Florida Museum of Natural History
  • Gainesville, United States
Recent publications
During the last 10 years, the Erythrina stem borer moth, Terastia meticulosalis, emerged as a pest of cultivated coral trees (Erythrina spp.) in California. Erythrina trees are valued for their moderate drought resistance and beautiful flame‐like flowers. They are beloved enough to be considered Los Angeles's official “City Tree.” Thus, they are a valuable horticultural crop and are grown by many nurseries and occur throughout the landscape in coastal southern California. Coral trees have been heavily affected by T. meticulosalis recently. Using whole genome sequencing techniques, we analysed the origins of this and other infestations of Erythrina in coastal areas and found that they have likely originated from the repeated expansions of the native range of the species in Arizona, a process possibly driven by climatic factors and/or movement of plants by humans. We also found sufficient genetic differences between the western population of the moth and the rest of the New World populations to describe a new western subspecies, T. meticulosalis occidentalis Sourakov & Grishin ssp. n. (type locality USA: CA, San Diego Co., La Jolla). These findings are of economic importance for future attempts to control the moth's impact on activities surrounding the horticultural use of Erythrina spp. by the Californian landscape and nursery industries.
Rapid climate change is threatening biodiversity via habitat loss, range shifts, increases in invasive species, novel species interactions, and other unforeseen changes. Coastal and estuarine species are especially vulnerable to the impacts of climate change due to sea level rise and may be severely impacted in the next several decades. Species distribution modeling can project the potential future distributions of species under scenarios of climate change using bioclimatic data and georeferenced occurrence data. However, models projecting suitable habitat into the future are impossible to ground truth. One solution is to develop species distribution models for the present and project them to periods in the recent past where distributions are known to test model performance before making projections into the future. Here, we develop models using abiotic environmental variables to quantify the current suitable habitat available to eight Neotropical coastal species: four mangrove species and four salt marsh species. Using a novel model validation approach that leverages newly available monthly climatic data from 1960 to 2018, we project these niche models into two time periods in the recent past (i.e., within the past half century) when either mangrove or salt marsh dominance was documented via other data sources. Models were hindcast‐validated and then used to project the suitable habitat of all species at four time periods in the future under a model of climate change. For all future time periods, the projected suitable habitat of mangrove species decreased, and suitable habitat declined more severely in salt marsh species. Species distribution modeling can project the potential future distributions of species under scenarios of climate change using bioclimatic data and georeferenced occurrence data. However, models projecting suitable habitat into the future are impossible to ground truth. Here, we overcome this limitation by developing species distribution models for the present and projecting them to periods in the recent past where distributions are known to test model performance before making projections into the future.
Elasmobranchs are characterised by the presence of placoid scales on their skin. These scales, structurally homologous to gnathostome teeth, are thought to have various ecological functions related to drag reduction, predator defense or abrasion reduction. Some scales, particularly those present in the ventral area, are also thought to be functionally involved in the transmission of bioluminescent light in deep-sea environments. In the deep parts of the oceans, elasmobranchs are mainly represented by squaliform sharks. This study compares ventral placoid scale morphology and elemental composition of more than thirty deep-sea squaliform species. Scanning Electron Microscopy and Energy Dispersive X-ray spectrometry, associated with morphometric and elemental composition measurements were used to characterise differences among species. A maximum likelihood molecular phylogeny was computed for 43 shark species incuding all known families of Squaliformes. Character mapping was based on this phylogeny to estimate ancestral character states among the squaliform lineages. Our results highlight a conserved and stereotypical elemental composition of the external layer among the examined species. Phosphorus-calcium proportion ratios (Ca/P) slightly vary from 1.8-1.9, and fluorine is typically found in the placoid scale. By contrast, there is striking variation in shape in ventral placoid scales among the investigated families. Character-mapping reconstructions indicated that the shield-shaped placoid scale morphotype is likely to be ancestral among squaliform taxa. The skin surface occupied by scales appears to be reduced in luminous clades which reflects a relationship between scale coverage and the ability to emit light. In luminous species, the placoid scale morphotypes are restricted to pavement, bristle-and spine-shaped except for the only luminescent somniosid, Zameus squamulosus, and the dalatiid Mollisquama mississippiensis. These results, deriving from an unprecedented sampling, show extensive morphological diversity in placoid scale shape but little variation in elemental composition among Squaliformes.
Darwin Core, the data standard used for sharing modern biodiversity and paleodiversity occurrence records, has previously lacked proper mechanisms for reporting what is known about the estimated age range of specimens from deep time. This has led to data providers putting these data in fields where they cannot easily be found by users, which impedes the reuse and improvement of these data by other researchers. Here we describe the development of the Chronometric Age Extension to Darwin Core, a ratified, community-developed extension that enables the reporting of ages of specimens from deeper time and the evidence supporting these estimates. The extension standardizes reporting about the methods or assays used to determine an age and other critical information like uncertainty. It gives data providers flexibility about the level of detail reported, focusing on the minimum information needed for reuse while still allowing for significant detail if providers have it. Providing a standardized format for reporting these data will make them easier to find and search and enable researchers to pinpoint specimens of interest for data improvement or accumulate more data for broad temporal studies. The Chronometric Age Extension was also the first community-managed vocabulary to undergo the new Biodiversity Informatics Standards (TDWG) review and ratification process, thus providing a blueprint for future Darwin Core extension development.
Warming temperatures are increasing rainfall extremes, yet arthropod responses to climatic fluctuations remain poorly understood. Here, we used spatiotemporal variation in tropical montane climate as a natural experiment to compare the importance of biotic versus abiotic drivers in regulating arthropod biomass. We combined intensive field data on arthropods, leaf phenology and in situ weather across a 1700-3100 m elevation and rainfall gradient, along with desiccation-resistance experiments and multi-decadal modelling. We found limited support for biotic drivers with weak increases in some herbivorous taxa on shrubs with new leaves, but no landscape-scale effects of leaf phenology, which tracked light and cloud cover. Instead, rainfall explained extensive interannual variability with maximum biomass at intermediate rainfall (130 mm month-1 ) as both 3 months of high and low rainfall reduced arthropods by half. Based on 50 years of regional rainfall, our dynamic arthropod model predicted shifts in the timing of biomass maxima within cloud forests before plant communities transition to seasonally deciduous dry forests (mean annual rainfall 1000-2500 mm vs. <800 mm). Rainfall magnitude was the primary driver, but during high solar insolation, the 'drying power of air' (VPDmax ) reduced biomass within days contributing to drought related to the El Niño-Southern Oscillation (ENSO). Highlighting risks from drought, experiments demonstrated community-wide susceptibility to desiccation except for some caterpillars in which melanin-based coloration appeared to reduce the effects of evaporative drying. Overall, we provide multiple lines of evidence that several months of heavy rain or drought reduce arthropod biomass independently of deep-rooted plants with the potential to destabilize insectivore food webs.
The large size and complexity of most fern genomes have hampered efforts to elucidate fundamental aspects of fern biology and land plant evolution through genome-enabled research. Here we present a chromosomal genome assembly and associated methylome, transcriptome and metabolome analyses for the model fern species Ceratopteris richardii . The assembly reveals a history of remarkably dynamic genome evolution including rapid changes in genome content and structure following the most recent whole-genome duplication approximately 60 million years ago. These changes include massive gene loss, rampant tandem duplications and multiple horizontal gene transfers from bacteria, contributing to the diversification of defence-related gene families. The insertion of transposable elements into introns has led to the large size of the Ceratopteris genome and to exceptionally long genes relative to other plants. Gene family analyses indicate that genes directing seed development were co-opted from those controlling the development of fern sporangia, providing insights into seed plant evolution. Our findings and annotated genome assembly extend the utility of Ceratopteris as a model for investigating and teaching plant biology.
Natural history collections (NHCs) have been indispensable to understanding longer‐term trends of the timing of seasonal events. Massive‐scale digitization of specimens promises to further enable phenological research, especially the ability to move towards a deeper understanding of drivers of change and how trait‐environment interactions shape phenological sensitivity. Despite the promise of NHCs to answer fundamental phenology questions, use of these data resources present unique and often overlooked challenges requiring specialized workflow steps, such as assembling multisource data, accounting for date imprecision, and making decisions about trade‐offs between data density and spatial resolution. We provide a set of key best practice recommendations and showcase these via a case study that utilizes NHC data to test hypotheses about spatiotemporal trends in adult Lepidoptera (i.e., butterflies and moths) flight timing across North America. Our case study is a worked example of these best practices, helping practitioners recognize and overcome potential pitfalls at each step, from data acquisition and cleaning, to delineating spatial units and proper estimation of phenological metrics and associated uncertainty, to building appropriate models. We confirm and extend the critical importance of voltinism and diapause strategy, but less‐so daily activity patterns, for predicting Lepidoptera phenology spatiotemporal trends. Our case study also showcases the unique power of NHC data to test existing hypotheses and generate new insights about temporal phenological trends. Specifically, migratory species and species that enter diapause as adults are advancing the start of flight periods in more recent years, even after accounting for climate context. These results highlight the physiological and adaptive differences between species with different overwintering strategies. We close by noting the value of partnerships between data scientists, museum experts, and ecological modelers to fully harness the power of digital data resources to address pressing global change challenges. These partnerships can extend approaches for integrating multiple data types to fully unlock our understanding of the tempo, mode, drivers, and outcomes of phenological changes at greater spatial, temporal, and taxonomic scales.
Softshell turtles (Trionychidae) display characteristic pits and ridges, or “sculpturing,” on the bony carapace. Variation in sculpturing pattern may be useful in classifying fossilized shell fragments. Although past attempts could discern qualitative differences in certain best‐case scenarios, many early taxonomic uses of sculpturing traits have been reevaluated as unreliable in the face of intraspecific variation. The potential of sculpturing to contain consistently reliable, quantitative, taxonomically informative traits remains underexplored. Here, we revisit this idea by quantifying trionychid shell patterning with topographic measurement techniques more commonly applied to nonhomologous quantification of mammalian teeth and geographic surface topography. We assess potential sources of variation and accuracy of these metrics for species identification. Carapaces of extant specimens used in this study included members of the species Apalone ferox, Apalone spinifera, and Amyda cartilaginea and were obtained from the herpetology collections of the Florida Museum of Natural History. 3D scans of shells were systematically sampled to create digital “fragments.” These fragments were quantified using three topographic measurements: Dirichlet Normal Energy (DNE), Relief Index (RFI), and Orientation Patch Count Rotated (OPCR). A nested MANOVA suggests there is significant variation at the species, individual, and carapace location levels of analysis. Linear discriminant analysis correctly predicts a sample's species identity from DNE, RFI, and OPCR 75.2% of the time. These promising results indicate that topographic measures may provide a method for identifying shell fragments that are currently identifiable only as Trionychidae indet. Future work should explore this approach in additional species and account for ontogenetic changes.
Understanding variation of traits within and among species through time and across space is central to many questions in biology. Many resources assemble species-level trait data, but the data and metadata underlying those trait measurements are often not reported. Here, we introduce FuTRES (Functional Trait Resource for Environmental Studies; pronounced few-tress), an online datastore and community resource for individual-level trait reporting that utilizes a semantic framework. FuTRES already stores millions of trait measurements for paleobiological, zooarchaeological, and modern specimens, with a current focus on mammals. We compare dynamically-derived extant mammal species' body size measurements in FuTRES with summary values from other compilations, highlighting potential issues with simply reporting a single mean estimate. We then show that individual-level data improves estimates of body mass – including uncertainty – for zooarchaeological specimens. FuTRES facilitates trait data integration and discoverability, accelerating new research agendas, especially scaling from intra- to interspecific trait variability.
Tree diversity and composition in Amazonia are known to be strongly determined by the water supplied by precipitation. Nevertheless, within the same climatic regime, water availability is modulated by local topography and soil characteristics (hereafter referred to as local hydrological conditions), varying from saturated and poorly drained to well‐drained and potentially dry areas. While these conditions may be expected to influence species distribution, the impacts of local hydrological conditions on tree diversity and composition remain poorly understood at the whole Amazon basin scale. Using a dataset of 443 1‐ha non‐flooded forest plots distributed across the basin, we investigate how local hydrological conditions influence 1) tree alpha diversity, 2) the community‐weighted wood density mean (CWM‐wd) – a proxy for hydraulic resistance and 3) tree species composition. We find that the effect of local hydrological conditions on tree diversity depends on climate, being more evident in wetter forests, where diversity increases towards locations with well‐drained soils. CWM‐wd increased towards better drained soils in Southern and Western Amazonia. Tree species composition changed along local soil hydrological gradients in Central‐Eastern, Western and Southern Amazonia, and those changes were correlated with changes in the mean wood density of plots. Our results suggest that local hydrological gradients filter species, influencing the diversity and composition of Amazonian forests. Overall, this study shows that the effect of local hydrological conditions is pervasive, extending over wide Amazonian regions, and reinforces the importance of accounting for local topography and hydrology to better understand the likely response and resilience of forests to increased frequency of extreme climate events and rising temperatures.
Allopreening occurs in many species of birds and is known for providing hygienic and social benefits. While this behavior has been extensively studied among conspecifics, its occurrence among different species remains little known. Outside of captive environments, only a few records of interspecific allopreening exist. In this study, we describe our observations of the interspecific allopreening behavior between Spot-necked (Stachyris strialata) and Nonggang Babblers (S. nonggangensis) in a non-captive environment in southern China. To our knowledge, these observations represent the first record of interspecific allopreening in the family Timaliidae. We suggest that this understudied behavior is most likely related to the dominant–subordinate relationship between these two species: either the dominant species preening the subordinate species to assert dominance or the subordinate species preening the dominant species to reduce tensions by appeasement. We also suggest interspecific allopreening may not be as rare as we thought if we study this behavior under circumstances where different species are close to each other. This study contributes to our understanding of not only the potential mechanism(s) behind interspecific allopreening but also the behavioral ecology of the vulnerable Nonggang Babbler.
A new species of land snail, Carychium jochumae n. sp., is described from northern Pakistan, representing a new country record for the genus. The new species is compared to the nominal species occurring on the Indian subcontinent: Carychium indicum Benson, 1849, C. boysianum Benson, 1864, C. khasiacum Godwin-Austen, 1876, and C. parietidentatum (Das & Aravind, 2021 Benson, W.H. (1849) Characters of Diplommatina, a new genus of terrestrial mollusks belonging to the family of Carychiadae, and of a second species contained in it; also a new species of Carychium inhabiting the western Himalaya. The Annals and Magazine of Natural History 4, 193–195.[Taylor & Francis Online] , [Google Scholar]), which are briefly discussed. urn:lsid:zoobank.org:pub:42EDF7BD-6C22-4918-B4F7-DFB0BF85A8FA
Caves are home to unique and fragile biotas with high levels of endemism. However, little is known about how the biotic colonization of caves has developed over time, especially in caves from middle and low latitudes. Subtropical East Asia holds the world's largest karst landform with numerous ancient caves, which harbor a high diversity of cave-dwelling organisms and are regarded as a biodiversity hotspot. Here, we assess the temporal dynamics of biotic colonization of subtropical East Asian caves through a multi-taxon analysis with representatives of green plants, animals, and fungi. We then investigate the consequences of paleonviromental changes on the colonization dynamics of these caves in combination with reconstructions of vegetation, temperature, and precipitation. We discover that 88% of cave colonization events occurred after the Oligocene-Miocene boundary, and organisms from the surrounding forest were a major source for subtropical East Asian cave biodiversity. Biotic colonization of subtropical East Asian caves during the Neogene was subject to periods of acceleration and decrease, in conjunction with large-scale, seasonal climatic changes and evolution of local forests. This study highlights the long-term evolutionary interaction between surface and cave biotas; our climate-vegetation-relict model proposed for the subtropical East Asian cave biota may help explain the evolutionary origins of other mid-latitude subterranean biotas.
The Caribbean Sea is the most species-rich sea in the Atlantic, largely due to its vast coral reef systems. However, its high biodiversity and endemism face unprecedented anthropogenic threats, including synergistic modern pressures from overfishing, climate change and bioinvasion. Archaeological data indicate initial human settlement of the Caribbean ~7000 years before present (yr BP), with regionally variable human impacts on fisheries through time based on standard morphological identification of fish bone. Such studies, however, are challenged by the low taxonomic resolution of archaeological fish bone identifications due to high species diversity and morphological similarity between members of different families or genera. Here, we present collagen fingerprinting (Zooarchaeology by Mass Spectrometry; ZooMS) as a method to overcome this challenge, applying it to 1000 archaeological bone specimens identified morphologically as ray-finned fish (superclass Actinopterygii) from 13 circum-Caribbean sites spanning ca. 3150-300 yr BP (years before present). The method successfully identified collagen-containing samples (n = 720) to family (21%), genus (57%), and species (13%) level. Of the 209 samples that were morphologically identified below superclass, collagen fingerprinting verified the taxo-nomic identity of 94% of these, but also refined the identifications to a lower [more precise] taxon in 45% of cases. The remaining 6% of morphological identifications were found to be incorrectly assigned. This study represents the largest application of ZooMS to archaeological fish bones to date and advances future research through the identification of up to 20 collagen biomarkers for 45 taxa in 10 families and 2 orders. The results indicate that refinement of ZooMS archaeological fish identifications in this study is limited not by the quality of the preserved collagen but by the extent of the available modern collagen reference collection. Thus, efforts should be directed towards expanding collagen fingerprint databases in the first instance. Significantly, the high-resolution taxonomic identifications of archaeological bone that ZooMS can offer make ancient fisheries data highly relevant to modern sustainability and conservation efforts in the Caribbean. Additionally, more precise identifications will allow archaeologists to address a variety of questions related to cultural fishing practices and changes in fish stocks through time. This study supports the use of ZooMS as an effective biochemical tool available for mass-taxonomic identification of archaeological fish bone samples spanning century to millennial time scales in the circum-Caribbean.
Premise: The Cactaceae of northwestern Mexico and the southwestern United States constitute a major component of the angiosperm biodiversity of the region. The Mammilloid clade, (Cactaceae, tribe Cacteae), composed of the genera Cochemiea, Coryphantha, Cumarinia, Mammillaria, and Pelecyphora is especially species rich. We sought to understand the timing, geographical and climate influences correlated with expansion of the Mammilloid clade, through the Sonoran Desert into Baja California. Methods: We reconstructed the historical biogeography of the Mammilloid clade, using Bayesian and maximum likelihood methods, based on a strongly supported molecular phylogeny. We also estimated divergence times, the timing of emergence of key characters, and diversification rates and rate shifts of the Mammilloid clade. Key results: We found that the most recent common ancestor of Cochemiea arrived in the Cape region of Baja California from the Sonoran Desert region approximately 5 million years ago, coinciding with the timing of peninsular rifting from the mainland, suggesting dispersal and vicariance as causes of species richness and endemism. The diversification rate for Cochemiea is estimated to be approximately 12 times that of the mean background diversification rate for angiosperms. Divergence time estimation shows that many of the extant taxa in Cochemiea and Baja California Mammillaria emerged from common ancestors 1 million to 200,000 years ago, having a mid-Pleistocene origin. Conclusions: Cochemiea and Mammillaria of the Baja California region are examples of recent, rapid diversification. Geological and climatic forces at multiple spatial and temporal scales are correlated with the western distributions of the Mammilloid clade. This article is protected by copyright. All rights reserved.
Advancing spring phenology is a well‐documented consequence of anthropogenic climate change, but it is not well understood how climate change will affect the variability of phenology year‐to‐year. Species’ phenological timings reflect adaptation to a broad suite of abiotic needs (e.g. thermal energy) and biotic interactions (e.g. predation and pollination), and changes in patterns of variability may disrupt those adaptations and interactions. Here, we present a geographically and taxonomically broad analysis of phenological shifts, temperature sensitivity, and changes in inter‐annual variability encompassing nearly 10,000 long‐term phenology time‐series representing over 1,000 species across much of the northern hemisphere. We show that the timings of leaf‐out, flowering, insect first‐occurrence, and bird arrival were the most sensitive to temperature variation and have advanced at the fastest pace for early‐season species in colder and less seasonal regions. We did not find evidence for changing variability in warmer years in any phenophase groups, though leaf‐out and flower phenology have become moderately but significantly less variable over time. Our findings suggest that climate change has not to this point fundamentally altered patterns of inter‐annual phenological variability. This article is protected by copyright. All rights reserved.
In tetrapods, fusion between elements of the appendicular skeleton is thought to facilitate rapid movements during running, flying, and jumping. Although such fusion is widespread, frogs stand out because adults of all living species exhibit fusion of the zeugopod elements (radius and ulna, tibia and fibula), regardless of jumping ability or locomotor mode. To better understand what drives the maintenance of limb bone fusion in frogs, we use finite element modeling methods to assess the functional consequences of fusion in the anuran radioulna, the forearm bone of frogs that is important to both locomotion and mating behavior (amplexus). Using CT scans of museum specimens, measurement tools, and mesh-editing software, we evaluated how different degrees of fusion between the radius and ulna affect the von Mises stress and bending resistance of the radioulna in three loading scenarios: landing, amplexus, and long-axis loading conditions. We find that the semi-fused state observed in the radioulna exhibits less von Mises stress and more resistance to bending than unfused or completely fused models in all three scenarios. Our results suggest that radioulna morphology is optimized to minimize von Mises stress across different loading regimes while also minimizing volume. We contextualize our findings in an evaluation of the diversity of anuran radioulnae, which reveals unique, permanent pronation of the radioulna in frogs and substantial variation in wall thickness. This work provides new insight into the functional consequences of limb bone fusion in anuran evolution.
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37 members
Edward L Stanley
  • Herpetology
James D Williams
  • Ichthyology and Malacology
Andrew D Warren
  • McGuire Center for Lepidoptera and Biodiversity
Gainesville, United States
Head of institution
Douglas S. Jones