Science Enabled by Specimen Data

Issaly, E. A., M. C. Baranzelli, N. Rocamundi, A. M. Ferreiro, L. A. Johnson, A. N. Sérsic, and V. Paiaro. 2023. Too much water under the bridge: unraveling the worldwide invasion of the tree tobacco through genetic and ecological approaches. Biological Invasions. https://doi.org/10.1007/s10530-023-03189-y

Understanding how, and from where, invasive species were introduced is critical for revealing the invasive mechanism, explaining the invasion success, and providing crucial insights for effective management. Here, we combined a phylogeographic approach with ecological niche modeling comparisons to elucidate the introduction mode and source of Nicotiana glauca , a native South American species that is now invasive worldwide. We tested three different scenarios based on the invasion source—random native, restricted native, and bridgehead invasive—considering genetic diversity and climatic niche comparisons among native and invaded areas. We found three genetic lineages geographically and climatically differentiated within the native range. Only one of these genetic groups contained the invasive haplotypes, but showed no climatic niche overlap with any invaded area. Conversely, one invaded area located in western South America, with more genetic diversity than other invaded areas but less than the native range, showed climatic niche overlap with almost all other invaded areas worldwide. These findings indicate that N. glauca first likely invaded the southernmost areas beyond its native range, forming a bridgehead invasive source, from which the species subsequently invaded other regions around the world. Invasiveness would have been fostered by changes in the environmental preferences of the species in the bridgehead area, towards drier, colder and less seasonal climates, becoming the actual source of invasion to areas climatically similar throughout the world. The fine scale resolution analyses combining genetic and climatic approaches within the native range were essential to illuminating the introduction scenario of this invasive species.

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.

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.

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. https://doi.org/10.1016/j.palwor.2023.07.003

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.

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.

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.

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.

Silva, C. P., D. N. López, P. I. Naulin, and S. A. Estay. 2023. Can suitability indices predict plant growth in the invaded range? The case of Acacias species. Frontiers in Plant Science 14. https://doi.org/10.3389/fpls.2023.1125019

IntroductionForestry in many parts of the world depends on exotic species, making this industry a source of invasions in some countries. Among others, plantations of the genus Pinus, Eucalyptus, Acacia, Populus, and Pseudotsuga underpin the forestry industry and are a vital component of many countries economies. Among woody plants, the cosmopolitan genus Acacia includes some of the most commonly planted trees worldwide. In order to prevent, manage and control invasive plant species, one of the most used tools is species distribution models. The output of these models can also be used to obtain information about population characteristics, such as spatial abundance patterns or species performance. Although ecological theory suggests a direct link between fitness and suitability, this link is often absent. The reasons behind the lack of this relationship are multiple. Chile is one of the countries where Acacia species, in particular, A. dealbata and A. melanoxylon, have become invaders. MethodsHere, we used climatic and edaphic variables to predict thepotentially suitable habitats for A. dealbata and A. melanoxylon in continental Chile and evaluate if the suitability indices obtained from these models are associated with the observed performance of the trees along the country. ResultsOur models show that variable importance showed significant similarities between the variables that characterize each species’ niche. However, despite the high accuracy of our models, we did not observe an association between suitability and tree growth.DiscussionThis disconnection between suitability and performance can result from multiple causes, from structural limitations, like the lack of biotic interactions in the models, to methodological issues, like the usefulness of the performance metric used. Whatever the scenario, our results suggest that plans to control invasive species should be cautious in assuming this relationship in their design and consider other indicators such as species establishment success.

Vicente, S., H. Trindade, C. Máguas, and J. J. Le Roux. 2023. Genetic analyses reveal a complex introduction history of the globally invasive tree Acacia longifolia. NeoBiota 82: 89–117. https://doi.org/10.3897/neobiota.82.87455

AbstractAcacialongifolia (Sydney golden wattle) is considered one of the most problematic plant invaders in Mediterranean-type ecosystems. In this study, we investigate the species’ invasion history by comparing the genetic diversity and structure of native (Australia) and several invasive range (Brazil, Portugal, South Africa, Spain, and Uruguay) populations and by modelling different introduction scenarios using these data. We sampled 272 A.longifolia individuals – 126 from different invasive ranges and 146 from the native range – from 41 populations. We genotyped all individuals at four chloroplast and 12 nuclear microsatellite markers. From these data we calculated diversity metrics, identified chloroplast haplotypes, and estimated population genetic structure based on Bayesian assignment tests. We used Approximate Bayesian Computation (ABC) models to infer the likely introduction history into each invaded country. In Australia, population genetic structure of A.longifolia appears to be strongly shaped by the Bass Strait and we identified two genetic clusters largely corresponding to mainland Australian and Tasmanian populations. We found invasive populations to represent a mixture of these clusters. Similar levels of genetic diversity were present in native and invasive ranges, indicating that invasive populations did not go through a genetic bottleneck. Bayesian assignment tests and chloroplast haplotype frequencies further suggested a secondary introduction event between South Africa and Portugal. However, ABC analyses could not confidently identify the native source(s) of invasive populations in these two countries, probably due to the known high propagule pressure that accompanied these introductions. ABC analyses identified Tasmania as the likely source of invasive populations in Brazil and Uruguay. A definitive native source for Spanish populations could also not be identified. This study shows that tracing the introduction history of A.longifolia is difficult, most likely because of the complexity associated with the extensive movement of the species around the world. Our findings should be considered when planning management and control efforts, such as biological control, in some invaded regions.

Reichgelt, T., W. G. Lee, and D. E. Lee. 2022. The extinction of Miocene broad-leaved deciduous Nothofagaceae and loss of seasonal forest biomes in New Zealand. Review of Palaeobotany and Palynology: 104779. https://doi.org/10.1016/j.revpalbo.2022.104779

Quantitative leaf mass per area reconstructions and prevalence of plicate vernation in broad-leaved Nothofagaceae fossils reveal that deciduousness was common in the middle to late Miocene of New Zealand. This functional type was subsequently lost, as modern-day New Zealand Nothofagaceae have small leaves that live for at least a year. Moreover, fully deciduous trees across all plant families are rare in the current New Zealand flora. Based on modern-day distribution in the Southern Hemisphere, broad-leaved deciduous Nothofagaceae occupy regions with consistently large seasonal differences in precipitation and cloud cover, relative to other functional types in the family (evergreen, small-leaved). Specifically, broad-leaved deciduous Nothofagaceae are in leaf in summer when cloud cover and precipitation are low, but are leafless in winter when cloud cover and precipitation is high. Notably, the seasonal difference in precipitation and cloud cover are more important in explaining deciduousness in Nothofagaceae than winter temperatures. Therefore, potential summer photosynthetic gains likely determine deciduousness in Nothofagaceae. Miocene palaeoclimate reconstructions reveal that New Zealand broad-leaved deciduous Nothofagaceae also thrived in a climate with larger seasonal precipitation differences than today, in an overall warmer climate. We suggest that deciduous Nothofagaceae in the New Zealand flora went extinct as the global climate cooled and summer photosynthetic gains diminished, as summers became progressively rainier and cloudier, favoring an evergreen habit.