Science Enabled by Specimen Data

Rubino, M. J., A. J. McKerrow, N. M. Tarr, and S. G. Williams. 2022. Methods for evaluating Gap Analysis Project habitat distribution maps with species occurrence data. Techniques and Methods.

The National Gap Analysis Project created species habitat distribution models for all terrestrial vertebrates in the United States to support conservation assessments and explore patterns of species richness. Those models link species to specific habitats throughout the range of each species. For most vertebrates, there are not enough occurrence data to drive inductive, range-wide species habitat distribution models at high spatial and thematic resolution. However, it is possible to use occurrence data for model evaluation. The combination of citizen science, formal species survey work, and digitized specimen archives are making millions of observations available to the scientific community. Our challenge is to combine the mostly unstructured data into metrics that help us characterize and understand patterns of biodiversity. In this work, we propose two model-evaluation metrics. The first, a buffer proportion assessment, is based on the proportion of habitat in the range relative to the mean proportion of habitat around each of the species’ occurrence records. The second is a measure of the sensitivity (proportion of true presence) to buffer distances around occurrence records. The buffer proportion is a modification of model prevalence versus point prevalence metric, whereby comparison to a null model allows us to determine if the model performs better or worse than random. In this report, we describe the workflow used to compile and filter the species occurrence records from online resources (for example, the Global Biodiversity Information Facility) and show results for a single species, Desmognathus quadramaculatus (black-bellied salamander). For the salamander, 222 occurrence points met our criteria for inclusion in the evaluation. We found the model performed better than random with a buffer proportion index of 1.745, indicating about 5 times as much habitat was found adjacent to known occurrence records than would be expected from randomly located sites throughout the range. Sensitivity increased with larger buffer distances and leveled off to around 0.7 between 1,000- and 2,000-meter buffer distances, indicating the model is likely best suited for scales exceeding 1,000 meters. We plan to report the buffer proportion assessment and sensitivity metrics along with the full species model reports to increase understanding of the model’s performance and to use the metrics to help prioritize revisions to the models.

Yu, S.-E., S.-L. Dong, Z.-X. Zhang, Y.-Y. Zhang, G. Sarà, J. Wang, and Y.-W. Dong. 2022. Mapping the potential for offshore aquaculture of salmonids in the Yellow Sea. Marine Life Science & Technology 4: 329–342.

Mariculture has been one of the fastest-growing global food production sectors over the past three decades. With the congestion of space and deterioration of the environment in coastal regions, offshore aquaculture has gained increasing attention. Atlantic salmon ( Salmo salar ) and rainbow trout ( Oncorhynchus mykiss ) are two important aquaculture species and contribute to 6.1% of world aquaculture production of finfish. In the present study, we established species distribution models (SDMs) to identify the potential areas for offshore aquaculture of these two cold-water fish species considering the mesoscale spatio-temporal thermal heterogeneity of the Yellow Sea. The values of the area under the curve (AUC) and the true skill statistic (TSS) showed good model performance. The suitability index (SI), which was used in this study to quantitatively assess potential offshore aquaculture sites, was highly dynamic at the surface water layer. However, high SI values occurred throughout the year at deeper water layers. The potential aquaculture areas for S. salar and O. mykiss in the Yellow Sea were estimated as 52,270 ± 3275 (95% confidence interval, CI) and 146,831 ± 15,023 km 2 , respectively. Our results highlighted the use of SDMs in identifying potential aquaculture areas based on environmental variables. Considering the thermal heterogeneity of the environment, this study suggested that offshore aquaculture for Atlantic salmon and rainbow trout was feasible in the Yellow Sea by adopting new technologies (e.g., sinking cages into deep water) to avoid damage from high temperatures in summer.

Jablonski, D., R. Masroor, and S. Hofmann. 2022. On the edge of the Shivaliks: An insight into the origin and taxonomic position of Pakistani toads from the Duttaphrynus melanostictus complex (Amphibia, Bufonidae). Zoosystematics and Evolution 98: 275–284.

AbstractThe common Asian toad Duttaphrynusmelanostictus (Schneider, 1799) complex has a wide distribution ranging from western foothills of the Himalaya to the easternmost range of the Wallacea, with the evidence of human-mediated introductions to some other areas. In the entire distribution range, the complex is formed by several evolutionary clades, distributed mostly in South-East Asia with unresolved taxonomy. In the northwestern edge of its distribution (Pakistan), the name D.melanostictushazarensis (Khan, 2001) has been assigned to local populations but its biological basis remained, so far, understudied and unvalidated. Therefore, we re-evaluated the available genetic data (mitochondrial and nuclear) to show the relationships between Pakistani populations (including the type locality of D.m.hazarensis) and others from across the range. Our results showed that Pakistani populations are associated with one, deeply diverged, well-supported and widely distributed clade (so-called Duttaphrynus sp. 1 according to 16S, or clade B based on tRNAGly-ND3), that has already been detected in previous studies. This clade is further distributed in India, Nepal, Bangladesh, Malaysia, Singapore, and Indonesia and is characterized by a low level of genetic variability. This further suggests that both natural, as well as potential human-mediated dispersal, might have played an important role in setting up the current phylogeographic and distribution pattern of this clade. The clade is deeply divergent from other clades of the complex and represents a taxonomically unresolved entity. We here argue that the clade Duttaphrynus sp. 1/B represents a distinct species for which the name Duttaphrynusbengalensis (Daudin, 1802) comb. nov. is applicable, while the description of D.m.hazarensis does not satisfy the rules of the International Code of Zoological Nomenclature.

Bosso, L., S. Smeraldo, D. Russo, M. L. Chiusano, G. Bertorelle, K. Johannesson, R. K. Butlin, et al. 2022. The rise and fall of an alien: why the successful colonizer Littorina saxatilis failed to invade the Mediterranean Sea. Biological Invasions.

Understanding what determines range expansion or extinction is crucial to predict the success of biological invaders. We tackled this long-standing question from an unparalleled perspective using the failed expansions in Littorina saxatilis and investigated its present and past habitat suitability in Europe through Ecological Niche Modelling. This intertidal snail is a typically successful Atlantic colonizer and the earliest confirmed alien species in the Mediterranean Sea, where, however, it failed to thrive despite its high dispersal ability and adaptability. We explored the environmental constraints affecting its biogeography, identified potential glacial refugia in Europe that fuelled its post-glacial colonisations and tested whether the current gaps in its distribution are linked to local ecological features. Our results suggested that L. saxatilis is unlikely to be a glacial relict in the Mediterranean basin. Multiple Atlantic glacial refugia occurred in the Last Glacial Maximum, and abiotic environmental features such as salinity and water temperature have influenced the past and current distributions of this snail and limited its invasion of the Mediterranean Sea. The snail showed a significant overlap in geographic space and ecological niche with Carcinus maenas , the Atlantic predator, but distinct from Pachygrapsus marmoratus , the Mediterranean predator, further pointing to Atlantic-like habitat requirements for this species. Abiotic constrains during introduction rather than dispersal abilities have shaped the past and current range of L. saxatilis and help explaining why some invasions have not been successful. Our findings contribute to clarifying the processes constraining or facilitating shifts in species’ distributions and biological invasions.

Widmer, B. W., T. M. Gehring, B. W. Heumann, and K. E. Nicholson. 2022. Climate change and range restriction of common salamanders in eastern Canada and the United States. The Journal of Wildlife Management 86.

The sensitivity of amphibian species to shifts in environmental conditions has been exhibited through long‐term population studies and the projection of ecological niche models under expected conditions. Species in biodiversity hotspots have been the focus of ample predictive modeling studies, while, despite their significant ecological value, wide‐ranging and common taxa have received less attention. We focused on predicting range restriction of the spotted salamander (Ambystoma maculatum), blue‐spotted salamander (A. laterale), four‐toed salamander (Hemidactylium scutatum), and red‐backed salamander (Plethodon cinereus) under future climate scenarios. Using bias‐corrected future climate data and biodiversity database records, we developed maximum entropy (MaxEnt) models under current conditions and for climate change projections in 2050 and 2070. We calculated positivity rates of species localities to represent proportions of habitat expected to remain climatically suitable with continued climate change. Models projected under future conditions predicted average positivity rates of 91% (89–93%) for the blue‐spotted salamander, 23% (2–41%) for the spotted salamander, 4% (0.7–9%) for the four‐toed salamander, and 61% (42–76%) for the red‐backed salamander. Range restriction increased with time and greenhouse gas concentration for the spotted salamander, four‐toed salamander, and red‐backed salamander. Common, widespread taxa that often receive less conservation resources than other species are at risk of experiencing significant losses to their climatic ranges as climate change continues. Efforts to maintain populations of species should be focused on regions expected to experience fewer climatic shifts such as the interior and northern zones of species' distributions.

Rautsaw, R. M., G. Jiménez-Velázquez, E. P. Hofmann, L. R. V. Alencar, C. I. Grünwald, M. Martins, P. Carrasco, et al. 2022. VenomMaps: Updated species distribution maps and models for New World pitvipers (Viperidae: Crotalinae). Scientific Data 9.

Beyond providing critical information to biologists, species distributions are useful for naturalists, curious citizens, and applied disciplines including conservation planning and medical intervention. Venomous snakes are one group that highlight the importance of having accurate information given their cosmopolitan distribution and medical significance. Envenomation by snakebite is considered a neglected tropical disease by the World Health Organization and venomous snake distributions are used to assess vulnerability to snakebite based on species occurrence and antivenom/healthcare accessibility. However, recent studies highlighted the need for updated fine-scale distributions of venomous snakes. Pitvipers (Viperidae: Crotalinae) are responsible for >98% of snakebites in the New World. Therefore, to begin to address the need for updated fine-scale distributions, we created VenomMaps, a database and web application containing updated distribution maps and species distribution models for all species of New World pitvipers. With these distributions, biologists can better understand the biogeography and conservation status of this group, researchers can better assess vulnerability to snakebite, and medical professionals can easily discern species found in their area. Measurement(s) Species Distributions Technology Type(s) Geographic Information System • Species Distribution Model (MaxEnt/kuenm) Factor Type(s) Occurrence Records • Environmental Data Sample Characteristic - Organism Crotalinae Sample Characteristic - Location North America • South America

Marshall, B. M., C. T. Strine, C. S. Fukushima, P. Cardoso, M. C. Orr, and A. C. Hughes. 2022. Searching the web builds fuller picture of arachnid trade. Communications Biology 5.

Wildlife trade is a major driver of biodiversity loss, yet whilst the impacts of trade in some species are relatively well-known, some taxa, such as many invertebrates are often overlooked. Here we explore global patterns of trade in the arachnids, and detected 1,264 species from 66 families and 371 genera in trade. Trade in these groups exceeds millions of individuals, with 67% coming directly from the wild, and up to 99% of individuals in some genera. For popular taxa, such as tarantulas up to 50% are in trade, including 25% of species described since 2000. CITES only covers 30 (2%) of the species potentially traded. We mapped the percentage and number of species native to each country in trade. To enable sustainable trade, better data on species distributions and better conservation status assessments are needed. The disparity between trade data sources highlights the need to expand monitoring if impacts on wild populations are to be accurately gauged and the impacts of trade minimised. Trade in arachnids includes millions of individuals and over 1264 species, with over 70% of individuals coming from the wild.

Barends, J. M., and B. Maritz. 2022. Dietary Specialization and Habitat Shifts in a Clade of Afro-Asian Colubrid Snakes (Colubridae: Colubrinae). Ichthyology & Herpetology 110.

Speciation through niche divergence often occurs as lineages of organisms colonize and adapt to new environments with novel ecological opportunities that facilitate the evolution of ecologically different phenotypes. In snakes, adaptive diversification may be driven by the evolution of traits relating to changes in their diets. Accordingly, habitatmediated differences in prey available to ancestral snakes as they colonized and occupied novel dynamic landscapes are likely to have been a strong selective agent behind the divergence and radiation of snakes across the globe. Using an ancestral reconstruction approach that considers the multivariate nature of ecological phenotypes while accounting for sampling variation between taxa, we explored how diet and macro-habitat use coevolved across a phylogeny of 67 species of Afro-Asian colubrine snakes. Our results show that the most recent common ancestor of this clade was likely a dietary generalist that occupied tropical forests in Asia. Deviations from this generalist diet to a variety of specialist diets each dominated by the utilization of single prey types repeatedly occurred as ancestral colubrines shifted from tropical forests to savanna and grassland habitats across Africa. We additionally found that dietary specialist species were on average smaller in maximum length than dietary generalists, congruent with established predator-size, preydiversity dynamics in snakes. We speculate that adaptive divergence in ancestral colubrines arose as a result of a selective regime that favored diets comprised of terrestrial prey, and that partitioning of different prey types led to the various forms of dietary specialization evident in these lineages today. Our findings provide new insights into the ecological correlates associated with the evolution of diet in snakes, thereby furthering our understanding of the driving forces behind patterns of snake diversification.

Yi, X., and E. K. Latch. 2022. Nuclear phylogeography reveals strong impacts of gene flow in big brown bats. Journal of Biogeography 49: 1061–1074.

Aim Understanding speciation mechanisms requires disentangling processes that promote and erode population-level divergence. Three hypotheses are raised that contemporary population structure is mainly shaped by refugial isolation, gene flow or both. Testing these hypotheses requires range-wide phylogeography and integrative analyses across scales. Here we aimed to (1) re-estimate the previously unresolved nuclear divergence within a widespread bat; (2) test the above three phylogeographical hypotheses and (3) inform conservation management under climatic change. Location North America including the Caribbean. Taxon The big brown bat (Eptesicus fuscus). Methods We collected range-wide samples and genome-wide markers using restriction site-associated DNA sequencing. Population structure was analysed by clustering methods and spatial estimations. Nuclear phylogeographical divergence was estimated using tree methods (concatenation and coalescence) and network analyses (TreeMix). Phylogeographical hypotheses were tested by comparing alternative evolutionary scenarios using demographic modelling. Species distribution modelling was used to help identify Pleistocene refugia and predict future range shifts under climatic change. Results We identified three populations in the Caribbean, eastern and western North America. The western population further split into three phylogeographical clades: Pacific, southwestern North America and Mexico. Discordance among mitochondrial and nuclear topologies reflected strong impacts of gene flow without sex bias. Demographic modelling supported scenarios of historical isolation followed by secondary gene flow and estimated Holocene divergence times. Species distribution was essentially continuous during glaciation with possible regional isolation, and northward range shifts were predicted under future climatic change. Main Conclusions Contemporary population divergence of big brown bats was shaped by both historical isolation and secondary gene flow, supporting the third phylogeographical hypothesis. While climatic change likely triggered initial divergence, ongoing gene flow has largely impacted the dynamic within-species evolution and generated population divergence without speciation.

Gainsbury, A. M., E. G. Santos, and H. Wiederhecker. 2022. Does urbanization impact terrestrial vertebrate ectotherms across a biodiversity hotspot? Science of The Total Environment 835: 155446.

Urbanization is increasing at an alarming rate altering biodiversity. As urban areas sprawl, it is vital to understand the effects of urbanization on biodiversity. Florida is ideal for this research; it has many reptile species and has experienced multiple anthropogenic impacts. Herein, we aim to evaluate human impacts on registered reptile richness across an urbanization gradient in Florida. The expectation is that highly urbanized areas would harbor a lower number of species. To represent urbanization, we used Venter et al. (2016) human footprint index. We downloaded georeferenced occurrence records from the Global Biodiversity Information Facility to collate species richness. We ran generalized linear regressions controlling for spatial autocorrelation structure to test the association between urbanization and reptile records across Florida. We found a positive association between urbanization and registered reptiles across Florida for total and non-native species richness; however, a lack of association occurred for native species. We performed rarefaction curves due to an inherent bias of citizen science data. The positive association was supported for non-native reptile species richness with greater species richness located at urban centers. Interestingly, total and native species richness were largest at low as well as moderate levels of urbanization. Thus, moderately urbanized areas may have the potential to harbor a similar number of reptile species compared to areas with low urbanization. Nevertheless, a difference exists in sample completeness between the urbanization categories. Thus, a more systematic monitoring of reptile species across an urbanization gradient, not only focusing on urban and wild areas but also including moderate levels of urbanization, is needed to provide informed conservation strategies for urban development planning. Advances in environmental sensors, environmental DNA, and citizen science outreach are necessary to implement if we are to effectively monitor biodiversity at the accelerated rate of urbanization.