Science Enabled by Specimen Data

Cousins-Westerberg, R., N. Dakin, L. Schat, G. Kadereit, and A. M. Humphreys. 2023. Evolution of cold tolerance in the highly stress-tolerant samphires and relatives (Salicornieae: Amaranthaceae). Botanical Journal of the Linnean Society. https://doi.org/10.1093/botlinnean/boad009

Low temperature constitutes one of the main barriers to plant distributions, confining many clades to their ancestrally tropical biome. However, recent evidence suggests that transitions from tropical to temperate biomes may be more frequent than previously thought. Here, we study the evolution of cold and frost tolerance in the globally distributed and highly stress-tolerant Salicornieae (Salicornioideae, Amaranthaceae s.l.). We first generate a phylogenetic tree comprising almost all known species (85-90%), using newly generated (n = 106) and published nuclear-ribosomal and plastid sequences. Next, we use geographical occurrence data to document in which clades and geographical regions cold-tolerant species occur and reconstruct how cold tolerance evolved. Finally, we test for correlated evolution between frost tolerance and the annual life form. We find that frost tolerance has evolved independently in up to four Northern Hemisphere lineages but that annuals are no more likely to evolve frost tolerance than perennials, indicating the presence of different strategies for adapting to cold environments. Our findings add to mounting evidence for multiple independent out-of-the-tropics transitions among close relatives of flowering plants and raise new questions about the ecological and physiological mechanism(s) of adaptation to low temperatures in Salicornieae.

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.

Velasco, N., N. Andrade, C. Smit, and R. Bustamante. 2023. Climatic niche convergence through space and time for a potential archaeophyte (Acacia caven) in South America. Scientific Reports 13. https://doi.org/10.1038/s41598-023-35658-8

AbstractBased on the niche conservatism hypothesis, i.e. the idea that niches remain unchanged over space and time, climatic niche modelling (CNM) is a useful tool for predicting the spread of introduced taxa. Recent advances have extended such predictions deeper in time for plant species dispersed by humans before the modern era. The latest CNMs successfully evaluate niche differentiation and estimate potential source areas for intriguing taxa such as archaeophytes (i.e., species introduced before 1492 AD). Here, we performed CNMs for Acacia caven, a common Fabaceae tree in South America, considered an archaeophyte west of the Andes, in Central Chile. Accounting for the infraspecific delimitation of the species, our results showed that even when climates are different, climatic spaces used by the species overlap largely between the eastern and western ranges. Despite slight variation, results were consistent when considering one, two, or even three-environmental dimensions, and in accordance with the niche conservatism hypothesis. Specific distribution models calibrated for each region (east vs west) and projected to the past, indicate a common area of occupancy available in southern Bolivia—northwest Argentina since the late Pleistocene, which could have acted as a source-area, and this signal becomes stronger through the Holocene. Then, in accordance with a taxon introduced in the past, and comparing regional vs continental distribution models calibrated at the infraspecific or species level, the western populations showed their spread status to be mostly in equilibrium with the environment. Our study thus indicates how niche and species distribution models are useful to improve our knowledge related to taxa introduced before the modern era.

Clemente, K. J. E., and M. S. Thomsen. 2023. High temperature frequently increases facilitation between aquatic foundation species: a global meta‐analysis of interaction experiments between angiosperms, seaweeds, and bivalves. Journal of Ecology. https://doi.org/10.1111/1365-2745.14101

Many studies have quantified ecological impacts of individual foundation species (FS). However, emerging data suggest that FS often co‐occur, potentially inhibiting or facilitating one another, thereby causing indirect, cascading effects on surrounding communities. Furthermore, global warming is accelerating, but little is known about how interactions between co‐occurring FS vary with temperature.Shallow aquatic sedimentary systems are often dominated by three types of FS: slower‐growing clonal angiosperms, faster‐growing solitary seaweeds, and shell‐forming filter‐ and deposit‐feeding bivalves. Here, we tested the impacts of one FS on another by analyzing manipulative interaction experiments from 148 papers with a global meta‐analysis.We calculated 1,942 (non‐independent) Hedges’ g effect sizes, from 11,652 extracted values over performance responses, such as abundances, growths or survival of FS, and their associated standard deviations and replication levels. Standard aggregation procedures generated 511 independent Hedges’ g that was classified into six types of reciprocal impacts between FS.We found that (i) seaweeds had consistent negative impacts on angiosperms across performance responses, organismal sizes, experimental approaches, and ecosystem types; (ii) angiosperms and bivalves generally had positive impacts on each other (e.g., positive effects of angiosperms on bivalves were consistent across organismal sizes and experimental approaches, but angiosperm effect on bivalve growth and bivalve effect on angiosperm abundance were not significant); (iii) bivalves positively affected seaweeds (particularly on growth responses); (iv) there were generally no net effects of seaweeds on bivalves (except for positive effect on growth) or angiosperms on seaweeds (except for positive effect on ‘other processes’); and (v) bivalve interactions with other FS were typically more positive at higher temperatures, but angiosperm‐seaweed interactions were not moderated by temperature.Synthesis: Despite variations in experimental and spatiotemporal conditions, the stronger positive interactions at higher temperatures suggest that facilitation, particularly involving bivalves, may become more important in a future warmer world. Importantly, addressing research gaps, such as the scarcity of FS interaction experiments from tropical and freshwater systems and for less studied species, as well as testing for density‐dependent effects, could better inform aquatic ecosystem conservation and restoration efforts and broaden our knowledge of FS interactions in the Anthropocene.

Jiménez-López, D. A., M. J. Carmona-Higuita, G. Mendieta-Leiva, R. Martínez-Camilo, A. Espejo-Serna, T. Krömer, N. Martínez-Meléndez, and N. Ramírez-Marcial. 2023. Linking different resources to recognize vascular epiphyte richness and distribution in a mountain system in southeastern Mexico. Flora: 152261. https://doi.org/10.1016/j.flora.2023.152261

Mesoamerican mountains are important centers of endemism and diversity of epiphytes. The Sierra Madre of Chiapas in southeastern Mexico is a mountainous region of great ecological interest due to its high biological richness. We present the first checklist of epiphytes for this region based on a compilation of various information sources. In addition, we determined the conservation status for each species based on the Mexican Official Standard (NOM-059-SEMARNAT-2010), endemism based on geopolitical boundaries, spatial completeness with inventory completeness index, richness distribution with range maps, and the relationship between climatic variables (temperature and rainfall) with species richness using generalized additive models. Our dataset includes 9,799 records collected between 1896-2017. Our checklist includes 708 epiphytes within 160 genera and 26 families; the most species-rich family was Orchidaceae (355 species), followed by Bromeliaceae (82) and Polypodiaceae (79). There were 74 species within a category of risk and 59 species considered endemic. Completeness of epiphyte richness suggests that sampling is still largely incomplete, particularly in the lower parts of the mountain system. Species and family range maps show the highest richness at high elevations, while geographically richness increases towards the southeast. Epiphyte richness increases with increased rainfall, although a unimodal pattern was observed along the temperature gradient with a species richness peak between 16-20 C°. The Sierra Madre of Chiapas forms a refuge to more than 40% of all epiphytes reported for Mexico and its existing network of protected areas overlaps with the greatest epiphyte richness.

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.

Jacquemyn, H., T. Pankhurst, P. S. Jones, R. Brys, and M. J. Hutchings. 2023. Biological Flora of Britain and Ireland: Liparis loeselii. Journal of Ecology. https://doi.org/10.1111/1365-2745.14086

This account presents information on all aspects of the biology of Liparis loeselii (L.) Rich. (Fen Orchid) that are relevant to understanding its ecological characteristics and behaviour. The main topics are presented within the standard framework of the Biological Flora of Britain and Ireland: distribution, habitat, communities, responses to biotic factors, responses to environment, structure and physiology, phenology, floral and seed characters, herbivores and disease, history and conservation.Liparis loeselii is a small terrestrial orchid that has a circumboreal distribution and is widespread in Europe and North America. Despite its wide distribution, the species is locally rare and has declined considerably in most of its range. In Britain, the species has a disjunct distribution and is now known to occur consistently at only six sites in eastern England and three in south Wales. It is absent from Ireland. Its most characteristic habitats in Britain are inland fens and coastal dune slacks, but outside Britain it can also be found in wet meadows, marshes, forested seep springs, at lake borders or on mats of floating peat.Populations of Liparis loeselii in dune slacks tend to be short‐lived, and can rapidly increase in size or decrease and disappear as environmental conditions change. The species does not tolerate high nutrient concentrations or low pH. It is susceptible to drought, which reduces seed germination, seedling recruitment and adult survival. Heavy predation by rabbits and rodents has been observed under drought conditions.Liparis loeselii reproduces both by sexual reproduction, and by vegetative propagation through the production of pseudobulbs. Although flowers are accessible to insects, entomophilous pollination is unusual, and most sexual reproduction is the result of selfing. Fruits ripen late in the growing season (mid‐October) and the dust‐like seeds are dispersed during winter by wind and water. Germination occurs during the following growing season and is supported by a wide variety of mycorrhizal fungi.Since the late 19th century Liparis loeselii has declined considerably in Britain and elsewhere in Europe, primarily due to habitat destruction and loss, natural succession, and habitat desiccation due to drainage. As a result, the species has been listed as endangered in the Bern Convention and the European Habitat Directive (92/43/EEC), and is the focus of intensive conservation efforts in many countries. Restoration of habitat by mowing, extensive grazing, peat removal, and the creation of new habitat by dune slack formation in dune systems and peat removal in fens may prolong population persistence and promote establishment of new populations.

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.

Wilson Brown, M. K., and E. B. Josephs. 2023. Evaluating niche changes during invasion with seasonal models in Capsella bursa‐pastoris. American Journal of Botany. https://doi.org/10.1002/ajb2.16140

Premise Researchers often use ecological niche models to predict where species might establish and persist under future or novel climate conditions. However, these predictive methods assume species have stable niches across time and space. Furthermore, ignoring the time of occurrence data can obscure important information about species reproduction and ultimately fitness. Here, we assess compare ecological niche models generated from full-year averages to seasonal models Methods In this study, we generate full-year and monthly ecological niche models for Capsella bursa-pastoris in Europe and North America to see if we can detect changes in the seasonal niche of the species after long-distance dispersal. Key Results We find full-year ecological niche models have low transferability across continents and there are continental differences in the climate conditions that influence the distribution of C. bursa-pastoris. Monthly models have greater predictive accuracy than full-year models in cooler seasons, but no monthly models are able to predict North American summer occurrences very well. Conclusions The relative predictive ability of European monthly models compared to North American monthly models suggests a change in the seasonal timing between the native range to the non-native range. These results highlight the utility of ecological niche models at finer temporal scales in predicting species distributions and unmasking subtle patterns of evolution.

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.