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K–T TRANSITION GREENHOUSE AND EMBRYOGENESIS DYSFUNCTION IN THE DINOSAURIAN EXTINCTIONS

Dewey Max McLean
Department of Geological Sciences
Virginia Polytechnic Institute and State University
Blacksburg, VA 24061

ABSTRACT

The dinosaurs became extinct 65 million years ago during the K–T transition mass extinction that defines the Cretaceous–Tertiary boundary. Debate exists over whether the extinctions were caused by asteroid impact or Deccan Traps volcanism. Impact–induced global blackout and refrigeration known as an "impact winter," and volcanism–induced climatic warming known as a "greenhouse" have been invoked as killing mechanisms.

Temporal linkage of physical phenomenon with a mass extinction does not establish causality. A killing mechanism preserved in the record must be isolated and coupled physiologically to the organisms that became extinct.

The K–T record lacks definitive evidences of an impact winter. Carbon cycle perturbation and warming are reflected in the d13C and d18O records. Several K–T phenomena: marine transgression, reduced photosynthesis of terrestrial and marine floras, reduced weathering rates, K–T boundary eruption of 90 percent of the Deccan Traps lavas, and possible K–T asteroid/comet impact produced a major K–T transition greenhouse.

A greenhouse triggered dinosaurian extinctions via heat–induced embryogenesis dysfunction. Females experiencing warming suffered reduced blood flow to the uterine tract, damaging fertilized eggs and embryos and killing them in numbers to reduce population sizes to the point of extinction.

INTRODUCTION

Several times in earth history, the biosphere has experienced discrete intervals of intense extinctions known as mass extinctions. Since the late 1970s and early 1980s, the cause of mass extinctions has become the topic of intense scientific debate. Of all the great mass extinction events, the one defining the Cretaceous–Tertiary (K–T) boundary 65 million years ago (during which the dinosaurs died out) has most caught scientific and public imagination and has now become the subject of one of the great debates in the history of science.

Of all the theories ever devised to account for the K–T extinctions, two have become dominant since the early 1980s. One is that 65 million years ago, a giant asteroid slammed into earth, blasting dust into the stratosphere blocking out sunlight and turning earth’s surface into the blacked out and frozen hell of an "impact winter." The other is that the Deccan Traps mantle plume volcanism in India flooded earth’s surface with carbon dioxide trapping heat from the sun and causing the hot climatic hell of a "greenhouse." Proponents of each theory are called "impactors" and "volcanists," respectively.

An exciting topic, the K–T debate has attracted researchers from many fields of science. The heterogeneity, while stimulatory, has created a major impediment to understanding of the K–T world. This problem involves the development of polarities, or thematic antitheses.

Major thematic antitheses concerning the K–T debate are: (1) extraterrestrial impact versus terrestrial mantle plume volcanism, (2) K–T boundary short–duration abrupt extinctions versus K–T transition long–duration gradual bioevolutionary turnover, (3) impact winter in which impact dust blocked out sunlight, blacking out and chilling earth’s surface versus a CO2–induced greenhouse, (4) vertebrate extinctions via impact winter cold and dark versus greenhouse warming damage to reproductive physiology, and (5) marine extinctions via impact–induced acidification of the surface of the oceans versus acidification via uptake by the marine mixed layer of volcanic CO2. These antitheses must be removed as part of seeking cause to the K–T extinctions.

The temporal linkage of physical phenomena such as impact events or volcanism with mass extinctions does not prove that the phenomena caused the extinctions. To establish causality between event and extinction, a killing mechanism preserved in the record must be isolated and coupled physiologically to the organisms that became extinct to account via known principles or laws of nature for their demise.

The purpose of this paper is to attempt to remove antithesis concerning K–T transition climate change and, in the process, unify the K–T geobiological record via carbon cycle perturbation and greenhouse conditions. The record contains no definitive evidences of a K–T boundary impact winter (McLean, 1991a).

The state of the biosphere at any time is a function of the rate of solar–earth–space (S-E-S) energy flow. As the flow rate changes, the state of the biosphere must change accordingly. During K–T transition time, convergence of several phenomena (marine transgression, reduced photosynthesis of terrestrial and marine floras, reduced weathering rates, K-T boundary eruption of 90 percent of the Deccan Traps lavas, and possible K–T asteroid/comet impact) produced a major carbon cycle perturbation that altered the S-E–S flow rate, and thus the state of the biosphere. The latter change was manifested in K–T transition biological turnover, or mass extinctions. For the dinosaurian extinctions, I will propose that embryogenesis dysfunction caused by greenhouse warming reduced population sizes to the point of extinction. Dinosaur females experiencing warming would have suffered reduction of blood flow to the uterine tract, heat–damaging fertilized eggs and embryos and killing them in sufficient numbers to drive the dinosaurs into extinction. This is a continuation of work I began in the 1970s.

INTEGRATED EARTH SYSTEMS AND THE STATE OF THE BIOSPHERE

System Dynamics

So alien, ancient, and complicated was the K–T transition world that to resolve antitheses and to unify it requires viewing it within the perspective of the universal dynamics that govern evolution of earth’s biosphere. This involves addressing multidisciplinary integrative systems analyses, solar–earth–space energy flow (the dominant energy flow driving earth’s surficial processes, and the biosphere), and physicochemical and biological systems behavior and interactions through time, etc. System dynamics methodology allows handling of large amounts of multidisciplinary data in ways to illuminate otherwise elusive processes and principles.

Figure 1 is a causal loop diagram from system dynamics methodology. It shows how processes operating within earth systems, and interactions between systems, operating via the carbon cycle, influence the solar–earth–space energy flow system. The latter is the dominant energy flow system driving earth’s surficial processes, including those of the biosphere. The state of the biosphere at any time is a function of the rate of solar–earth–space energy flow.

Causal loop diagrams provide the first step in evaluating system behavior. They allow visualization of interrelations between system variables and expose feedback loops within individual systems, and between adjoining systems. They are developed by assembling pertinent variables, and then correlating the variables with one another as causally–related pairs where one member of the pair acts as an independent variable, and the other as a dependent variable.

Independent and dependent variable pairs are connected to one another by an arrow which is interpreted to read "affects," "influences," or "causes," and which expresses asymmetrical and irreversible relationships between the variables. The independent variable is at the base of the arrow, and the dependent variable is at the arrowhead. Correlation between variables is either positive or negative and is expressed by a plus or minus sign placed by the arrowhead. Correlation is positive if the independent and dependent variables both either increase or decrease in value, and negative if they respond differently from one another. The causal pairs are next integrated with other variable pairs, exposing relationships that might otherwise not be apparent. Often, causal pairs will close upon themselves, exposing feedback loops.

Feedback is either positive or negative, and is expressed as the polarity of a feedback loop. The polarity is indicated by a (+) or (–) sign within a curved, partially closed arrow placed within the feedback loop. Polarity is determined by counting the minus signs at the arrowheads within a feedback loop. An even number indicates positive polarity (positive feedback), and an odd number negative polarity (negative feedback). Positive feedback produces exponential growth or collapse. Conversely, negative feedback expresses goal–seeking behavior, and stability. Causal loop diagrams are used as a basis for developing flow diagrams which allow mathematical analysis of the behavior of systems.

Systems Interactions and the State of the Biosphere

Solar–earth-space energy flow system (Figure 1, along top): Earth’s biosphere (earth’s life of earth and its environment) is an intermediate system in contact with a hot energy source (the sun), and a cold heat sink (outer space). Solar energy is the dominant energy flux for biological organization, and the organizing factor for ecology (Morowitz, 1979). Except for energy supplied from the sun which drives photosynthesis, the biosphere is self–sufficient with H2O, O2, and all nutrients supplied by utilization and recycling of materials already in the system. Morowitz (1979) defines the biosphere as that part of the terrestrial surface which is ordered by the flow of energy mediated by photosynthesis.

The solar–earth–space energy flow rate is influenced by greenhouse gas composition of earth’s atmosphere; H2O and CO2 are the dominant greenhouse gases. Greenhouse gases trap heat from the sun via the greenhouse effect, raising earth’s surface temperature by about 30°K, to 288°K (Levine, 1986). Water vapor accounts for about two thirds of the greenhouse effect. If not for greenhouse warming, earth’s surface would be too cold to support life.

The solar–earth–space energy flow maintains the biosphere as a nonequilibrium, open, working system. Without solar–earth–space energy flow, the biosphere would decay into thermodynamical equilibrium. The biosphere self–organizes as a function of solar–earth–space energy flow at both the macroscopic and molecular levels (Morowitz, 1979).

Solar–earth–space energy flow is influenced by many variable processes: release of mantle CO2 onto earth’s surface, marine transgressions and regressions, areal coverage of terrestrial flora, weathering rates, abundance of marine algae, impact events, and orbital dynamics, etc. Discussion follows:

Core–mantle system (Figure 1, lower right): According to the homogeneous accretion model after earth formed as a protoplanet it melted, causing earth to differentiate into a core, mantle, crust, hydrosphere, and an atmosphere. In the process, earth inherited a hot interior. Through time, earth is losing its internal heat to the cold space heat sink surrounding earth. The energy outflow forced by this thermal gradient determines the direction and rate of evolution of the earth, itself (Maj, 1984).

The flow of heat from the interior of the earth to space operates as a great heat engine to drive earthly processes such as mantle convection, plate tectonics, and degassing of the greenhouse gases H2O vapor and CO2 onto earth’s surface. Earth is analogous to a wind–up clock that is allowed to spontaneously run down through time. Through time, as earth loses it internal heat to space, these processes will slow down, and eventually cease. Earth’s physiochemical spheres can only evolve through time, and along with them, the biosphere.

Mantle temperature and viscosity function together to establish a balance between internal heat production and loss (Tozer, 1972). Loss of heat from the interior of the earth is controlled via negative feedback loops operating at the core–mantle interface. Verhoogen (1980) proposed steady state between internal heat/entropy production and heat loss.

Earth loses most of its internal heat steadily to space via the ocean ridge systems. Hotspots account for between 5 to 10 percent of the heat and magma (Davies, 1988; Sleep, 1990), in which mantle plumes may function as safety valves for heat escape. Mantle plume pulses may result via chaos in mantle convection in which sluggish convection alternates with periods of vigorous convection. Such volcanism can extrude vast amounts of basaltic lavas onto earth’s surface in a geologically short duration. Basu et al. (1993; and Basu pers. comm.) indicate that 90 percent of the Deccan Traps lava pile erupted at K–T boundary time 65 million years ago in the short span of 100,000 to 200,000 years.

According to Olson (1992), much of the Cretaceous was characterized by vigorous volcanism in which the rate of oceanic crust production was about twice that of today via melting of one or several, massive thermal superplumes emanating from the deep mantle beneath the Pacific and Indian plates. The Deccan Traps fits the concept of a superplume.

Over long time periods, surficial systems and sinks become adjusted to existing mantle CO2 flux rates. The sudden additional CO2 released onto earth’s surface by mantle plume volcanism overwhelms surficial systems, disrupting the carbon cycle and the solar–earth–space energy flow system. Those disruptions make the components of the biosphere work to remain in autopoiesis, and may force them into new domains. I have long proposed that the K–T extinctions were a function of a carbon cycle perturbation associated with the Deccan Traps volcanism in India (McLean, 1981, and later).

Marine eustacy (Figure 1, right center): Marine transgressions and regressions affect global climatology in several ways. Because the heat capacity of water is greater than that of land, more solar radiation is absorbed during times of transgressions than during times of low stands of sea level. Thus, transgressions produce warmer and more equable climates than do regressions. High evaporation rates associated with widespread epeiric seas increase the concentration of the dominant greenhouse H2O vapor in the atmosphere, enhancing greenhouse warming. Regressions produce the opposite effects.

Terrestrial floras and weathering rates (Figure 1, right center): Transgressions and regressions also influence the areal distribution of terrestrial plants, and weathering rates, and thus global climatology.

In the late 1970s, I proposed that marine transgressions and regressions influence land/marine plant ecosystem ratios and thus atmospheric CO2/O2 ratios (McLean, 1978b). Modern land floras account for about 70 percent of the global productivity. Marine regressions, by allowing expansion of terrestrial floras, increase photosynthesis and atmospheric pO2 and reduce pCO2. Marine transgressions produce the opposite effect. Land floras have probably dominated marine algal productivity since the middle of the Paleozoic.

Expansion of land floras increases chemical weathering rates, reducing atmospheric pCO2 by the following process (after Berner, 1993). Vascular land plants accelerate chemical weathering by their secretion of acids, providing ground litter for the microbial production of CO2 and holding and recycling moisture in the soil. Weathering of Ca–Mg silicate rocks on the continents, is followed by precipitation of the Ca and Mg as carbonate minerals in the oceans, regulating atmospheric CO2 on a multimillion–year time scale. The reactions are: CO2 + CaSiO3 ---> CaCO3 + SiO2, and CO2 + MgSiO3 ---> MgCO3 + SiO2. In addition to accelerating weathering, plants provided a source of bacterially resistant organic matter for burial in sediments. Berner (1993) argues that removal of atmospheric CO2 by massive burial of sedimentary organic materials in the Carboniferous and Permian periods—evidenced by abundant coals—caused the Permo–Carboniferous glaciation, the most extensive and longest glaciation of the entire Phanerozoic.

Volk (1989) suggested that Late Cretaceous and Early Tertiary diversification and proliferation of angiosperm–deciduous ecosystems increased mineral weathering, drawing down atmospheric pCO2, and causing global cooling.
Knoll and James (1987) showed that different ecosystems cause weathering of soil minerals at different rates. Angiosperm–deciduous systems lose soil K, Mg, and Ca at rates three to four times higher than do conifer–evergreen ecosystems.

Marine coccolithophorids (Figure 1, lower left): Varying abundances of marine coccolithophorids can influence atmospheric pCO2. In the late 1970s, I evoked K–T collapse of the coccolithophorids as cause of a terminal Mesozoic greenhouse (1978a, and later).

During times of abundance, coccolithophorids draw down both atmospheric and marine mixed layer pCO2 via their influence upon the Williams–Riley "pump." This is a process whereby surficial CO2 becomes incorporated into particulates and settles gravitationally to become stored in marine sedimentary reservoirs.

As photosynthetic organisms, coccolithophorids consume CO2, incorporating it into organic particulates. They also produce CaCO3 coccoliths. Thus, the coccolithophorids are a important sink for CO2 storage in the deep oceans. During times of coccolithophorid reduction, the CO2 that they normally consume accumulates in the marine mixed layer and in the atmosphere, disrupting the solar–earth–space energy flow system, and enhancing greenhouse warming.

The coccolithophorids and other marine algae (all protoctists) influence solar–earth–space energy flow by another method. They release DMS (dimethyl sulfide) into the atmosphere where it serves as condensation nuclei for clouds. Whereas high algal productivity enhances cloud cover over the oceans low productivity reduces cloud cover, enhancing climatic warming. Rampino and Volk (1988) indicate that the K–T collapse of the coccolithophorids could have produced global warming of 6°C or more.

Impact events (Figure 1, lower middle): Asteroid or comet impacts might trigger greenhouse conditions via injection of H2O vapor into the atmosphere (Emiliani et al., 1981) or by CO2 injection via impact upon carbonate terranes (O’Keefe and Ahrens, 1988, 1989; Sigurdsson et al., 1991). The Chicxulub structure on Yucatan has been proposed as a K–T boundary impact site (Hildebrand, et al., 1991; Sharpton et al., 1992).

Orbital variations (Figure 1, lower left): As earth orbits about the sun it wobbles on its axis. Orbital variations are reflected in the sedimentary and climatological records as cyclical patterns known as Milankovitch cycles. I have linked Milankovitch cycles to the Pleistocene–Holocene mammalian extinctions but cannot currently link them to the K–T transition mass extinctions.

THE LATE CRETACEOUS AND K–T TRANSITION DINOSAURIAN EXTINCTIONS

This section addresses system changes occurring before and during the K–T transition, drawing upon principles developed in the preceding section. In addressing the dinosaurian extinctions, two time intervals must be addressed: (1) a long–duration Late Cretaceous climatic cooling, during which many types of dinosaurs were dwindling away and disappearing, and (2) a K–T transition greenhouse warming beginning about 10,000 years before the K–T boundary and extending at least 200,000 thousand years into Early Tertiary, that would have triggered the final phase dinosaurian extinctions.

Late Cretaceous Climatic Cooling and the Dinosaurs

Late Cretaceous marine regression: During Late Cretaceous, epeiric seas flooded parts of the continents. Near the end of Cretaceous, major regression was occurring. That the regression was coeval with climatic cooling was recently confirmed by Stott and Kennett (1988, 1990).

Regression would have contributed to climatic cooling. Because of water’s heat capacity, it absorbs and retains solar radiation. Regression, by reducing the areal extent of epeiric seas, would have caused climatic cooling. Lowered evaporation rates associated with the reduced areal extent of epeiric seas would have reduced the atmospheric H2O vapor level, and thus the greenhouse effect, contributing to climatic cooling.

Terrestrial floras, and weathering rates: The Late Cretaceous marine regression would have allowed expansion of highly productive terrestrial floras, drawing down atmospheric CO2 via photosynthesis, triggering anti–greenhouse cooling. Expansion of terrestrial floras, increasing weathering rates, would have further reduced atmospheric pCO2, contributing to Late Cretaceous climatic cooling.

Marine coccolithophorids: The coccolithophorids were abundant during Late Cretaceous producing great chalk deposits. High photosynthesis rates in conjunction with the Williams–Riley "pump" would have reduced atmospheric and marine mixed layer pCO2. High coccolithophorid productivity would have elevated DMS (dimethyl sulfide) levels in the atmosphere over the oceans, enhancing cloud cover, and climatic cooling.

Dinosaurs: Dinosaurs were generally dwindling away during Late Cretaceous (Sullivan, 1987; Sloan et al., 1986; Rigby et al., 1994). Archibald and Bryant (1990) implicate habitat disruption associated with marine regression in the vertebrate extinctions. Spotila et al. (1991) noted that modern large reptiles physiologically resemble mammals in terms of heat production and heat loss, that metabolic rates of mammals and reptiles may converge at very large size, and that for large animals the distinction between endothermy (warm blooded) and ectothermy (cold blooded) lose much of their meaning. For modern large mammals, environmental temperatures below the optimum for conception lower fertility by reducing estrual activity, perhaps via effects of cold temperatures on metabolic and endocrine adjustments needed to maintain body heat, and possibly to sperm damage.

Large dinosaurian body size would have been advantageous by damping out short–term climatic fluctuations, and allowing maintenance of stable body temperatures (Spotila et al., 1973). However, in the long–duration Late Cretaceous cooling, thermal inertia conferred by large size would have been disadvantageous, and dinosaur body temperatures would sooner or later have cooled off sufficiently to interfere with physiological life processes, including those of reproduction.

K–T TRANSITION GREENHOUSE WARMING

In the 1970s, I proposed that greenhouse conditions had triggered the K–T mass extinctions (McLean, 1978a). By 1979, I was isolating the Deccan Traps mantle plume volcanism in India as the source of the K–T carbon cycle perturbation and, in 1981, proposed at several meetings (Toronto AAAS, Ottawa K–TEC II, and Snowbird I) that Deccan Traps mantle CO2 degassing had triggered the K–T transition greenhouse.

About the same time, the Alvarez asteroid team at Berkeley proposed that impact of an asteroid with earth had blasted dust into the stratosphere blocking out sunlight and plunging earth into the dark and cold of an impact winter triggering K–T boundary extinctions (Alvarez et al., 1980).

Faced with thematic antithesis concerning K–T climate change, I began a search for evidences of a K–T boundary impact winter of magnitude to trigger mass extinctions. A decade of search did not produce definitive evidences of a K–T boundary impact winter (McLean, 1991). Conversely, the K–T transition record beginning about 5,000 to 10,000 years below the K–T boundary and extending at least 200,000 years into Early Tertiary is one of CO2–induced greenhouse climatic warming.

K–T transition marine transgression: Just preceding K–T boundary time, the Late Cretaceous marine regression ceased, and marine transgression began anew. This transgression produced a sea-level rise of up to 130 meters (Donovan et al., 1988; Haq et al., 1987; Hallam, 1989). Gerta Keller (pers. comm.) indicated that the reversal from regression to transgression occurred about 5,000 to 10,000 years before K–T boundary time. Keller et al. (1993) indicated that transgressive cycle extended throughout early Paleocene until interrupted by two short–term sea level low stands at about 50,000 and 230,000 years after the K–T boundary, after which transgression resumed and normal marine conditions were established.

This latest Cretaceous transgressive phase would, in itself, have contributed to K–T transition warming. Because the heat capacity of water is greater than that of land, more solar radiation would have been absorbed than during the preceding regressive stage. Expansion of epeiric seas would have increased evaporation rates, increasing the concentration H2O vapor in the atmosphere, further enhancing greenhouse warming.

Terrestrial floras and weathering rates: By flooding highly productive terrestrial floras, the K–T transition transgression would trigger atmospheric CO2 buildup. Carbon dioxide that terrestrial floras consume via photosynthesis and lock up into organic particulates that are stored in the sedimentary repository would have built up in the atmosphere, contributing to greenhouse warming. With decrease in terrestrial plant productivity, weathering rates would have decreased also contributing to atmospheric CO2 buildup and greenhouse warming.

Marine coccolithophorids: The near collapse of the marine coccolithophorids at the K–T boundary (Pospichal, 1994) would have triggered atmospheric CO2 buildup via disruption of the marine Williams–Riley pump. Also, reduced coccolithophorid productivity would have reduced DMS (dimethyl sulfide) production, decreasing cloud cover and enhancing K–T transition climatic warming.

Deccan Traps volcanism: The Deccan Traps fits the category of a superplume. When it burst through the crust it could have very quickly flooded earth’s surface with mantle CO2, triggering abrupt K–T transition greenhouse warming. A great rift extends generally east–west across India. Seismic data indicate that it crosses the Moho into the mantle (McLean, 1985a, 1985b). Thus, when the Deccan Traps plume head passed beneath the Narmada Son rift, basaltic lavas were able to quickly flood through it along a great distance. According to Basu et al. (1993, and Basu, pers. comm.), about 90 percent of the vast Deccan Traps erupted right on K–T boundary time 65.0 million years ago, pouring out its vast volume of basaltic lavas in 100,000 to 200,000 years. Duncan and Pyle (1988) note that Deccan Traps erupted rapidly, that there is no significant difference in age from the stratigraphically oldest to the youngest rocks, and that they were coeval with events at the K–T boundary. Keller (1993) notes that northern high latitude warming beginning 5000 to 10,000 years before the K–T boundary may be related to major global volcanism accompanied by a greenhouse effect and rapid global warming.

Rapid eruption of the vast Deccan Traps lava fields would have flooded earth’s surface with CO2, overwhelming systems and sinks, triggering rapid K–T transition greenhouse warming (McLean, 1985a, 1985b 1985c; 1988).

K–T transition stable isotope record: As indicated in Figure 2 (the Brazos River section, after Keller and Barrera, 1990) both the d13C and d18O records show negative excursions beginning at the K–T boundary and persisting through the K–T transition.

The d18O excursion coincides almost precisely with the duration of the Deccan Traps volcanism, marine transgression, reduction of land floras and weathering rates, and collapse of the marine coccolithophorids, and almost certainly reflects K–T transition greenhouse warming. Keller (1993) cited evidence of northern high latitude warming beginning 5,000 to 10,000 years before the K–T boundary (from Schmitz et al., 1992; Keller et al., 1993).

The d13C negative excursion has been interpreted as severely reduced marine surface–water productivity (Boersma and Shackleton, 1981; Perch–Nielsen, et al., 1982; Zachos and Arthur, 1986; Zachos et al., 1989). However, I have argued that it might reflect, in part, mantle release of 13C–depleted mantle carbon onto earth’s surface by the Deccan Traps volcanism (McLean, 1985a). Recent work by Deines et al. (1993) on inclusions in diamonds from the Orapa kimberlite, Botswana, Africa, provides new information on lower mantle chemistry, and I now propose that the d13C negative excursion marks the time of outpourings of the bulk of Deccan Traps lavas. According to Deines et al. (1993), d13C variability in the mantle may increase with depth and at greater depths low d13C carbon may occur more frequently. They base this conclusion on websteritic inclusions in diamonds. Those inclusions are transitional between peridotitic and eclogitic minerals, are characterized by a unique combination of high chrome and iron content, and have d13C values ranging from –15.2 to –22.4‰. The unique combination of high chrome and iron content seems to rule out a subduction origin of the low d13C host. Dienes et al. (1993) indicate that the frequency of low d13C carbon may increase with increasing mantle depth, that the 13C depleted carbon may be a primary mantle feature.

If the Deccan Traps mantle plume originated at the core–mantle interface as some geodynamicists indicate, it could have transported 13C–depleted CO2 to earth’s surface where it became incorporated in coccolithophorid and foraminiferal CaCO3 mineralogy, accounting for a least a portion of the K–T transition d13C negative excursion.

K–T iridium enrichment: In 1981, I proposed that the K–T boundary iridium enrichment was released onto earth’s surface by the Deccan Traps mantle plume volcanism at the Toronto AAAS national meeting (McLean, 1981a), at the Ottawa K–TEC II (1981b), and at the Snowbird I conference (1981c). It is now known that the hotspot volcano that produced the Deccan Traps, Piton de la Fournaise on Reunion, is still releasing iridium today (Toutain and Meyer, 1989).

Canudo et al. (1991) note that all deep sea sections have a hiatus at the K–T boundary that spans from 70,000 to 400,000 years of earliest Tertiary. Keller (1993) indicates that iridium is often concentrated at the K–T boundary because of dissolution or nondeposition of other sediments.

However, some K–T sections have multiple iridium spikes. The Braggs section in Alabama has three: one in late Maastrichtian, one near the K–T boundary, and one within faunal Zone NP1. Donovan et al. (1988) note that the iridium spikes coincide with marine–flooding surfaces interpreted as parasequence boundaries. The iridium was not introduced into the atmosphere during a unique event at the K–T boundary but was present in the atmosphere for a longer period of time. Globally the K–T boundary is marked by marine terrigenous–sediment starvation. The decrease in terrigenous sedimentation associated with a global K–T transition rise in sea level was a fundamental part of the process that concentrated the iridium.

Chicxulub structure on Yucatan: If the Chicxulub structure on Yucatan is a K–T boundary impact feature as proposed by Hildebrand, et al. (1991) and Sharpton et al. (1992), it could have triggered a K–T boundary greenhouse via injection into the atmosphere of H2O (Emiliani et al., 1981) or CO2 (O’Keefe and Ahrens, 1988, 1989; Sigurdsson et al., 1991).

K–T DINOSAURIAN EXTINCTIONS: GREENHOUSE-REPRODUCTIVE PHYSIOLOGY COUPLING

Because the dinosaurs are extinct, models must be created to assess how they fit thermally into their world. Not all models agree. Whether the dinosaurs were endothermic (or warm–blooded, producing most of their body heat metabolically) or ectothermic (or cold–blooded, getting most of their body heat from the environment), is the topic of spirited debate. Whatever the case, they were likely homeothermic (or able to maintain a fairly constant body temperature), and not poikilothermic, (unable to maintain precise control of body temperature) (Cloudsley–Thompson, 1978).

Of available models, that developed by Spotila et al. (1991) seems well thought out and reasonable. I will integrate that model with a K–T transition greenhouse in attempt to account for the terminal extinctions of the dinosaurs. Based on the conclusions of Spotila et al. (1991) that: (1) large modern reptiles physiologically resemble mammals in terms of heat production and heat loss, (2) metabolic rates of mammals and reptiles may converge at very large size, and (3) the distinction between endothermy (warm blooded) and ectothermy (cold blooded) lose much of their meaning for large animals, I propose that the environmental heat–conception failure coupling that operates among modern mammals is extendable to the dinosaurs. I will develop that coupling for mammals, and then apply it to the dinosaurs.

Mammals: For modern mammals, conception rates and fertility decrease during summer in temperate, subtropical and tropical climates (Badinga et al., 1985; Gwazdauskas et al., 1973; Gwazdauskas et al., 1975; Ingraham et al., 1974; Johnson, 1985; Thatcher, 1974). Loss of fertility is attributable to effects of heat upon the female reproductive system. Embryo damage and death can occur in air temperatures that pose little danger to adults.

In high air temperatures, an adult female mammal shunts blood to superficial tissues and respiratory muscles to dissipate heat to the environment. This action reduces the flow of blood to the core (abdominal viscera, nonrespiratory muscles, and reproductive tract). Blood flow to the uterine tract is a developing embryo's source of oxygen, nutrients, water, and hormones (Senger et al., 1967; Bazer et al., 1969; Barron, 1970). It also moves damaging heat away from the embryo (Abrams et al., 1971; Gwazdauskas et al., 1974). Reduction of uterine blood flow can damage, or kill, developing embryos. The higher the environmental temperature, the greater the reduction of uterine blood flow.

Mammals are considered to be homeotherms. However, mammalian core temperature varies daily and seasonally. Bligh (1985) notes that mammals do not have precise control over core temperature, and that finely controlled homeothermy is not a mammalian characteristic.

Figure 3 (after Yousef et al., 1968) shows that core temperature varies as a function of air temperature for lactating European–origin cattle. Up to a point, mammals can maintain a steady state core temperature, but above that the core temperature rises. For Holstein, Jersey, and Brown Swiss cattle, core temperatures begin to rise at 70°, 75°, and 81°F (21°, 24°, and 27°C). The air temperature where core temperature begins to rise in most domestic animals is from 28° to 32°C. High humidity lowers the air temperature at which core temperature begins to rise.

Core temperature rises during the day, and large mammals spend considerable time during the day in hyperthermia. To avoid continual hyperthermia, animals must lose this excess heat during the cool night.

Optimum embryo development occurs at an optimum, nearly constant, uterine temperature. A temperature rise of 1.8-2.7°F (1.0-1.5°C) above optimum can kill an embryo. Figure 4 (after Badinga et al., 1985, based on artificial inseminations for over 12,000 Florida cattle) shows that conception rates drop sharply when the maximum air temperature on the day after insemination exceeds 86°F (30°C). First cleavage of the fertilized egg occurs about a day following insemination, and it is most vulnerable to maternal heat stress at that time. Frank Gwazdauskas (Dairy Science, VPI & SU, pers. comm.) noted that about 50% of cattle embryos die under natural conditions (10% in the first 4 days, and 40% between 6 to 15 days), implicating reduced blood supply to the oviducts as a factor.

Maternal heat stress–induced embryo death may involve alterations in synthesis of conceptus proteins involved in embryonic development and maternal recognition of pregnancy (Putney et al., 1988). Heat stress retards embryonic development. Embryo death may result from its failure to produce biochemical signals, causing corpus luteum regression. The preattachment conceptus produces proteins critical to maintenance of the corpus luteum and continuation of pregnancy (Northey and French 1980; Betteridge et al. 1984; Bartol et al. 1985; Knickerbocker et al. 1986a). Also, heat–induced alterations of the uterine endometrium may cause pregnancy failure.

Dinosaurs: Knowledge that large modern reptiles physiologically resemble mammals in terms of heat production and heat loss, that metabolic rates of mammals and reptiles may converge at very large size, and that the distinction between endothermy (warm blooded) and ectothermy (cold blooded) seemingly lose much of its meaning for large animals (Spotila et al., 1991) permits extending environmental heat–conception failure coupling operative in modern mammals to the dinosaurs.

Based on studies of metabolism of the modern leatherback turtle (the largest marine turtle, and at 1000 kg one of the largest living reptiles) and simulations of dinosaurs, Paladino et al. (1990) coined the term "gigantothermy." Gigantotherms are able to maintain constant high body temperatures via large body size, low metabolic rates, use of peripheral tissues as insulation, and use of variable blood flow between the core and skin. Large modern reptiles such as leatherback and green turtles, Komodo dragons, and giant tortoises are gigantotherms.

The leatherback turtle provides the best model for the study of gigantothermy in living reptiles (Spotila et al., 1991). Using peripheral tissues as insulation and changing blood flow, it maintains a body temperature of 30°C in Arctic waters of 10°C or less, and avoids overheating in tropical seas.

Paladino et al. (1990) note that gigantothermy would have allowed large dinosaurs with low metabolic rates to live in a wide variety of habitats without undue thermal stress, including the polar regions in late Cretaceous when polar climates were much milder and more equable than they are today. Large dinosaurs would not have faced a thermoregulatory challenge more severe than that overcome by leatherbacks in the North Atlantic today (Spotila et al., 1991).

In fact, during the Cretaceous, dinosaurs lived near the poles (Brouwers et al., 1987; Rich et al. 1988; Clemens and Nelms, 1993). In winter, small species may have hibernated, but larger species surely migrated to more warmer regions. Based on estimates of dinosaur body fat, Spotila et al. (1991) concluded that dinosaurs could have migrated long distances using fat as the energy supply, migrating farther if ectothermic than endothermic.

For dinosaurs, control of blood flow to the skin would have been effective in controlling body temperature. Via such control, intermediate–sized dinosaurs with a leatherback–like metabolic rate could have maintained appropriate core temperatures. The effects of changes in blood flow to the skin would have been greatest in the largest dinosaurs. Those with low skin blood flow would have been warmer than those with high blood flow, regardless of their cardiac output (Spotila et al., 1991) .

Whereas the thermal inertia inherent in large body size would have permitted the dinosaurs to remain homeothermic during short–duration climatic changes, it would have been disadvantageous during long–duration changes. Spotila et al. (1973) note that large body size would have been advantageous by damping out climatic fluctuations on the order of days or weeks allowing maintenance of stable body temperatures, but that seasonal variation in climate would have been of great significance to large dinosaurs. Studies on tortoise thermoregulation by Cloudsley–Thompson and Butt (1977) indicated that overheating would have been a problem for large dinosaurs.

In fact, overheating is a problem for any large animal in a warm climate. This is true for ectotherms and endothermic homeotherms. Any positive heat production places a large animal in heat stress. Cloudsley–Thompson (1978, p41) noted that medium sized dinosaurs with small surface–to–volume ratio would retain its heat overnight. Seasonal change would present a problem, and such animals might experience difficulty staying cool in a warm environment.

Spotila et al. (1991) note that leatherbacks heat up while on a beach and, if restrained in a net overnight, warm up as much as 2°C, a striking heat gain for an animal with the thermal inertia of a large sea turtle. If anything, leatherbacks have a problem dumping heat in a warm terrestrial environment. Cloudsley–Thompson and Butt (1977) noted that hot summers rather than cold winters would have been responsible for the extinction of the dinosaurs.

Sloan (1976) noted that species become extinct by failing to reproduce as rapidly as their members die, or by a reduction in population density or an increase in intensity of selection. That comment seems appropriate for the K–T transition dinosaurian extinctions.

During Late Cretaceous, dinosaurs were attempting to adapt to long–duration climatic cooling. The abrupt reversal to K–T transition greenhouse warming would have triggered chaos among dinosaurian reproductive systems. In effect, the dinosaurs would have gone into a thermal net that caught relatively large animals. Whereas the thermal inertia inherent of large body size would have been advantageous to large dinosaurs facing climate cooling, their small surface–to–volume ratio ratios would have been disadvantageous during warming, and they would have retained excessive body heat. Small size is advantageous in a rapidly warming world.

Female dinosaurs, attempting to thermoregulate in a greenhouse world, would have shunted blood supply to the skin, reducing the flow of blood to the uterine tract where fertilization takes place, causing it to heat above optimum for fertilized eggs and embryos. Maternal hyperthermy transmitted to fertilized egg during the first cleavage triggered massive embryo death likely triggered the K–T transition final phase of the dinosaurian extinctions. The mechanics of the final phase of the dinosaurian extinctions are shown in Figure 5 (McLean, 1991b), a causal loop diagram depicting a greenhouse physiological killing mechanism applicable to mammals, birds, and reptiles.

The contentions of Sheehan et al. (1991) and Russell (1984) that the dinosaurs disappeared fairly abruptly at the K–T boundary accord excellently with the K–T transition greenhouse extinction model developed herein.

CONCLUSIONS

In considering the extinctions of the dinosaurs, two time intervals must be addressed: (1) a long–duration Late Cretaceous climatic cooling, during which many lineages of dinosaurs were dwindling away and disappearing, and (2) a K–T transition greenhouse warming beginning about 10,000 years before the K–T boundary and extending at least 200,000 thousand years into Early Tertiary, that would have triggered the final phase dinosaurian extinctions.

Late Cretaceous climatic cooling: Late Cretaceous climatic cooling can be accounted for via integration of a number of factors. The documented Late Cretaceous marine regression by reducing the extent of epeiric seas would, in itself, have contributed to cooling. Because of its thermal capacity, water absorbs and retains solar radiation more effectively than does land. Replacing water by land would have triggered climatic cooling.

Regression would also have allowed expansion of highly productive terrestrial floras, increasing rates of photosynthesis and storage of organics into sedimentary reservoirs, and drawing down atmospheric pCO2. Reduction of the latter would create anti–greenhouse climatic cooling. Also, expansion of terrestrial floras would have increased weathering rates, further reducing atmospheric pCO2.

In the oceans, high abundance of the coccolithophorids would have reduced atmospheric pCO2, creating anti–greenhouse cooling. Also, these organisms release DMS (dimethyl sulfide), which serves as cloud nuclei, into the atmosphere. High production of DMS would have enhanced cloud cover over the oceans, contributing to Late Cretaceous climatic cooling.

Long–duration Late Cretaceous climatic cooling would have been detrimental to large ectothermal dinosaurs. During short–duration temperature changes, large size and its small surface–to–volume ratios confer a thermal inertia and some degree of homeothermy. However, steady, long–duration cooling, would have been detrimental to large ectotherms by preventing them from taking advantage of short periods of warming. Through time, their core temperatures would have cooled sufficiently to disrupt physiological life processes, including those of reproduction.

K–T transition greenhouse warming: A number of phenomena converged at K–T boundary time 65 million years ago to make a major carbon cycle perturbation, and greenhouse warming, a virtual certainty.

First, marine transgression beginning just before K–T boundary time would have expanded epeiric seas, enhancing absorption of solar radiation. Enhanced evaporation rates associated with expanded epeiric seas would have contributed to greenhouse warming.

Transgression would have caused reduction of terrestrial floras, reducing rates of photosynthesis and storage of organics and contributing to increase in atmospheric pCO2, and greenhouse warming. Decreased weathering rates associated with reduced terrestrial plant productivity would have also contributed to increase in atmospheric pCO2, enhancing greenhouse warming.

In the ocean, the marine coccolithophorids suffered catastrophic reduction at about the K–T boundary, disrupting the Williams–Riley pump, and contributing to K–T transition greenhouse conditions. Reduction of the coccolithophorids would also have reduced DMS production and cloud cover, enhancing climatic warming.

The Deccan Traps volcanism was another major source of CO2 release into the atmosphere. About 90 percent of the vast Deccan Traps lava pile erupted at K–T boundary time 65 million years ago. The d13C negative excursion at the K–T boundary perhaps marks the time of the massive outpourings of the Deccan Traps lavas.
Lastly, a K–T impact event could have contributed to greenhouse warming by releasing H2O and CO2 into the atmosphere.

Greenhouse warming during the K–T transition accounts for the final phase of the dinosaurian extinctions. Dinosaurs that were adapting to long–duration Late Cretaceous climatic cooling would have literally gone into a greenhouse heat thermal wall. Large female ectothermic dinosaurs attempting to survive in a hot new world would have increasingly shunted blood supply to the skin, reducing blood supply to the uterine tract where conception takes place, and where embryos must develop. Climate–induced reduction of uterine blood flow would have killed increasing numbers of dinosaur embryos, reducing population numbers until the dinosaurs finally dwindled away into oblivion.

ACKNOWLEDGMENTS

I thank Dr. Frank Gwazdauskas, Professor of Dairy Science, Virginia Polytechnic Institute and State University, Blacksburg, Virginia, whose pioneering work on effects of climate on mammalian reproduction, and counsel, provided direction for much of my work on the effects of carbon cycle perturbations upon the biosphere.

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