Improving the relevance of paleontology to climate change policy.

Paleontology has provided invaluable basic knowledge on the history of life on Earth. The discipline can also provide substantial knowledge to societal challenges such as climate change. The long-term perspective of climate change impacts on natural systems is both a unique selling point and a major obstacle to becoming more pertinent for policy-relevant bodies like the Intergovernmental Panel on Climate Change (IPCC). Repeated experiments on the impacts of climate change without anthropogenic disturbance facilitate the extraction of climate triggers in biodiversity changes. At the same time, the long timescales over which paleontological changes are usually assessed are beyond the scope of policymakers. Based on first-hand experience with the IPCC and a quantitative analysis of its cited literature, we argue that the differences in temporal scope are less of an issue than inappropriate framing and reporting of most paleontological publications. Accepting that some obstacles will remain, paleontology can quickly improve its relevance by targeting climate change impacts more directly and focusing on effect sizes and relevance for projections, particularly on higher-end climate change scenarios.

Deep-time climate legacies affect origination rates of marine genera.

Biodiversity dynamics are shaped by a complex interplay between current conditions and historic legacy. The interaction of short- and long-term climate change may mask the true relationship of evolutionary responses to climate change if not specifically accounted for. These paleoclimate interactions have been demonstrated for extinction risk and biodiversity change, but their importance for origination dynamics remains untested. Here, we show that origination probability in marine fossil genera is strongly affected by paleoclimate interactions. Overall, origination probability increases by 27.8% [95% CI (27.4%, 28.3%)] when a short-term cooling adds to a long-term cooling trend. This large effect is consistent through time and all studied groups. The mechanisms of the detected effect might be manifold but are likely connected to increased allopatric speciation with eustatic sea level drop caused by sustained global cooling. We tested this potential mechanism through which paleoclimate interactions can act on origination rates by additionally examining a proxy for habitat fragmentation. This proxy, continental fragmentation, has a similar effect on origination rates as paleoclimate interactions, supporting the importance of allopatric speciation through habitat fragmentation in the deep-time fossil record. The identified complex nature of paleoclimate interactions might explain contradictory conclusions on the relationship between temperature and origination in the previous literature. Our results highlight the need to account for complex interactions in evolutionary studies both between and among biotic and abiotic factors.

Climate change disrupts core habitats of marine species.

Driven by climate change, marine biodiversity is undergoing a phase of rapid change that has proven to be even faster than changes observed in terrestrial ecosystems. Understanding how these changes in species composition will affect future marine life is crucial for conservation management, especially due to increasing demands for marine natural resources. Here, we analyse predictions of a multiparameter habitat suitability model covering the global projected ranges of >33,500 marine species from climate model projections under three CO2 emission scenarios (RCP2.6, RCP4.5, RCP8.5) up to the year 2100. Our results show that the core habitat area will decline for many species, resulting in a net loss of 50% of the core habitat area for almost half of all marine species in 2100 under the high-emission scenario RCP8.5. As an additional consequence of the continuing distributional reorganization of marine life, gaps around the equator will appear for 8% (RCP2.6), 24% (RCP4.5), and 88% (RCP8.5) of marine species with cross-equatorial ranges. For many more species, continuous distributional ranges will be disrupted, thus reducing effective population size. In addition, high invasion rates in higher latitudes and polar regions will lead to substantial changes in the ecosystem and food web structure, particularly regarding the introduction of new predators. Overall, our study highlights that the degree of spatial and structural reorganization of marine life with ensued consequences for ecosystem functionality and conservation efforts will critically depend on the realized greenhouse gas emission pathway.

Past and future decline of tropical pelagic biodiversity.

A major research question concerning global pelagic biodiversity remains unanswered: when did the apparent tropical biodiversity depression (i.e., bimodality of latitudinal diversity gradient [LDG]) begin? The bimodal LDG may be a consequence of recent ocean warming or of deep-time evolutionary speciation and extinction processes. Using rich fossil datasets of planktonic foraminifers, we show here that a unimodal (or only weakly bimodal) diversity gradient, with a plateau in the tropics, occurred during the last ice age and has since then developed into a bimodal gradient through species distribution shifts driven by postglacial ocean warming. The bimodal LDG likely emerged before the Anthropocene and industrialization, and perhaps ∼15,000 y ago, indicating a strong environmental control of tropical diversity even before the start of anthropogenic warming. However, our model projections suggest that future anthropogenic warming further diminishes tropical pelagic diversity to a level not seen in millions of years.

Emergence patterns of locally novel plant communities driven by past climate change and modern anthropogenic impacts.

Anthropogenic disturbance and climate change can result in dramatic increases in the emergence of new, ecologically novel, communities of organisms. We used a standardised framework to detect local novel communities in 2135 pollen time series over the last 25,000 years. Eight thousand years of post-glacial warming coincided with a threefold increase in local novel community emergence relative to glacial estimates. Novel communities emerged predominantly at high latitudes and were linked to global and local temperature change across multi-millennial time intervals. In contrast, emergence of locally novel communities in the last 200 years, although already on par with glacial retreat estimates, occurred at midlatitudes and near high human population densities. Anthropogenic warming does not appear to be strongly associated with modern local novel communities, but may drive widespread emergence in the future, with legacy effects for millennia after warming abates.

Out of the extratropics: the evolution of the latitudinal diversity gradient of Cenozoic marine plankton.

Many ecological and evolutionary hypotheses have been proposed to explain the latitudinal diversity gradient, i.e. the increase in species richness from the poles to the tropics. Among the evolutionary hypotheses, the 'out of the tropics' (OTT) hypothesis has received considerable attention. The OTT posits that the tropics are both a cradle and source of biodiversity for extratropical regions. To test the generality of the OTT hypothesis, we explored the spatial biodiversity dynamics of unicellular marine plankton over the Cenozoic era (the last 66 Myr). We find large-scale climatic changes during the Cenozoic shaped the diversification and dispersal of marine plankton. Origination was generally more likely in the extratropics and net dispersal was towards the tropics rather than in the opposite direction, especially during the warmer climates of the early Cenozoic. Although migration proportions varied among major plankton groups and climate phases, we provide evidence that the extratropics were a source of tropical microplankton biodiversity over the last 66 Myr.

Increase in marine provinciality over the last 250 million years governed more by climate change than plate tectonics.

Amidst long-term fluctuations of the abiotic environment, the degree to which life organizes into distinct biogeographic provinces (provinciality) can reveal the fundamental drivers of global biodiversity. Our understanding of present-day biogeography implies that changes in the distribution of continents across climatic zones have predictable effects on habitat distribution, dispersal barriers and the evolution of provinciality. To assess marine provinciality through the Phanerozoic, here we (a) simulate provinces based on palaeogeographic reconstructions and global climate models and (b) contrast them with empirically derived provinces that we define using network analysis of fossil occurrences. Simulated and empirical patterns match reasonably well and consistently suggest a greater than 15% increase in provinciality since the Mesozoic era. Although both factors played a role, the simulations imply that the effect of the latitudinal temperature gradient has been twice as important in determining marine provinciality as continental configuration.

Victims of ancient hyperthermal events herald the fates of marine clades and traits under global warming.

Organismic groups vary non-randomly in their vulnerability to extinction. However, it is unclear whether the same groups are consistently vulnerable, regardless of the dominant extinction drivers, or whether certain drivers have their own distinctive and predictable victims. Given the challenges presented by anthropogenic global warming, we focus on changes in extinction selectivity trends during ancient hyperthermal events: geologically rapid episodes of global warming. Focusing on the fossil record of the last 300 million years, we identify clades and traits of marine ectotherms that were more prone to extinction under the onset of six hyperthermal events than during other times. Hyperthermals enhanced the vulnerability of marine fauna that host photosymbionts, particularly zooxanthellate corals, the reef environments they provide, and genera with actively burrowing or swimming adult life-stages. The extinction risk of larger sized fauna also increased relative to non-hyperthermal times, while genera with a poorly buffered internal physiology did not become more vulnerable on average during hyperthermals. Hyperthermal-vulnerable clades include rhynchonelliform brachiopods and bony fish, whereas resistant clades include cartilaginous fish, and ostreid and venerid bivalves. These extinction responses in the geological past mirror modern responses of these groups to warming, including range-shift magnitudes, population losses, and experimental performance under climate-related stressors. Accordingly, extinction mechanisms distinctive to rapid global warming may be indicated, including sensitivity to warming-induced seawater deoxygenation. In anticipation of modern warming-driven marine extinctions, the trends illustrated in the fossil record offer an expedient preview.

Geographical limits to species-range shifts are suggested by climate velocity.

The reorganization of patterns of species diversity driven by anthropogenic climate change, and the consequences for humans, are not yet fully understood or appreciated. Nevertheless, changes in climate conditions are useful for predicting shifts in species distributions at global and local scales. Here we use the velocity of climate change to derive spatial trajectories for climatic niches from 1960 to 2009 (ref. 7) and from 2006 to 2100, and use the properties of these trajectories to infer changes in species distributions. Coastlines act as barriers and locally cooler areas act as attractors for trajectories, creating source and sink areas for local climatic conditions. Climate source areas indicate where locally novel conditions are not connected to areas where similar climates previously occurred, and are thereby inaccessible to climate migrants tracking isotherms: 16% of global surface area for 1960 to 2009, and 34% of ocean for the 'business as usual' climate scenario (representative concentration pathway (RCP) 8.5) representing continued use of fossil fuels without mitigation. Climate sink areas are where climate conditions locally disappear, potentially blocking the movement of climate migrants. Sink areas comprise 1.0% of ocean area and 3.6% of land and are prevalent on coasts and high ground. Using this approach to infer shifts in species distributions gives global and regional maps of the expected direction and rate of shifts of climate migrants, and suggests areas of potential loss of species richness.

The biogeographical imprint of mass extinctions.

Mass extinctions are defined by extinction rates significantly above background levels and have had substantial consequences for the evolution of life. Geographically selective extinctions, subsequent originations and species redistributions may have changed global biogeographical structure, but quantification of this change is lacking. In order to assess quantitatively the biogeographical impact of mass extinctions, we outline time-traceable bioregions for benthic marine species across the Phanerozoic using a compositional network. Mass extinction events are visually recognizable in the geographical depiction of bioregions. The end-Permian extinction stands out with a severe reduction of provinciality. Time series of biogeographical turnover represent a novel aspect of the analysis of mass extinctions, confirming concentration of changes in the geographical distribution of benthic marine life.

Reliable estimates of beta diversity with incomplete sampling.

Beta diversity, the compositional variation among communities or assemblages, is crucial to understanding the principles of diversity assembly. The mean pairwise proportional dissimilarity expresses overall heterogeneity of samples in a data set and is among the most widely used and most robust measures of beta diversity. Obtaining a complete list of taxa and their abundances requires substantial taxonomic expertise and is time consuming. In addition, the information is generally incomplete due to sampling biases. Based on the concept of the ecological significance of dominant taxa, we explore whether determining proportional dissimilarity can be simplified based on dominant species. Using simulations and six case studies, we assess the correlation between complete community compositional data and reduced subsets of a varying number of dominant species. We find that gross beta diversity is usually depicted accurately when only the 80th percentile or five of the most abundant species of each site is considered. In data sets with very high evenness, at least the 10 most abundant species should be included. Focusing on dominant species also maintains the rank-order of beta diversity among sites. Our new approach will allow ecologists and paleobiologists to produce a far greater amount of data on diversity patterns with less time and effort, supporting conservation studies and basic science.

Continuous evolutionary change in Plio-Pleistocene mammals of eastern Africa.

Much debate has revolved around the question of whether the mode of evolutionary and ecological turnover in the fossil record of African mammals was continuous or pulsed, and the degree to which faunal turnover tracked changes in global climate. Here, we assembled and analyzed large specimen databases of the fossil record of eastern African Bovidae (antelopes) and Turkana Basin large mammals. Our results indicate that speciation and extinction proceeded continuously throughout the Pliocene and Pleistocene, as did increases in the relative abundance of arid-adapted bovids, and in bovid body mass. Species durations were similar among clades with different ecological attributes. Occupancy patterns were unimodal, with long and nearly symmetrical origination and extinction phases. A single origination pulse may be present at 2.0-1.75 Ma, but besides this, there is no evidence that evolutionary or ecological changes in the eastern African record tracked rapid, 100,000-y-scale changes in global climate. Rather, eastern African large mammal evolution tracked global or regional climatic trends at long (million year) time scales, while local, basin-scale changes (e.g., tectonic or hydrographic) and biotic interactions ruled at shorter timescales.

Persistent ecological shifts in marine molluscan assemblages across the end-Cretaceous mass extinction.

Contemporary biodiversity loss and population declines threaten to push the biosphere toward a tipping point with irreversible effects on ecosystem composition and function. As a potential example of a global-scale regime shift in the geological past, we assessed ecological changes across the end-Cretaceous mass extinction based on molluscan assemblages at four well-studied sites. By contrasting preextinction and postextinction rank abundance and numerical abundance in 19 molluscan modes of life--each defined as a unique combination of mobility level, feeding mode, and position relative to the substrate--we find distinct shifts in ecospace utilization, which significantly exceed predictions from null models. The magnitude of change in functional traits relative to normal temporal fluctuations at far-flung sites indicates that molluscan assemblages shifted to differently structured systems and faunal response was global. The strengths of temporal ecological shifts, however, are mostly within the range of preextinction site-to-site variability, demonstrating that local ecological turnover was similar to geographic variation over a broad latitudinal range. In conjunction with varied site-specific temporal patterns of individual modes of life, these spatial and temporal heterogeneities argue against a concerted phase shift of molluscan assemblages from one well-defined regime to another. At a broader ecological level, by contrast, congruent tendencies emerge and suggest deterministic processes. These patterns comprise the well-known increase of deposit-feeding mollusks in postextinction assemblages and increases in predators and predator-resistant modes of life, i.e., those characterized by elevated mobility and infaunal life habits.

Diversity partitioning during the Cambrian radiation.

The fossil record offers unique insights into the environmental and geographic partitioning of biodiversity during global diversifications. We explored biodiversity patterns during the Cambrian radiation, the most dramatic radiation in Earth history. We assessed how the overall increase in global diversity was partitioned between within-community (alpha) and between-community (beta) components and how beta diversity was partitioned among environments and geographic regions. Changes in gamma diversity in the Cambrian were chiefly driven by changes in beta diversity. The combined trajectories of alpha and beta diversity during the initial diversification suggest low competition and high predation within communities. Beta diversity has similar trajectories both among environments and geographic regions, but turnover between adjacent paleocontinents was probably the main driver of diversification. Our study elucidates that global biodiversity during the Cambrian radiation was driven by niche contraction at local scales and vicariance at continental scales. The latter supports previous arguments for the importance of plate tectonics in the Cambrian radiation, namely the breakup of Pannotia.

Adding fossil occupancy trajectories to the assessment of modern extinction risk.

Besides helping to identify species traits that are commonly linked to extinction risk, the fossil record may also be directly relevant for assessing the extinction risk of extant species. Standing geographical distribution or occupancy is a strong predictor of both recent and past extinction risk, but the role of changes in occupancy is less widely assessed. Here we demonstrate, based on the Cenozoic fossil record of marine species, that both occupancy and its temporal trajectory are significant determinants of risk. Based on extinct species we develop a model on the additive and interacting effects of occupancy and its temporal changes on extinction risk. We use this model to predict extinction risk of extant species. The predictions suggest a moderate risk for marine species on average. However, some species seem to be on a long-term decline and potentially at a latent extinction risk, which is not considered in current risk assessments.

Equatorial decline of reef corals during the last Pleistocene interglacial.

The Last Interglacial (LIG; ca. 125,000 y ago) resulted from rapid global warming and reached global mean temperatures exceeding those of today. The LIG thus offers the opportunity to study how life may respond to future global warming. Using global occurrence databases and applying sampling-standardization, we compared reef coral diversity and distributions between the LIG and modern. Latitudinal diversity patterns are characterized by a tropical plateau today but were characterized by a pronounced equatorial trough during the LIG. This trough is governed by substantial range shifts away from the equator. Range shifts affected both leading and trailing edges of species range limits and were much more pronounced in the Northern Hemisphere than south of the equator. We argue that interglacial warming was responsible for the loss of equatorial diversity. Hemispheric differences in insolation during the LIG may explain the asymmetrical response. The equatorial retractions are surprisingly strong given that only small temperature changes have been reported in the LIG tropics. Our results suggest that the poleward range expansions of reef corals occurring with intensified global warming today may soon be followed by equatorial range retractions.

Differential niche dynamics among major marine invertebrate clades.

The degree to which organisms retain their environmental preferences is of utmost importance in predicting their fate in a world of rapid climate change. Notably, marine invertebrates frequently show strong affinities for either carbonate or terrigenous clastic environments. This affinity is due to characteristics of the sediments as well as correlated environmental factors. We assessed the conservatism of substrate affinities of marine invertebrates over geological timescales, and found that niche conservatism is prevalent in the oceans, and largely determined by the strength of initial habitat preference. There is substantial variation in niche conservatism among major clades with corals and sponges being among the most conservative. Time-series analysis suggests that niche conservatism is enhanced during times of elevated nutrient flux, whereas niche evolution tends to occur after mass extinctions. Niche evolution is not necessarily elevated in genera exhibiting higher turnover in species composition.

Diffuse, Adult-Onset Nesidioblastosis/Non-Insulinoma Pancreatogenous Hypoglycemia Syndrome (NIPHS): Review of the Literature of a Rare Cause of Hyperinsulinemic Hypoglycemia.

Differential diagnosis of hypoglycemia in the non-diabetic adult patient is complex and comprises various diseases, including endogenous hyperinsulinism caused by functional ß-cell disorders. The latter is also designated as nesidioblastosis or non-insulinoma pancreatogenous hypoglycemia syndrome (NIPHS). Clinically, this rare disease presents with unspecific adrenergic and neuroglycopenic symptoms and is, therefore, often overlooked. A combination of careful clinical assessment, oral glucose tolerance testing, 72 h fasting, sectional and functional imaging, and invasive insulin measurements can lead to the correct diagnosis. Due to a lack of a pathophysiological understanding of the condition, conservative treatment options are limited and mostly ineffective. Therefore, nearly all patients currently undergo surgical resection of parts or the entire pancreas. Consequently, apart from faster diagnosis, more elaborate and less invasive treatment options are needed to relieve the patients from the dangerous and devastating symptoms. Based on a case of a 23-year-old man presenting with this disease in our department, we performed an extensive review of the medical literature dealing with this condition and herein presented a comprehensive discussion of this interesting disease, including all aspects from epidemiology to therapy.

An Uncommon Cause of Recurrent Presyncope, Dizziness, and Tachycardia: A Case Report of Diffuse, Adult-Onset Nesidioblastosis/Non-Insulinoma Pancreatogenous Hypoglycemia Syndrome (NIPHS).

Neurovegetative and autonomic symptoms are common presentations of various diseases, ranging from psychosomatic to severe organic disorders. A 23-year-old man presented with a history of recurrent presyncope, dizziness, and tachycardia. Repeated diagnostic work-up in various clinical settings could not identify any definite cause for approximately eight years. However, the incidental detection of postprandial and exercise-induced hypoglycemia was suggestive of an insulin-related disorder. A 72 h plasma glucose fasting test revealed endogenous hyperinsulinism. Upon imaging studies, no tumor mass potentially indicating insulinoma could be detected. 68Ga-DOTA-Exendin-4 PET/CT showed diffuse tracer enrichment throughout the whole pancreas. A subtotal pancreatectomy was performed, and the diagnosis of diffuse, adult-onset nesidioblastosis was established histopathologically. This corresponds to the clinical findings of a functional ß-cell disorder, also known as non-insulinoma pancreatogenous hypoglycemia syndrome (NIPHS). After nine months, the symptoms recurred, making complete pancreatectomy necessary. Postoperative laboratory evaluation exhibited no residual endogenous C-peptide production. This case illustrates the diagnostic challenges in patients presenting with unspecific, neurovegetative and autonomic symptoms with a severe and rare underlying cause.

Climate change and marine life.

A Marine Climate Impacts Workshop was held from 29 April to 3 May 2012 at the US National Center of Ecological Analysis and Synthesis in Santa Barbara. This workshop was the culmination of a series of six meetings over the past three years, which had brought together 25 experts in climate change ecology, analysis of large datasets, palaeontology, marine ecology and physical oceanography. Aims of these workshops were to produce a global synthesis of climate impacts on marine biota, to identify sensitive habitats and taxa, to inform the current Intergovernmental Panel on Climate Change (IPCC) process, and to strengthen research into ecological impacts of climate change.