxia' should be used only with respect to 'normoxic' relate specifically to oxygen avail- living (i.e. not fossil) organisms, and that only ability, with these two parameters being only the other '-oxic' terms should be applied to approximately correlated. describe the oxygen status of environments. A further problem is that it is extremely When applied to environments or facies the difficult to determine a critical level of oxygen- '-oxic' terminology should refer to conditions as ation that applies to a whole biological com- they exist in the bottom water, i.e. within 1 m munity. The oxygen sensitivity of organisms above the sediment surface. As the same '-oxic' varies with temperature, their general mode of terminology is employed for sediment dia- life (e.g. deep or shallow infaunal versus epi- genetic studies, it must be made explicitly clear faunal benthos), their general levels of activity, when these terms are being used to refer to their mobility and capability to migrate, their within-sediment conditions. The main differ- life cycle stage (maturity, size, moulting period- ence within sediments is that the oxic diagenetic icity), whether they are normally associated zone is often free of oxygen, and that the with sandy or muddy substrates, the rate suboxic regime involves manganese reduction of oxygen decrease (acclimitization time), and and iron reduction as well as denitrification. their tolerance to sulphide. In general the least tolerant forms are active shallow infaunal or epifaunal benthos that live in or on normally Biological impact of oxygen deficiency on well-oxygenated sandy substrates (Theede et al. modern shelves 1969). Small or juvenile organisms are often relatively more tolerant of low oxygen (e.g. The changes that occur across relatively stable Shumway et al. 1983) because of their lower oxygen gradients (e.g. Rhoads & Morse 1971; respiratory demands and their more favourable Nichols 1976; Rosenberg 1977) are probably surface area: volume ratios (as is reflected in not a reliable guide to the effects of periodic or the reduction of burrow diameters with declin- seasonal oxygen depletion in most shelf regimes. ing oxygen; Aller 1982; Savrda et al. 1984). Open shelf areas effected by such oxygen de- However, for the same reason, juvenile aerobic pletion are often exposed to much greater, organisms are generally more susceptible to more rapid, and more stressful variations in sulphide, and if oxygen becomes so low that oxygenation (Chapman & Shannon 1985, 1987; Downloaded from http://sp.lyellcollection.org/ by guest on September 24, 2021

MODERN & ANCIENT CONTINENTAL SHELF ANOXIA 7

Table 2. Recommended terminology for low oxygen regimes and the resulting biofacies in marine environments

Oxygenation regime Oxygen Environments Physiological ml/l Facies Biofacies regime

8.0-2.0 Oxic Aerobic Normoxic 2.0-0.2 Dysoxic Dysaerobic Hypoxic 2.0-1.0 moderate 1.0-0.5 severe 0.5-0.2 extreme 0.2-0.0 Suboxic Quasi-anaerobic

0.0 (HzS) Anoxic Anaerobic Anoxic

No tes: (1) The upper limit of dysaerobic and dysoxic has been moved from 1.0 to 2.0 ml/1 to take into account shelf observations (see text). (2) The lower limit of dysaerobic and dysoxic has been moved from 0.1 to 0.2 ml/1 because the latter appears to mark the end of bioturbation, the limit of accuracy of the Winkler method, and the appearance of water column denitrification. It is also the lower limit for most zooplankton (Judkins 1980). (3) Dysoxic has been subdivided into three ranges which appear to be of biological significance (see text); note the boundaries represent approximate doubling or halving of the oxygen. These boundaries can be loosely linked with observations of species succession along organic enrichment gradients in modern sediments (Fig. 1), but there is little realistic evidence for an oxygen-specific subdivision of the dysaerobic biofacies (particularly in ancient shelf sediments). (4) Suboxic refers to waters with very low oxygen concentrations that are characterised by nitrate reduction, based on the original definition of the term (Breck 1974). Water column denitrification is of great chemical oceanographic significance. The corresponding quasi-anaerobic biofacies occurs in laminated sediments without fossilising macrofauna that yield an in situ benthic microfauna and/or evidence of in situ benthic polychaetes. Bacteria operating in this regime may be referred to as 'microaerophilic'. (5) The exaerobic biofacies may in part correspond with the quasi-anaerobic biofacies (when stable sulphide- oxidizing bacterial mats are developed), but probably does not form part of the normal sequence in most shelf settings. (6) As biofacies are formed over extended periods of time they will probably have formed under varying oxygenation conditions; cited oxygen values thus represent only the mean oxygenation range, not stable conditions.

Justic et al. 1987; Breitburg 1990; cf. Thompson Tunnicliffe 1981; Burd & Brinkhurst 1984, et al. 1985, p169; but see also Wishner et al. 1985). This presumably reflects their lack of 1990). The following observations are based exposure to H2S being generated by basinal only on shelf data. The effects of periodic oxy- sediments, The stage in the life cycle is critical gen depletion on shelf faunas are progressive for the survival of crustacea as they are particu- and occur in several intergradational stages larly susceptible to oxygen stress when moulting (Table 3). (Burd & Brinkhurst 1984, 1985; Pollock & The oxygen levels at which fish are said to Shannon 1987). show avoidance reactions are predominantly in Changes in the wind stress field can lead to the range 1.0-2.0 ml/1, with most having gone marked shifts in the distribution of oxygen- by the time the lower end of this range is depleted bottom waters on the shelf (e.g. Steime reached (Tulkki 1965; Lepp~ikoski 1971; May & Sindermann 1978; Chapman & Shannon 1973; Davis 1975; Levings 1980; Leming & 1987). Where such water moves onshore it is Stuntz 1984; Malmgren-Hansen et al. 1984; often observed to 'herd' the mobile fauna into Renaud 1986b; Baden et al. 1990). Shelf crus- shallow waters (Loesch 1960; May 1973; Steimle tacea generally migrate at below 2 ml/I or are & Sindermann 1978; Arntz 1981; Stefanon & killed once values reach 0.3-0.5 ml/1 (Officer Boldrin 1982; Officer et al. 1984; Tolmazin et al. 1984; Bailey et al. 1985; Renaud 1986; 1985; Pollock & Shannon 1987). As these Baden et al. 1990). The adults of some galatheid 'jubilees' may be correlated with periods of taxa may be able to tolerate 0.1-0.15 ml/1 minimal winds (Turner et al. 1987), they may provided they remain inactive and are resting also reflect the natural 'upward and outward' on rocky substrates on the flanks of a basin (e.g. expansion of dysoxic conditions (see below). Downloaded from http://sp.lyellcollection.org/ by guest on September 24, 2021

8 R.V. TYSON & T. H. PEARSON

Table 3. Progressive effects of low oxygen on modern anoxic sulphidic water to the surface (Str0m shelf faunas (based on JCrgensen 1980; Stachowitsch 1936; Copenhagen 1953; Otsubo et al. 1991). 1984; Weigelt & Rumohr 1986; Baden et al. 1990, and A review of the appropriate literature indi- other sources cited in the text). Dissolved oxygen cates that shelf benthos become stressed (with ranges should only be considered approximate. increased mortality of stenoxic taxa) once bot- 2.0-1.0 ml/l (A) Avoidance and migration by tom water oxygen declines to values in the nekton and some mobile range 2.0 to 1.4 ml/1 at 0.5-1.0 m above epifauna (which may eventually the bottom (Andersin et al. 1978; Steimle produce crowding ('jubilees') & Sindermann 1978; Leppakoski 1980; and subsequent mortalities in Westernhagen & Dethlefsen 1983; Officer et al. coastal shallows if the only 1984; Justic et al. 1987). The initial effects of available escape route is oxygen depletion thus appear to occur at 0.5- onshore). 1.0 ml/1 higher dissolved oxygen values on the 1.4-1.0 ml/1 (B) Behavioural responses to stress shelf than they do in more stable areas such as by stenoxic benthic fauna oxygen minima (cf. Rhoads & Morse 1971). (infauna progressively emerges: This is presumably because the normal shelf crustaceans and asteroid faunas are less acclimatised, are exposed to echinoderms emerge and raise wider and more rapid changes, and because their bodies off the sediment, they often include a higher initial proportion of deep infaunal euryoxic bivalves cease burrowing and show stenoxic organisms. Shelf faunas suffer very greater extension of their severe effects in the range 1.0-0.5 ml/l (May siphons, other bivalves start to 1973; Zarkanellas 1979; J0rgensen 1980; 'gape', mobile benthos moves Lepp~ikoski 1980; Arntz 1981; Tolmazin 1985; to any available higher Arntz & Rumohr 1986; Westernhagen et al. 'ground'). 1986; Baden et al. 1990). Below 0.5 ml/i there is 1.0-0.7 ml/1 (C) Emergence of euryoxic infauna usually no long-term survival of shelf macro- (evacuation of sediment, first fauna, in part because of the increasing influence by small then by larger of sulphide toxicity (Fig. 1). individuals, emerged infaunal Reported experimentally determined survival bivalves lie on their sides and times of invertebrates at 2.0 to 0.7 ml/1 of extend siphons vertically). dissolved oxygen are generally of the order of 1.0-0.5 ml/l (D) Physical inactivity. 2-14 days depending upon the taxa concerned and the extent of simultaneous exposure to (E) Duration or severity of conditions exceeds homeostatic sulphide (e.g. Brafield 1963; Shick 1976; capabilities and mortalities J0rgensen 1980; Shumway et al. 1983; F6llmi & occur (initially of stenoxic then Grimm 1990). This is in good agreement with euryoxic forms, with juveniles the field observations of Stachowitsch (1984, succumbing before adults, and and this volume) which show complete destruc- macrofauna before meiofauna). tion of the benthic community can occur within the space of two weeks once bottom water values have declined below about 1.4 ml/1. However, if the fauna is allowed sufficient time to acclimatise, some elements may be able to Although they may provide windfall catches for survive under such conditions for 40-60 days coastal fisherman, they are often associated (Theede et al. 1969; Thurberg & Goodlett 1979). with mass mortality, partly due to overcrowding, The rate of oxygen consumption is thus a critical and partly because many of the refugees are parameter. Polychaetes are especially tolerant, demersal deepwater forms that are severely and through the development of a variety stressed in warm, shallow, and mixed waters of behavioural and/or metabolic adaptations (Arntz 1981). Consequently, where there is no (Fig. 2) can survive up to 2.0-4.5 days even in circulation to homogenize bottom water oxygen the presence of some sulphide (Groenendaal distributions below the thermocline, the ascent 1980). The 'thiobiotic' soft-bodied meiofauna is of dysoxic to anoxic water may cause preferen- much more tolerant than the macrofauna (e.g. tial crowding within or just below the pyc- Elmgren 1978; Powell et al. 1983). nocline, rather than above it (Kitching et al. Clearly, a very major influence on the benthic 1976; Arntz 1981; Burd & Brinkhurst 1983). fauna is the rise of the redox potential disconti- Mass mortalities are also associated with up- nuity (RPD) within the sediment and thus the welling or overturns that bring oxygen poor or increasing likelihood of exposure to H2S. This Downloaded from http://sp.lyellcollection.org/ by guest on September 24, 2021

MODERN & ANCIENT CONTINENTAL SHELF ANOXIA 9

Fig. 1. Diagrammatic representation of faunal changes along a gradient of organic enrichment in relation to changing levels of oxygen in the water immediately overlying the sediment surface. (a) Successional change along the gradient in relation to changing oxygen levels in the overlying water and to depth of faunal penetration and bioturbation in the sediments (after Pearson & Rosenberg 1978); the interface ~line between the dark and light shading in the sediments represents the redox discontinuity zone. (b) Faunal abundance and composition at various points along such a gradient in a highly enriched sediment from the west of Scotland. A, normal communities found in unenriched sediments under oxic conditions at the interface, and including crustaceans, echinoderms, molluscs and various vermiform taxa. B, -- enriched communities composed principally of polychaete taxa but including small bivalve and gastropod molluscs and small crustaceans. C, -- highly enriched communities comprising only a few polychaete, oligochaete and nematode vermiform taxa. D, -- impoverished vermiform community with only occasional polychaete and nematode taxa surviving. Downloaded from http://sp.lyellcollection.org/ by guest on September 24, 2021

Fig. 2. Illustration of changing behaviour in the polychaete Malacoceros fuliginosus in response to changing oxygen concentrations in the water overlying the sediment surface. This species is a typical opportunistic inhabitant of highly enriched sediments in western European coastal areas. (a) Life position under fully oxic conditions. The worm inhabits a burrow penetrating some 20-30 mm into the sediment and picks detrital particles from the sediment surface by means of a pair of flexible palps. (b) When oxygen levels fall below about 2.4 ml/1 the worms begin to emerge from their burrows and rise up into the water column whilst retaining burrow contact with their lower abdominal segments. (c) When oxygen levels fall below about 0.5 ml/1 adjacent worms begin undulatory body movements and ultimatcly form rapidly weaving clumps of animals. This spiral weaving behaviour has the effect of drawing down water from higher levels to the vicinity of the surface thus enhancing local oxygen levels. Ultimately if oxygen levels fall below 0.2 ml/1 activity ceases and the animals lie quiesent on the surface prior to death. Downloaded from http://sp.lyellcollection.org/ by guest on September 24, 2021

MODERN & ANCIENT CONTINENTAL SHELF ANOXIA 11 is caused by lower bottom oxygenation in- 1980; Carney 1989). Severe midwater oxygen creased sediment oxygen consumption due to a depletion (suboxic conditions) are thus rare higher flux of metabolizable organic matter, below depths of 1500 m in the modern ocean and/or an increase in bottom temperature (e.g. (Kamykowski & Zentara 1990; see also Ankar & Jansson 1973; Pearson & Rosenberg Table 1). However, on the shelves the supply of 1978; J0rgensen 1980; Arntz 1981; Weigelt & organic matter is probably a less critical vari- Rumohr 1986). Any fall in oxygen content of able, as there are often adequate amounts to the bottom water below about 0.5-1.0 ml/1 will result in some degree of oxygen depletion (at result in reduced bioturbation by the infauna least 50%) provided that the downward mixing (e.g. Savage 1976), and thus decreased venti- of oxygenated surface water is sufficiently re- lation of the sediment (Fig. 1A). The RPD stricted by vertical density gradients (pyc- subsequently rises to within 1-2 mm of the noclines) produced by surface warming sediment surface, which may eventually become (thermoclines), freshwater run-off (haloclines), blackened and release H2S into the bottom or a combination of the two. water (e.g. Tulkki 1965; Lepp~ikoski 1969; To get oxygen depletion vertical mixing must Kitching et al. 1976; Kolmel 1979; J0rgensen be restricted by stratification of the water 1980; Stefanon & Boldrin 1982). However, part column, but this traps nutrients in the bottom of this blackened appearance may be due to the water and tends to cut off the supply of organic accumulation of a layer of progressively darken- matter whose decay is ultimately responsible ing organic 'floc' on the bottom (e.g. Malone for the oxygen depletion. In shelf waters the 1979; Harper et al. 1981, and this volume; resolution of this paradox is generally provided Dethlefsen & Westernhagen 1983; Stachowitsch by the seasonal alternation between the mixed 1984). The rising RPD obliges aerobic organ- and stratified states described earlier. The decay isms to progressively emerge from the sediment of planktonic matter during stratified periods, and may cause surface crowding and 'windfalls' the consequent release of vital nutrients, and of food for any demersal fish that are still pre- their recycling back into the surface waters dur- sent (e.g. Weigelt & Rumohr 1986). ing renewed mixing, are critical to maintaining Although the RPD rises within the sediment the efficiency and high productivity of shelf as bottom water oxygen declines, the redox waters. value of surface sediments is often little affected Oxygen depletion below the thermocline is unless values drop below about 0.7 ml/1 commonly observed to develop first and to be (Hargrave 1972; May 1973; Stanley et al. 1981), most severe in topographic depressions on the and surface blackening may only occur at sea floor. Dysoxic to anoxic waters are fre- ~<0.5 ml/1. However, once this has occurred, quently observed to expand upwards and out- the high oxygen demand of organic-rich sedi- wards during the summer (e.g. Kitching et al. ments may subsequently maintain the surface of 1976; Rosenberg 1977; Arntz et al. 1976; Arntz the sediment in this state for several months 1981). This indicates insufficient circulation even after the oxygen content of the bottom below the pycnocline to homogenize the dis- water has improved to 2.0-4.0 ml/l solved oxygen content of the bottom water. (Lepp~ikoski 1969; Kolmel 1979). The mainten- However, the principal cause of this pattern is ance of such a reduced surface layer clearly probably the 'focusing' of fine sediment and inhibits benthic recolonization, even when the suspended organic matter in these areas (e.g. oxygen content of the bottom water is not Douglas 1981; Huc 1988; Tyson, in prep- limiting in itself (Lepp~ikoski 1969). aration). Sediments deposited below thermo- cline depth are thus generally more fine-grained and organic-rich than those deposited above Oxygen depletion in modern sheff because of purely hydrodynamic factors (Tyson environments 1985; see Westernhagen et al. 1986; Pollehne 1986). The greater oxygen demand of these organic-rich sediments, and of the fresh seston General observations being focused in these depressions results in a Oxygen deficiency occurs when the oxygen significant local increase in the organic loading demand created by the decay of metabolizable and makes these areas prone to early and more organic matter exceeds the rate of oxygen severe deoxygenation. Areas underlain by supply. Below depths of about 100 m, doubling organic-rich sediment are thus likely to be far the water depth approximately halves the aver- more susceptible to the development of dysoxia, age percentage of primary production that but such conditions can develop over areas of reaches the sediment-water interface (Suess relict fine sands (such as in the Middle Atlantic Downloaded from http://sp.lyellcollection.org/ by guest on September 24, 2021

12 R. V. TYSON & T. H. PEARSON

Bight) if large amounts of metabolizable organic to support high primary production and thus matter are periodically available (Mahoney increase the subsequent rate of oxygen con- 1979; Falkowski et al. 1980). Indeed, such areas sumption. Excluding deepwater silled fjord may be even more seriously affected because basins, anoxia is most frequent during the their fauna contains a higher proportion of summer months even in estuarine areas where 'stenoxic' forms. there is a halocline throughout the year Many, but not all, of the modern anoxic and (Rosenberg 1977; J0rgensen 1980; Arntz 1981; periodically anoxic shelf basins occur in enclosed Taft et al. 1980; Turner et al. 1987). or semi-enclosed protected situations where a The density gradient in the seasonal thermo- mass of deepwater is topographically isolated cline is dependent upon winter temperatures from the main shelf watermass by the surround- (as reflected by the bottom water), the duration ing land and one or several shallow sills (see and intensity of insolation during the spring and Healy & Harada 1991). In conjunction with a summer, and the frequency, duration, and pycnocline, such a configuration acts to reduce magnitude of mixing. The strength of haloclines the volume of the bottom water (and thus the will additionally depend upon the magnitude oxygen reservoir) laterally as well as vertically, and timing of the spring run-off. In estuarine and to restrict or prevent exchange with deep areas the gradient in the halocline may be in- open water. Examples of such basins include creased by the wind-driven 'ponding' of run-off various anoxic deep water fjords and the deep against the coast, and by the intrusion of normal basins of the Baltic (Str0m 1936; Deuser 1975; shelf bottom water into inshore areas (e.g. Grasshoff 1975), Harrington Sound in Bermuda Seliger et al. 1985; Pokryfki & Randall 1987; (Beers & Herman 1969), Lough Hyne in Ireland Breitburg 1990). The deep Baltic basins rep- (Kitching et al. 1976; Kitching 1987), Elefsis resent an extreme variant of the latter phenom- Bay in Greece (Zarkanellas 1979), and the Seto enon, with marine water being periodically Inland Sea (Harim-nada) of Japan. However, injected into an otherwise freshwater basin other areas with periodic anoxia occur on com- (Kullenberg 1983). At normal marine salinites a pletely open shelves (e.g. the Middle Atlantic change of 1%o has the same effect on density as Bight, the northern Gulf of Mexico, and the a 7~ change in temperature (Schopf 1980); Namibian and Peruvian shelves), or open thermal diffusivity is also 100 times that for salt shelves within large enclosed or semi-enclosed (Wilde & Berry 1984). Salinity is thus generally basins (e.g. the northern Adriatic, and the a more potent stratifying agent, and a 10% northwestern shelf of the Black Sea). In such decrease in surface salinity (about 3.5%0) is cases it would appear that shelf-slope hydro- sufficient to produce stratification. Conse- graphic fronts may effectively 'seal off' the shelf quently, under 'normal' conditions, dysoxic to bottom water at its oceanward margin, and/or anoxic conditions are probably localized in the that the oxygen demand on the shallow shelf vicinity of river plumes (Turner & Allen 1982; simply exceeds the ability of any cross shelf Justi6 1987; Van der Zwaan & Jorissen, this circulation to bring about acceptable levels of volume). However, more extensive shelf anoxia oxygenation. would appear to be due to thermal stratification. Nearly all anoxic episodes occur during the summer or earliest autumn (especially in August Controls on modern seasonal shelf anoxia or September) when the stratification of open shelf waters is controlled by the thermocline. A An abundance of metabolizable organic matter number of anoxic events on open shelves have (i.e. high organic loading), will undoubtedly been associated with unusually high spring run- promote more rapid oxygen consumption, and off (e.g. in the New York Bight in 1976, the all other factors being equal, increase the prob- northern Gulf of Mexico, and the northern ability of dysoxia or anoxia in shelf bottom Adriatic in 1977). However, the halocline does waters. The necessary level of organic loading not appear to play a key role during the anoxic will depend upon other physical factors (see phase (Gordon et al. 1976; Armstrong 1979; below). In some shelf settings it would appear Pokryfki & Randall 1987), and the latter usually that other factors so dispose them towards shows a 1-2 month lag time compared with summer dysoxia or anoxia that abnormally high maximum run-off. Its main role may be to organic loading is not a critical parameter (e.g. provide an initial stabilization of the water Westernhagen et al. 1986; Turner et al. 1987; column, restricting the downward mixing of Pokryfki & Randall 1987). the importance of heat, and thus promoting earlier formation and high organic loading as a precondition for anoxia consolidation of the seasonal thermocline. How- is probably greatest in more open and deeper ever, the run-off may also provide the nutrients shelf settings, especially where the sediments Downloaded from http://sp.lyellcollection.org/ by guest on September 24, 2021

MODERN & ANCIENT CONTINENTAL SHELF ANOXIA 13 are normally sandy. Even when high organic bottom shallows up toward and may temporarily loading occurs, it does not necessarily indicate parallel the base of the seasonal thermocline 'high productivity' per se; it may reflect circu- (e.g. Starr & Steimle 1979; Turner & Allen lation patterns that lead to inshore concen- 1982; Tolmazin 1985; Pokryfki & Randall 1987). tration of flagellate phytoplankton (e.g. The width and depth of such zones is obviously Falkowski et al. 1980). dependent upon bottom topography, but as It should be noted that flagellate plankton are thin bottom water layers are inherently unstable most abundant during stratified conditions, es- (cf. KuUenberg 1983), low levels of turbulence pecially where high nutrient levels occur at the (from winds, tides, and currents) are essential if base of the pycnocline and the latter lies within complete mixing is to be prevented (displacing the euphotic zone (e.g. Margalef et al. 1979). the stratified zone further offshore into deeper The occurrence of flagellate blooms can only waters where the bottom water would be help accelerate oxygen consumption and drive thicker). A knowledge of bottom circulation, the system towards anoxia (e.g. Pieterse & Van bottom depth and topography, and thermocline der Post 1967; Falkowski et al. 1980), but they depth makes it possible to predict those areas are partly symptomatic of the stratified con- that are particularly vulnerable to anoxia at dition, rather than a primary cause. However, increased organic loading levels or following long-term observations clearly show that the early springs. Temporal variations are also frequency of anoxic events in many shelf areas important. Deeper thermoclines (and thus has increased due to pollution, higher nutrient thinner bottom waters) are most common fol- loading, and increased primary productivity lowing milder rather than colder winters, be- over the last few decades (e.g. Officer et al. cause the thermal gradient is lower, and mixing 1984; Tolmazin 1985; Justi6 1987, this volume; can extend to greater depths, leading to a thick- Justi~ et al. 1987; Baden et al. 1990). ening of the thermocline at the expense of the At any particular level of organic loading, the bottom water (Falkowski et al. 1980). extent of oxygen depletion is found to be de- Bottom water oxygenation normally declines pendent upon three main factors: the strength progressively after the establishment of the of the pycnocline (Armstrong 1979; Renaud seasonal thermocline. Oxygen values on open 1986a; Tolmazin 1985; Turner et al. 1987), the shelves generally reach their annual minimum initial oxygen content and volume of the bottom of about 3 ml/l within a period of two to three water (Armstrong 1979; Gade & Edwards 1980; months, usually by June or July (e.g. Gordon Falkwoski et al. 1980; Turner et al. 1987), and et al. 1976; Armstrong 1979). Further deterio- the duration of the stratified period (Armstrong ration is normally prevented by increased levels 1979; Falkowski et al. 1980; Stefanon & Boldrin of mixing during late summer into autumn. If 1982; Seliger et al. 1985; Westernhagen et al. higher organic loading, a stronger pycnocline, 1986; Stachowitsch, this volume). and/or extension of the stratified period are An analysis of published data on natural superimposed upon this general pattern, critical anoxia on open shelves (exclusive of oxygen oxygen values (<2 ml/1) are likely to be attained minimum zones) shows that this phenomenon during August or September, if not earlier. occurs mostly in waters that are less than 60 m The smaller the volume of the bottom water, deep, and where the thickness of the (sub- the lower its initial oxygen content at the start pycnocline) bottom water layer is between 1 of the stratified period, and the quicker it can and 10 m thick (or 20 m at most). The depth of become deoxygenated. Gade & Edwards (1980) the seasonal shelf thermocline is generally much note that in 'stagnant' bodies less than 10-20 m less variable than the total depth of the shelf, thick the rate of oxygen depletion may be up to and usually lies between 10 and 40 m, although five times greater than in deeper stratified the haloclines of estuarine areas may stabilise at waters, often exceeding 0.8 ml/month. In such shallower depths (0.5-10.0 m). Thus, for the situations complete anoxia can be produced bottom water to be only 10 m or less in thickness within the space of one to three months after generally requires that the total water depth the initation of stable stratification (e.g. Beers should be no more than about 60 m, which is & Herman 1969; Armstrong 1979; Gade & what is observed. Furthermore, one can also Edwards 1980; Falkowski et al. 1980; see that in situ anoxia is unlikely in waters less Westernhagen et al. 1986; Justi6 et al. 1987). than 10-15 m deep, unless these are salinity The influence of the thickness of the bottom stratified or very sheltered from wind-driven water layer also means that the severity of mixing. oxygen depletion should be greatest inshore Areas of thin (1-10 m) bottom water zones (where the thermocline is closest to the bottom) generally reflect near-coast situations where the and decrease offshore as the bottom water layer Downloaded from http://sp.lyellcollection.org/ by guest on September 24, 2021

14 R.V. TYSON & T. H. PEARSON thickens (as is observed by Armstrong 1979; leading to rapid bottom anoxia. This is especially Tolmazin 1985; Turner et al. 1987; Pokryfki & true in relatively sheltered shallow inshare bays Randall 1987). Notable examples of seasonal where the bottom water is only 5-20 m thick open shelf anoxia have resulted from the estab- (e.g. Pieterse & Van der Post 1967; Ahumada lishment of the seasonal thermocline by early et al. 1983; Bailey & Chapman 1987; Tarazona spring, some 1-2 months ahead of the normal et al. 1988). Although the productivity clearly schedule, and/or its persistence through controls the deposition of the organic-rich sedi- October, one month longer than the norm. ments in such areas, it is the stratification (by Consequently, through early warming (with or the permanent and/or seasonal thermoclines) without initial stabilization of the water column that allows the decay of these sediments to by a strong halocline) and reduced levels of produce dysoxic to anoxic bottom conditions wind mixing, the stratified period can sometimes and an intense oxygen minimum zone on the be extended to seven or eight months of the continental margin. year. Examples of seasonal open shelf anoxia resulting from prolonged stratification have been documented by Armstrong (1979), Ancient epeiric sea anoxia Falkowski et al. (1980), Stefanon & Boldrin (1982), Seliger et al. (1985), and Westernhagen Some of the important characteristics of ancient et al. (1986). dysoxic-anoxic episodes and their resulting sedi- ments are summarized in Table 4. This summary is by no means extensive, but we have sought to Shelf dysoxia-anoxia in upwelling regions highlight those particular features that must be The occurrence of dysoxia-anoxia on the adequately accounted for by any model that is shelves of upwelling regions has many simi- proposed to explain these episodes. We also larities to the patterns described above, but the acknowledge that each particular event has its higher levels of productivity result in much own peculiar characteristics and that we are greater organic loading (see Arntz et al. and making generalizations that do not necessarily Bailey, this volume). Western intensification of the subtropical gyral circulation of the oceans results in a regional east-west tilt of the perma- nent ocean thermocline which brings it up to Table 4. Important characteristics of ancient epeiric shallow depths on the eastern margins of the sea dysoxic-anoxic facies (after Tyson 1989a) oceans (Dietrich et al. 1980). Where the inclined thermocline extends over the upper slope and High TOC content (3-60%) narrow shelves on the western coasts of the Overwhelming dominance of marine amorphous continents between latitudes of 15 to 40 ~, wind- organic matter (Type II or IIS kerogen) driven coastal upwelling can tap nutrient-rich Presence of marine nektonic and planktonic faunas water from below the pycnocline (100-200 m) Organic-walled plankton dominated by prasinophyte algae and result in very high productivity in the Benthos absent or of low diversity (often high euphotic zone (Barber & Smith 1981; Barber & dominance, high density) Chavez 1986). Bottom currents permitting, this Subtle palaeoecological and geochemical variations leads to the deposition of very organic-rich shelf (e.g. common but sporadic presence of benthic and upper slope sediments with very high oxy- fauna) gen demand. Chapman & Shannon (1985) note General absence of bottom current activity and that in the Benguela upwelling region dysoxic- coarse clastics anoxic shelf water is only formed where the Mostly associated with the early part of transgressive inshore shelf sediments are fine-grained and sequences organic-rich. Association with warmer palaeoclimatic episodes Maximum development in basinal depocentres Upwelling itself appears to be a net supplier 'Mid-continent' location of oxygen (Bailey et al. 1985), and thus the most Large areal extent (often > 100 000 km2) with sheet intense oxygen depletion occurs after periods of geometry intense upwelling when the water column be- Long-distance correlation of many beds and 'event comes temporarily stratified by a strong thermo- horizons' cline (e.g. Du Pleiss 1967; Pieterse & Van der Commonly exhibit cyclic pattern on Milankovitch Post 1967; Chapman & Shannon 1985; Pollock scale & Shannon 1987). The very large amount of 'Synchronous' development, regionally and on different continents metabolizable organic matter then degrades Variable correlation with oceanic anoxia (in time) under conditions of minimal oxygen renewal, Downloaded from http://sp.lyellcollection.org/ by guest on September 24, 2021

MODERN & ANCIENT CONTINENTAL SHELF ANOXIA 15 apply in all cases. A great diversity of ation in redox states related to Milankovitch depositional models have been proposed for cycles. Variations in the orbital obliquity of the dysoxic-anoxic "black shale' facies, and some Earth lead to significant variations in insolation of the more important varieties are briefly listed at lower and middle latitudes (i.e. variations in in Table 5. The two most popular models in seasonality), with greatest variation at palaeo- recent years have probably been the salinity latitudes of 20-30 ~ Greater seasonality results stratification model (low salinity surface layer) in stronger thermal contrasts between land and and the oxygen minimum impingement model. sea, increased flow of air from over the oceans We do not believe that either of these models towards the land, and a strengthened summer can adequately explain the characteristics given 'monsoon' (or at least greater precipitation). in Table 4 (Tyson 1985, 1989a; see also Such models have been use extensively to ac- Oschmann 1988; Wignall & Hallam, this count for Quaternary sapropel-bearing se- volume). quences in the deep Eastern Mediterranean (e.g. Rossignol-Strick et al. 1982) and have also been applied to mid-Cretaceous sediments (e.g. Critique of the 'estuarine' salinity Barron et al. 1985, Arthur et al. 1987). By contrast, Herbert & Fischer (1986) believe that stratification model the mid-Cretaceous cyclic anoxic events were The idea of run-off producing a low salinity 'anti-monsoonal', occurring during periods of surface layer that stratifies the epeiric sea and minimal seasonal contrast. They attribute this results in bottom anoxia has been largely based to modulation of seasonal temperature contrast on an extrapolation from modern silled basins and its effects on thermocline stability, wind which show this phenomenon (such as the Black stress, and bottom water formation. Sea and various fjords). One of its major attrac- There are some significant problems associ- tions is that run-off and basin water balance can ated with the application of the model to epi- be directly tied to climate models, and thus sodes of ancient epeiric sea anoxia. The first is those sediment sequences showing cyclic vari- that we have no reliable means of determining absolute palaeosalinities. Any absence or im- poverishment of the pelagic and nektonic fauna does not necessarily relate to salinity and may Table 5. Previous models used to explain dysoxic to anoxic facies of ancient epeiric shelf seas (after Tyson be a response to dysoxic conditions rather than 1989a). The models are not necessarily mutually an indicator of their cause. Furthermore, ap- exclusive. parently stenohaline faunas are often recorded throughout large parts of these sequences, or in (1) Stratified basin models associated aerobic biofacies at the margins of (a) Stable estuarine salinity stratification the seas. Perhaps most significantly, strong (b) Stable thermal or mixed thermohaline haloclines are usually spatially limited by sharp stratification fronts; low salinity water (20-30%0) does not Stable anti-estuarine stratification (high salinity bottom water): usually spread out across the whole shelf but (i) due to evaporation occurs in discrete plumes (see Van der Zwaan (ii) due to halokinesis and sea bed salt & Jorissen, this volume). In confined and rela- solution tively small silled basins a basin-wide 'brackish' (iii) due to submarine discharge of saline layer may be able to accumulate, but in the formation water extensive epeiric seas it is most unlikely that a (2) Impingement and penetration of expanded regional halocline could develop or be main- Oxygen Minimum Zone (fiom ocean to shelf) tained on the necessary scale. Salinity is only (3) Upwelling models likely to have caused local effects; run-off will (a) Coastal upwelling (b) OMZ penetration with establishment of very undoubtedly have occurred, but it may have large scale shelf upwelling cells been no more important than in most modern (4) Sea level/bottom topography models shelf areas (see Gordon et al. 1976). One might (a) Reduced mixing at increased water depth also have supposed that the influence of fresh- (sufficient for stable stratification) water would have been greatest during low sea- (b) Shallow, restricted circulation during early levels and regressions (as is indeed suggested by transgressions gives local pockets of organic facies variations, Tyson, in prep- stagnation (bottom topography) aration), but dysoxic-anoxic conditions are (c) Reduced exchange with adjacent oxygenated most widespread during early transgressions ocean and decreased tidal mixing due to widening of shelves and extensive shallows (superimposed on either high or low initial sea levels). Downloaded from http://sp.lyellcollection.org/ by guest on September 24, 2021

16 R. V. TYSON & T. H. PEARSON

Critique of oxygen minimum penetration productivity may increase during transgressions (due to the greater area of shelf seas) this does models not necessarily increase the organic loading per The oxygen minimum zone (OMZ) is an oceanic unit area and would not lead to oxygen depletion feature caused by the decay of plankton immedi- by itself (Tyson 1985, 1987). ately below the permanent thermocline. In most areas this results in only a 25-50% reduction in the initial oxygen concentration at these depths An actualistic model for ancient epeiric sea and is insufficient to have significant biological dysoxia- anoxia or geochemical effects. However, where up- welling leads to high productivity along the Using our preceeding analysis of modern shelf ocean margins, the much greater water column dysoxia-anoxia, we propose an actualistic model and sediment oxygen demand may lead to for the origin of black shale facies in ancient dysoxic to suboxic conditions. The intensity of epeiric seas (after Tyson 1989a). Oschmann the OMZ is directly linked to the intensity of (1988, 1990, and this volume) has conducted a upwelling, and thus greater wind mixing and similar exercise, though his model emphasises more vigorous circulation (e.g. Southam et al. different aspects and involves large-scale circu- 1982). In shallow epeiric seas, where mixing lation patterns which we do not consider an involves a much higher proportion of the water essential feature of the model. column, an increase in wind-driven circulation is largely incompatible with the stratified con- ditions necessary for anoxia (Tyson 1985, 1987). Initiation and occurrence of seasonal The OMZ penetration model proposes that dysoxia-anoxia during some periods of high sea level, the oxy- gen minimum zone on the margin of the conti- Sea-level rise must eventually reach a point nent was drawn into the epeiric sea once the when most of the offshore parts of epeiric seas latter became sufficiently deep for the perma- are deep enough to develop a thermocline on nent thermocline to maintain its integrity (e.g. at least a seasonal time scale. The thickness see Heckel, this volume). However, palaeo- of the summer sub-thermocline bottom water geographic data are often incompatible with the layer would initially be small. In addition, idea of a continuous oxygen depleted watermass astronomically-forced climatic variations super- extending across the margin and into the epeiric imposed on longer term global warming trends sea. Even at times of high sea level, epeiric (related to the sea-level rise) may have resulted black shale facies may be restricted to dis- in cyclic shifts towards climates characterized continuous deeper sub-basins, clearly showing by earlier springs, longer summers, and less that they are not related to a single extensive intense winter mixing (cf. Herbert & Fischer OMZ layer. Various shallow water facies often 1986). Consequently the length of the seasonal occur both within and near the margins of the stratification period may have shown cyclic epeiric seas; any mixing in shallow areas would changes between four and seven or more months promote a decoupling of the circulation pat- of the year. At warmer temperatures rates of terns, separating the ocean margin and internal oxygen consumption would have increased, epeiric sea circulations by a frontal system (even oxygen solubilities would have decreased, and more so than at the present day). thermocline stability would have been greater The upwelling that ultimately generates the (due to the increased density gradients at higher OMZ is likely to occur in the area of the first water temperatures). The combination of a thin significant shoaling encountered. Even if this bottom water layer, prolonged stratification, were not the case, upwelling is a spatially restric- lower mixing and higher oxygen demand would ted phenomenon and would be expected to undoubtedly have resulted in summer dysoxia result in linear or lobate belts of organic-rich or anoxia being widespread throughout all the sediments along the coasts of the epeiric sea offshore areas of the epeiric sea during the (wind patterns permitting), rather than the sheet appropriate parts of Milankovitch cycles. Such geometry and relative uniformity typical of regular annual dysoxia and/or anoxia would epeiric black shales. The occurrence of a strong have resulted in the widespread elimination of and stable permanent ocean thermocline across benthic faunas. Recolonization of such large a low latitude epeiric sea would probably de- areas would have been difficult, if not impossible crease the general level of productivity because for the larger and slower-growing taxa in nutrients would be locked up in the bottom the short periods available between annual water. It should be noted that although global dysoxic-anoxic episodes. Most fossilising shelly Downloaded from http://sp.lyellcollection.org/ by guest on September 24, 2021

MODERN & ANCIENT CONTINENTAL SHELF ANOXIA 17

benthic taxa would have disappeared from the permanently and truly anoxic to have resulted offshore stratified areas, leaving only opportun- in the observed laminated black shales provided ist polychaetes or occasionally other euryoxic the following three conditions apply. taxa during temporary improvements. In deep water areas within the epeiric sea (e.g. strongly subsiding sub-basins), the water- (i) Severe dysoxia to anoxia occurred regu- mass stratification may have become so stable larly and over a very wide area (often only in as to be 'permanent', leading to a 'meromictic' the lower few centimetres or metres of the condition. The bottom water in such deep areas water column, or rarely, extending up to the would have been better able to resist overturn pycnocline). because of its higher volume, and may have (ii) The ambient bottom oxygenation, scale become isolated by a permanent thermocline. of the defaunated areas, and/or the highly re- Any partial overturn and mixing would release ducing state of the sediment surface prevented nutrients and tend to result in bursts of new recolonisation by bioturbating macrofaunal production, high sedimentation of metaboliz- taxa, and usually by any calcified taxa at all. able organic matter, and even greater oxygen (iii) Only the most euryoxic (largely sessile demand. Such an effect probably makes anoxia epifaunal) taxa ever recolonized the sediment, self-sustaining or self-accelerating unless there and only during periods of improved but still is a very major overturn of the basin, or an dysoxic oxygenation when sulphur oxidising increased frequency of regular overturns, as in bacterial mats probably covered the surface of the modern Baltic this century (see Fonselius the sediment and inhibited H2S release (i.e. 1972; Kullenberg 1983). The conditions in such resulting in an exaerobic biofacies). deep sub-basins may thus also have become progressively more severe with time until tbese It is considered that the seasonal model is more depressions were finally 'flushed' by some major able to account for the subtle palaeoecological change in circulation. If able to resist oxy- variations that are observed in many epeiric genation during the 'unfavourable' parts of black shale sequences. In particular, we consider Milankovitch cycles, the longer duration of con- the dynamic origin of the dysaerobic (or 'poi- tinuous anoxia would result in an atypically kiloaerobic' sensu Oschmann) biofacies as a thick (rather than cyclic) development of black product of temporal variability is much more shale facies in these meromictic sub-basins. realistic than relating it to a static pycnocline or Their sediments would also have been truly OMZ (cf. Byers 1979; see discussion in Tyson anoxic, whereas in shallower waters dysoxic 1987; Oschmann 1990, this volume). The conditions with episodic anoxia were probably seasonal anoxia model can embrace a wide range more typical because of the potentially greater of possible conditions depending upon climate, influence of mixing events. Such contrasts are water depth and productivity, and is far more clearly seen between shelf and deep graben flexible than any of the other geological models. facies within the Late Jurassic Kimmeridge Clay Slight changes in one or several parameters (Tyson 1985, 1989b: Oschmann 1988). easily permit temporary benthic colonization It is not clear how well geologists can discrimi- for one or a few years to be interspersed with nate between sediments deposited in regimes azoic periods of variable duration. The model where the water column is continuously truly represents a logical extension of a modern situ- anoxic, and those where this condition occurred ation and is thus relatively easy to visualise, only seasonally but without any intermediary even though the palaeogeographic situation and development of an oxidized surface layer or any the sea level differ markedly from the present benthic colonization. Most studies have not day. It is perhaps possible that stable stratifi- been sufficiently detailed or multi-disciplinary cation, and thus permanent true anoxia, may to make confident conclusions. It is clear that a have become periodically established over large precise assessment of palaeo-oxygenation trends areas of epeiric seas, but the critical evidence to requires the combined study of the macrofauna, assess this is not yet available. However, the microfauna, ichnofauna, sedimentology, or- occurrence of localized permanent anoxia in ganic petrology, palynology, and organic and deep sub-basins is beyond doubt. inorganic geochemistry. However, as illustrated A significant disadvantage of stable stratifi- by many of the geological papers in this volume, cation models is that such situations tend to be the more intensively we study epeiric black associated with 'nutrient trapping', and thus a shales the less 'anoxic' they generally appear. negative feedback mechanism that decreases Comparison with the modern day suggests that oxygen demand. The seasonal model does not bottom conditions need not have remained suffer from such problems. Downloaded from http://sp.lyellcollection.org/ by guest on September 24, 2021

18 R. V. TYSON & T. H. PEARSON

Termination of black shale deposition in quently, as water depth increases less metaboliz- epeiric seas able organic matter reaches the sea floor, and the sub-pycnocline and sediment oxygen de- As sea level continues to rise following the early mand is subsequently lower. The depth of the phase of a transgression there should be a signifi- mixed layer is also important. Where it is com- cant increase in the ratio of the thickness of the paratively shallow and of the order of 10-15 m, seasonal bottom water layer to the total water some 30-40% of the primary production may depth. This would increase the deep summer be sedimented, but only 20% where it is at a oxygen reservoir, such that critical levels would depth of 50-100 m (Hargrave 1972; Wollast be unlikely to be reached or maintained for 1983). This is because as the mixed layer significant periods. In an extensive shelf sea a deepens, organic matter is retained in suspen- small increase in the thickness of the bottom sion longer and more is therefore degraded water can produce a very large increase in its within the water column. Also, the deeper the volume (particularly once its thickness exceeds mixed layer, the more photosynthesis tends to bottom relief), and the system may therefore be be light-limited, and the lower the primary quite sensitive to such variations. At the present production (Hargrave 1980). The organic matter day seasonal open shelf anoxia generally seems sedimented from deeper mixed layers is more to occur at depths of no more than about 60 m degraded (due to more resuspension and longer (exclusive of upwelling regions). residence times), and supports lower rates of The geological record shows that eustatic benthic respiration (Hargrave 1980). Conse- events associated with black shale deposition quently, if the mixed layer depth deepens during can be superimposed on either relatively low the later stages of transgression (while the bot- or high (but not maximum) global sea levels, tom water layer also thickens), oxygen demand implying that the initial depth of the epeiric sea may also fall for this reason. may have varied significantly prior to the devel- opment of anoxia. This suggests the thickness of the bottom water layer, at least as it is Conclusions determined by the total depth, may not be the only significant variable. However, if it were, 1. The integration of biological and geological what would such a model predict? We would knowledge is essential to a full understanding of expect anoxia to be associated mainly with trans- the incidence and consequences of natural and gressions during generally low sea levels, but anthropogenically induced oxygen depletion with (minor) regressions during generally high events in the marine continental shelf sea levels. Some black shale events are indeed environment. associated with regressive changes, such as dur- 2. Consideration of the factors underlying the ing the early Barremian, and perhaps the occurrence of dysoxic-anoxic events in modern Cenomanian-Turonian in NW Europe (Tyson shelf seas leads to the suggestion that an actu- & Funnell 1987). This perhaps emphasises the alistic seasonal model gives the best explanation importance of not confusing high 'global' sea for dysoxic- anoxic facies in most ancient epeiric levels with water depth per se; high global sea seas. levels have a greater influence on the lateral 3. The thickness of the bottom water layer extent of shelf seas than they do on their actual beneath a seasonal pycnocline is apparently depth. Indeed, if the total (emergent and sub- critical to the establishment of a seasonal anoxia mergent) topography of the shelf is relatively in mid-latitude shelf areas. This in turn is a subdued, lateral changes should be expected to function of water column depth and bottom be far greater than changes in actual water topography in relation to pycnocline depth. depth in the offshore areas. More detailed data Extensive anoxia is thus unlikely in depths are needed to appraise the implications of this greater than 60 m in those open shelf areas that model. are unaffected by upwelling and/or the influence Another significant depth-related factor is of oxygen minimum zones. This may have sig- the variation in the flux of metabolizable organic nificant implications for the water depths of matter. Although the synthesis of Suess (1980) ancient epeiric seas. Areas where the summer could detect no statistically significant decline in bottom water is less than 10 m thick are es- carbon flux with depth in the upper 200 m of pecially prone to dysoxia-anoxia, particularly the water column, JOrgensen (1982), Wollast if subjected to higher organic loading, or if the (1983), and Christensen (1989) indicate that a stratification period is extended to seven or three- to ten-fold decrease occurs between more months by an early spring and/or late coastal waters and a depth of 300 m. Conse- autumn. Such an extension may be caused by Downloaded from http://sp.lyellcollection.org/ by guest on September 24, 2021

MODERN & ANCIENT CONTINENTAL SHELF ANOXIA 19 anomalous weather conditions or longer-term Aeronautical Administration Professional Paper, global climatic shifts. 11, 137-150. 4. As haloclines are generally stronger than ARNTZ, W. E. 1981. Zonation and dynamics of macro- thermoclines, localised dysoxia-anoxia may be benthos biomass in an area stressed by oxygen most common in salinity-stratified areas adjac- deficiency. In: BARREtt, G. W. & ROSENBERG, R. (eds) Stress Effects on Natural Ecosystems. Wiley, ent to rivers. However, more extensive shelf Chichester, 215-225. dysoxia-anoxia is probably related to the , BRUNSWIG, D. & SARNTHE1N,M. 1976. Zonation seasonal thermocline. The more important of molluscs and molluscan shells in the Kiel general role of run-off may be to provide an Bay channel system (western Baltic Sea). initial stabilization of the water column, and Senckenbergiana Maritima, 8, 189-269. thus promote earlier formation of the seasonal -- & RUMOHR, H. 1986. Fluctuations of benthic thermocline in coastal waters. It may also pro- macrofauna during succession and in an estab- vide the nutrients to fuel higher organic loading. lished community, Meeresforschung, 31, 97-114. 5. Enclosed basins are frequently subject to 97 - 114. ARTHUR, M. A., SCHLANGER,S. O. ~ JENKYNS, H. C. more prolonged periods of oxygen depletion 1987. The Cenomanian-Turonian Oceanic when bottom water flushing periodicities are Anoxic Event, II. Palaeoceanographic controls dependent on global climatic forcing on inter- on organic-matter production and preservation. annual or even geological timescales. In: BROOKS, J. & FLEET, A. J. (eds) Marine 6. Shelf faunas are probably generally more Petroleum Source Rocks. Geological Society, sensitive to oxygen stress than those in oxygen London, Special Publication, 26, 401-420. minimum zones (OMZ) on the continental BADEN, S. P., Loo, L.-O., P1HL, L. & ROSENBERG, R. margin. This reflects the higher ambient oxygen 1990. Effects of eutrophication on benthic com- concentration and thus higher proportion of munities including fish: Swedish west coast. Ambio, 19, 113-122. stenoxic organisms and the lack of acclimatiz- BAILEY, G. W., BYERS, C. J. DE B. & LIPSCHITZ, S. ation, and also the greater range and rate of R. 1985. Seasonal variations of oxygen deficiency change in oxygenation that are experienced on in waters off southern South West Africa in 1975 the shelf. Models based solely on OMZ data and 1976 and its relation to the catchability and may be unrepresentative for normal shelf areas. distribution of the Cape Rock Lobster Jasus 7. These conclusions have critical implications lalandii. South African Journal of Marine both for the interpretation of ancient dysoxic- Research, 3, 197-214. anoxic 'black shale' facies and for the prediction & CHAPMAN, P. 1985. The nutrient status of the of those contemporary anoxic events which St Helena Bay Region in February 1979. In: SHANNON, L. V. (ed.) South African Ocean Color might result as a consequence of future sea- and Upwelling Experiment, Sea Fisheries Re- level changes driven by global warming. search Institute, Cape Town, 125-145. BARBER, R. T. & CHAVEZ, F. P. 1986. Ocean varia-

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