Perspective Past natural history and ecological biodiversity modelling

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1 Systematics and Biodiversity (2012), 10(3): Perspective Past natural history and ecological biodiversity modelling VALENTÍ RULL Botanic Institute of Barcelona (IBB-CSIC-ICUB), Pg. del Migdia s/n, Barcelona, Spain (Received 20 May 2011; revised 7 August 2012; accepted 7 August 2012) In a recent paper, Ricklefs (2012) argued that the current emphasis on theoretical models undermines the relevance of natural history in ecology and advocated a return to observation of the natural world. This comment notes that part of the natural history observations needed to address keystone ecological patterns and processes are in often ignored past records. As demonstrated by Ricklefs, the origin and maintenance of extant biodiversity are used to illustrate the potential usefulness of past natural history in theoretical ecology and modelling. It is concluded that rather than testing current theories, past natural history calls for their reformulation. Key words: biological diversity, ecological theory, modelling, natural history, palaeoecology Introduction Naturalists should celebrate the latest paper by Robert E. Ricklefs (2012), whose central point is the defence of natural history the observation of the natural world to decipher its patterns as the basis for ecological study. The core tenet of Ricklefs essay can be condensed in the following paragraphs: Whereas the origins of ecology were firmly grounded in direct observation of nature, the emergence of strong theory in ecology appears to have changed our perspective on natural history, to the point that observation is often used to serve theory rather than test predictions and find inspiration for new ideas (p. 432) and I argue that natural history observation and thinking are essential to understanding the origin, maintenance, and significance of biodiversity (p. 423). Ricklefs (2012) develops these ideas using the example of extant biodiversity patterns in the debate between two competing views the neutral theory and the niche theory and concludes that neither can provide satisfactory answers to the diversity problem unless they start to observe the natural world to guide their reasoning. Many ecologists agree or think in a similar way but, sometimes, the pronouncement of a recognized authority is necessary to make a strong point from something that would seem trivial or that is currently taken for granted and rarely explicitly addressed. In this sense, the Ricklefs (2012) paper is very welcome, especially coming from a leading ecologist with a significant theoretical background. Correspondence to: Valentí Rull. vrull@ibb.csic.es This comment aims to emphasize the need to consider an aspect of natural history that is usually underrated, even ignored, in theoretical ecology and modelling: the past (see Colles et al., 2009 and Rull, 2012a for an extended discussion and literature on the subject). Past natural history is considered in this comment as the body of empirical observations and reasoning from past ecosystems (or from the past of extant ecosystems) obtained by palaeoecological tools, with the contribution of palaeogenetics and molecular phylogenetics. Such observations are needed to unravel a number of keystone ecological patterns and processes, including diversity, succession, equilibrium with the environment, stability, resilience, range shifts, niche conservatism, and responses to environmental shifts that cannot be properly understood through short-term studies only (Rull, 2012a). As a number of palaeoecologists the so-called ecological palaeoecologists whose aim is genuinely ecological rather than merely palaeoenvironmental reconstruction (Rull, 2010) and scholars from other disciplines (evolutionary biology, biogeography and molecular phylogeny) are already aware of these points, this comment is primarily intended for ecologists working on present-day ecosystems (neoecologists), theorists and modellers, who consider past evidence as a matter of history without relevance for the understanding of present-day ecological patterns and processes. This is not a review of the potential contributions of palaeoecology to ecology and ecological theory but a call to rescue this often forgotten part of natural history to test ecological hypotheses involving time-dependent ISSN print / online C 2012 The Natural History Museum

2 262 V. Rull processes, to calibrate and validate theoretical models, to check the validity of their assumptions, and to obtain inspiration for further developments in both, as Ricklefs (2012) recommends. In this commentary, Ricklef s arguments are supported and complemented by showing the value of past natural history, a topic not explicitly addressed in his essay, using empirical evidence. Ecological palaeoecology and related disciplines Palaeoecology is not merely palaeoenvironmental or palaeoclimatic reconstruction. Ecological palaeoecologists define palaeoecology as the ecology of the past (Birks & Birks, 1980, p. 1) or the branch of ecology that studies (the) past (of) ecological systems and their trends in time using fossils and other proxies (Rull, 2010, p. 4). Under this framework, ecology is viewed as a broad discipline embracing palaeoecology (the past), neoecology (the present) and predictive ecology (the future). A fundamental principle of ecological palaeoecology is that ecological time is a continuum, and the subdivision into past, present and future is a human construction (Rull, 2012a). Therefore, ecological palaeoecologists are not palaeoscientists whose data may be of interest for ecology but ecologists working on other time scales with different methods. Neoecology and palaeoecology have the same objective, which is the understanding of the ecological functioning of the biosphere (Rull, 2010). To properly understand extant communities, their origin, assembly, composition, biodiversity and functioning processes occurring at centennial to millennial time scales, when extant species and their communities were already in play, are especially relevant (Jackson, 2001). The already well-consolidated field of DNA analysis of extant species and their corresponding phylogenetic and phylogeographic applications and the emerging and promising field of palaeogenetics, which addresses ancient DNA (both a part of natural history), complement palaeoecological observations to provide more robust interpretations of past ecosystems and their temporal trends (Cavender-Bares et al., 2009; Hofreiter et al., 2012). One of the best examples of this synergy is the study of diversity patterns and their origin and maintenance, the main topic discussed by Ricklefs (2012) in the paper commented on here. In a similar analysis, Mittelbach et al. (2007) gathered palaeontological and phylogenetic data to test the time-area and diversification hypotheses about the latitudinal diversity gradient and concluded that diversity is positively correlated with the age and area of the considered regions and that diversification rates seem to have been higher in the tropics than in extra-tropical areas. Ricklefs (2012) addresses the subject from a more general perspective under the debate of neutral vs. niche hypotheses, and he pleads for data from natural history for proper testing. These data already exist, at least in part, and come from a synergy among palaeoecology, phylogeography and palaeogenetics, as discussed below. Past natural history and current diversity Diversity is a balance between speciation and extinction through time, and any hypothesis trying to explain its patterns should account for the available empirical data on both processes and their external and internal community drivers (Ricklefs, 2007; MacColl, 2011). One of the key elements usually ignored by theorists and modellers is the age of origin of species, which is not the same as many models implicitly assume, often inadvertently. This implies that available species pools for community assembly have not been constant through time and, therefore, communities have changed their composition and successional trends accordingly. Extinction and range shifts have also been factors of community change. Most of these community shifts have been the result of environmental changes during all time scales, including predictable changes linked to astronomic drivers and unpredictable contingency arising from abrupt events or surprises unexpected non-linear responses linked to abrupt threshold-crossing changes manifested as jumps in the palaeoecological records (Overpeck, 1996; Bennett, 1997; Vegas-Vilarrúbia et al., 2011). A complicating element is the fact that species respond in an individualistic fashion to environmental shifts, as demonstrated some decades ago by palaeoecology (West, 1964; Coope, 1979; Davis, 1981; Huntley & Birks, 1983; Elias, 1994) and confirmed by further studies (review in Rull, 2012a). A corollary is that diversity has been changing (and will continue to change) over time at both community and planetary levels, and the present patterns are merely a snapshot of this trend. Speciation timing and drivers An example of the process of species emergence with time is available from the Neotropics, where a meta-analysis of the available data showed that extant species have been originated in a more or less continual fashion, with no significant bursts from the Oligocene ( 25 million years ago) to the Late Pleistocene (<1 million years ago). Therefore, the origin of extant species is not synchronic but diachronic. The groups with more ancient species are amphibians and fishes, whereas those with a higher percentage of young species are insects, vascular plants and birds. Other groups, such as reptiles, molluscs and mammals, are intermediate (Rull, 2008). Based on these and other similar data (e.g. Hoorn et al., 2010), it has been disputed whether neotropical diversification has been linked to external drivers, such as, for example, palaeogeographic and palaeotopographic changes driven by plate tectonics or Quaternary global and

3 Ecological biodiversity modelling 263 recurrent climatic changes (glaciations). A thorough evaluation suggests that the high extant neotropical diversity cannot be attributed to the action of one or a few events during specific time intervals; rather, it is the result of complex ecological and evolutionary trends initiated by tectonic events and maintained by the action of climatic changes as well as synergy between them at all time scales (Rull, 2011). Extinction Extinction is difficult to address, as the only conclusive empirical evidence available is the fossil record, which is too fragmentary for a conclusive assessment (Quental & Marshall, 2010). A more recent extinction event that could have affected extant biodiversity patterns was the global megafaunal extinction, which occurred between and years ago, when approximately 90 largebodied (>40 kg) mammalian genera vanished, likely due to human pressure and favoured by climate changes (Koch & Barnosky, 2006). It is reasonable to assume that the involved extant communities would be very different in both diversity and composition if these animals were still alive. Concerning the latitudinal diversity gradients, it has also been proposed that extinction linked to Pleistocene glacial interglacial cycles could have caused the impoverishment of extratropical areas, thus enhancing the diversity in contrast with the tropics (McGlone, 1996). So far, such a hypothesis is unsupported by palaeoecological data, which show that acclimation, adaptation and range shifts rather than extinction have been the usual biotic responses to environmental shifts (Huntley, 2007; Willis et al., 2010). Such a conclusion, however, may be compromised by the lack of sufficient taxonomic resolution of the fossils involved, a handicap that could be overcome using palaeogenetics to identify them at the species level whenever possible (Hofreiter et al., 2012). Regardless, extinction is a highly contingent phenomenon that is difficult to model under either deterministic or stochastic theoretical designs, even using palaeontological and molecular phylogenetic empirical data (Mittelbach et al., 2007; Ricklefs, 2007). Individualistic behaviour and equilibrium with the environment The influence of individualistic responses at the species level to environmental shifts on community composition and diversity was demonstrated by earlier ecological palaeoecologists, such as Richard G. West (1964) and Margaret B. Davis (1981). The classical reconstruction by Davis (1981) showed that trees from temperate North American forests survived in refuge areas during the maximum ice expansion corresponding to the Last Glacial Maximum, which occurred approximately years ago. During the subsequent deglaciation, these trees recolonized the continent by northern expansion, showing conspicuous differences in source area, response lags, migration routes and speed. As a consequence, the composition and diversity of temperate forests that led to their present-day features were not constant over time but depended on the particular species combination present in a given area for each time interval. The same trends have been confirmed for many animal and plant species in both North America and Europe (Huntley & Birks, 1983; Hewitt, 1999). Davis (1983, 1984) concluded that the postglacial spread of the involved forests was not always in equilibrium with climate, and given the instability of climate at all time scales, communities have been in disequilibrium, constantly adjusting to the environment and continually lagging and failing to achieve equilibrium before the onset of a new change. Neutral vs. niche theories in the light of past natural history Past natural history provides significant insights into not only the origin and maintenance of extant biodiversity patterns but also the potential environmental drivers involved, which should be considered to formulate explanatory and predictive hypotheses and to reconsider the foundations and assumptions of top-down theoretical models. In the context presented by Ricklefs (2012), the palaeoecological and molecular phylogenetic findings quoted above seriously challenge the neutral theory for two main reasons. First, this theoretical proposal does not consider asynchrony in speciation and the action of changing external (environmental) agents of diversification, two paramount elements in the origin of extant diversity patterns. Second, the realization that community composition and diversity changes depend on individualistic niche features of the component species (response lags, migration rates, etc.) contradicts one of the central tenets of the neutral theory, as does the assumption that niche differences are not relevant for community assembly, structure and dynamics (Hubbell, 2005). Clark & McLachlan (2003) went further and carried out a specific test of neutral theory using palynological evidence on Holocene forest expansion trends in eastern North America. They found that contrary to the predictions of neutral theory, tree pollen abundances did not drift at random but reached relatively constant values, and variances tended to stabilize or decline. This is a very illustrative case of disagreement between the proposals of a top-down model and actual empirical observations. It is true that the neutral theory considers speciation an element of the past but only as a theoretical modelling tool, as none of the examples trying to demonstrate the validity of this hypothesis uses actual data on speciation from palaeoecology or genetic studies but only theoretical assumptions. Niche theory, although favoured by some of these past observations, still has room for improvement and change

4 264 V. Rull through past empirical evidence, mainly in aspects such as speciation diachronism and niche conservatism in time, an issue that is still debated (e.g. Hawkins et al., 2007). The extinction contingency is also a drawback for both neutral and niche approaches. Therefore, in the case of biological diversity, rather than testing current models and theories (e.g. Mittelbach et al., 2007), the role of past natural history would be to contribute to reformulate them or to build new ones with more realistic assumptions; in the words of Ricklefs (2012),...find inspiration for new ideas (p. 432). Some modelling insights Such new models and theories should be bottom-up designs based on natural history (both past and present) rather than top-down constructions based on physical reductionist proposals, which are inconsistent with most biological phenomena (Mayr, 2004). Trying to force complex biological systems and their evolution to follow simple physical rules makes no sense (e.g. Rull, 2012b). Models should not be selected by their mathematical elegance or complexity (van der Koppel, 2007) but for their biological robustness and the accuracy of their predictions. Black box models also seem inadequate, as the involved biological processes are a key component of ecological functioning and cannot be ignored. A possible strategy to develop a new generation of ecological models based on natural history would be to identify a set of observations from the natural world that should not be violated by the initial model assumptions (in this case, for example, speciation diachronism, environmental instability, dynamic non-equilibrium, extinction contingency, individualistic behaviour, etc.) to select the best type of modelling techniques to be used. Natural history should be present in any stage of model development but especially in parameterizing and calibrating the tools and validating the outcomes with actual observations. In diversity, the goodness of fit with observed diversification trends with time rather than with single snapshots reflecting current patterns should be required. The models should not be static and axiomatic but constantly revised according to the progress of natural history observations. In summary, models and theories trying to explain the origin and maintenance of biodiversity should emerge from the actual reality of biological systems, and physical analogies and mathematical outfits should be at their service, not the reverse. This endeavour requires a change of mentality in theorists and modellers, even in naturalists, which would be the main handicap for its success, but it is truly necessary. Acknowledgements Funding was provided by the former Ministry of Science and Innovation (project CGL /BOS) and the BBVA Foundation (project BIOCON ). The author is grateful to the referees (B. Hawkins and R. I. Vane-Wright) for their helpful comments and suggestions that contributed to the improvement of the original manuscript. References BENNETT, K.D Evolution and Ecology, the Pace of Life. Cambridge University Press, Cambridge. BIRKS, H.J.B. & BIRKS, H.H Quaternary Palaeoecology. Edward Arnold, London. CAVENDER-BARES, J.,KOZAK, K.H., FINE, P.V.A. & KEMBEL, S.W The merging of community ecology and phylogenetic biology. Ecology Letters 12, CLARK, J.S.& MCLACHLAN, J.S Stability of forest diversity. Nature 423, COLLES, A., LIOW, L.H.& PRINZING, A Are specialists at risk under environmental change? Neoecological, paleoecological and phylogenetic approaches. Ecology Letters 12, COOPE, G.R Late Cenozoic fossil Coleoptera: evolution, biogeography and ecology. 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