Science Enabled by Specimen Data

Short, A. W., J. S. V. Sebastian, J. Huang, G. Wang, M. Dassanayake, P. M. Finnegan, J. D. Parker, et al. 2024. Comparative transcriptomics of the chilling stress response in two Asian mangrove species Bruguiera gymnorhiza and Rhizophora apiculata. Tree Physiology. https://doi.org/10.1093/treephys/tpae019

Abstract Low temperatures largely determine the geographic limits of plant species by reducing survival and growth. Interspecific differences in the geographic distribution of mangrove species have been associated with cold tolerance, with exclusively tropical species being highly cold-sensitive and subtropical species being relatively cold-tolerant. To identify species-specific adaptations to low temperatures, we compared the chilling stress response of two widespread Indo-West Pacific mangrove species from Rhizophoraceae with differing latitudinal range limits—Bruguiera gymnorhiza (subtropical range limit) and Rhizophora apiculata (tropical range limit). For both species, we measured the maximum photochemical efficiency of photosystem II (Fv/Fm) as a proxy for the physiological condition of the plants and examined gene expression profiles during chilling at 15 °C and 5 °C. At 15 °C, B. gymnorhiza maintained a significantly higher Fv/Fm than R. apiculata. However, at 5 °C, both species displayed equivalent Fv/Fm values. Thus, species-specific differences in chilling tolerance were only found at 15 °C, and both species were sensitive to chilling at 5 °C. At 15 °C, B. gymnorhiza down-regulated genes related to the light reactions of photosynthesis and up-regulated a gene involved in cyclic electron flow regulation, while R. apiculata down-regulated more RuBisCo related genes. At 5 °C, both species repressed genes related to CO2 assimilation. The down-regulation of genes related to light absorption and up-regulation of genes related to cyclic electron flow regulation are photoprotective mechanisms that likely contributed to the greater PSII photochecmical efficiency of B. gymnorhiza at 15 °C. The results of this study provide evidence that the distributional range limits and potentially the expansion rates of plant species are associated with differences in the regulation of photosynthesis and photoprotective mechanisms under low temperatures.

Rocha, J., P. J. Nunes, A. Pinto, L. Fenina, A. L. Afonso, A. R. Seixas, R. Cruz, et al. 2024. Ecological adaptation of Australian Myrtaceae through the leaf waxes analysis: Corymbia citriodora, Eucalyptus gunnii, and Eucalyptus globulus. Flora 310: 152435. https://doi.org/10.1016/j.flora.2023.152435

Seeking to get insight into the close relationship between plant waxes and the climatic conditions of plants’ original biomes, the leaves of three Myrtaceae from the eastern Australian-Tasmanian region (Corymbia citriodora (Hook.) K.D.Hill & L.A.S.Johnson (lemon-scented gum), Eucalyptus gunnii Hook. (cider gum), and Eucalyptus globulus Labill. (blue gum)) were selected. The present study relied on the analysis of juvenile leaf samples of the three species collected at the Botanical Garden of the University of Trás-os-Montes e Alto Douro (Portugal) during the driest and warmest period of the year (July), to ensure the same environmental conditions as the Australian species from December to February, for cider gum and blue gum, and from June to September, for lemon-scented gum. Both surfaces of the leaves of the three Myrtaceae species exhibit superhydrophobic behavior. They are covered with wax tubules, but these are thicker and the surface is smoother in the case of cider gum. From the chemical standpoint, the leaf waxes of the three species revealed a prevalence of β-diketones and sterols over alcohols, alkanes, and esters. The relative ketone/sterol concentration ratio demonstrated an environmental dynamic variation with climate, i.e., with the ombrothermic regimes. The highest concentration of β-diketone and the lowest concentration of sterols was observed for species from dryer conditions (lemon-scented gum), whereas the reverse trend was found for species from wetter conditions (cider gum and blue gum).The present work strongly suggests that the chemical composition of leaf waxes, rather than wettability, seems to be directly correlated with environmental variability at the species’ natural site. The methodology proposed here opens exciting new prospects for the investigation of the environmental dynamics of terrestrial plants.

Li, Y., F. Ding, M. Hao, S. Chen, D. Jiang, P. Fan, Y. Qian, et al. 2023. The implications for potential marginal land resources of cassava across worldwide under climate change challenges. Scientific Reports 13. https://doi.org/10.1038/s41598-023-42132-y

The demand for energy plants is foreseen to grow as worldwide energy and climate policies promote the use of bioenergy for climate change mitigation. To avoid competing with food production, it’s critical to assess future changes in marginal land availability for energy plant development. Using a machine learning method, boosted regression tree, this study modeled potential marginal land resources suitable for cassava under current and different climate change scenarios, based on cassava occurrence records and environmental covariates. The findings revealed that, currently, over 80% of the 1357.24 Mha of available marginal land for cassava cultivation is distributed in Africa and South America. Under three climate change scenarios, by 2030, worldwide suitable marginal land resources were predicted to grow by 39.71Mha, 66.21 Mha, and 39.31Mha for the RCP4.5, RCP6.0, and RCP8.5 scenarios, respectively; by 2050, the potential marginal land suitable for cassava will increase by 38.98Mha, 83.02 Mha, and 55.43Mha, respectively; by 2080, the global marginal land resources were estimated to rise by 40.82 Mha, 99.74 Mha, and 21.87 Mha from now, respectively. Our results highlight the impacts of climate change on potential marginal land resources of cassava across worldwide, which provide the basis for assessing bioenergy potential in the future.

Rodríguez-Merino, A. 2023. Identifying and Managing Areas under Threat in the Iberian Peninsula: An Invasion Risk Atlas for Non-Native Aquatic Plant Species as a Potential Tool. Plants 12: 3069. https://doi.org/10.3390/plants12173069

Predicting the likelihood that non-native species will be introduced into new areas remains one of conservation’s greatest challenges and, consequently, it is necessary to adopt adequate management measures to mitigate the effects of future biological invasions. At present, not much information is available on the areas in which non-native aquatic plant species could establish themselves in the Iberian Peninsula. Species distribution models were used to predict the potential invasion risk of (1) non-native aquatic plant species already established in the peninsula (32 species) and (2) those with the potential to invade the peninsula (40 species). The results revealed that the Iberian Peninsula contains a number of areas capable of hosting non-native aquatic plant species. Areas under anthropogenic pressure are at the greatest risk of invasion, and the variable most related to invasion risk is temperature. The results of this work were used to create the Invasion Risk Atlas for Alien Aquatic Plants in the Iberian Peninsula, a novel online resource that provides information about the potential distribution of non-native aquatic plant species. The atlas and this article are intended to serve as reference tools for the development of public policies, management regimes, and control strategies aimed at the prevention, mitigation, and eradication of non-native aquatic plant species.

Maurin, O., A. Anest, F. Forest, I. Turner, R. L. Barrett, R. C. Cowan, L. Wang, et al. 2023. Drift in the tropics: Phylogenetics and biogeographical patterns in Combretaceae. Global Ecology and Biogeography. https://doi.org/10.1111/geb.13737

Aim The aim of this study was to further advance our understanding of the species-rich, and ecologically important angiosperm family Combretaceae to provide new insights into their evolutionary history. We assessed phylogenetic relationships in the family using target capture data and produced a dated phylogenetic tree to assess fruit dispersal modes and patterns of distribution. Location Tropical and subtropical regions. Time Period Cretaceous to present. Major Taxa Studied Family Combretaceae is a member of the rosid clade and comprises 10 genera and more than 500 species, predominantly assigned to genera Combretum and Terminalia, and occurring on all continents and in a wide range of ecosystems. Methods We use a target capture approach and the Angiosperms353 universal probes to reconstruct a robust dated phylogenetic tree for the family. This phylogenetic framework, combined with seed dispersal traits, biome data and biogeographic ranges, allows the reconstruction of the biogeographical history of the group. Results Ancestral range reconstructions suggest a Gondwanan origin (Africa/South America), with several intercontinental dispersals within the family and few transitions between biomes. Relative abundance of fruit dispersal types differed by both continent and biome. However, intercontinental colonizations were only significantly enhanced by water dispersal (drift fruit), and there was no evidence that seed dispersal modes influenced biome shifts. Main Conclusions Our analysis reveals a paradox as drift fruit greatly enhanced dispersal distances at intercontinental scale but did not affect the strong biome conservatism observed.

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.

Pang, S. E. H., J. W. F. Slik, D. Zurell, and E. L. Webb. 2023. The clustering of spatially associated species unravels patterns in tropical tree species distributions. Ecosphere 14. https://doi.org/10.1002/ecs2.4589

Complex distribution data can be summarized by grouping species with similar or overlapping distributions to unravel spatial patterns and separate trends (e.g., of habitat loss) among spatially unique groups. However, such classifications are often heuristic, lacking the transparency, objectivity, and data‐driven rigor of quantitative methods, which limits their interpretability and utility. Here, we develop and illustrate the clustering of spatially associated species, a methodological framework aimed at statistically classifying species using explicit measures of interspecific spatial association. We investigate several association indices and clustering algorithms and show how these methodological choices drive substantial variations in clustering outcomes and performance. To facilitate robust decision‐making, we provide guidance on choosing methods appropriate to one's study objective(s). As a case study, we apply our framework to modeled tree distributions in Borneo and subsequently evaluate the impact of land‐cover change on separate species groupings. Based on the modeled distribution of 390 tree species prior to anthropogenic land‐cover changes, we identified 11 distinct clusters that unraveled ecologically meaningful patterns in Bornean tree distributions. These clusters then enabled us to quantify trends of habitat loss tied to each of those specific clusters, allowing us to discern particularly vulnerable species clusters and their distributions. This study demonstrates the advantages of adopting quantitatively derived clusters of spatially associated species and elucidates the potential of resultant clusters as a spatially explicit framework for investigating distribution‐related questions in ecology, biogeography, and conservation. By adopting our methodological framework and publicly available codes, practitioners can leverage the ever‐growing abundance of distribution data to better understand complex spatial patterns among species distributions and the disparate effects of global changes on biodiversity.

Richard-Bollans, A., C. Aitken, A. Antonelli, C. Bitencourt, D. Goyder, E. Lucas, I. Ondo, et al. 2023. Machine learning enhances prediction of plants as potential sources of antimalarials. Frontiers in Plant Science 14. https://doi.org/10.3389/fpls.2023.1173328

Plants are a rich source of bioactive compounds and a number of plant-derived antiplasmodial compounds have been developed into pharmaceutical drugs for the prevention and treatment of malaria, a major public health challenge. However, identifying plants with antiplasmodial potential can be time-consuming and costly. One approach for selecting plants to investigate is based on ethnobotanical knowledge which, though having provided some major successes, is restricted to a relatively small group of plant species. Machine learning, incorporating ethnobotanical and plant trait data, provides a promising approach to improve the identification of antiplasmodial plants and accelerate the search for new plant-derived antiplasmodial compounds. In this paper we present a novel dataset on antiplasmodial activity for three flowering plant families – Apocynaceae, Loganiaceae and Rubiaceae (together comprising c. 21,100 species) – and demonstrate the ability of machine learning algorithms to predict the antiplasmodial potential of plant species. We evaluate the predictive capability of a variety of algorithms – Support Vector Machines, Logistic Regression, Gradient Boosted Trees and Bayesian Neural Networks – and compare these to two ethnobotanical selection approaches – based on usage as an antimalarial and general usage as a medicine. We evaluate the approaches using the given data and when the given samples are reweighted to correct for sampling biases. In both evaluation settings each of the machine learning models have a higher precision than the ethnobotanical approaches. In the bias-corrected scenario, the Support Vector classifier performs best – attaining a mean precision of 0.67 compared to the best performing ethnobotanical approach with a mean precision of 0.46. We also use the bias correction method and the Support Vector classifier to estimate the potential of plants to provide novel antiplasmodial compounds. We estimate that 7677 species in Apocynaceae, Loganiaceae and Rubiaceae warrant further investigation and that at least 1300 active antiplasmodial species are highly unlikely to be investigated by conventional approaches. While traditional and Indigenous knowledge remains vital to our understanding of people-plant relationships and an invaluable source of information, these results indicate a vast and relatively untapped source in the search for new plant-derived antiplasmodial compounds.

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.

Reichgelt, T., A. Baumgartner, R. Feng, and D. A. Willard. 2023. Poleward amplification, seasonal rainfall and forest heterogeneity in the Miocene of the eastern USA. Global and Planetary Change 222: 104073. https://doi.org/10.1016/j.gloplacha.2023.104073

Paleoclimate reconstructions can provide a window into the environmental conditions in Earth history when atmospheric carbon dioxide concentrations were higher than today. In the eastern USA, paleoclimate reconstructions are sparse, because terrestrial sedimentary deposits are rare. Despite this, the eastern USA has the largest population and population density in North America, and understanding the effects of current and future climate change is of vital importance. Here, we provide terrestrial paleoclimate reconstructions of the eastern USA from Miocene fossil floras. Additionally, we compare proxy paleoclimate reconstructions from the warmest period in the Miocene, the Miocene Climatic Optimum (MCO), to those of an MCO Earth System Model. Reconstructed Miocene temperatures and precipitation north of 35°N are higher than modern. In contrast, south of 35°N, temperatures and precipitation are similar to today, suggesting a poleward amplification effect in eastern North America. Reconstructed Miocene rainfall seasonality was predominantly higher than modern, regardless of latitude, indicating greater variability in intra-annual moisture transport. Reconstructed climates are almost uniformly in the temperate seasonal forest biome, but heterogeneity of specific forest types is evident. Reconstructed Miocene terrestrial temperatures from the eastern USA are lower than modeled temperatures and coeval Atlantic sea surface temperatures. However, reconstructed rainfall is consistent with modeled rainfall. Our results show that during the Miocene, climate was most different from modern in the northeastern states, and may suggest a drastic reduction in the meridional temperature gradient along the North American east coast compared to today.