How many dinosaur species were there? Fossil bias and true richness estimated using a Poisson sampling model

The fossil record is a rich source of information about biological diversity in the past. However, the fossil record is not only incomplete but has also inherent biases due to geological, physical, chemical and biological factors. Our knowledge of past life is also biased because of differences in academic and amateur interests and sampling efforts. As a result, not all individuals or species that lived in the past are equally likely to be discovered at any point in time or space. To reconstruct temporal dynamics of diversity using the fossil record, biased sampling must be explicitly taken into account. Here, we introduce an approach that uses the variation in the number of times each species is observed in the fossil record to estimate both sampling bias and true richness. We term our technique TRiPS (True Richness estimated using a Poisson Sampling model) and explore its robustness to violation of its assumptions via simulations. We then venture to estimate sampling bias and absolute species richness of dinosaurs in the geological stages of the Mesozoic. Using TRiPS, we estimate that 1936 (1543–2468) species of dinosaurs roamed the Earth during the Mesozoic. We also present improved estimates of species richness trajectories of the three major dinosaur clades: the sauropodomorphs, ornithischians and theropods, casting doubt on the Jurassic–Cretaceous extinction event and demonstrating that all dinosaur groups are subject to considerable sampling bias throughout the Mesozoic.     

The completeness of the fossil record of mesozoic birds: implications for early avian evolution

Many palaeobiological analyses have concluded that modern birds (Neornithes) radiated no earlier than the Maastrichtian, whereas molecular clock studies have argued for a much earlier origination. Here, we assess the quality of the fossil record of Mesozoic avian species, using a recently proposed character completeness metric which calculates the percentage of phylogenetic characters that can be scored for each taxon. Estimates of fossil record quality are plotted against geological time and compared to estimates of species level diversity, sea level, and depositional environment. Geographical controls on the avian fossil record are investigated by comparing the completeness scores of species in different continental regions and latitudinal bins. Avian fossil record quality varies greatly with peaks during the Tithonian-early Berriasian, Aptian, and Coniacian-Santonian, and troughs during the Albian-Turonian and the Maastrichtian. The completeness metric correlates more strongly with a 'sampling corrected' residual diversity curve of avian species than with the raw taxic diversity curve, suggesting that the abundance and diversity of birds might influence the probability of high quality specimens being preserved. There is no correlation between avian completeness and sea level, the number of fluviolacustrine localities or a recently constructed character completeness metric of sauropodomorph dinosaurs. Comparisons between the completeness of Mesozoic birds and sauropodomorphs suggest that small delicate vertebrate skeletons are more easily destroyed by taphonomic processes, but more easily preserved whole. Lagerst?tten deposits might therefore have a stronger impact on reconstructions of diversity of smaller organisms relative to more robust forms. The relatively poor quality of the avian fossil record in the Late Cretaceous combined with very patchy regional sampling means that it is possible neornithine lineages were present throughout this interval but have not yet been sampled or are difficult to identify because of the fragmentary nature of the specimens.     

Dinosaur diversity and the rock record

Palaeobiodiversity analysis underpins macroevolutionary investigations, allowing identification of mass extinctions and adaptive radiations. However, recent large-scale studies on marine invertebrates indicate that geological factors play a central role in moulding the shape of diversity curves and imply that many features of such curves represent sampling artefacts, rather than genuine evolutionary events. In order to test whether similar biases affect diversity estimates for terrestrial taxa, we compiled genus-richness estimates for three Mesozoic dinosaur clades (Ornithischia, Sauropodomorpha and Theropoda). Linear models of expected genus richness were constructed for each clade, using the number of dinosaur-bearing formations available through time as a proxy for the amount of fossiliferous rock outcrop. Modelled diversity estimates were then compared with observed patterns. Strong statistically robust correlations demonstrate that almost all aspects of ornithischian and theropod diversity curves can be explained by geological megabiases, whereas the sauropodomorph record diverges from modelled predictions and may be a stronger contender for identifying evolutionary signals. In contrast to other recent studies, we identify a marked decline in dinosaur genus richness during the closing stages of the Cretaceous Period, indicating that the clade decreased in diversity for several million years prior to the final extinction of non-avian dinosaurs at the Cretaceous–Palaeocene boundary.     

No post-Cretaceous ecosystem depression in European forests? Rich insect-feeding damage on diverse middle Palaeocene plants,Menat, France

Insect herbivores are considered vulnerable to extinctions of their plant hosts. Previous studies of insect-damaged fossil leaves in the US Western Interior showed major plant and insect herbivore extinction at the Cretaceous–Palaeogene (K–T) boundary. Further, the regional plant–insect system remained depressed or ecologically unbalanced throughout the Palaeocene. Whereas Cretaceous floras had high plant and insect-feeding diversity, all Palaeocene assemblages to date had low richness of plants, insect feeding or both. Here, we use leaf fossils from the middle Palaeocene Menat site, France, which has the oldest well-preserved leaf assemblage from the Palaeocene of Europe, to test the generality of the observed Palaeocene US pattern. Surprisingly, Menat combines high floral diversity with high insect activity, making it the first observation of a ‘healthy’ Palaeocene plant–insect system. Furthermore, rich and abundant leaf mines across plant species indicate well-developed host specialization. The diversity and complexity of plant–insect interactions at Menat suggest that the net effects of the K–T extinction were less at this greater distance from the Chicxulub, Mexico, impact site. Along with the available data from other regions, our results show that the end-Cretaceous event did not cause a uniform, long-lasting depression of global terrestrial ecosystems. Rather, it gave rise to varying regional patterns of ecological collapse and recovery that appear to have been strongly influenced by distance from the Chicxulub structure.     

Species–energy relationship in the deep sea: a test using the Quaternary fossil record

Little is known about the processes regulating species richness in deep‐sea communities. Here we take advantage of natural experiments involving climate change to test whether predictions of the species–energy hypothesis hold in the deep sea. In addition, we test for the relationship between temperature and species richness predicted by a recent model based on biochemical kinetics of metabolism. Using the deep‐sea fossil record of benthic foraminifera and statistical meta‐analyses of temperature‐richness and productivity‐richness relationships in 10 deep‐sea cores, we show that temperature but not productivity is a significant predictor of species richness over the past c. 130 000 years. Our results not only show that the temperature‐richness relationship in the deep‐sea is remarkably similar to that found in terrestrial and shallow marine habitats, but also that species richness tracks temperature change over geological time, at least on scales of c. 100 000 years. Thus, predicting biotic response to global climate change in the deep sea would require better understanding of how temperature regulates the occurrences and geographical ranges of species.     

Species richness change across spatial scales

Humans have elevated global extinction rates and thus lowered global scale species richness. However, there is no a priori reason to expect that losses of global species richness should always, or even often, trickle down to losses of species richness at regional and local scales, even though this relationship is often assumed. Here, we show that scale can modulate our estimates of species richness change through time in the face of anthropogenic pressures, but not in a unidirectional way. Instead, the magnitude of species richness change through time can increase, decrease, reverse, or be unimodal across spatial scales. Using several case studies, we show different forms of scale‐dependent richness change through time in the face of anthropogenic pressures. For example, Central American corals show a homogenization pattern, where small scale richness is largely unchanged through time, while larger scale richness change is highly negative. Alternatively, birds in North America showed a differentiation effect, where species richness was again largely unchanged through time at small scales, but was more positive at larger scales. Finally, we collated data from a heterogeneous set of studies of different taxa measured through time from sites ranging from small plots to entire continents, and found highly variable patterns that nevertheless imply complex scale‐dependence in several taxa. In summary, understanding how biodiversity is changing in the Anthropocene requires an explicit recognition of the influence of spatial scale, and we conclude with some recommendations for how to better incorporate scale into our estimates of change.     

Early Cenozoic increases in mammal diversity cannot be explained solely by expansion into larger body sizes

A prominent hypothesis in the diversification of placental mammals after the Cretaceous–Palaeogene (K/Pg) boundary suggests that the extinction of non-avian dinosaurs resulted in the ecological release of mammals, which were previously constrained to small body sizes and limited species richness. This ‘dinosaur incumbency hypothesis’ may therefore explain increases in mammalian diversity via expansion into larger body size niches, that were previously occupied by dinosaurs, but does not directly predict increases in other body size classes. To evaluate this, we estimate sampling-standardized diversity patterns of terrestrial North American fossil mammals within body size classes, during the Cretaceous and Palaeogene. We find strong evidence for post-extinction diversity increases in all size classes. Increases in the diversity of small-bodied species (less than 100 g, the common body size class of Cretaceous mammals, and much smaller than the smallest non-avialan dinosaurs (c. 400 g)) were similar to those of larger species. We propose that small-bodied mammals had access to greater energetic resources or were able to partition resources more finely after the K/Pg mass extinction. This is likely to be the result of a combination of widespread niche clearing due to the K/Pg mass extinctions, alongside a suite of biotic and abiotic changes that occurred during the Late Cretaceous and across the K/Pg boundary, such as shifting floral composition, and novel key innovations among eutherian mammals.     

Local–regional richness relationship in fouling assemblages – Effects of succession

The number of species in a local habitat depends on local and regional processes. One common approach to explore ecological saturation of local richness has been to plot local versus regional richness. We expand this approach by incorporating two dimensions of diversity – taxonomic and functional – and different successional ages of marine fouling communities. In four different biogeographic regions (Mediterranean Sea, NE Atlantic, Western Baltic Sea and North Sea) 60 experimental units made from artificial substratum were deployed for colonization. Local richness was assessed as the average number of species and functional groups (FG) per unit area while regional richness was estimated as the estimated (Jack 2) asymptote of the accumulation curves for species or FG in local panel communities. Our findings indicate that the nature of the relationship between local and regional diversity is sensitive to successional stage and the dimension of diversity considered. However, as a general pattern, for taxonomic and functional richness, the slope of the local–regional relationship increased in the course of succession. We discuss how this pattern could have been produced by a combination of low number of recruiting species and incomplete competitive exclusion as is typical for early succession.     

From richer to poorer: successful invasion by freshwater fishes depends on species richness of donor and recipient basins

Evidence for the theory of biotic resistance is equivocal, with experiments often finding a negative relationship between invasion success and native species richness, and large‐scale comparative studies finding a positive relationship. Biotic resistance derives from local species interactions, yet global and regional studies often analyze data at coarse spatial grains. In addition, differences in competitive environments across regions may confound tests of biotic resistance based solely on native species richness of the invaded community. Using global and regional data sets for fishes in river and stream reaches, we ask two questions: (1) does a negative relationship exist between native and non‐native species richness and (2) do non‐native species originate from higher diversity systems. A negative relationship between native and non‐native species richness in local assemblages was found at the global scale, while regional patterns revealed the opposite trend. At both spatial scales, however, nearly all non‐native species originated from river basins with higher native species richness than the basin of the invaded community. Together, these findings imply that coevolved ecological interactions in species‐rich systems inhibit establishment of generalist non‐native species from less diverse communities. Consideration of both the ecological and evolutionary aspects of community assembly is critical to understanding invasion patterns. Distinct evolutionary histories in different regions strongly influence invasion of intact communities that are relatively unimpacted by human actions, and may explain the conflicting relationship between native and non‐native species richness found at different spatial scales.     

Tree diversity promotes predatory wasps and parasitoids but not pollinator bees in a subtropical experimental forest

From regional to global scales, anthropogenic environmental change is causing biodiversity loss and reducing ecosystem functionality. Previous studies have investigated the relationship between plant diversity and functional insect communities in temperate and also in tropical grasslands and forests. However, few studies have explored these dynamics in subtropical forests. Here, cavity-nesting Hymenoptera and associated parasitoids were collected across a controlled tree diversity experiment in subtropical China to test how predatory wasps, bees and parasitoids respond to tree species richness. Abundance and species richness of predatory wasps and parasitoids were positively correlated with tree species richness, while bee abundance and bee species richness were unrelated to tree species richness. Our results indicate that tree species richness increases the abundance and species richness of important communities such as predators and parasitoids. Moreover, the results highlight the importance of subtropical forests in maintaining abundance and species richness of key functional insect groups.     

Reprint of: Tree diversity promotes predatory wasps and parasitoids but not pollinator bees in a subtropical experimental forest

From regional to global scales, anthropogenic environmental change is causing biodiversity loss and reducing ecosystem functionality. Previous studies have investigated the relationship between plant diversity and functional insect communities in temperate and also in tropical grasslands and forests. However, few studies have explored these dynamics in subtropical forests. Here, cavity-nesting Hymenoptera and associated parasitoids were collected across a controlled tree diversity experiment in subtropical China to test how predatory wasps, bees and parasitoids respond to tree species richness. Abundance and species richness of predatory wasps and parasitoids were positively correlated with tree species richness, while bee abundance and bee species richness were unrelated to tree species richness. Our results indicate that tree species richness increases the abundance and species richness of important communities such as predators and parasitoids. Moreover, the results highlight the importance of subtropical forests in maintaining abundance and species richness of key functional insect groups.     

Plant species diversity and grazing in the Scandinavian mountains - patterns and processes at different spatial scales

There is a long tradition of grazing by semi‐domestic reindeer and sheep in alpine and sub‐alpine Scandinavian habitats, but present management regimes are questioned from a conservation point of view. In this review we discuss plant diversity patterns in the Scandinavian mountains in a global, regional and local perspective. The main objective was to identify processes that influence diversity at different spatial scales with a particular focus on grazing. In a global perspective the species pool of the Scandinavian mountains is limited. partly reflecting the general latitudinal decline of species but also historical and ecological factors operating after the latest glaciation. At the local scale, both productivity and disturbance are primary factors structuring diversity, but abiotic factors such as soil pH, snow distribution and temperature are also important. Although evidence is scarce, grazing favours local species richness in productive habitats, whereas species richness decreases with grazing when productivity is low. Regional patterns of plant diversity is set by, 1) the species pool. 2) the heterogeneity and fragmentation of communities, and 3) local diversity of each plant community. We suggest that local shifts in community composition depend both on the local grazing frequency and the return‐time of the plant community after a grazing session. In addition, an increasing number of grazing‐modified local patches homogenises the vegetation and is likely to reduce the regional plant diversity. The time scale of local shifts in community composition depends on plant colonisation and persistence, From a mechanistic point of view, diversity patterns at a regional scale also depend on the regional dynamics of single species. Colonisation is usually a slow and irregular process in alpine environments, whereas the capacity for extended local persistence is generally high. Although the poor knowledge of plant regional dynamics restricts our understanding of how grazing influences plant diversity, we conclude that grazing is a key process for maintaining biodiversity in the Scandinavian mountains.     

The extinction of the dinosaurs

Non‐avian dinosaurs went extinct 66 million years ago, geologically coincident with the impact of a large bolide (comet or asteroid) during an interval of massive volcanic eruptions and changes in temperature and sea level. There has long been fervent debate about how these events affected dinosaurs. We review a wealth of new data accumulated over the past two decades, provide updated and novel analyses of long‐term dinosaur diversity trends during the latest Cretaceous, and discuss an emerging consensus on the extinction's tempo and causes. Little support exists for a global, long‐term decline across non‐avian dinosaur diversity prior to their extinction at the end of the Cretaceous. However, restructuring of latest Cretaceous dinosaur faunas in North America led to reduced diversity of large‐bodied herbivores, perhaps making communities more susceptible to cascading extinctions. The abruptness of the dinosaur extinction suggests a key role for the bolide impact, although the coarseness of the fossil record makes testing the effects of Deccan volcanism difficult.     

Variation in freshwater fish assemblages along a regional elevation gradient in the northern Andes,Colombia

Studies on elevation diversity gradients have covered a large number of taxa and regions throughout the world; however, studies of freshwater fish are scarce and restricted to examining their changes along a specific gradient. These studies have reported a monotonic decrease in species richness with increasing elevation, but ignore the high taxonomic differentiation of each headwater assemblage that may generate high β‐diversity among them. Here, we analyzed how fish assemblages vary with elevation among regional elevation bands, and how these changes are related to four environmental clines and to changes in the distribution, habitat use, and the morphology of fish species. Using a standardized field sampling technique, we assessed three different diversity and two structural assemblage measures across six regional elevation bands located in the northern Andes (Colombia). Each species was assigned to a functional group based on its body shape, habitat use, morphological, and/or behavioral adaptations. Additionally, at each sampling site, we measured four environmental variables. Our analyses showed: (1) After a monotonic decrease in species richness, we detected an increase in richness in the upper part of the gradient; (2) diversity patterns vary depending on the diversity measure used; (3) diversity patterns can be attributed to changes in species distribution and in the richness and proportions of functional groups along the regional elevation gradient; and (4) diversity patterns and changes in functional groups are highly correlated with variations in environmental variables, which also vary with elevation. These results suggest a novel pattern of variation in species richness with elevation: Species richness increases at the headwaters of the northern Andes owing to the cumulative number of endemic species there. This highlights the need for large‐scale studies and has important implications for the aquatic conservation of the region.     

Time for a rethink: time sub‐sampling methods in disparity‐through‐time analyses

Disparity‐through‐time analyses can be used to determine how morphological diversity changes in response to mass extinctions, or to investigate the drivers of morphological change. These analyses are routinely applied to palaeobiological datasets, yet, although there is much discussion about how to best calculate disparity, there has been little consideration of how taxa should be sub‐sampled through time. Standard practice is to group taxa into discrete time bins, often based on stratigraphic periods. However, this can introduce biases when bins are of unequal size, and implicitly assumes a punctuated model of evolution. In addition, many time bins may have few or no taxa, meaning that disparity cannot be calculated for the bin and making it harder to complete downstream analyses. Here we describe a different method to complement the disparity‐through‐time tool‐kit: time‐slicing. This method uses a time‐calibrated phylogenetic tree to sample disparity‐through‐time at any fixed point in time rather than binning taxa. It uses all available data (tips, nodes and branches) to increase the power of the analyses, specifies the implied model of evolution (punctuated or gradual), and is implemented in R. We test the time‐slicing method on four example datasets and compare its performance in common disparity‐through‐time analyses. We find that the way we time sub‐sample taxa can change our interpretations of the results of disparity‐through‐time analyses. We advise using multiple methods for time sub‐sampling taxa, rather than just time binning, to gain a better understanding disparity‐through‐time.     

Global loss of avian evolutionary uniqueness in urban areas

Urbanization, one of the most important anthropogenic impacts on Earth, is rapidly expanding worldwide. This expansion of urban land‐covered areas is known to significantly reduce different components of biodiversity. However, the global evidence for this effect is mainly focused on a single diversity measure (species richness) with a few local or regional studies also supporting reductions in functional diversity. We have used birds, an important ecological group that has been used as surrogate for other animals, to investigate the hypothesis that urbanization reduces the global taxonomical and/or evolutionary diversity. We have also explored whether there is evidence supporting that urban bird communities are evolutionarily homogenized worldwide in comparison with nonurban ones by means of using evolutionary distinctiveness (how unique are the species) of bird communities. To our knowledge, this is the first attempt to quantify the effect of urbanization in more than one single diversity measure as well as the first time to look for associations between urbanization and phylogenetic diversity at a large spatial scale. Our findings show a strong and globally consistent reduction in taxonomic diversity in urban areas, which is also synchronized with the evolutionary homogenization of urban bird communities. Despite our general patterns, we found some regional differences in the intensity of the effect of cities on bird species richness or evolutionary distinctiveness, suggesting that conservation efforts should be adapted locally. Our findings might be useful for conservationists and policymakers to minimize the impact of urban development on Earth's biodiversity and help design more realistic conservation strategies.     

The Fynbos and sUcculent Karoo biomes do not have exceptional local ant richness

Background

The Fynbos (FB) and Succulent Karoo biomes (SKB) have high regional plant diversity despite relatively low productivity. Local diversity in the region varies but is moderate. For insects, previous work suggests that strict phytophages, but not other taxa, may have high regional richness. However, what has yet to be investigated is whether the local insect species richness of FB and SKB is unusual for a region of this productivity level at this latitude, and whether regional richness is also high. Here we determine whether this is the case for ants.

Methodology/Principal Findings

We use species richness data from pitfall traps in the FB and SKB in the Western Cape Province, South Africa and a global dataset of local ant richness extracted from the literature. We then relate the globally derived values of local richness to two energy-related predictors—productive energy (NDVI) and temperature, and to precipitation, and compare the data from the FB and SKB with these relationships. We further compare our local richness estimates with that of similar habitats worldwide, and regional ant richness with estimates derived from other regions. The local ant species richness of the FB and SKB falls within the general global pattern relating ant richness to energy, and is similar to that in comparable habitats elsewhere. At a regional scale, the richness of ants across all of our sites is not exceptional by comparison with other regional estimates from across the globe.

Conclusions/Significance

Local richness of ants in the FB and SKB is not exceptional by global standards. Initial analyses suggest that regional diversity is also not exceptional for the group. It seems unlikely that the mechanisms which have contributed to the development of extraordinarily high regional plant diversity in these biomes have had a strong influence on the ants.     

Small Theropod Teeth from the Late Cretaceous of the San Juan Basin,Northwestern New Mexico and Their Implications for Understanding Latest Cretaceous Dinosaur Evolution

Studying the evolution and biogeographic distribution of dinosaurs during the latest Cretaceous is critical for better understanding the end-Cretaceous extinction event that killed off all non-avian dinosaurs. Western North America contains among the best records of Late Cretaceous terrestrial vertebrates in the world, but is biased against small-bodied dinosaurs. Isolated teeth are the primary evidence for understanding the diversity and evolution of small-bodied theropod dinosaurs during the Late Cretaceous, but few such specimens have been well documented from outside of the northern Rockies, making it difficult to assess Late Cretaceous dinosaur diversity and biogeographic patterns. We describe small theropod teeth from the San Juan Basin of northwestern New Mexico. These specimens were collected from strata spanning Santonian – Maastrichtian. We grouped isolated theropod teeth into several morphotypes, which we assigned to higher-level theropod clades based on possession of phylogenetic synapomorphies. We then used principal components analysis and discriminant function analyses to gauge whether the San Juan Basin teeth overlap with, or are quantitatively distinct from, similar tooth morphotypes from other geographic areas. The San Juan Basin contains a diverse record of small theropods. Late Campanian assemblages differ from approximately co-eval assemblages of the northern Rockies in being less diverse with only rare representatives of troodontids and a Dromaeosaurus-like taxon. We also provide evidence that erect and recurved morphs of a Richardoestesia-like taxon represent a single heterodont species. A late Maastrichtian assemblage is dominated by a distinct troodontid. The differences between northern and southern faunas based on isolated theropod teeth provide evidence for provinciality in the late Campanian and the late Maastrichtian of North America. However, there is no indication that major components of small-bodied theropod diversity were lost during the Maastrichtian in New Mexico. The same pattern seen in northern faunas, which may provide evidence for an abrupt dinosaur extinction.     

Connecting species richness, abundance and body size in deep-sea gastropods

Aim This paper examines species richness, abundance, and body size in deep‐sea gastropods and how they vary over depth, which is a strong correlate of nutrient input. Previous studies have documented the empirical relationships among these properties in terrestrial and coastal ecosystems, but a full understanding of how these patterns arise has yet to be obtained. Examining the relationships among macroecological variables is a logical progression in deep‐sea ecology, where patterns of body size, diversity, and abundance have been quantified separately but not linked together. Location 196–5042 m depth in the western North Atlantic. Method Individuals analysed represent all Vetigastropoda and Caenogastropoda (Class Gastropoda) with intact shells, excluding Ptenoglossa, collected by the Woods Hole Benthic Sampling Program (3424 individuals representing 80 species). Biovolume was measured for every individual separately (i.e. allowing the same species to occupy multiple size classes) and divided into log₂ body size bins. Analyses were conducted for all gastropods together and separated into orders and depth regions (representing different nutrient inputs). A kernel smoothing technique, Kolmogorov‐Smirnov test of fit, and OLS and RMA were used to characterize the patterns. Results Overall, the relationship between the number of individuals and species is right skewed. There is also a positive linear relationship between the number of individuals and the number of species, which is independent of body size. Variation among these relationships is seen among the three depth regions. At depths inferred to correspond with intermediate nutrient input levels, species are accumulated faster given the number of individuals and shift from a right‐skewed to a log‐normal distribution. Conclusion A strong link between body size, abundance, and species richness appears to be ubiquitous over a variety of taxa and environments, including the deep sea. However, the nature of these relationships is affected by the productivity regime and scale at which they are examined.