Impact of Past Global Warming on Biodiversity

IMPACT OF PAST GLOBAL WARMING ON BIODIVERSITY

Gregory J. Retallack University of Oregon

I. Introduction oxygen isotopic composition Ratio of common iso- II. Proxies for the Past topes of oxygen (16Oand18O) analyzed in a mass III. Correlation between Biodiversity and Global spectrometer and reported in delta notation (d18O) Warming relative to a standard (usually Peedee Belemnite) and IV. Environmental Consequences of Past Global reported in parts per thousand (permil), used as a Warming proxy for paleotemperature and global ice volume. V. Biotic Consequences of Past Global Warming soil Bk horizon Level within a soil of carbonate VI. Conclusions (calcite or dolomite) enrichment in the form of nodules, mottles, rhizoconcretions, or filaments, used as a proxy for paleoprecipitation. soil salinization index Molar ratio of soda and pot- GLOSSARY ash over alumina, determined by whole-rock chemical analysis, and used as a proxy for carbon isotope composition Ratio of common iso- paleotemperature. topes of carbon (12C and 13C) analyzed in a mass stomatal index Percentage of stomatal openings com- spectrometer and reported in delta notation (d13C) pared with epidermal cells, used with fossil plant relative to a standard (usually Peedee belemnite) cuticles as a proxy for past atmospheric CO2 levels. and reported in parts per thousand (permil), used as a proxy for atmospheric methane abundance. chemical index of alteration Molar ratio of alumina over alumina plus soda, potash, lime, and magne- GLOBAL WARMING due to anthropogenic atmos- sia, determined by whole-rock chemical analysis, pheric pollution with greenhouse gases will have and used as a proxy for the residue (alumina) ver- significant biotic effects in the coming century. Pre- sus solutes (soda, potash, lime, and magnesia) of dicting those effects from among the noise of natural hydrolytic weathering, used as a proxy for paleo- geographic and temporal variation will be difficult precipitation. until the effects are too profound to be reversed. For- methane clathrate Methane (CH4) gas frozen in ice tunately, the fossil record includes numerous instances within deep submarine sedimentary pore space or of abrupt global warming coincident with spikes in permafrost. concentration of greenhouse gases, and furnishes a

Encyclopedia of Biodiversity Copyright & 2007 Elsevier Inc. All rights of reproduction in any form reserved. 1 2 ______IMPACT OF PAST GLOBAL WARMING ON BIODIVERSITY______

variety of predictions of environmental and biotic CR.Paleo. Eocene Oligo. Miocene P. Q. consequences of global warming. 3 (a) Marine foraminifera carbon isotope value 2

1 C marine C

13 0

foram (‰) foram I. INTRODUCTION −1

(b) Marine foraminifera oxygen isotope value A variety of natural processes appear to have dramat- 0 ically increased atmospheric greenhouse gases in the 2

geological past: asteroid impact, ﬂood-basalt volcanic marine O

foram(‰) 18 eruption, release of submarine or permafrost methane 4

clathrates, and contact metamorphism of coal meas- e

ual 20 (c) Montana paleosol Bt chemistry

ures by igneous intrusions (Retallack and Krull, 2006). 15

C) ° ( 10 Abrupt transients of atmospheric CO2 in the past are

temperatur 5 discernible from proxies such as the stomatal index of ann Mean fossil plants (Retallack, 2002) and carbon isotopic (d) Montana paleosol Bt chemistry 1000 composition of pedogenic carbonate (Tabor et al., ual 800 2004). Abrupt transients in atmospheric CH4 are dis- 600 (mm) 400

cernible from proxies such as carbon isotopic compo- precipitation Mean ann Mean sition of organic matter (Retallack and Krull, 2006). (e) Utah−Montana paleosol Bk depth These indications of atmospheric conditions can be 1000 matched with indications of temperature change, such ual 800 600

as the oxygen isotopic composition of marine shells (mm)

400 precipitation (Veizer et al., 2000) and desalinization of soils (Shel- ann Mean 200 don et al., 2002). Other climatic consequences of CO2- (f) Ginkgo stomatal index induced warming include changes in mean annual 6000 precipitation from depth to carbonate (Retallack, 5000

4000 retaceous

2005a) and degree of base depletion of paleosols (ppmV) 3000 2 Mid-Miocene 2000 End-Eocene

(Sheldon et al., 2002). These indications of global CO

End-Paleocene change can be compared with past records of life, such 1000 End-C as biodiversity (Sepkoski, 1996). Indications are al- 70 60 50 40 30 20 10 0 ready clear that some past global warmings due to in- Age (Ma) creases in greenhouse gases were hardships for life and FIGURE 1 Cenozoic global change indicators: (a) carbon isotopic detrimental to biodiversity. composition of benthic foraminifera (Zachos et al.,2001), (b) oxygen isotopic composition of benthic foraminifera (Zachos et al.,2001), (c) mean annual temperature of paleosols in Montana inferred from paleosol salinization index (Sheldon et al., 2002), (d) mean annual II. PROXIES FOR THE PAST precipitation of paleosols in Montana inferred from paleosol chemical index of alteration (Sheldon et al., 2002), (e) mean annual precip- A critical difference between evidence from the fossil itation of paleosols in Utah and Montana inferred from depth to Bk horizon in paleosols (Retallack, 2005b), (f ) CO2 concentration in the record and studies of the modern environment is the atmosphere estimated from the stomatal index of fossil Ginkgo leaves limitation of preservation. Measurements such as air (Retallack, 2002). Times of high CO2 are generally warm and wet. temperature measured directly today must be inferred for the geological past from proxy measurements, which are preserved features of rocks or fossils known to vary with temperature. Such proxy measurements depend A. Paleotemperature for their accuracy on the degree to which they are known to covary with temperature today,and the degree A popular proxy for global marine paleotemperature is to which they have resisted alteration during burial. the inverse relationship between temperature and 18 There are more such proxies than can be adequately oxygen isotopic value (d O) of carbonate in shells discussed in this short account, which is limited to of marine foraminifera (Zachos et al., 2001), mollusks explaining proxies applied to two time series of global and brachiopods (Veizer et al., 2000). Water vapor 16 warmings in the Cenozoic (Fig. 1) and Permian (Fig. 2). with the light isotope ( O) evaporates from a cold ______IMPACT OF PAST GLOBAL WARMING ON BIODIVERSITY______3

CAPermian TRI. proxy for oceanic paleotemperature is compromised Guada- Lop- Cisuralian lupian ingian by global ice volumes, which are a separate reservoir dominated by the light isotope (16O). As either a

ng.

an global ice volume or local temperature signal, marine gurian

haipi

Wordian Roadian biogenic carbonate oxygen isotopic composition is an

Asselian

Gzhelian

Artinskian Kun

Capitani

Sakmarian Greisbach.

W Changhsing. important global change indicator (Fig. 1b). Dis- (a) Peltasperm stomatal index 14,000 entangling the different signals of ice volume and and paleosol carbonate 12,000 (ppm) temperature from oxygen isotope values requires in- 2 10,000 8000 dependent proxies for ice volume or temperature, 6000 which have their own problems. Another problem is Paleosol 4000 burial recrystallization of fossils, especially small, po- 2000

13 rous fossils such as foraminifera. Observations of clam

Atmospheric CO Peltasperm C

m or brachiopod shells in petrographic thin sections or (b) Carbon isotopes 4 arine cararine the scanning electron microscope for original biogenic Sovetashan 2

‰) marine carbonate 0 microstructure are sufﬁcient to rule out burial alter-

bonate (

arine −20 ation (Veizer et al., 2000). atter ( atter −25 A proxy for paleotemperature on land is based on

nonm Talcher nonmarine C ‰) observations that warmer climates have greater evapo- − organic matter 13 30

transpiration than colder climates, and thus leach organic m organic (c) Sydney basin paleosols more alkali cations from soils. The soil salinization and glendonites 15 - index, or molar ratio of potash plus soda to alumina in

C) ° the clay-enriched subsurface (Bw or Bt) horizons of

ual e ( 10 - soils, shows a clear inverse relationship with mean 5 - annual temperature in North American soils (Sheldon

0 et al., 2002). Such estimates of paleotemperature from

Mean ann temperatur - paleosols show trends broadly comparable with ma-

) 1200 (d) Texas−Oklahoma paleosols rine isotopic records (Fig. 1c). This paleosol proxy for

n (mm 1000 paleotemperature can be compromised by burial al- mian 800 teration of soil clay mineral composition, particularly

End- Cisuralian

End-Per illitization, which can be assessed by X-ray dif-

Guadalupian End- recipitatio 600 fractograms of clay (Retallack, 2001).

ual p 400

n Other indications of paleotemperature on land are

erous

an 200 nif not so fully quantiﬁed, but nevertheless locally useful

arbo

C (Fig. 2c). Deeply weathered kaolinitic soils (Ultisols) Mean 0 305 295 285 275 265 255 245 are not found at mean annual temperatures lower than Age (Ma) 121C, whereas soils with ice disruption (Gelisols) are found in regions with mean annual temperature no FIGURE 2 Permian global change indicators: (a) CO2 concentration in the atmosphere estimated from the stomatal index of fossil Le- more than 01C. Similarly, ikaite crystals (CaCO3 pidopteris leaves (Retallack, 2005c) and carbon isotopic composition 6H2O) or their pseudomorphs (glendonites) are large of paleosols (Tabor et al.,2004), (b) carbon isotopic composition of spindle-shaped structures within sediment of lake or marine limestone from Sovetashan, Armenia (Baud et al.,1989)andof ocean bottoms, and unstable in waters warmer than organic carbon from Talcher, India (de Wit et al.,2002), (c) paleo- 1 temperature indicated by glendonites and paleosols from the Hunter 5 C(Retallack, 2005c). Valley, New South Wales, Australia (Retallack, 2005c), (d) paleoprecipitation from depth to Bk horizons in paleosols of Oklahoma and Texas, USA (Retallack, 2005c). Times of high CO2 are generally warm and wet, and some are also times of signiﬁcant negative carbon iso- B. Paleoprecipitation tope excursions. The increased depth to carbonate nodules (Bk horizon) in modern soils with increasingly humid climates ocean more readily than water vapor with the heavy was ﬁrst documented eastwards from the Rocky isotope (18O), thus leaving ocean water and bicarbo- Mountains, USA. This relationship was subsequently nate used in shell manufacture isotopically heavier shown to be a global phenomenon, and attributed to (more positive in standard d18O notation permil). This increases in acidifying soil respiration with rainfall 4 ______IMPACT OF PAST GLOBAL WARMING ON BIODIVERSITY______

(Retallack, 2005a). Long sequences of paleosols show 10,000 (a) Ginkgo−Lepidopteris considerable variation in paleoprecipitation (Figs. 1e, 8000 Stomatal index 2d). This measure of paleosols is compromised by

(ppmV) compaction due to burial, but corrections are applied 2 6000 based on unfolding of formerly planar features or on ric CO 4000 thickness of overburden. Corrections for different levels of atmospheric carbon dioxide can also be 2000 made, but these are not very large (40 mm per annum Atmosphe more rainfall for ﬁve times preindustrial level of CO2), 70 (b) Marine invertebrate genera because atmospheric variations in carbon dioxide 60

ion (%) levels are dwarfed by soil respiration in most soils. 50

Another proxy for paleoprecipitation is based on xtinct 40 observations that wet climate soils are more leached of 30 alkali and alkaline earth cations than dry climate soils. neric e 20 The chemical index of weathering without potash, or molar ratio of alumina, lime, magnesia, and soda to alu- 10

Marine ge mina in the clay-enriched subsurface (Bw or Bt) horizons 0 300 250 200 150 100 50 0 of soils shows a clear relationship with mean annual Age (Ma) precipitation in North American soils (Sheldon et al., 2002). This geochemical proxy shows trends comparable FIGURE 3 (a) Records of atmospheric CO2 at geological stage with the physical proxy of calcic horizon depth in the boundaries from stomatal index of Ginkgo and Lepidopteris (after Retallack, 2002; emended following Wynn, 2003)and(b)ofper- same paleosols (Fig. 1d). Leaving out potash, a common centage generic extinction at those same geological stage boundaries soil cation, obviates problems with burial illitization from compilations of shelly marine invertebrate taxonomy for the past (Retallack, 2001). The chief problems with this proxy 300 My. After Sepkoski (1996). are local refreshing of soil fertility, for example, by limestone colluvium or volcanic ash, which are best detected through petrographic thin sections of the paleosols. preparable in sufﬁcient volume to obtain statistically valid stomatal index counts (Retallack, 2002). Another proxy for atmospheric CO2 is the carbon C. Atmospheric CO2 and CH4 isotopic composition of pedogenic carbonate. Plant-

A useful proxy for atmospheric CO2 is the stomatal respired CO2 in soil pores has much more light carbon 12 13 index of fossil leaves. This paleobotanical paleo- ( C) than heavy carbon ( C) because of the very barometer is based on the observation that plant marked preference of photosynthesis for the light iso- leaves have fewer stomates when atmospheric CO2 is tope. Animal and microbe-respired CO2 in soil pores is high than when atmospheric CO2 is low (Wynn, also isotopically light because the food chain starts 2003). Stomatal index is the number of stomatal with plant material. In contrast, the isotopic compo- openings as a percent of epidermal cell numbers, and sition of CO2 in the atmosphere is isotopically heavy is preferable to measures of stomatal density, because it CO2 degassed from volcanoes, and the mixing of these is less affected by competing effects of aridity, salinity, two end-members is a function of atmospheric CO2 and soil nutrient deﬁciency. A major limitation of this partial pressures. The approach is compromised by ef- approach is that sensitivity to carbon dioxide is taxon- fects of soil temperature and productivity, which can in speciﬁc, and few taxa span long periods of geological part be compensated by geochemical and petrographic time. The living fossil Ginkgo biloba has been used as a study of paleosols (Tabor et al., 2004). A more serious standard for atmospheric CO2 estimates from con- limitation is temporal variation in isotopic composition generic fossils back some 230 My (Retallack, 2002). of the atmosphere, which can be approximated from Other fossils of Lepidopteris in the same 230–200 mil- analysis of organic matter of the same age as the soil lion-year-old deposits as Ginkgo fossils have similar carbonate (Retallack, 2002). This requires large sam- stomatal anatomy and index, and can be used to ex- ples because carbonate nodular soils of dry climates are tend atmospheric CO2 estimates back 300 My lean for organic matter. This is a potentially volumi- (Figs. 1f, 2a, 3). The principal limitation of this ap- nous source of past atmospheric CO2 estimates, be- proach is its requirement of preserved plant cuticles cause calcareous paleosols are common (Figs. 2a, d). ______IMPACT OF PAST GLOBAL WARMING ON BIODIVERSITY______5

A proxy for atmospheric CH4 is the carbon isotopic III. CORRELATION BETWEEN composition of organic matter, such as fossil leaves, wood, humus, or dispersed organic matter. The carbon BIODIVERSITY AND GLOBAL WARMING isotopic values of methane reflect an unusual domi- nance of 12Cover13C. Whereas most organic matter Many data on paleotemperature and paleoprecipita- 13 tion are now available, and no clear relationship ranges from 22% to 30%d C, thermogenic CH4 is 35% to 55%, typically 40%, and biogenic emerges between them and biodiversity. This is to be expected because climate is so heterogeneous around CH4 is 35% to 120%, typically 60% (Clayton, 1998). These measurable differences are preserved in the world that climate change may induce diversity loss in one part of the world but diversity gains else- plants because atmospheric CH4 oxidizes within about where. An exception is atmospheric CO2 levels and a decade to isotopically unusual CO2, which is then used for photosynthesis, and buried with the death of marine generic extinction (Fig. 3), which shows po- the plant. The carbon isotopic anomaly at the Perm- sitive correlation (Fig. 4). With 42 degrees of freedom ian–Triassic boundary is so profound in both marine and a t value of 6.7, this relationship is highly signi- and nonmarine rocks worldwide (Fig. 2b) that release ficant (po0.0001). to the atmosphere of some 2000 Gt of methane are The relationship between CO2–CH4 greenhouse required (Berner, 2002). This is an enormous atmos- and extinction is best understood in extreme cases, pheric injection of a mass of methane equivalent to the such as the End-Permian mass extinction, widely ac- carbon in all current terrestrial biomass and soil car- knowledged to be the greatest life crisis in Earth his- bon (1 Gt is 1015 g). A limitation with this proxy is that tory (Sepkoski, 1996). An abrupt increase in the amount of methane can only be calculated if an atmospheric CO2 is indicated at 250 Ma by stomatal original isotopic composition is assumed: Berner’s es- index decline of seed ferns (Fig. 2a), and contempo- timate was calculated for biogenic values of –60%, and raneous transient CH4 outburst is indicated by mark- is low compared with estimates assuming thermogenic edly lower carbon isotopic composition of organic values of –40%. Sources of such large amounts of matter and marine carbonate worldwide (Fig. 2b). methane include outburst from submarine methane Modeling of this atmospheric pollution event with clathrates and thermal alteration of coals by volcanic reducing gases may have resulted in geologically rapid intrusions (Retallack and Krull, 2006). (over some 20,000 years) drawdown of atmospheric O2 from levels of 35%, which is higher than present levels of 21%, to levels as little as 12% (Berner, 2002). Such an atmospheric redox crisis has suggested several D. Biodiversity mechanisms of extinction for different kinds of organ- Past biodiversity is estimated from the numbers of isms. families, genera, or species of fossils within particular In the sea, the most lethal effect would have been geological periods or stages. For truly global coverage excess CO2 (hypercapnia) and low O2 (hypoxia). This such estimates come from literature compilations, for example the Treatise of Invertebrate Paleontology, and now increasingly from computer databases. The most 70 robust of these is the record of skeletonized marine y = 0.0059x + 10.115 60 R2 = 0.52 invertebrates (Sepkoski, 1996), but estimates of plant and vertebrate diversity are also available (Benton, 50 1995). Such proxies of biodiversity suffer from funda- 40 mental limitations of preservational bias and study bias. They are clearly an underestimate of past diver- eric (%)extinction 30 sity because many weakly skeletonized and soft-bod- 20 ied creatures are preserved only in rare amber or black 10 shales. There is also a clear bias between groups, with Marine gen trilobites, for example, attracting more taxonomic at- 0 tention than corals. Some periods of time are better 0 2000 4000 6000 8000 10,000 represented by rocks than others, because of changes Atmospheric CO2 (ppmV) in sea level, and so have inflated diversity compared FIGURE 4 Cross-correlation between CO2 and extinction levels at with less well-represented times. geological stage boundaries shown in Fig. 3. 6 ______IMPACT OF PAST GLOBAL WARMING ON BIODIVERSITY______would adversely affect skeletonized organisms with of global warming can now be observed in multiple limited ventilatory capacity such as corals and bra- examples. Past global warmings furnish a variety of chiopods, which were mostly extinct, rather than more environmental expectations for global warmings of the muscular bivalves and ammonoids, which survived in future. great numbers but limited diversity. Corals may also have been affected by postapocalyptic global warming, inducing expulsion of zooxanthellae and coral blea- A. Soil Acidification ching. No coral reefs are known for the first 6 My of Increased atmospheric CO2 creates greater volumes of the Triassic, a conspicuous ‘‘reef gap’’ in the fossil carbonic acid (H2CO3), which is the chief proton record of coral reefs extending back to the Ordovician. source for hydrolytic weathering. Atmospheric acidity Among land plants, the most lethal effect would be is minor compared with the effect of soil respiration, low O2 (hypoxia) in soil solution, endangering root which can raise soil CO2 levels to 100 times that of the respiration, especially in swampy soils already chal- atmosphere and generate large volumes of carbonic lenged for aeration by waterlogging. This would acid. Furthermore, increases in rainfall (Figs. 1d, e, adversely affect swamp plants such as glossopterids 2d) and temperature (Figs. 1c, 2c) with higher atmos- and lycopsids, which became extinct, with less-severe pheric CO2 levels raise both primary and secondary effects on surviving horsetails, true ferns, seed ferns, productivity of soils, and thus soil respiration. Thus, a and conifers. No peat swamps are known for the first variety of related effects accelerate chemical weather- 6 My of the Triassic, as indicated by a ‘‘coal gap,’’ which ing at times of high atmospheric CO2, more rapidly is the most profound break in the record of coals since depleting soils of alkaline soil nutrient cations such as their first appearance in Devonian rocks. Ca2þ ,Mg2þ ,Kþ , and Na þ . The result is the spread of Among land vertebrates, atmospheric O2 depletion base-poor kaolinitic soils (Ultisols and Oxisols) and (hypoxia) would have resulted in conditions at sea soil-weathering products (bauxites) to high paleolat- level more like those found at high altitude today, lea- itudes at times of CO2 greenhouses (Retallack, 2001). ding to death by pulmonary edema. Surviving vertebrates were primarily small burrowing species, preadapted to poorly ventilated spaces, and with bony B. Marine Alkalinization palate, large chests, and short limbs common in high- altitude vertebrates today (Retallack and Krull, 2006). Increased chemical weathering at times of high CO2 The Permian–Triassic boundary crisis was extreme, has the effect of adding more soluble ions to groundwater and ultimately the sea. The ocean is thus buff- a global warming and atmospheric redox perturbation of unusual magnitude. Other comparable events of ered with bases, mainly bicarbonate (HCO3 ), which is the conjugate base to carbonic acid. Also enhanced in lesser magnitude (Figs. 1–3) had less-severe effects on 2þ biodiversity (Fig. 4). A base level of about 10% generic groundwater and the ocean are basic cations (Ca , Mg2þ ,Kþ , and Na þ ), which are important biological extinction at very low levels of atmospheric CO2 re- flects typical differences in biota from one geological nutrients. Moderate levels of oceanic fertilization stage to another, and may be an artifact of long spans would have promoted coral and shellfish growth, of geological time used to calculate extinction rates. and thus limestone formation. High levels of fertiliza- Nevertheless, background rates of biodiversity loss tion promote seafloor anoxia, and pyritic black shale grade insensibly into global mass extinctions. formation, commonly seen at times of global warming. Extreme alkalinization may explain abiotic precipitation of seafloor fans of calcite (Knoll et al., 1996). IV. ENVIRONMENTAL CONSEQUENCES OF PAST GLOBAL WARMING C. More Humid Climate Global warming induced by CO2 increases the water The 18 events of global greenhouse in the past 300 My vapor holding capacity of the atmosphere. Water vapor (Fig. 3) give a new perspective on the current ant- itself is a powerful greenhouse gas, thus amplifying hropogenic greenhouse. Instead of a unique event, CO2-induced warming. Unlike CO2, however, water is current global warming can be considered among an regularly rained out of atmosphere and so is not a array of earlier global warming events showing a spec- primary control of greenhouse warming. Thus, it is not trum of severity. Consistent environmental correlates surprising to find evidence from both chemical ______IMPACT OF PAST GLOBAL WARMING ON BIODIVERSITY______7 weathering and depth of calcic horizons in paleosols G. Shrinking Cryosphere that times of high CO2 were also times of greater mean annual precipitation (Figs. 1d, e, 2d). Global warming results in melting of polar and alpine ice caps and glaciers, and surrounding regions of periglacial soils. In accord with this view, glacial till- ites, varved shales, and dropped pebbles are limited in D. Enhanced Climatic Seasonality temporal distribution to well-defined ‘‘Ice Ages.’’ The Tropical monsoonal climates have very pronounced ice age of the past 1.6 My is presaged by high-latitude dry seasons interspersed with short deluges of rain, ice-rafted debris as old as 30 Ma. With the exception of and soils of such climate have a distinctive spread of some possible Valanginian (138 Ma) ice-rafted debris pedogenic nodules throughout the soil profile. Less in South Australia there are no reported glacial de- seasonal climates in contrast have carbonate nodules posits, even at high latitudes as far back as Late Perm- within well-defined (Bk) horizons. Thickness of soil ian (258 Ma). The Late Devonian to Middle Permian with nodules is a proxy for the difference between the Ice Age, well known especially from the high-latitude mean precipitation of the driest and wettest month, southern supercontinent of Gondwana is at a time of and seasonality of precipitation as well as mean annual low atmospheric CO2, judging from stomatal index precipitation both increase during atmospheric CO2 (Fig. 3). From then back to another ice age of the Late spikes (Retallack, 2005a). Ordovician, there is again little evidence of glacial facies (Hambrey and Harland, 1981), and indications from paleosols of high CO2 (Mora et al., 1996). The fossil record of ice-disrupted soils, or Gelisols, and E. Increased Runoff associated tundra and taiga ecosystems, also supports

Increased rainfall at times of atmospheric CO2 spikes evidence from glacial facies for a reduced cryosphere would be expected to result in increased stream runoff, at times of global warming (Retallack, 2001). with the complication that increased rainfall also ap- pears to increase plant productivity and stature and thus soil moisture retention. In the extreme case of the V. BIOTIC CONSEQUENCES OF PAST Permian–Triassic boundary, increased runoff in a post- GLOBAL WARMING apocalyptic greenhouse of the earliest Triassic is ap- parent from a change in stream architecture from The various environmental effects of global warming meandering to braided, and appearance of beds of outlined above are closely interrelated with a variety of eroded soil clods (Retallack, 2005b). Such changes are biotic changes recorded in the fossil record. As with not so obvious in lesser atmospheric CO2 spikes, such environmental consequences, many biotic conse- as the middle Miocene warm-wet spike in Montana quences are interrelated. (Fig. 1c–e). A. Reduced Plant Transpiration

Times of high CO2 are not only times of low stomatal F.Rising Sea Level index (Figs. 1f, 2a), but also times of reduced stomatal Shrinking ice caps and thermal expansion of the ocean aperture and of increased cuticle thickness of leaves leads to marine transgressions at times of high atmos- (Retallack, 2002). These effects appear to be direct pheric CO2. The record of sea level change through plant responses to high CO2 levels, and lessened de- time supports this deduction (Haq and Al-Qahtani, mand for air intake at the stomate. The effect of all 2005). Especially striking are expansions of large epi- these changes is to reduce transpiration of water by continental seaways on stable continental platforms. In vegetation, which in turn lowers atmospheric mois- Utah, for example, most Mesozoic rocks are nonma- ture, raises soil water tables, and increases stream rine, but these red eolian, fluvial, and pedogenic red runoff (Beerling, 2005). beds include thin marine limestones: Sinbad Lime- stone (Smithian, 249 Ma), Virgin Limestone (Spathian, B. Increased Plant Sclerophylly 247 Ma), Carmel Formation (Callovian, 164 Ma), and Tropic formation (Cenomanian, 94 Ma). These were Times of high CO2 are marked by an abun- all times of high atmospheric CO2 (Fig. 3). dance of photosynthetic shoots rather than leaves, of 8 ______IMPACT OF PAST GLOBAL WARMING ON BIODIVERSITY______needle-leaves rather than broadleaves, and of densely G. Wetland Eutrophication veined leaves rather than loosely veined leaves (Beer- ling, 2005; Retallack, 2005c). These various indica- Wetland paleosols at times of high CO2 include min- tions of increased sclerophylly may be a response to erals such as siderite and berthierine indicating un- declining soil nutrient status with soil acidification or usually anoxic conditions in close association with root to increased plant consumption by animals and traces and burrows (Sheldon and Retallack, 2002). At- pathogens. mospheric hypoxia may explain these differences, but so could increased microbial productivity under warmer and wetter conditions, because microbial res- C. Increased Leaf Herbivory piration depletes oxygen from stagnant groundwater. Large collections of fossil leaves commonly contain examples of a variety of insect and fungal damage, but H. Oceanic Eutrophication the proportion of damaged leaves is greater at times of Times of high CO are also times of black, pyritic shales high CO (Wilf et al., 2001). Increased abundance of 2 2 with paper clams and other fossils tolerant of hypoxia fungi at times of high CO is also indicated by scle- 2 (Knoll et al.,1996), reduced area and extinction of rotinite in coals and spores and hyphae in palynofloras tropical coral reefs (Wiedlich et al.,2003), and blooms (Retallack and Krull, 2006). This may be a secondary of microfossil dinoflagellates and diatoms (Siesser, effect of the greater primary and secondary pro- 1995). These geological observations could be conse- ductivity ecosystems under warmer and wetter condi- quences of oceanic eutrophication with nutrient cations tions, or perhaps also a consequence of the spread to from increased terrestrial weathering, but also plausible higher latitudes of animals and pathogens formerly is direct chemical reduction from an hypoxic atmos- limited by seasonal freezing. phere (Retallack and Krull, 2006), coral death by blea- ching as zooxanthellae were expelled in warming water D. Tropical Plant Geographic Expansion (Wiedlich et al.,2003), and phytoplankton blooms tracking increased climatic seasonality (Siesser, 1995). The spread into polar regions of tropical plants such as palms with large frost-insensitive terminal meristems at times of high CO2 is probably a consequence of global warming. Such geographic expansion of trop- VI. CONCLUSIONS ical plants has been especially important for North Anthropogenic global warming due to atmospheric pol- American broadleaf vegetation, which contains many lution by CO and CH is commonly regarded as un- Asiatic and European taxa which migrated via Be- 2 4 precedented, but the rock and fossil record indicates ringian and North Atlantic land bridges and islands many comparable past atmospheric redox crises. Com- (Wing, 1998). monalities among these past events allow a better un- derstanding of global warming induced by greenhouse E. Tropical Animal Geographic Expansion gases. Biodiversity generally declined during geologically rapid global warmings due to CO2 and CH4 emis- Times of high CO2 and mild polar climates also en- sions from volcanic eruption and intrusion, meteorite abled migration to high latitudes of tropical animals impacts, or outbursts from submarine and permafrost such as primates and crocodiles (Markwick, 1994). As methane clathrates. Extreme cases of greenhouse re- for plants, such migrations also allowed transconti- lease to the atmosphere are the great mass extinctions of nental biotic interchange via high-latitude land bridges the fossil record, when many creatures died from the such as Beringia (Clyde and Gingerich, 1998). effects of hypoxia, hypercapnia, and pulmonary edema. At lower levels of greenhouse gases, such lethal effects F.Helical Animal Burrows were limited in area to high altitudes, stagnant wetlands, oligotrophic coral reefs, and deep ocean basins. Helical animal burrows are rare in the fossil record, Some consequences of global warming such as in- presumably requiring more effort than straight ramps. creased precipitation and warmth extending to high- Helical burrows are common at times of high CO2 and latitude intercontinental land bridges had the effects of global warming, perhaps because helicoidal airflow is increasing biodiversity. Hardships such as soil acidifi- self-ventilating (Meyer, 1999). cation and increased seasonality of climate selected for ______IMPACT OF PAST GLOBAL WARMING ON BIODIVERSITY______9 sclerophyllous, thickly cutinized plants. Hardships such Retallack, G. J. (2001). Soils of the Past: An Introduction to Pale- as hypoxia selected for greater respiratory scope in an- opedology, 2nd ed., p. 600. Blackwell, Oxford. imals. Such adaptations added to biodiversity. The ef- Retallack, G. J. (2002). Carbon dioxide and climate over the past 300 Myr. Proc. Roy. Soc. Lond. Philos. Trans. 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