Science Enabled by Specimen Data

McCulloch-Jones, E. J., T. Kraaij, N. Crouch, and K. T. Faulkner. 2023. Assessing the invasion risk of traded alien ferns using species distribution models. NeoBiota 87: 161–189. https://doi.org/10.3897/neobiota.87.101104

Risk analysis plays a crucial role in regulating and managing alien and invasive species but can be time-consuming and costly. Alternatively, combining invasion and impact history with species distribution models offers a cost-effective and time-efficient approach to assess invasion risk and identify species for which a comprehensive risk analysis should take precedence. We conducted such an assessment for six traded alien fern species, determining their invasion risk in countries where they are traded. Four of the species (Dicksonia antarctica, Dryopteris erythrosora, Lygodium japonicum, and Phlebodium aureum) showed limited global distributions, while Adiantum raddianum and Sphaeropteris cooperi had broader distributions. A. raddianum, however, was the only species found to pose a high invasion risk in two known trade countries – the USA and Australia – and requires a complete risk analysis to determine the appropriate regulatory responses. Dicksonia antarctica, Phlebodium aureum (for New Zealand), and Dryopteris erythrosora (for the USA) posed a medium risk of invasion due to the lack of evidence of impacts, and a complete risk analysis is thus deemed less crucial for these species in these countries. For other species, suitable environments were not predicted in the countries where they are traded, thus the risk of invasion is low, and a complete risk analysis is not required. For species in countries where suitable environments are predicted but no trade information or presence data are available, risk assessments are recommended to better determine the risk posed. Despite the relatively limited potential global distribution of the studied ferns relative to other major plant invaders (e.g., Pinus spp. and Acacia spp.), their history of invasion, documented impacts in pristine environments, and high propagule pressure from trade warrants concern, possibly necessitating legislative and regulatory measures in environmentally suitable regions.

Andersen, J. C., and J. S. Elkinton. 2023. Climate suitability analyses compare the distributions of invasive knotweeds in Europe and North America with the source localities of their introduced biological control agents. Ecology and Evolution 13. https://doi.org/10.1002/ece3.10494

Climate suitability analyses based on ecological niche modeling provide a powerful tool for biological control practitioners to assess the likelihood of establishment of different candidate agents prior to their introduction in the field. These same analyses could also be performed to understand why some agents establish more easily than others. The release of three strains of Aphalara itadori (Shinji) (Hemiptera: Pysllidae), each from a different source locality in Japan, for the biological control of invasive knotweed species, Reynoutria spp. Houtt. (Caryophyllales: Polygonaceae), provides an important opportunity to compare the utility of climate suitability analyses for identifying potential climate‐based limitations for successful biological control introductions. Here, we predict climate suitability envelopes for three target species of knotweed in Europe and two target species of knotweed in North America and compare these suitability estimates for each of these species to the source localities of each A. itadori strain. We find that source locality of one strain, the Kyushu strain, has little‐to‐no suitability compared to other locations in Japan based on knotweed records from Europe, supporting an earlier study based on North American Japanese knotweed records. The source locality of a second strain, the Murakami strain, was predicted to have medium‐to‐high suitability based on records of knotweeds from North America. In contrast, European records of Reynoutria × bohemica Chrtek & Chrtková and Reynoutria sachalinensis (F. Schmidt) Nakai predicted no suitability for this locality compared to other locations in Japan, while European records for Reynoutria japonica Houtt. predicted low suitability. The source locality of the final strain, the Hokkaido strain, was predicted as having medium‐to‐high suitability based on knotweed records of all examined species from both North America and Europe.

Graham, C. D. K., E. J. Forrestel, A. L. Schilmiller, A. T. Zemenick, and M. G. Weber. 2023. Evolutionary signatures of a trade-off in direct and indirect defenses across the wild grape genus Vitis. Evolution. https://doi.org/10.1093/evolut/qpad140

Evolutionary correlations between chemical defense and protection by mutualist bodyguards have been long predicted, but tests of these pattern remain rare. We use a phylogenetic framework to test for evolutionary correlations indicative of trade-offs or synergisms between direct defense in the form of plant secondary metabolism, and indirect defense in the form of leaf domatia, across 33 species in the wild grape genus, Vitis. We also performed a bioassay with a generalist herbivore to associate our chemical phenotypes with herbivore palatability. Finally, we tested whether defensive traits correlate with the average abiotic characteristics of each species’ contemporary range and whether these correlations were consistent with plant defense theory. We found a negative evolutionary correlation between domatia size and the diversity of secondary metabolites in Vitis leaf tissue across the genus, and also that leaves with a higher diversity and richness of secondary metabolites were less palatable to a generalist herbivore, consistent with a trade-off in chemical and mutualistic defense investment. Predictions from plant defense theory were not supported by associations between investment in defense phenotypes and abiotic variables. Our work demonstrates an evolutionary pattern indicative of a trade-off between indirect and direct defense strategies across the Vitis genus.

Hill, A., M. F. T. Jiménez, N. Chazot, C. Cássia‐Silva, S. Faurby, L. Herrera‐Alsina, and C. D. Bacon. 2023. Apparent effect of range size and fruit colour on palm diversification may be spurious. Journal of Biogeography. https://doi.org/10.1111/jbi.14683

Aim Fruit selection by animal dispersers with different mobility directly impacts plant geographical range size, which, in turn, may impact plant diversification. Here, we examine the interaction between fruit colour, range size and diversification rate in palms by testing two hypotheses: (1) species with fruit colours attractive to birds have larger range sizes due to high dispersal ability and (2) disperser mobility affects whether small or large range size has higher diversification, and intermediate range size is expected to lead to the highest diversification rate regardless of disperser. Location Global. Time Period Contemporary (or present). Major Taxa Studied Palms (Arecaceae). Methods Palm species were grouped based on likely animal disperser group for given fruit colours. Range sizes were estimated by constructing alpha convex hull polygons from distribution data. We examined disperser group, range size or an interaction of both as possible drivers of change in diversification rate over time in a likelihood dynamic model (Several Examined State-dependent Speciation and Extinction [SecSSE]). Models were fitted, rate estimates were retrieved and likelihoods were compared to those of appropriate null models. Results Species with fruit colours associated with mammal dispersal had larger ranges than those with colours associated with bird dispersal. The best fitting SecSSE models indicated that the examined traits were not the primary driver of the heterogeneity in diversification rates in the model. Extinction rate complexity had a marked impact on model performance and on diversification rates. Main Conclusions Two traits related to dispersal mobility, range size and fruit colour, were not identified as the main drivers of diversification in palms. Increased model extinction rate complexity led to better performing models, which indicates that net diversification should be estimated rather than speciation alone. However, increased complexity may lead to incorrect SecSSE model conclusions without careful consideration. Finally, we find palms with more mobile dispersers do not have larger range sizes, meaning other factors are more important determinants of range size.

Wilf, P., and R. M. Kooyman. 2023. Do Southeast Asia’s paleo‐Antarctic trees cool the planet? New Phytologist. https://doi.org/10.1111/nph.19067

Many tree genera in the Malesian uplands have Southern Hemisphere origins, often supported by austral fossil records. Weathering the vast bedrock exposures in the everwet Malesian tropics may have consumed sufficient atmospheric CO2 to contribute significantly to global cooling over the past 15 Myr. However, there has been no discussion of how the distinctive regional tree assemblages may have enhanced weathering and contributed to this process. We postulate that Gondwanan‐sourced tree lineages that can dominate higher‐elevation forests played an overlooked role in the Neogene CO2 drawdown that led to the Ice Ages and the current, now‐precarious climate state. Moreover, several historically abundant conifers in Araucariaceae and Podocarpaceae are likely to have made an outsized contribution through soil acidification that increases weathering. If the widespread destruction of Malesian lowland forests continues to spread into the uplands, the losses will threaten unique austral plant assemblages and, if our hypothesis is correct, a carbon sequestration engine that could contribute to cooler planetary conditions far into the future. Immediate effects include the spread of heat islands, significant losses of biomass carbon and forest‐dependent biodiversity, erosion of watershed values, and the destruction of tens of millions of years of evolutionary history.

Robin-Champigneul, F., J. Gravendyck, H. Huang, A. Woutersen, D. Pocknall, N. Meijer, G. Dupont-Nivet, et al. 2023. Northward expansion of the southern-temperate podocarp forest during the Early Eocene Climatic Optimum: Palynological evidence from the NE Tibetan Plateau (China). Review of Palaeobotany and Palynology: 104914. https://doi.org/10.1016/j.revpalbo.2023.104914

The debated vegetation response to climate change can be investigated through palynological fossil records from past extreme climate conditions. In this context, the early Eocene (53.3 to 41.2 million years ago (Ma)) is often referred to as a model for a greenhouse Earth. In the Xining Basin, situated on the North-eastern Tibetan Plateau (NETP), this time interval is represented by an extensive and well-dated sedimentary sequence of evaporites and red mudstones. Here we focus on the palynological record of the Early Eocene Climatic Optimum (EECO; 53.3 to 49.1 Ma) and study the fossil gymnosperm pollen composition in these sediments. In addition, we also investigate the nearest living relatives (NLR) or botanical affinity of these genera and the paleobiogeographic implications of their occurrence in the Eocene of the NETP. To reach our objective, we complemented transmitted light microscopy with laser scanning- and electron microscopy techniques, to produce high-resolution images, and illustrate the morphological variation within fossil and extant gymnosperm pollen. Furthermore, a morphometric analysis was carried out to investigate the infra- and intrageneric variation of these and related taxa. To place the data in context we produced paleobiogeographic maps for Phyllocladidites and for other Podocarpaceae, based on data from a global fossil pollen data base, and compare these with modern records from GBIF. We also assessed the climatic envelope of the NLR. Our analyses confirm the presence of Phyllocladidites (NLR Phyllocladus, Podocarpaceae) and Podocarpidites (NLR Podocarpus, Podocarpaceae) in the EECO deposits in the Xining Basin. In addition, a comparative study based on literature suggests that Parcisporites is likely a younger synonym of Phyllocladidites. Our findings further suggest that the Phyllocladidites specimens are derived from a lineage that was much more diverse than previously thought, and which had a much larger biogeographical distribution during the EECO than at present. Based on the climatic envelope of the NLR, we suggest that the paleoclimatic conditions in the Xining Basin were warmer and more humid during the EECO. We conclude that phylloclade-type conifers typical of the southern-temperate podocarp forests, had a northward geographical expansion during the EECO, followed by extirpation.

Huang, T., J. Chen, K. E. Hummer, L. A. Alice, W. Wang, Y. He, S. Yu, et al. 2023. Phylogeny of Rubus (Rosaceae): Integrating molecular and morphological evidence into an infrageneric revision. TAXON. https://doi.org/10.1002/tax.12885

Rubus (Rosaceae), one of the most complicated angiosperm genera, contains about 863 species, and is notorious for its taxonomic difficulty. The most recent (1910–1914) global taxonomic treatment of the genus was conducted by Focke, who defined 12 subgenera. Phylogenetic results over the past 25 years suggest that Focke's subdivisions of Rubus are not monophyletic, and large‐scale taxonomic revisions are necessary. Our objective was to provide a comprehensive phylogenetic analysis of the genus based on an integrative evidence approach. Morphological characters, obtained from our own investigation of living plants and examination of herbarium specimens are combined with chloroplast genomic data. Our dataset comprised 196 accessions representing 145 Rubus species (including cultivars and hybrids) and all of Focke's subgenera, including 60 endemic Chinese species. Maximum likelihood analyses inferred phylogenetic relationships. Our analyses concur with previous molecular studies, but with modifications. Our data strongly support the reclassification of several subgenera within Rubus. Our molecular analyses agree with others that only R. subg. Anoplobatus forms a monophyletic group. Other subgenera are para‐ or polyphyletic. We suggest a revised subgeneric framework to accommodate monophyletic groups. Character evolution is reconstructed, and diagnostic morphological characters for different clades are identified and discussed. Based on morphological and molecular evidence, we propose a new classification system with 10 subgenera: R. subg. Anoplobatus, R. subg. Batothamnus, R. subg. Chamaerubus, R. subg. Cylactis, R. subg. Dalibarda, R. subg. Idaeobatus, R. subg. Lineati, R. subg. Malachobatus, R. subg. Melanobatus, and R. subg. Rubus. The revised infrageneric nomenclature inferred from our analyses is provided along with synonymy and type citations. Our new taxonomic backbone is the first systematic and complete global revision of Rubus since Focke's treatment. It offers new insights into deep phylogenetic relationships of Rubus and has important theoretical and practical significance for the development and utilization of these important agronomic crops.

Ecke, F., B. A. Han, B. Hörnfeldt, H. Khalil, M. Magnusson, N. J. Singh, and R. S. Ostfeld. 2022. Population fluctuations and synanthropy explain transmission risk in rodent-borne zoonoses. Nature Communications 13. https://doi.org/10.1038/s41467-022-35273-7

Population fluctuations are widespread across the animal kingdom, especially in the order Rodentia, which includes many globally important reservoir species for zoonotic pathogens. The implications of these fluctuations for zoonotic spillover remain poorly understood. Here, we report a global empirical analysis of data describing the linkages between habitat use, population fluctuations and zoonotic reservoir status in rodents. Our quantitative synthesis is based on data collated from papers and databases. We show that the magnitude of population fluctuations combined with species’ synanthropy and degree of human exploitation together distinguish most rodent reservoirs at a global scale, a result that was consistent across all pathogen types and pathogen transmission modes. Our spatial analyses identified hotspots of high transmission risk, including regions where reservoir species dominate the rodent community. Beyond rodents, these generalities inform our understanding of how natural and anthropogenic factors interact to increase the risk of zoonotic spillover in a rapidly changing world. Many rodent species are known as hosts of zoonotic pathogens, but the ecological conditions that trigger spillover are not well-understood. Here, the authors show that population fluctuations and association with human-dominated habitats explain the zoonotic reservoir status of rodents globally.

Campbell, L. C. E., E. T. Kiers, and G. Chomicki. 2022. The evolution of plant cultivation by ants. Trends in Plant Science. https://doi.org/10.1016/j.tplants.2022.09.005

Outside humans, true agriculture was previously thought to be restricted to social insects farming fungus. However, obligate farming of plants by ants was recently discovered in Fiji, prompting a re-examination of plant cultivation by ants. Here, we generate a database of plant cultivation by ants, identify three main types, and show that these interactions evolved primarily for shelter rather than food. We find that plant cultivation evolved at least 65 times independently for crops (~200 plant species), and 15 times in farmer lineages (~37 ant taxa) in the Neotropics and Asia/Australasia. Because of their high evolutionary replication, and variation in partner dependence, these systems are powerful models to unveil the steps in the evolution and ecology of insect agriculture.

Zhang, X., X. Ci, J. Hu, Y. Bai, A. H. Thornhill, J. G. Conran, and J. Li. 2022. Riparian areas as a conservation priority under climate change. Science of The Total Environment: 159879. https://doi.org/10.1016/j.scitotenv.2022.159879

Identifying climatic refugia is important for long-term conservation planning under climate change. Riparian areas have the potential to provide climatic refugia for wildlife, but literature remains limited, especially for plants. This study was conducted with the purpose of identifying climatic refugia of plant biodiversity in the portion of the Mekong River Basin located in Xishuangbanna, China. We first predicted the current and future (2050s and 2070s) potential distribution of 50 threatened woody species in Xishuangbanna by using an ensemble of small models, then stacked the predictions for individual species to derive spatial biodiversity patterns within each 10 × 10 km grid cell. We then identified the top 17 % of the areas for spatial biodiversity patterns as biodiversity hotspots, with climatic refugia defined as areas that remained as biodiversity hotspots over time. Stepwise regression and linear correlation were applied to analyze the environmental correlations with spatial biodiversity patterns and the relationships between climatic refugia and river distribution, respectively. Our results showed potential upward and northward shifts in threatened woody species, with range contractions and expansions predicted. The spatial biodiversity patterns shift from southeast to northwest, and were influenced by temperature, precipitation, and elevation heterogeneity. Climatic refugia under climate change were related closely to river distribution in Xishuangbanna, with riparian areas identified that could provide climatic refugia. These refugial zones are recommended as priority conservation areas for mitigating the impacts of climate change on biodiversity. Our study confirmed that riparian areas could act as climatic refugia for plants and emphasizes the conservation prioritization of riparian areas within river basins for protecting biodiversity under climate change.