Science Enabled by Specimen Data

Barrett, C. F., C. W. Corbett, and H. L. Thixton-Nolan. 2023. A lack of population structure characterizes the invasive Lonicera japonica in West Virginia and across eastern North America1,2. The Journal of the Torrey Botanical Society 150.

Invasive plant species cause massive ecosystem damage globally yet represent powerful case studies in population genetics and rapid adaptation to new habitats. The availability of digitized herbarium collections data, and the ubiquity of invasive species across the landscape make them highly accessible for studies of invasion history and population dynamics associated with their introduction, establishment, spread, and ecological interactions. Here we focus on Lonicera japonica, one of the most damaging invasive vine species in North America. We leveraged digitized collections data and contemporary field collections to reconstruct the invasion history and characterize patterns of genomic variation in the eastern USA, using a straightforward method for generating nucleotide polymorphism data and a recently published, chromosome-level genome for the species. We found an overall lack of population structure among sites in northern West Virginia, USA, as well as across sites in the central and eastern USA. Heterozygosity and population differentiation were both low based on FST analysis of molecular variance, principal components analysis, and cluster-based analyses. We also found evidence of high inbreeding coefficients and significant linkage disequilibrium, in line with the ability of this otherwise outcrossing, perennial species to propagate vegetatively. Our findings corroborate earlier studies based on allozyme data, and suggest that intentional, human-assisted spread explains the lack of population structure, as this species was planted for erosion control and as an ornamental, escaping cultivation repeatedly across the USA.

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.

McCulloch-Jones, E. J., T. Kraaij, N. Crouch, and K. T. Faulkner. 2023. Assessing the invasion risk of traded alien ferns using species distribution models. NeoBiota 87: 161–189.

Risk analysis plays a crucial role in regulating and managing alien and invasive species but can be time-consuming and costly. Alternatively, combining invasion and impact history with species distribution models offers a cost-effective and time-efficient approach to assess invasion risk and identify species for which a comprehensive risk analysis should take precedence. We conducted such an assessment for six traded alien fern species, determining their invasion risk in countries where they are traded. Four of the species (Dicksonia antarctica, Dryopteris erythrosora, Lygodium japonicum, and Phlebodium aureum) showed limited global distributions, while Adiantum raddianum and Sphaeropteris cooperi had broader distributions. A. raddianum, however, was the only species found to pose a high invasion risk in two known trade countries – the USA and Australia – and requires a complete risk analysis to determine the appropriate regulatory responses. Dicksonia antarctica, Phlebodium aureum (for New Zealand), and Dryopteris erythrosora (for the USA) posed a medium risk of invasion due to the lack of evidence of impacts, and a complete risk analysis is thus deemed less crucial for these species in these countries. For other species, suitable environments were not predicted in the countries where they are traded, thus the risk of invasion is low, and a complete risk analysis is not required. For species in countries where suitable environments are predicted but no trade information or presence data are available, risk assessments are recommended to better determine the risk posed. Despite the relatively limited potential global distribution of the studied ferns relative to other major plant invaders (e.g., Pinus spp. and Acacia spp.), their history of invasion, documented impacts in pristine environments, and high propagule pressure from trade warrants concern, possibly necessitating legislative and regulatory measures in environmentally suitable regions.

Graham, C. D. K., E. J. Forrestel, A. L. Schilmiller, A. T. Zemenick, and M. G. Weber. 2023. Evolutionary signatures of a trade-off in direct and indirect defenses across the wild grape genus Vitis. Evolution.

Evolutionary correlations between chemical defense and protection by mutualist bodyguards have been long predicted, but tests of these pattern remain rare. We use a phylogenetic framework to test for evolutionary correlations indicative of trade-offs or synergisms between direct defense in the form of plant secondary metabolism, and indirect defense in the form of leaf domatia, across 33 species in the wild grape genus, Vitis. We also performed a bioassay with a generalist herbivore to associate our chemical phenotypes with herbivore palatability. Finally, we tested whether defensive traits correlate with the average abiotic characteristics of each species’ contemporary range and whether these correlations were consistent with plant defense theory. We found a negative evolutionary correlation between domatia size and the diversity of secondary metabolites in Vitis leaf tissue across the genus, and also that leaves with a higher diversity and richness of secondary metabolites were less palatable to a generalist herbivore, consistent with a trade-off in chemical and mutualistic defense investment. Predictions from plant defense theory were not supported by associations between investment in defense phenotypes and abiotic variables. Our work demonstrates an evolutionary pattern indicative of a trade-off between indirect and direct defense strategies across the Vitis genus.

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.

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.

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.

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.

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.

Song, X.-J., G. Liu, Z.-Q. Qian, and Z.-H. Zhu. 2023. Niche Filling Dynamics of Ragweed (Ambrosia artemisiifolia L.) during Global Invasion. Plants 12: 1313.

Determining whether the climatic ecological niche of an invasive alien plant is similar to that of the niche occupied by its native population (ecological niche conservatism) is essential for predicting the plant invasion process. Ragweed (Ambrosia artemisiifolia L.) usually poses serious threats to human health, agriculture, and ecosystems within its newly occupied range. We calculated the overlap, stability, unfilling, and expansion of ragweed’s climatic ecological niche using principal component analysis and performed ecological niche hypothesis testing. The current and potential distribution of A. artemisiifolia was mapped by ecological niche models to identify areas in China with the highest potential risk of A. artemisiifolia invasion. The high ecological niche stability indicates that A. artemisiifolia is ecologically conservative during the invasion. Ecological niche expansion (expansion = 0.407) occurred only in South America. In addition, the difference between the climatic and native niches of the invasive populations is mainly the result of unpopulated niches. The ecological niche model suggests that southwest China, which has not been invaded by A. artemisiifolia, faces an elevated risk of invasion. Although A. artemisiifolia occupies a climatic niche distinct from native populations, the climatic niche of the invasive population is only a subset of the native niche. The difference in climatic conditions is the main factor leading to the ecological niche expansion of A. artemisiifolia during the invasion. Additionally, human activities play a substantial role in the expansion of A. artemisiifolia. Alterations in the A. artemisiifolia niche would help explain why this species is so invasive in China.

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.

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.

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.