Crikey, it’s been 3 months already?! *panics* At Imperial College, new PhD students have to produce an initial plan of study within the first three months of setting off, and submit it for independent assessment. Having uploaded mine just now (not in the slightest bit late..), I figured I’d share it here! It’s a broad outline of what I’m aiming to do for the next wad of months – any comments or feedback will be massively appreciated!
Proposed title of thesis: Diversity crash at the Jurassic/Cretaceous boundary: a forgotten mass extinction?
Life on Earth is currently experiencing a biodiversity crisis (Barnosky et al., 2011). Preserving biodiversity is essential for ecosystem health, as well as for social, economic and environmental services. Our understanding of the internal dynamics of large-scale extinctions is in its infancy, particularly in terms of how particular groups of organisms respond to environmental and ecological perturbations (extrinsic factors) and how this interplays with their morphological and physiological constraints (intrinsic factors). To understand this, we must consult the fossil and geological records, which combined contain the only historical document of the fluctuating co-evolution of Earth systems and its biota.
Five mass extinctions are already well-known from the Phanerozoic eon (the last 540 million years). However, the presence and magnitude of these ‘events’ along with natural fluctuations in biodiversity through time has recently been reassessed from previous interpretation and reading of the raw fossil record; that is, no longer assuming that what we find in the fossil record perfectly reflects biodiversity at the time. There are numerous anthropogenic and geological megabiases (e.g., the area of rock preserved, the relationship between exposure, rock volume, and outcrop, preservation potential of different organisms, heterogeneous collection histories from around the globe; Smith et al., 2001; Smith and McGowan, 2007; Kalmar and Currie, 2010; Lloyd et al., 2011) that affect our observations and interpretation of the fossil record and historical diversity that must be accounted for before we can hope to reveal a clear signal of biological patterns.
The Jurassic/Cretaceous (J/K) boundary was originally considered to be a mass extinction event, but subsequently downgraded following reassessment. Recent research has hinted that there may be a biodiversity decline around this time, when the above mentioned biases are compensated for, in specific groups (e.g., sauropod dinosaurs, marine tetrapods; Benson and Butler, 2011; Mannion et al., 2011), as well as important macroevolutionary transitions throughout this period (e.g., clade replacement). Therefore, this time provides an excellent opportunity to investigate the macroevolutionary and ecological dynamics that affected tetrapod history during a significant period of their evolution.
I will augment an online data set (The Paleobiology Database [www.paleodb.org]) of all fossil occurrences (as part of a larger international research effort) that reflects what we know of the fossil record throughout this interval, focussing specifically on Late Jurassic and Early Cretaceous tetrapods. Following this, I will assemble biodiversity curves, and apply correction methods to establish and remove the sampling biases that cloud genuine patterns in biodiversity. Furthermore, I will investigate the ecological, geographical, environmental, and morphological and physiological factors, within and between different groups of organisms (e.g., squamates, crocodiles, dinosaurs) and at different hierarchical levels, to determine which of these are tied to patterns of extinction and survival. I expect to find dynamic couplings between ecologically similar or sympatric organisms, as well as a link of some sort between climate and alpha biodiversity.
This work will seek for meaningful relationships between patterns of biodiversity, functional morphology, morphological disparity (Brusatte et al., 2011), and environmental parameters in groups that either have extant relatives or functional or ecological analogues alive today. That way, we may gain insight into how these organisms will respond to current and on-going environmental threats (e.g., global climatic disruption), and be able to contribute to model-based predictions that might play a role in biodiversity conservation. Using the fossil record is the only way to understand how these patterns and processes fluctuate, and has a large role to play in how we tackle the threat of declining global biodiversity. To compensate for discrepancies in time scales between the recent, future, and Mesozoic, temporal scaling corrections may have to be applied; but even without this additional phase, the research plays an important role in guiding our understanding of the processes that have shaped the historical development of life on Earth, undoubtedly one of the greatest stories preserved within our planet.
As well as this core part of the project, I will be conducting a taxonomic and phylogenetic analysis of a group of crocodylomorphs called atoposaurids. Atoposaurids spanned the J/K boundary, and are unique among crocodiles with their distinct ‘dwarfism’. They are currently relatively poorly understood among other crocodile groups and in need of a taxonomic overhaul. Through a thorough systematic revision it is expected that they will form a good group for a small case study investigating intra-group patterns, processes and responses to environmental and ecological perturbations over the J/K boundary and beyond. Furthermore, they play an important role in our understanding of crocodylomorph diversity patterns and evolutionary history.
This project aims to compliment and build upon a vast series of on-going research into investigating the patterns and processes that have impacted upon tetrapod evolution throughout the Mesozoic era (e.g., Benson et al., 2010; Butler et al., 2010). Recent research has focussed on aspects such as evolution of maximum body size through time in a phylogenetic context, faunal and ecological turnovers, and the interaction of large clades and biodiversity patterns (i.e., origination, extinction, and standing diversity trends through time; see also Ezard et al., 2011). These represent a large leap forward from earlier studies of taxonomic diversity during the 1960s to 1980s, primarily involving marine invertebrates, largely through the development of advanced quantitative techniques and the development of large taxonomic databases.
The fossil record provides the only direct documentation for how biodiversity has evolved throughout geological history. Reconstructed biodiversity curves representing the trajectories of life through time have typically relied on raw taxonomic counts of described taxa from specific time intervals. Typically, these counts are conducted at higher taxonomic levels than the species, although the validity of constructing curves in such a way has been strongly questioned by their statistical association with sampling biases (e.g. Lloyd et al., 2011). These biases act to confound our raw reading and interpretation of the fossil record, but new standardisation techniques are going some way towards ameliorating them and providing a clearer visualisation of biodiversity through time.
There have been many recent studies considering the interaction of geological biases and the diversity of Mesozoic terrestrial and marine tetrapods (e.g., with pterosaurs, dinosaurs, and anomodont synapsids), which have largely found palaeobiodiversity within these clades to correspond to geological sampling and human sampling intensity (e.g., the Lagerstatten effect). Although correlation does not imply causation, a common cause relationship between both apparent geological biases and observed diversity curves is not supported (Butler et al., 2011), implying that sampling biases are, at least in the case of Mesozoic dinosaurs, imposing a first-order control on observed biodiversity patterns.
Mass extinctions have been extensively studied in the past, in terms of their causes, duration, recovery time, and biotic impact (for a varied selection, see Wignall, 2001; Tarailo and Fastovsky, 2012; and Wang et al., 2012). Conversely, relatively little has been uncovered about more detailed selectivity patterns throughout these periods of biological stress. The reasons for this apparent attraction are in part due to their scientific interest, as mass extinctions represent periods of extreme biotic and/or environmental upheaval. As well as this, public intrigue is also captured (none more so than the end-Cretaceous mass extinction and the loss of the non-avian dinosaurs), making them useful for social engagement with current palaeontology and geoscience issues. As the Earth is currently entering a biodiversity crisis, often being hailed as the sixth mass extinction, it has never been more critical that a historical view of extinction patterns and processes be understood in depth, in that we might learn about their dynamics and use this to prevent negative impacts on biodiversity in the future.
3. Aims and objectives
The specific goal of this project is to observe the internal diversity dynamics among clades of taxonomically, ecologically, and morphologically diverse groups of terrestrial tetrapods to assess what happened over the course of the J/K interval. Dissection of patterns will be between environmental and ecological, and morphological and physiological parameters to decouple diversity trends from potential causative correlates (i.e., ecomorphological selectivity, while accounting for phylogenetic non-independence; see Friedman, 2009) and determine how the contemporary biota and Earth system processes co-evolved. This project will also be a useful standing point to compare and evaluate the relative performances of sampling standardisation techniques, based on the taxonomic and temporal focus.
With respect to the atoposaurids, the objective is to produce a statistically rigorous assessment of their intra-clade phylogenetic relationships. Further deduction is required of their position among the larger crocodylomorph lineage, as they are often but inconsistently recovered at the base of Neosuchia, the lineage that led to the ascent of modern crocodilians. Further to this, a more detailed look into the ecological and morphological factors that contributed to their extensive temporal span and niche occupation will be a target.
The core data set for this project is the Palaeontology Database, a digital and dynamic catalogue of global taxonomic occurrences that is currently variably complete for different groups and periods (Alroy, 2003). Once the data collection for the desired period and taxonomic groups is complete, this will form the basis for generation of biodiversity curves, which in turn will be the foundation for all subsequent analyses.
With respect to the atoposaurid-based portion of this project, I am in the process of creating a database of all atoposaurid museum collections, as well as creating the basis for a number of papers revising the clade. Planned visits for early 2013 include Dorset, Cambridge, and Oxford museums, and further visits to the Natural History Museum in London, where I have focussed my initial studies of the group during this first three months., Later on this year and in 2014, I will visit collections in Europe (primarily in France and Germany) and also Russia, as well as further afield if deemed appropriate. The purpose of these visits will be to redescribe their anatomy, provide anatomical diagrams, and construct a character matrix for all atoposaurids (and several of their close relatives) to account for new material and first-hand revisions. This will form the basis for a phylogenetic analysis, taxonomic revision, and subsequent systematic macroevolutionary analyses.
Raw taxonomic biodiversity curves can be created using software inbuilt into the Palaeobiology Database. However, as mentioned, apparent biodiversity can be strongly influenced or distorted by phylogenetic and sampling biases. For the former part of this, I will use phylogenetic trees to reconstruct ghost lineages within clades to correct for stratigraphic absence of species (a ghost lineage pulls the temporal range of a species back to the origin of the split between itself and that of its closest sister taxon). This allows us to infer diversity in the fossil record during time intervals of poor preservation, as well as compensating for known taxonomic occurrences that are not preserved within the fossil record.
Many metrics currently exist for countering the effects of geological sampling, including counts of fossil-bearing units (i.e., geological formations), map or outcrop area, rock volume estimates, as well as counts of fossil collections to account for ‘worker effort’ by palaeontologists (e.g., Smith 2001; Bush et al., 2004; Upchurch et al., 2011; but see Dunhill 2012 and Benton et al., 2012). Much of the information required for this is available through the Palaeobiology Database or in published data series. Such metrics will be used to correct the raw taxonomic data, which itself will be sub-divided into higher-level taxonomic units to facilitate the analysis of intra- and inter-clade variation. Benson and Mannion (2012) demonstrated the applicability of multi-variate regression modelling, combined with correction through sampling proxies, to unravel the dynamics of vertebrate diversification (using sauropodomorph dinosaurs as a case study), in a methodology that will be replicated in this study once data collection is completed. Other methods to employ include rarefaction, randomised subsampling techniques (e.g., Lloyd 2012), as well as possibly extrapolation indices based on ecological theory and modified survivorship analysis (see Alroy, 2003 for examples).
These data will be divided into geographical units (e.g., continent-level) to observe geographic occurrences and potential sympatric series (see, for example, how using regional datasets can be used to reassess extinction events, in Longrich et al., 2012). The Palaeobiology Database is fully compatible with this, with taxonomic occurrences being constrained to geographically-defined collections; it is fully recognised that global sampling intensity of the fossil record is not homogeneous (Benson et al., 2013). These taxonomic data will also be sub-divided into time bins, representing either 1 million year time-slices or by geological Stage. Careful filtering will be applied here to account for pervasive stratigraphic uncertainty in some taxa. Continent-level pairwise comparisons between groups will be conducted to see if diversity patterns correspond on this scale and whether they differ between geographical locations within groups. This will most likely require that I learn how to implement specific software packages using the programming language R during the research.
With a global dataset, it will also be possible to delineate potential signals for patterns such as latitudinal biodiversity gradients (e.g., Willig et al., 2003; Valentine et al., 2008), a current area of research interest for some (including my primary supervisor), with direct applications to understanding how the origin of these patterns arose in modern biota. The determination of the interaction of large-scale biodistributional patterns such as this in the fossil record, and the manner in which they have evolved through time, is only possible through the compilation of large occurrence datasets, as facilitated by the Palaeobiology database, and forms one of the cornerstones of current palaeontological research (see Mannion et al., 2012). Biodiversity curves will also be compared to environmental parameters, such as palaeoceanographic variations across the J/K boundary (Tremolda et al., 2006).
Alroy, J. (2003) Global databases will yield reliable measures of global biodiversity, Paleobiology, 29(1), 26-29
Barnosky, A.D., Matzke, N., Tomiya, S., Wogan, G. O. U., Swartz, B., Quental, T. B., Marshall, C., McGuire, J. L., Lindsey, E. L., Maguire, K. C., Mersey, B. and Ferrer, E. A. (2011) Has the Earth’s sixth mass extinction already arrived?, Nature Reviews, 471, 51-57
Benson, R. B. J., Mesozoic marine tetrapod diversity: mass extinctions and temporal heterogeneity in geological megabiases affecting vertebrates, Proceedings of the Royal Society B, 277, 829-834
Benson, R. B. J. and Butler, R. J. (2011) Uncovering the diversification history of marine tetrapods: ecology influences the effect of geological sampling biases, In: Comparing the Geological and Fossil Records: Implications for Biodiversity Studies, eds. McGowan, A. J. and Smith, A. B., Geological Society of London, Special Publications, 358, 191-208
Benson, R. B. J. and Mannion P. D. (2012) Multi-variate models are essential for understanding vertebrate diversification in deep time, Biology Letters, 8, 127-130
Benton, M. J., Dunhill, A. M., Lloyd, G. T. and Marx, F. G. (2012) Assessing the quality of the fossil record: insights from vertebrates, In: Comparing the Geological and Fossil Records: Implications for Biodiversity Studies, eds. McGowan, A. J. and Smith, A. B., Geological Society of London, Special Publications, 358, 63-94
Brusatte, S. L., Montanari, S., Yi, H.Y. and Norell, M. A. (2011) Phylogenetic corrections for morphological disparity analysis: new methodology and case studies, Paleobiology, 37(1), 1-22
Bush, A. M., Markey, M. J. and Marshall, C. R. (2004) Removing bias from diversity curves: the effects of spatially organised biodiversity on sampling-standardisation, Paleobiology, 30(4), 666-686
Butler, R. J., Benson, R. B. J., Carrano, M. T., Mannion, P. D. and Upchurch, P. (2010) Sea level, dinosaur diversity and sampling biases: investigating the ‘common cause’ hypothesis in the terrestrial realm, Proceedings of the Royal Society B, doi: 10.1098/rspb.2010.1754
Dunhill, A. M. (2012) Problems with using rock outcrop area as a paleontological sampling proxy: rock outcrop and exposure area compared with coastal proximity, topography, land use, and lithology, Paleobiology, 38(1), 126-143
Ezard, T. H. G., Aze, T., Pearson, P. N. and Purvis, A. (2011) Interplay between changing climate and species’ ecology drives macroevolutionary dynamics, Science, 332, 349-351
Friedman, M. (2009) Ecomorphological selectivity among marine teleost fishes during the end-Cretaceous extinction, Proceedings of the National Academy of Sciences, doi: 10.1073/pnas.0808468106
Kalmar, A. and Currie, D. J. (2010) The completeness of the continental fossil record and its impact on patterns of diversification, Paleobiology, 36(1), 51-60
Lloyd. G. T. (2012) A refined modelling approach to assess the influence of sampling on palaeodiversity curves: new support for declining Cretaceous dinosaur richness, Biology Letters, doi: 10.1098/rsbl.2011.0210
Lloyd, G. T., Young, J. R. and Smith, A. B. (2011) Taxonomic structure of the fossil record is shaped by sampling bias, Systematic Biology, doi: 10.1093/sysbio/syr076
Longrich, N. R., Bhullar, B.-A. S. and Gauthier, J. A. (2012) Mass extinction of lizards and snakes at the Cretaceous-Palaeogene boundary, Proceedings of the National Academy of Sciences, doi: 10.1073/pnas.1211526110
Mannion, P. D., Upchurch, P., Carrano, M. T. and Barrett, P. M. (2011) Testing the effect of the rock record on diversity: a multidisciplinary approach to elucidating the generic richness of sauropodomorph dinosaurs through time, Biological Reviews, 86, 157-181
Mannion, P. D., Benson, R. B. J., Upchurch, P., Butler, R. B. J., Carrano, M. T. and Barrett, P. M. (2012) A temperate palaeodiversity peak in Mesozoic dinosaurs and evidence for Late Cretaceous geographical partitioning, Global Ecology and Biogeography, doi: 10.1111/j.1466-8238.2011.00735.x
Smith, A. B. (2001) Large-scale heterogeneity of the fossil record: implications for Phanerozoic biodiversity studies, Philosophical Transactions of the Royal Society of London B, 356, 351-367
Smith, A. B., Gale, A. S. and Monks, N. E. A. (2001) Sea-level change and rock-record bias in the Cretaceous: a problem for extinction and biodiversity studies, Paleobiology, 27(2), 241-253
Smith, A. B. and McGowan, A. J. (2007) The shape of the marine Phanerozoic palaeodiversity curve: how much can be predicted from the sedimentary rock record of Western Europe?, Palaeontology, 50(4), 765-774
Tarailo, D. A. and Fastovsky, D. E. (2012) Post-Permo-Triassic terrestrial vertebrate recovery: southwestern United States, Paleobiology, 38(4), 644-663
Tremolda, F., Bornemann, A., Bralower, T. J., Koeberl, C. and van de Schootbrugge, B. (2006) Paleoceanographic changes across the Jurassic/Cretaceous boundary: the calcareous phytoplankton response, Earth and Planetary Science Letters, 241, 361-371
Upchurch, P., Mannion, P. D., Benson, R. B. J., Butler, R. J. and Carrano, M. T. (2011) Geological and anthropogenic controls on the sampling of the terrestrial fossil record: a case study from the Dinosauria, In: Comparing the Geological and Fossil Records: Implications for Biodiversity Studies, eds. McGowan, A. J. and Smith, A. B., Geological Society of London, Special Publications, 358, 209-240
Valentine, J. W., Jablonski, D., Krug, A. Z. and Roy, K. (2008) Incumbency, diversity and latitudinal gradients, Paleobiology, 34(2), 169-178
Wang, S. C., Zimmerman, A. E., McVeigh, B. S., Everson, P. J. and Wong, H. (2012) Confidence intervals for the duration of a mass extinction, Paleobiology, 38(2), 265-277
Wignall, P. B. (2001) Large igneous provinces and mass extinctions, Earth Science Reviews, 53, 1-33
Willig, M. R., Kaufman, D. M. and Stevens, R. D. (2003) Latitudinal gradients of biodiversity: pattern, process, scale, and synthesis, Annual Reviews of Ecology, Evolution and Systematics, 34, 273-309
As part of my personal development as a research scientist, I also write for the European Geosciences Union about my PhD and the broader field of Palaeontology as a form of science communication, produce a palaeontology-themed podcast series called Palaeocast, will begin writing for Nature Education shortly around the topic of geoscience education, and have an active role in science policy matters as part of Imperial College’s Science Communication Forum. These are all extraneous activities that, although not strictly part of the formal PhD process, are part of my early development as a professional researcher and science writer and communicator, which are ultimately the targets of any scientist (following, of course, the production of a thesis).