Science Enabled by Specimen Data

Novoa, A., H. Hirsch, M. L. Castillo, S. Canavan, L. González, D. M. Richardson, P. Pyšek, et al. 2023. Genetic and morphological insights into the Carpobrotus hybrid complex around the world. NeoBiota 89: 135–160.

The genus Carpobrotus N.E.Br. comprises between 12 and 25 species, most of which are native to South Africa. Some Carpobrotus species are considered among the most damaging invasive species in coastal dune systems worldwide. In their introduced areas, these species represent a serious threat to native species and significantly impact soil conditions and geochemical processes. Despite being well studied, the taxonomy of Carpobrotus remains problematic, as the genus comprises a complex of species that hybridize easily and are difficult to distinguish from each other. To explore the population genetic structure of invasive Carpobrotus species (i.e., C. acinaciformis and C. edulis) across a significant part of their native and non-native ranges, we sampled 40 populations across Argentina, Italy, New Zealand, Portugal, South Africa, Spain, and the USA. We developed taxon-specific microsatellite markers using a Next Generation Sequencing approach to analyze the population genetic structure and incidence of hybridization in native and non-native regions. We identified three genetically distinct clusters, which are present in both the native and non-native regions. Based on a set of selected morphological characteristics, we found no clear features to identify taxa morphologically. Our results suggest that the most probable sources of global introductions of Carpobrotus species are the Western Cape region of South Africa and the coastline of California. We suggest that management actions targeting Carpobrotus invasions globally should focus on preventing additional introductions from the east coast of South Africa, and on searching for prospective biocontrol agents in the Western Cape region of South Africa.

ter Huurne, M. B., L. J. Potgieter, C. Botella, and D. M. Richardson. 2023. Melaleuca (Myrtaceae): Biogeography of an important genus of trees and shrubs in a changing world. South African Journal of Botany 162: 230–244.

The number of naturalised and invasive woody plant species has increased rapidly in recent decades. Despite the increasing interest in tree and shrub invasions, little is known about the invasion ecology of most species. This paper explores the global movement of species in the genus Melaleuca (Myrtaceae; here including the genus Callistemon). We assess the global introduction history, distribution and biogeographic status of the genus. Various global species occurrence databases, citizen science (iNaturalist), and the literature were used.Seventy-two species [out of 386 Melaleuca species; 19%] have been introduced to at least 125 regions outside their native range. The main regions of global Melaleuca introductions are Southeast Asia, the southern parts of North America, south-eastern South America, southern Africa and Europe. The earliest record of a Melaleuca species outside of the native range of the genus is 1789. First records of Melaleuca species outside their native range were most commonly recorded in the 1960s, with records from all over the world. The main reasons for Melaleuca introductions were for use in the tea tree (pharmaceutical value) and ornamental horticulture industries. Melaleuca introductions, naturalizations and invasions are recent compared to many other woody plant taxa. Experiences in Florida and South Africa highlight the potential of Melaleuca species to spread rapidly and have significant ecological impacts. It is likely that the accumulating invasion debt will result in further naturalization and invasion of Melaleuca species 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.

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.

Geier, C., J. M. Bouchal, S. Ulrich, D. Uhl, T. Wappler, S. Wedmann, R. Zetter, et al. 2023. Potential pollinators and paleoecological aspects of Eocene Ludwigia (Onagraceae) from Eckfeld, Germany. Palaeoworld.

Paleogene flower-insect interactions and paleo-pollination processes are, in general, poorly understood and fossil evidence for such floral and faunal interactions are rarely reported. To shed light on angiosperm flower-insect interactions, we investigated several hundred fossil flowers and insects from the middle Eocene Fossil Lagerstätte of Eckfeld, Germany. During our work, we discovered a unique fossil Ludwigia flower (bud) with in situ pollen. The ecological preferences (climate, biome, habitat, etc.) of extant Ludwigia and the paleoecological configurations of the fossil plant assemblage support the taxonomic affiliation of the flower bud and an Eocene presence of Ludwigia in the vicinity of the former Lake Eckfeld. Today’s Ludwigia are mostly pollinated by Hymenoptera (bees). Therefore, we screened all currently known hymenopteran fossils from Eckfeld but found no Ludwigia pollen adhering to any of the specimens. On the contrary, we discovered Ludwigia pollen adhering to two different groups of Coleoptera (beetles). Our study suggests that during the Eocene of Europe, Ludwigia flowers were visited and probably pollinated by beetles and over time there was a shift in primary flower visitors/pollinators, from beetles to bees, sometime during the late Paleogene to Neogene.

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.

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.

Wilf, P., and R. M. Kooyman. 2023. Do Southeast Asia’s paleo‐Antarctic trees cool the planet? New Phytologist.

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.

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.

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.

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.

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.

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.

Cosme, M. 2023. Mycorrhizas drive the evolution of plant adaptation to drought. Communications Biology 6.

Plant adaptation to drought facilitates major ecological transitions, and will likely play a vital role under looming climate change. Mycorrhizas, i.e. strategic associations between plant roots and soil-borne symbiotic fungi, can exert strong influence on the tolerance to drought of extant plants. Here, I show how mycorrhizal strategy and drought adaptation have been shaping one another throughout the course of plant evolution. To characterize the evolutions of both plant characters, I applied a phylogenetic comparative method using data of 1,638 extant species globally distributed. The detected correlated evolution unveiled gains and losses of drought tolerance occurring at faster rates in lineages with ecto- or ericoid mycorrhizas, which were on average about 15 and 300 times faster than in lineages with the arbuscular mycorrhizal and naked root (non-mycorrhizal alone or with facultatively arbuscular mycorrhizal) strategy, respectively. My study suggests that mycorrhizas can play a key facilitator role in the evolutionary processes of plant adaptation to critical changes in water availability across global climates. Phylogenetic comparative analysis using data of 1,638 species of angiosperms and gymnosperms suggests that the evolution of plant adaptation to critical environmental change in water availability across global climates is dependent on mycorrhizas.