Terrestrial Ecosystems Through the Miocene: Responses to CO 2 Fluctuations

Transcription

1 1 Terrestrial Ecosystems Through the Miocene: Responses to CO 2 Fluctuations The Earth s biosphere is currently in the midst of a major mass extinction, in which large terrestrial organisms have been some of the most severely affected. The causes of this extinction are many, but scientists universally agree that deforestation, overhunting, and anthropogenic climate change are major contributors. A sudden crash in biodiversity has the potential to destabilize ecosystems, so efforts have been taken to stop this extinction in its tracks. Political and social initiatives have attempted to reduce the impact of deforestation and overhunting, but the continual changes to Earth s climate have kept ecosystems in jeopardy. The human influx of greenhouse gases to the atmosphere therefore looms as the next great challenge for the biosphere to overcome. Since it is impossible to quickly remedy or reverse climatic trends, conservation efforts must predict how ecosystems will reorganize in response to climatic forcing. To make these predictions, it is prudent to study past intervals of rapid climate change; researchers can use what is preserved in the rock to study how plants and animals responded to past intervals of climate change, which can yield powerful insights into the processes that underlie the response of the biosphere to rapid, significant fluctuations in climate. While the geological record preserves many intervals of climate change, the Miocene Epoch of the Neogene Period (23 to 5.3 million years ago) is one of the best periods to study in the effort to understand present climate change. The Earth s landmasses were in much the same position in the Miocene as they are today, with the same ocean basins existing at approximately their present size (Strömberg, 2011). Oceanic and atmospheric dynamics were, therefore, likely similar to those of the present, enabling researchers to directly compare Miocene conditions to those of today. The organisms present in the Miocene were also similar to those alive at present. While few species or genera have persisted from the Miocene to the present day, ecosystems comprised primarily of closely-related animals and plants. The major clades of plants had all evolved by the early Miocene; relatives of modern horses, cattle, elephants, and pigs fed upon them while evading the relatives of today s cats and dogs (Benton, 2005). The availability of modern animals for study makes it possible to draw more confident and numerous inferences regarding their extinct cousins. The Miocene geologic record also preserves rapid significant changes in climate proxies such as carbon and oxygen isotopes, indicating that the Earth s climate was in major flux at that time (Mihlbachler et al., 2011; Kürschner et al., 2008). Anthropogenic climate change is progressing alarmingly fast, so changes to the biosphere will likely align more with past rapid change than with past gradual change. The occurrence of a similar biosphere in similar global conditions during a period of rapidly changing climate gives the Miocene special importance in the effort to predict the consequences of anthropogenic warming.

2 2 Analyses of Miocene rocks with a variety of techniques strongly suggest that the epoch experienced rapid global warming, which is likely analogous to the one we are experiencing now. One technique that detected this warming was the use of oxygen isotopes. The measurement of δ 18 O defined as the ratio of 18 O to 16 O in a sample relative to that of a standard ratio has proven a useful proxy for many variables, including precipitation levels and global temperature. Measurements of δ 18 O in the shells of benthic foraminifera throughout the Cenozoic Era show an overall trend toward enrichment in the heavy isotope (more 18 O relative to 16 O) Fig. 1. δ 18 O and δ 13 C of benthic foram shells through the Cenozoic. More negative values of δ 18 O indicate warmer deep ocean temperatures, which imply high global temperatures. Positive shifts in δ 13 C also imply higher ocean temperatures; such shifts indicate less dissolved CO 2 in seawater, and gases are less soluble in warm water. Note the negative shift in δ 18 O and concurrent positive shift in δ 13 C in the Mid-Miocene. From Zachos et al. (2001). since the end of the Mesozoic; this can be seen in Figure 1. (Zachos et al., 2008; Mihlbachler et al., 2011). As benthic foram shells incorporate more 18 O in colder conditions, scientists interpret this as a decrease of global temperatures. Such a trend makes intuitive sense, given the wellknown warm climate of the Mesozoic. However, analyses also reveal three unique spikes in temperature, which appear as sharp negative shifts in δ 18 O. Two of these occur during the early part of the Cenozoic, in the Paleocene and Eocene Epochs; the last one, however, occurred during the Middle Miocene, from approximately 17 to 14 million years ago. Additional evidence supports the existence of this warm period, which is known as the Mid Miocene Climatic

3 3 Optimum or MMCO. For example, cold-blooded vertebrates such as turtles and crocodylians, which can only survive in warm conditions, thrived in central Europe from 18 to 14 million years ago; before and after this time range, they only appear in more southerly locations (Böhme, 2003). Furthermore, a positive excursion in δ 13 C in the shells of ocean-bottom phytoplankton is obvious in the Mid Miocene. These organisms prefer to photosynthesize light carbon-12 to heavy carbon-13, but lose their preference when dissolved CO 2 is scarce. Since gases are less soluble in water at higher temperatures, less dissolved CO 2 would have been available to phytoplankton in a period of global warming, which would cause the δ 13 C in their shells to increase markedly (Zachos et al., 2001). An increased atmospheric concentration of greenhouse gases is often the mechanism for periods of global warming. Greenhouse gases like CO 2 re-radiate outgoing longwave radiation and thereby heat the Earth s surface. Many studies have verified that atmospheric CO 2 tracks global temperature quite closely throughout the Phanerozoic (Kürschner, 2008). While the Paleocene and Eocene temperature increases have been definitively linked to rapid rises in atmospheric CO 2 (Zachos et al., 2008), evidence tying the Mid-Miocene Climatic Optimum (MMCO) to such an event is equivocal. Geochemical proxies for atmospheric CO 2 levels, such as δ 13 C in fossil soils and the δ 11 B in marine sediments, have suggested that CO 2 concentrations have remained below 500 ppm since the beginning of the Miocene 23 million years ago, with no evidence for a spike coinciding with the MMCO that is large enough to have caused such a drastic event (Strömberg, 2011; Zhang et al., 2013; Bender, 2013). Biological proxies, however, strongly support a short-term spike in atmospheric CO 2 coinciding with the MMCO. The stomatal density of fossilized plant leaves has been used to estimate ancient CO 2 levels. Stomata are pores on a plant s leaves, which open and close to control gas exchange between the leaf and atmosphere. They are the gateway through which plants inspire CO 2 for photosynthesis. The density of stomata on plant leaves is inversely correlated with contemporary CO 2 levels; at high levels of atmospheric CO 2, plants require less stomata to inspire their CO 2 (Woodward, 1987). An analysis of stomatal index (stomatal density normalized to the size of the leaf) of the fossilized leaves of extant tree species revealed a sharp drop and subsequent rise in stomatal index between 17 and 14 million years ago. This is consistent with a concurrent rapid rise and drop in atmospheric CO 2 (Kürschner, 2008). Since this proxy for CO 2 levels derives from the adaptations plants adopt to deal with their contemporary climate, it likely represents the true conditions of the time. Additional support for high atmospheric CO 2 during the MMCO comes from disparate sources. Attempts by climate modelers to simulate Cenozoic temperatures using the low CO 2 levels suggested by some isotopic proxies was met with failure; unless atmospheric dynamics during the Miocene differed fundamentally from today s conditions (an unlikely scenario, due to the similar positions of the continents and planetary topology during the Miocene and the present), such high temperatures would require 800 ppm of CO 2 in the atmosphere, double the concentration advocated by researchers such as Strömberg and Zhang (Goldner et al., 2014). Furthermore, massive volcanic

4 4 eruptions in Europe and North America are known from the Early- and Mid-Miocene. Volcanic eruptions are a major source of CO 2, so these eruptions would have released a significant amount of the gas into the atmosphere in time for it to accumulate and cause the MMCO. (Kürschner, 2008; Zachos et al., 2001). Powerful evidence supporting the existence of high CO 2 coinciding with the MMCO comes from the study of the assemblage of fossil mammals in what is now the Great Plains of North America. During the MMCO, the Great Plains region supported a woodland savannah habitat, with 500 to 1000 mm of annual precipitation. The vegetation was diverse, with trees, bushes, and primitive grasses coexisting side by side. Due to the concurrent climatic optimum, temperatures were much warmer than they are today, by as much as 10 C; this allowed a woodland savannah, which requires warm temperatures, to develop at such high latitudes. The best present-day analogue for the Mid-Miocene Great Plains is Africa s woodland savannah. Comparisons with this analogue, however, strongly suggest that the Mid-Miocene s atmosphere had much more CO 2 than today s (Janis et al., 2004). Despite the apparent similarity between modern African savannahs and the Mid Miocene Great Plains, the two ecosystems differ markedly in their diversity of ungulate mammals. The African woodland savannah is the most ungulate-rich grassland on Earth today, hosting over 20 species of ungulate 4 of them are browsers (which eat the leaves of trees and bushes) and 18 are grazers (which eat mainly grass) or mixed feeders (which eat both grass and leaves) (Janis et al., 2004). The richness of the African savannah, however, pales in comparison to that of the Mid-Miocene Great Plains, which preserves over 30 coexisting species of ungulate. Scientists can diagnose the diet of fossil herbivores by examining their teeth; higher-crowned ( hypsodont teeth) evolve in response to increasing levels of dietary abrasion, which usually correlates with the incorporation of abrasive grasses into the diet. Browsing species, which do not usually experience much abrasion, do not bother evolving high-crowned teeth and retain the ancestral brachydont (low-crowned) teeth (Janis et al., 2000). At its most diverse, the Great Plains boasted an astounding 19 browsing species, with 11 species of grazers or mixed feeders. Thus, the two ecosystems have completely different structures grazers and mixed feeders dominate the modern woodland savannah, while in the Mid-Miocene Great Plains browsers outnumbered grazers, with both comprising significant portions of the fauna. The latter ecosystem had more total large herbivores than the African woodland savannah, or indeed any modern fauna. Notably, there were more browser species in the Mid-Miocene Great Plains than there are today in even the most diverse forests, where browsers are expected to dominate. While no other time in the Cenozoic had an herbivorous fauna quite like that of the Mid-Miocene Great Plains (indeed, by the Late Miocene, the ecosystem structure in the region greatly resembled that of modern Africa), other contemporary ecosystems seem to have been similar: the South American La Venta locality seems to preserve similarly high browser richness, possibly confirming a global anomaly in ecosystem structure at this time (Janis et al., 2004).

5 5 The amount of carbon an ecosystem s vegetation fixes is the fundamental limit on the number of herbivores the ecosystem can support. With greater productivity, there is more available food for herbivores, so more species can survive. Therefore, Mid-Miocene ecosystems were likely able to support an anomalously high number of herbivores because they were very productive. Increased rainfall can increase plant productivity, but grassland ecosystems cannot survive when precipitation is excessively high trees take over and the region yields to forest. There are many indications that increased rainfall cannot have caused Mid-Miocene productivity to increase among them, the fact that paleobotanical data shows that the Great Plains was indeed grassland during the MMCO, the fact that oxygen isotopic evidence is inconsistent with increased rainfall, and the fact that ecosystems all over the globe show similar diversity. The best explanation for this phenomenon is a global rise in atmospheric CO 2 levels. Experimental evidence shows that plants have higher photosynthetic rates and grow faster in conditions of high CO 2 therefore, a rise in CO 2 could augment the vegetation in a region without fundamentally changing the area s biome. Primary productivity would increase, and the region would be able to support a far greater number of herbivores; since the vegetation in a woodland savannah is diverse, a highly productive woodland savannah could have high numbers of browsers and grazers, as is seen in the fossil record. Since rising atmospheric CO 2 is a global event, this would also explain why faunas worldwide show similar change (Janis et al., 2004). The unusually high ungulate diversity in the Great Plains during the MMCO serves as a powerful (if indirect) indicator that elevated CO 2 levels caused the climatic optimum to occur. Why the geochemical and biological proxies for the CO 2 content of the Mid-Miocene atmosphere yield conflicting data is not yet clear more research remains to be done to determine if it is the geochemical record or the paleobiological record that is lying about the conditions of the time. It seems wisest to trust the latter; paleobiological climate proxies represent the direct result of the interaction of organisms with their environment, so confounds are unlikely. Stomatal index has been found to accurately predict known CO 2 levels at different times in the past and terrestrial ecosystem structures indicate a period of unusually high primary productivity. Furthermore, massive volcanic eruptions (geological events known to release large amounts of CO 2 ) have been dated as coinciding with the beginning of the MMCO. The simplest and best explanation that ties the multiple lines of evidence with what is known from the present day is that the Mid-Miocene Climatic Optimum was a period of elevated atmospheric CO 2, despite geochemical evidence to the contrary. The period of anomalous warmth in the Mid-Miocene came to an end after about 3 million years of optimal conditions, approximately 14 million years ago. A sudden positive shift in δ 18 O marks this cooling; the isotopic shift persists all the way to the present day, and represents the pronounced cooling trend of the later Cenozoic that culminated in the Pleistocene ice ages (Zachos et al., 2001). Since the Mid-Miocene Climatic Optimum was caused by an influx of CO 2 into the atmosphere, it follows that it would have ended when CO 2 levels dropped back to their prior values or below. Stomatal index measurements confirm that a drop in CO 2

6 6 occurred concurrently with the cooling that ended the MMCO (Kürschner, 2008). Decreased atmospheric CO 2 levels would have decreased the Earth s greenhouse effect, thereby lowering the planet s average temperature. The likely culprit for the observed drop in atmospheric CO 2 is the sustained uplift of the Himalayan Mountains and the Tibetan Plateau. Mountains, due to the high surface area they expose to incoming precipitation, are very susceptible to chemical weathering. Carbonic acid forms as a result of the interaction between water droplets and CO 2 in the upper atmosphere. When acidic precipitation reacts with silicate rocks, they dissolve and form bicarbonate, which remains in surface water or precipitates to form carbonate rocks; the bicarbonate incorporates the carbon from the carbonic acid, removing it from the atmosphere. The dissolution of silicate rocks is therefore an important sink for atmospheric CO 2 (Brady, 1991; Raymo and Ruddiman, 1992). As mountains form, their weight causes the Earth s crust to sag beneath them; this downward deflection creates large basins on each side of the mountain. As weathering and erosion occur on the mountains, these basins fill with sediment, burying local organic matter and preventing its carbon from returning to the atmosphere. Geochemical analyses of sediments in the Himalayan area have determined that, from the Mid-Miocene onward, both of the above methods of carbon burial were highly active. The latter method (the burial of organic carbon in sedimentary basins) was the primary means of removing carbon from the atmosphere; its net burial was 2-3 times that of carbon removal from silicate weathering (France-Lanord and Derry, 1997). The substantial amount of carbon burial occurring in the Mid-Miocene would have removed a great deal of carbon from circulation and thereby caused the amount in the atmosphere to decrease. With less CO 2 in the atmosphere, the Earth s greenhouse effect would have been dampened, and global temperatures would have declined. Thus, the continual uplift of the Himalayas and the Tibetan Plateau caused atmospheric CO 2 levels to drop, and likely brought about the end of the Mid- Miocene Climatic Optimum. The tectonically-driven CO 2 decrease in the Mid- to Late Miocene had a profound effect on terrestrial plant communities, primarily as a result of the differences in photosynthetic pathway among different plant lineages. Most plants use one of two photosynthetic pathways, which are known as C 3 and C 4. The vast majority of plant species use C 3, which is the more ancient technique; only 3 percent of species use C 4 photosynthesis, which probably evolved within the last 60 million years (Bender, 2013). C 3 plants are diverse, including forest plants (such as trees and shrubs) and primitive grasses, while most C 4 plants are advanced grasses. The success of grasses has caused C 4 photosynthesis to account for 25 percent of terrestrial photosynthesis at present, despite the fact that the pathway only exists in a minority of plant species (Edwards et al., 2010). The two photosynthetic pathways perform differently, and are advantageous in different climatic and environmental conditions (Ehleringer et al., 1997). C 3 photosynthesis is not metabolically costly, but can fail to distinguish CO 2 from O 2 in conditions of low CO 2 or high temperatures, which causes inefficient photosynthesis; C 4 photosynthesis, on the contrary, uses energy to concentrate CO 2 near the photosynthetic organelles, giving it greater

7 7 efficiency than C 3 during times of low CO 2 or high temperatures. The exact level of CO 2 at which C 4 becomes more efficient varies with temperature. C 4 photosynthesis also uses water more efficiently, so dry climates favor C 4 over C 3 (Edwards et al., 2010; Bender, 2013). Since the two photosynthetic pathways dominate in different environmental conditions, the primary pathway used in a paleoenvironment can serve as a proxy for the environmental conditions of the time. However, plant fossils are relatively rare, and anatomical characteristics are poor indicators of photosynthetic pathway. Fortunately, the two pathways leave very different carbon isotope signals in fossil soils; C 3 photosynthesis strongly favors the light isotope carbon-12, while C 4 does not have as strong a preference. The δ 13 C of C 3 -dominated environments is therefore far more negative (-27 ) than that of C 4 -dominated environments (- 13 ). Because animals re-precipitate the carbon they ingest when they form tooth enamel and bone, the isotopic signatures of the remains of herbivores can tell researchers what kinds of plants they ate and therefore what plants were common in their habitat, which in turn indicates their contemporary environmental conditions (Bender, 2013). If scientists detect isotopic shifts in fossil soils and mammal fossils in one area over time, it is thus good evidence of a pronounced shift in vegetation type and therefore in local environmental conditions. Isotopic analyses of fossil soils and mammal remains have shown that a major shift in photosynthetic pathway and vegetation type occurred with the pronounced cooling in the Late Miocene. This pattern is evident in Late Miocene rocks from all over the world. In the Siwalik Group in Northeast Pakistan, for instance, isotope ratios in ancient soil carbonates and mammal teeth show a pronounced positive shift from 8 to 5.5 million years ago; this strongly indicates that the region experienced a floral turnover, during which a C 3 -dominated ecosystem gave way to a C 4 -dominated one. Since most C 4 plants are grasses, researchers interpret this isotopic shift as the development of a C 4 savannah at the expense of C 3 forest in Northeast Pakistan. Additional support for this interpretation comes from the changing morphology of mammal teeth. Brachydont browsers and fruit-eaters were the major herbivores in the Siwalik fauna prior to 8 million years ago; by 5.5 million years ago, hypsodont grazers and mixed-feeders had almost completely replaced them. The proliferation of C 4 grasses at the expense of C 3 plants would have rendered the environment unable to support animals dependent on leaves or fruit; the unlucky herbivores would have had to emigrate from the area or face starvation (Badgley et al 2008). In the previously-discussed Great Plains region, a similar pattern is evident. Isotopic measurements reveal a major positive shift in the δ 13 C of ancient soil carbonates and mammal tooth enamel from 7 to 5.5 million years ago, reflecting the expansion of C 4 grasses in the ecosystem (Strömberg, 2011). The North American herbivorous fauna responded to the rise of C 4 grassland in a manner reminiscent of the Siwalik fauna. Hypsodonty and tooth abrasion increased markedly after 12 million years ago among the various horse species that lived at the time; this is likely a response to a more open and possibly more grass-rich habitat, which would have increased the abrasion they experienced in their diets (Mihlbachler et al., 2011). The abnormally high ungulate richness known from the Mid-Miocene did not persist. After the Mid-

8 8 Miocene Climatic Optimum ended 14 million years ago, browser diversity plummeted as grazer diversity moderately increased, indicating declining productivity and confirming the rise of pure grasslands (Janis et al., 2004). Given isotopic ratios, the grasses at this time were predominantly C 3, with some advanced C 4 forms also present; like in the Siwalik Group, C 4 grasses only took over 8 million years ago, which is presumably when CO 2 declined to a level unsuitable for C 3 plants to thrive (Edwards et al., 2010). The rise of C 4 grasses also occurred concurrently in South America, Africa, and East Asia. The proliferation of C 4 grasses is observed all around the world after 10 million years ago, at which point C 3 wooded grasslands and forests disappeared over much of their former range (Strömberg, 2011). The roughly simultaneous expansion of C 4 grasslands indicates that its cause was global in nature. The C 3 -C 4 transition in the Siwalik Group co-occurs with a positive excursion in the δ 18 O of ancient soil carbonates and mammal teeth, which signifies either increased temperature, decreased Fig. 2. The dominance of C 3 and C 4 grasses in different environmental conditions. Note that C 4 photosynthesis is favored when CO 2 is low. From Edwards et al. (2010). precipitation, or a change in the source of precipitation; this has commonly been taken as evidence that the transition was related to the origin of the Indian monsoon system (Quade and Cerling, 1993; Badgley et al., 2008; Barry et al., 2002). The increased seasonality of the region s precipitation would have made water scarce for a significant portion of the year; since C 4 plants use water more efficiently, they would have outcompeted C 3 plants. While the monsoon system likely did contribute to the floral turnover in South Asia, it cannot explain why the same transition occurred at the same time all over the world. A drop in atmospheric CO 2, however, could account for such an event. Since C 4 outperforms C 3 in conditions of lower CO 2 (as shown in Figure 2), a long-term decrease in atmospheric CO 2 would be expected to cause the former to take over from the latter. In areas that were already grass-rich or dominated (like the Great Plains region), primitive C 3 grasses would have yielded to advanced C 4 grasses; in woodlands, C 4 grasses would have taken over as C 3 trees and shrubs struggled to survive (Badgley et al., 2008; Edwards et al., 2010; Bender, 2013). While temperature also decreased during this time (which would normally be expected to favor C 3 ) due to the drop in atmospheric CO 2, grasslands only persisted in areas of relatively high temperatures; like today, they did not exist at high latitudes. The tectonically-driven drop in CO 2 led to a period of pronounced cooling that has persisted to the present day and resulted in the evolution of modern grassland ecosystems. The Miocene Epoch is an excellent period for the study of how climate change affects terrestrial ecosystems. It preserves the record of a pronounced rise and subsequent fall in atmospheric CO 2 levels within a short period of time; the plentiful fossils from the Mid- to Late

9 Miocene allow researchers to study the floral and faunal responses to intervals of climate change. The brief CO 2 peak that caused the Mid-Miocene Climatic Optimum was generated by extensive volcanic activity; the high CO 2 increased the primary productivity of terrestrial plants, which were then able to sustain an astoundingly diverse assemblage of large ungulate herbivores. As tectonic uplift in the Himalayan region enhanced chemical weathering and carbon burial, atmospheric CO 2 dropped, causing C 4 grasses, which had hitherto been minor components of the flora, to rise to dominance. Grassland ecosystems, which had previously existed in a more primitive state, approached a modern composition, while large swaths of C 3 forest gave way to grassland. The result was a widespread drop in the diversity of browsing ungulates as grazers became dominant. The Miocene CO 2 fluctuations are an important source of information for people attempting to predict the future consequences of anthropogenic CO 2 release and its associated warming and preemptively strike against its effects. 9

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