I have a chapter just out in a new book by Island Press, “Saving a Million Species“, exploring extinction risk from climate change. In it I address the evidence that past climates can explain past extinctions in the fossil record. I wrote this chapter a couple of years ago and this is a fast moving field so I would now have a lot to add to this, including some significant new general messages, but for what it’s worth, here’s the chapter.

Extinctions in deep time

Peter J. Mayhew

1. Introduction

Deep time is geologic time, extending to the origin of the planet.  For biologists in search of an understanding of extinction, the relevant portion of deep time is that in which life has existed on the planet – about the last 4 billion years (Cowen 2000).  Extinctions are first recorded when the fossil record is robust enough to offer insights into the arrival and disappearance of groups of organisms (Benton & Harper 2009). Extinctions in deep time can therefore only be identified over about the last 600 million years (Ma), an interval of time dominated by the Phanerozoic eon (540Ma to present).

This chapter will treat extinction processes over the length of the Phanerozoic, concentrating on events prior to 50Ma. The following chapter (Clyde, this volume) picks up the story from there.  This chapter deals primarily with marine extinctions, while subsequent chapters will focus on terrestrial vegetation and vertebrates, roughly following the ability to resolve these taxa in the fossil record.  The deep time record reflects multiple major extinction events.  I review the evidence of their relationship to climate and discuss possible insights they provide into extinction risk from future, human-driven climate change..


Nature of the Record

Life first flourished in the oceans, and marine fossils predate terrestrial fossils by hundreds of millions of years. Because of this, the longest datasets in the fossil record are for marine, rather than terrestrial communities. There are other reasons why studies of biodiversity through deep time tend to be marine; preservation conditions are much more favourable in marine environments, and many marine taxa have hard shelly components that fossilize well. For this reason, by far the most highly worked long term data set remains Sepkoski’s genus level synoptic compendium of marine animals and protists (Sepkoski 2002). Terrestrial fossils are available in more recent records, and are less often included in analyses of extinctions in deep time. However, the terrestrial record has not been ignored; terrestrial environments contain the majority of described species today, so potentially tell us more about the totality of extinction effects, and the majority of conservation work today is on terrestrial species, hence this is where a lot of interest lies. In addition, terrestrial taxa may have undergone diversification and extinction processes that are very different from those in the marine environment (Benton 1997, Kalmar & Currie 2010). Benton’s (1993) family level dataset is the most explored global compendium that includes terrestrial taxa.

Because only a small proportion of species have left fossilizable remains and only a small fraction of those have been discovered, the record is, obviously, more complete for higher taxonomic groups than for the individual species comprising those groups. Often it is also difficult to resolve fossil specimens to the species level, so extinctions are generally tracked at the genus or family level instead. However, this has not prevented scientists from drawing important conclusions about extinction, since genera and families go extinct as well, and it is certain that when a genus or family disappears, all species within it have become extinct.

There are other sources of bias in the record, and correcting for these may be important in interpreting the record of deep time extinctions. Possibly the most significant problem is the enormous variation across geological stages in the quantity of suitable rock records in which fossil remains can be discovered (Peters 2005). For studies spanning hundreds of millions of years this may pose difficulties, because samples will be unstandardized, with some stages being more intensively sampled than others. Whether an observed change in taxonomic richness reflects underlying biological processes, or whether it simply reflects underlying bias in preservation or discovery rate is therefore an ever-present question. Techniques and resources to overcome these biases in large scale studies are the subject of active research, and motivated the construction of the Paleobiology Database (PBDB) (Alroy et al. 2008). PBDB contains information on the occurrence, and sometimes abundance, of taxa in individual fossil beds, which allows researchers to implement standardized sub-sampling techniques to quantify richness, something that is not possible in the Sepkoski (2002) and Benton (1993) compendia which document first and last occurrences. Whilst PBDB is not taxonomically restricted in its scope, its utility is greatest for marine animals, where sample sizes are greatest. Whilst standardized samples are in general some improvement over unstandardized samples, the samples still contain only a small fraction of the true taxonomic richness.

Numerous extrinsic variables, including climate change, may explain variation in extinction rates, and it is helpful if variation in these variables over time can be estimated. For climate change, relevant variables include temperature, precipitation and related variables, as well as atmospheric CO2 levels, which exert important direct effects on organisms in both terrestrial and marine environments.  Temperature records for deep time come from proxies, such as d18O (Veizer et al. 2000).  The uptake of 18O is affected by the temperature of seawater.  Durable remnants of marine organisms, such as coral skeletons, can be assayed for 18O.  A one part per thousand change in d18O corresponds roughly to a temperature change of 1.5-2.0 degrees C.  Based on this temperature relationship, past seawater temperature and changes in seawater temperature can be inferred (e.g. Royer et al. 2004). Records for atmospheric CO2 concentrations are also derived from isotopic proxies: the isotopic content of organic carbon is sensitive to atmospheric CO2 concentrations, whilst weathering and degassing, both components of the long term carbon cycle, are associated with extreme 87Sr/86Sr ratios (Rothman 2002). However, explicit CO2 concentrations estimates are also derived from modeling changes in the long term carbon cycle itself based on a wider variety of informative inputs (e.g. Berner & Kothavala 2001). Changes in sea level can be inferred from documenting the extent and depth of marine sediments on continents (Hallam 1984). Other potential environmental influences on biodiversity and their evidence are discussed below.


The evidence linking deep time events to climate is controversial, for a number of reasons: chronologies and mechanisms are obscured by an incomplete and biased geologic record; there are no experimental controls or alternative treatments for comparison; deciphering causation and mechanism from observed correlations is difficult; there are often many alternative candidate explanations.  The remainder of this chapter first explores the variation in taxonomic richness and extinction across geological stages, and possible causes of this variation. Finally the evidence that climate change has played a role in generating some of that variation is examined.



Variation in Extinction Rates

A literal reading of the compendia databases of fossil taxa over time suggests that there has been a substantial increase in taxonomic richness over the last 600Ma on both land and sea, in which origination rates have exceeded extinction rates (Benton 1995, 1997) (Fig. 1).

Figure 1. Time series (10Ma intervals) of a) estimated low latitude sea surface temperature from Royer et al. (2004) b) per capita extinction rates (Ma-1) c) per capita origination rates (Ma-1) and d) standing diversity of all families in Benton (1993) using the maximum dating assumption (Benton 1995). Four mass extinctions indicated in b) are the end-Ordovician (O), late-Devonian (D), end-Permian (P) and end-Cretaceous (C). Reprinted from Mayhew (2010) with kind permission from Cambridge University Press.

Attempts to control for unequal sampling have somewhat mollified the increase in the marine realm in the Cenozoic (Alroy et al. 2008), but less in terrestrial taxa (Kalmar & Currie 2010 but see Davis et al. 2010). The general trends in richness are however punctuated by drops in which extinction rates temporarily rose to exceed origination. Per geological stage, extinction rate is approximately log-normally distributed (meaning the log of extinction rate follows a normal distribution) (Alroy 2008). This means that extinction rates are characterized by a mean log value, but they are occasionally very high, and also occasionally very low (Fig. 2).

Figure 2. The approximately log-normal distribution of extinction rates in the fossil record. Data are for all families from Benton (1993) using the maximum dating assumption (Benton 1995), with extinction quantified as Foote’s (2000) per capita rate, “q”. Datapoints are geological stages. The three stages on the right hand tail correspond to three of the iconic “Big Five” mass extinctions (from right, Tatarian (end-Permian), Rhaetian (end-Triassic), and Ashgillian (end-Ordovician). Note however that there are then eight stages in the next grouping to the left.

In addition to this variation around the mean log rate, there are trends through time; extinction rates, as well as origination rates, have tended to decrease through time (Benton 1995, Alroy 2008) (Fig. 1). The term “mass extinction” has come to be used to describe those stages where extinction rates are unusually high given the rates in neighbouring stages; in Raup & Sepkoski’s (1982) original analysis, they were those outside the 95% confidence interval of the linear regression of rate through time, and hence identified the iconic “Big Five” mass extinctions in the marine realm; the end-Ordovican, late-Devonian, end-Permian, end-Triassic and end-Cretaceous. The end-Permian and end-Cretaceous extinctions resulted in losses of 81% and 53% of marine animal genera (Alroy 2008), and hence probably much larger proportions of species. Despite becoming popular wisdom, the special designation accorded to the rates in these geological stages is not very well justified statistically; they are not unexpected once the data are logged, the rates do not all remain high when accounting for standing richness as well as interval duration, and they are not all repeated in both land and sea (Benton 1995, Alroy 2008). There is no bimodal distribution of rate intensities implied by the terms “background” and “mass” extinctions which are now in widespread scientific, as well as popular, use, making it arbitrary as to whether to refer to a “Big Five” or some other number of mass extinctions. Despite this, there is evidence that the intensity of extinction may determine its selectivity (e.g. Payne & Finnegan 2007), providing some justification for retaining the terms.


Possible Causes


Variation in extinction rate may be caused by both intrinsic (e.g. biotic) and extrinsic (e.g. abiotic) factors; a distinction characterized by the “Red Queen” as opposed to the  “Court Jester” (Benton 2009) or “Ace of Spades” (Mayhew, 2010) paradigms. The Red Queen paradigm posits that extinction dreives from biotic causes, and is ever-present. The Court Jester and Ace Spades in contrast posit that extinction is largely from abiotic causes, unpredictably in the case of the Court Jester (e.g. from impacts), and predictably in the case of the Ace of Spades (e.g. from climate). The fossil record suggests that both biotic and abiotic forces have affected extinction rates in deep time. There is evidence from a number of studies for density-dependent style processes. For example, in PBDB, drops in taxonomic richness tend to lead to lower extinction rates, whilst high extinction rates tend to lead to subsequent high origination rates (Alroy 2008). Similar trends, though differing in detail, have been found in other datasets (Kirchner & Weil 2000), and suggest that richness is in part a dynamic equilibrium, although one in which the equilibrium itself evolves through time, perhaps dramatically in terrestrial environments. These relationships are strongly suggestive of a role for biotic interactions such as competition.

Of the abiotic causes, both terrestrial (emanating from the Earth) and extra-terrestrial factors have been implicated. Terrestrial causes include sea level variation, volcanism, continental drift, atmospheric composition and global temperature change. Extra terrestrial causes include bolide impacts and cosmic ray flux. These variables may of course may be dependent on each other and result in interactive effects.

The area of marine transgressions over the continents is positively correlated with marine taxonomic diversity in the Sepkoski compendium (Purdy 2008). More than one proximate mechanism may be responsible for this association; it may reflect variation in habitable areas, thereby affecting extinction and origination rates. Alternatively it may reflect changes in the quantity of sedimentary deposits available for study. Both are likely (Peters 2006, 2008). The evidence that large igneous provinces can lead to high extinction rates is now extensive, and especially comes from Permian-Triassic boundary when the Siberian Traps large igneous province is known to have been active, leading to rapid global warming through CO2 outgassing (Wignall 2001, 2005). Sedimentary evidence suggests strongly that this coincided with a marine crisis, or euxinium, in which the ocean surface became largely anoxic (Meyer & Kump 2008) (Fig. 3).

Figure 3. Scenario for the onset of the end-Permian marine crisis, based on information in Ward (2006).

A more general role for large igneous provinces, and such marine euxinia, has been suggested, but no statistical studies have been done to corroborate this (Wignall 2005, Ward 2006).

Volcanism is associated with plate tectonics, which is also the cause of continental drift. Over the last 500Ma, the continents first coalesced into the supercontinent of Pangea, and then subsequently split apart. The distribution of continents is important because most described species on Earth today live in shallow epicontinental seas or on land. Because of the well-supported ecological species-area relationships (Gaston & Blackburn 2000) as well as evidence from biogeography that vicariance is an important force in adaptive radiation (McCarthy 2009), paleobiologists have long speculated that it could be one of the regulating forces of global taxonomic richness (Valentine & Moores 1970), though its effects are difficult to quantify with certainty. Certainly continental drift has also had important indirect effects through changing sea level, changing the latitudinal distribution of continents and shallow seas, hence their local climates, and because the degree of continentality on land affects local climate.

Atmospheric composition has mainly been investigated with respect to CO2 concentrations. There is a positive association between estimated CO2 concentrations and extinction rates in the Sepkoski compendium and in the Benton compendium (Cornette et al. 2002, Mayhew et al. 2008). CO2 might exert an effect on extinction independent of other environmental variables (such as through oceanic acidification), or merely be a reflection of those other variables (such as global climate variation).

Though biologists, even paleobiologists, may in the past have treated extra-terrestrial causes of extinction with derision, this has been dramatically reversed since the discovery of worldwide iridium deposits at the Cretaceous-Tertiary boundary (Alvarez et al. 1980). It is now well established that a bolide impact at this time in Mexico is likely to have had far reaching effects on ecosystems (Schulte et al. 2010), though whether the impact was the sole cause of extinction has been debated because of the coincident Deccan Traps large igneous province (Keller 2001). More generally the evidence that impacts are responsible for high extinction is weak, but one study has suggested that they might interact with volcanism such that geological intervals with both large igneous provinces and impacts experience differentially high extinction (Arens & West 2008).

Another extra-terrestrial factor implicated in extinction is the variation in cosmic ray flux reaching Earth. Unlike bolide impacts, cosmic rays are sourced from outside the solar system, and show estimated cycles of 62 and 140Ma that correlate with fluctuations in fossil data (Rohde & Muller 2005, Medvedev & Melott 2007, Mellott 2008). Over hundreds of millions of years, the solar system has rotated around the galactic centre, in and out of the plane of the galaxy and in and out of galactic spiral arms. Changes in cosmic neighbourhood are quite capable of affecting life on a planet (Ross 2009). One possible, though controversial, mechanism through which cosmic ray flux might affect life is through global climate (Shaviv & Veizer 2003), to which we now turn.

Global climate and its effects on extinction


Over the Phanerozoic, a variety of proxies suggest that global climate has fluctuated between relatively warm, greenhouse, modes in which evidence of high latitude glaciation is absent, and relatively cool, icehouse, modes in which it was present (Frakes et al. 1992). The cycle length of greenhouse peak to greenhouse peak is approximately 140Ma. The greenhouse modes are respectively Cambrian to Late Ordovican, Early Silurian to Early Carboniferous, Late Permian to Mid-Jurassic, and Early Cretaceous to early Eocene. The icehouse phases are sandwiched in between; respectively late Ordovician to early Silurian, early Carboniferous to late Permian, late Jurassic to early Cretaceous, and early Eocene to Present (Fig. 1). It is likely that there was shorter term variation around these general trends, but these fluctuations are generally known with less confidence. For this reason, deep time studies can say much more about the effect of warm or cool temperatures on extinction than about the rate of change of climate. Recent models also suggest a general long term cooling trend around which these modes are superimposed (Royer et al. 2004). What effects, if any has this variation had on extinction rates?

Both the Sepkoksi and Benton compendia show associations, after detrending, with estimated long term sea surface temperatures, generally representing the transition from greenhouse to icehouse modes (Mayhew et al. 2008). Under greenhouse modes, or high sea surface temperatures, extinction rates are mostly higher than average; under icehouse modes they may be low or high, leading to a general positive association between temperature and extinction rate, with moderate explanatory power (Figure 4).

Figure 4. Associations between the time series in Fig.1. In each case the raw datasets have been transformed to stabilize variance, detrended, and then mean standardized for plotting on the same scales. Inserts show the correlations between the plots. Closed circles are temperature, and open circles are extinction rate (a), origination rate (b) and standing diversity of families (c). Double open circles indicate the intervals with the five largest extinction rate residuals, corresponding to well-known mass extinction events; which from left to right in the time series are: end Ordovician, Late Devonian, end Permian (twice), end-Cretaceous. Lines are fitted curves using 25 d.f. splines. Reprinted from Mayhew et al. (2008) with kind permission of the Royal Society of London and Blackwell Scientific.

Because high atmospheric CO2 concentrations are associated with high global temperature (Royer et al. 2004), this finding is consistent with associations between taxonomic richness or extinction rates and CO2 found previously (Rothman 2001, Cornette et al. 2002). The association essentially derives from a rough and weak cycle of approximately 140Ma in fossil richness and rates, matching that of temperature, and, interestingly, that cycle appears to be preserved in PBDB (Mellott 2008). Coincident with this positive association is a negative, lagged, association with richness and a positive, lagged association with origination rates, implying that extinction changes first and then taxonomic richness and origination respond later.

Extinction rates can be high with any kind of global temperature; specifically, the late-Devonian, end-Permian and end-Cretaceous extinctions occurred close to greenhouse temperature peaks whilst the end-Ordovician extinction occurred during an icehouse trough. Fine-scale analyses of events at some of these stages also imply a causal relationship with temperature. The end-Permian marine crisis is likely to have been considerably enhanced by high sea-surface temperatures at this time, increasing the frequency of anoxia at the ocean surface (Benton 2005) (Fig. 3). In contrast, in the end-Ordovican, continental landmasses crossed the pole, triggering a rapid glaciation. Extinction has been attributed to a combination of rapid climate change, fluctuations in ocean circulation, and sea level regression (Sheehan 2001).

Whilst the long term macroevolutionary patterns outlined above cannot be used to predict future short term ecological responses, conducting a thought experiment of this type can, in principle, be instructive for comparative purposes. Predictions can be generated by comparing the detrended (residual) short term deviations in temperature with those in taxonomic richness and extinction rate. The slopes of these residuals describes the rise in extinction rate or loss of taxa for a one-degree rise in temperature. I apply these slopes to the Eocene, when taxonomic richness was relatively high, and background extinction rates low, as was typical for more recent geological epochs. Using these methods, a 4oC rise in temperature translates approximately to a seven-fold increase in family-level extinction rate in the Eocene but only to a 5% reduction in families globally. For marine genera a 4oC rise in temperature translates to a three-fold increase in extinction rate and 5% loss of genera. Note that uncertainty is very large because none of the relationships is very tight, and that effects might be underestimated for many reasons (e.g. short (<10Myr) term variation is not accounted for, origination mollifies drops in richness).


Whilst global analyses tend towards the opinion that high global temperatures enhance extinction rates over long time scales, and reduce richness, individual taxonomic groups sometimes show the opposite relationship at least over shorter time scales. For example, Dasycladalean algal richness has fluctuated generally in line with global temperature change over the Phanerozoic (Aguirre & Ridding 2005), and Jaramillo et al. (2006) found a similar pattern with Tertiary neotropical plant richness. Clearly, many organisms are generally favoured by warm environments, and in the absence of high extinction are expected to prosper (see Woodward & Kelly 2008).




The precise scale of the current-future biodiversity crisis is uncertain but probably falls somewhere within the higher range of those recorded in the history of life (May et al. 1995, Leakey & Lewin 1995, Pimm et al. 1995, McKinney 1998, Myers and Knoll 2001, Woodruff 2001, Thomas et al. 2004, Pimm et al. 2006, Hoegh-Guldburg et al. 2007, Wake 2008). Extinctions of a similar intensity have mostly occurred in deep time, hence they can inform on the likely consequences of such loss. Furthermore, over deep time there has been considerable change in the environmental variables that affect the fate of species today and in the near future, hence deep time can inform us on how these are likely to affect future extinction rates. Some of these variables, such as atmospheric CO2 concentrations, are expected to change so much on a global scale that the only empirical precedents come from deep time. Deep time studies currently suggest that over the history of life, greenhouse climates are not generally favourable for the persistence of taxa, and suggest that high global temperatures can lead to ecological and geochemical processes that can cause mass extinction. Furthermore, large scale biodiversity loss is unlikely to be replenished in the lifetime of our species (Alroy 2008). These are sobering messages given the pace and direction of current environmental change. The richness of the environmental and biological data in the fossil record has only just begun to be examined, and many questions remain: To what extent are the fossil patterns biological, geological or artefactual? How are the environmental variables inter-related and what is the pattern of causation among them and the biological variables? How can we use the past to model the future? The challenge for palaeobiologists is to extract the salient messages in time to make a difference to current biodiversity.

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