Science Enabled by Specimen Data

Anest, A., Y. Bouchenak-Khelladi, T. Charles-Dominique, F. Forest, Y. Caraglio, G. P. Hempson, O. Maurin, and K. W. Tomlinson. 2024. Blocking then stinging as a case of two-step evolution of defensive cage architectures in herbivore-driven ecosystems. Nature Plants. https://doi.org/10.1038/s41477-024-01649-4

Dense branching and spines are common features of plant species in ecosystems with high mammalian herbivory pressure. While dense branching and spines can inhibit herbivory independently, when combined, they form a powerful defensive cage architecture. However, how cage architecture evolved under mammalian pressure has remained unexplored. Here we show how dense branching and spines emerged during the age of mammalian radiation in the Combretaceae family and diversified in herbivore-driven ecosystems in the tropics. Phylogenetic comparative methods revealed that modern plant architectural strategies defending against large mammals evolved via a stepwise process. First, dense branching emerged under intermediate herbivory pressure, followed by the acquisition of spines that supported higher speciation rates under high herbivory pressure. Our study highlights the adaptive value of dense branching as part of a herbivore defence strategy and identifies large mammal herbivory as a major selective force shaping the whole plant architecture of woody plants. This study explores the evolution of two traits, branching density and spine presence, in the globally distributed plant family Combretaceae. These traits were found to have appeared in a two-step process in response to mammalian herbivory pressure, revealing the importance of large mammals in the evolution of plant architecture diversity.

Karimi, N., and M. M. Hanes. 2024. Patterns of Grewia (Malvaceae) diversity across geographic scales in Africa and Madagascar. Annals of Botany. https://doi.org/10.1093/aob/mcae009

Background and aims Quantifying spatial species richness is useful to describe biodiversity patterns across broad geographic areas, especially in large, poorly known plant groups. We explore patterns and predictors of species richness across Africa in one such group; the paleotropical genus Grewia L. (Malvaceae). Methods Grewia species richness was quantified by extracting herbarium records from GBIF and Tropicos and creating geographic grids at varying spatial scales. We assessed predictors of species richness using spatial regression models with 30 environmental variables. We explored species co-occurrence in Madagascar at finer resolutions using Schoener's index, and compared species’ range sizes and IUCN status among ecoregions. Lastly, we derived a trait matrix for a subset of species found in Madagascar to characterize morphological diversity across space. Key Results Grewia species occur in 50 countries in Africa, with the highest number of species in Madagascar (93, with 80 species endemic). Species richness is highest in Madagascar, with up to 23 Grewia species in a grid cell, followed by coastal Tanzania/Kenya (up to 13 species), and northern South Africa and central Angola (11 species each). Across Africa, higher species richness was predicted by variables related to aridity. In Madagascar, a greater range in environmental variables best predicted species richness, consistent with geographic grid cells of highest species richness occurring near biome/ecoregion transitions. In Madagascar we also observe increasing dissimilarity in species composition with increasing geographic distance. Conclusions The spatial patterns and underlying environmental predictors that we uncover in Grewia represent an important step in our understanding of plant distribution and diversity patterns across Africa. Madagascar boasts nearly twice the Grewia species richness, compared to the second most species-rich country in Africa, which might be explained by complex topography and environmental conditions across small spatial scales.

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. https://doi.org/10.3897/neobiota.89.109164

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.

Ngarega, B. K., P. Chaibva, V. F. Masocha, J. K. Saina, P. K. Khine, and H. Schneider. 2023. Application of MaxEnt modeling to evaluate the climate change effects on the geographic distribution of Lippia javanica (Burm.f.) Spreng in Africa. Environmental Monitoring and Assessment 196. https://doi.org/10.1007/s10661-023-12232-3

Lippia javanica is a typical indigenous plant species mostly found in the higher elevation or mountainous regions in southern, central, and eastern Africa. The ongoing utilization of the species for ethnobotanical applications and traditional uses, coupled with the changing climate, increases the risk of a potential reduction in its geographic distribution range in the region. Herein, we utilized the MaxEnt species distribution modelling to build the L. javanica distribution models in tropical and subtropical African regions for current and future climates. The MaxEnt models were calibrated and fitted using 286 occurrence records and six environmental variables. Temperatures, including temperature seasonality [Bio 4] and the maximum temperature of the warmest month [Bio 5], were observed to be the most significant determinants of L. javanica’s distribution. The current projected range for L. javanica was estimated to be 2,118,457 km 2 . Future model predictions indicated that L. javanica may increase its geographic distribution in western areas of the continent and regions around the equator; however, much of the geographic range in southern Africa may shift southwards, causing the species to lose portions of the northern limits of the habitat range. These current findings can help increase the conservation of L. javanica and other species and combat localized species loss induced by climate change and human pressure. We also emphasize the importance of more investigations and enhanced surveillance of traditionally used plant species in regions that are acutely susceptible to climate change.

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. https://doi.org/10.1016/j.sajb.2023.08.052

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.

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.

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.

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.

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.