Science Enabled by Specimen Data

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.

de Deus Vidal, J., C. B. Schmitt, and I. Koch. 2023. Comparative richness patterns of range sizes and life forms of Apocynaceae along forest–savanna transitions in Brazil. Botanical Journal of the Linnean Society.

Brazilian moist forests and savannas are some of the most species-rich biomes in the Neotropics. In the transition zones between these regions, ecotones often accumulate even higher taxonomic diversity. However, whether these ecotonal communities consist of overlapping species widespread from the neighbouring biomes or a specific set of locally adapted species still needs to be clarified. Regional differences in species richness may be influenced by factors such as species' environmental tolerances, life forms, or species’ range sizes. To investigate the species richness found in ecotones, we used the ‘milk-weed’ family (Apocynaceae), which comprises both widespread and narrowly distributed trees, lianas, and shrubs, as a model to evaluate if (i) their observed richness in ecotones is promoted by widespread species or by locally adapted species; (ii) trees, lianas, and shrubs show different richness patterns in savannas, ecotones, and forests; and (iii) species found in ecotones have broader environmental tolerances than other species in the family. We used a taxonomically curated georeferenced dataset to compare the range sizes of 643 species of Apocynaceae from 73 genera listed for Brazil, comprising 298 species with a liana life form and 345 trees, herbs, or shrubs. We recorded 335 predominantly forest species, 56 savanna species, and 152 ecotone species, for which we quantified species richness, areas of occurrence, precipitation, and temperature ranges and tested for differences in range sizes and environmental tolerances between habits and ecoregions. Our results indicate that (i) Apocynaceae species occurring in ecotones have wider geographical ranges than species not occurring in ecotones; (ii) lianas showed higher area-weighted richness in ecotones than other life forms; and (iii) species found in ecotones had broader environmental tolerances than species restricted to moist forests or savannas. These results indicate that the species richness found in ecotones between savannas and moist forests in Brazil is not necessarily a consequence of higher endemism and local adaptation but may also be a result of overlapping ranges of widespread species typically associated with neighbouring biomes. Together, our findings add to our understanding of ecotones and biomes as continuous, gradual biogeographical transitions instead of sharply defined ecological units.

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.

Onditi, K. O., W. Song, X. Li, S. Musila, Z. Chen, Q. Li, J. Mathenge, et al. 2023. Untangling key abiotic predictors of terrestrial mammal diversity patterns across ecoregions and species groups in Kenya. Ecological Indicators 154: 110595.

Understanding the interactions between abiotic (environmental and anthropogenic) factors and species diversity and distribution patterns is fundamental to improving the ecological representativeness of biodiversity management tools such as protected areas (PAs). However, significant knowledge gaps remain about how species’ ecological and evolutionary opportunities are associated with abiotic factors, especially in biodiversity-rich but economically ill-equipped countries such as Kenya. Here, we explored the interactions of terrestrial mammal diversity patterns and abiotic factors across species groups and ecoregions in Kenya. We coupled data on terrestrial mammal occurrences, phylogeny, functional traits, and environmental predictors in Kenya to derive multiple diversity indices, encompassing species richness and phylogenetic and functional richness, and mean pairwise and nearest taxon distances. We explored the interactions of these indices with several abiotic factors using multivariate regression analyses while adjusting for spatial autocorrelation. The results showed weak correlations between species richness versus the phylogenetic and functional diversity indices. The best-fit models explained variable proportions of diversity indices between species groups and ecoregions and consistently retained annual temperature and precipitation averages and seasonality and human footprint as the strongest predictors. Compared to the species-poor xeric northern and eastern Kenya regions, the predictors had weak associations with diversity variances in the species-rich mesic western and central Kenya regions, similar to focal species groups compared to ordinal classifications and the combined species pool. These findings illustrate that climate and human footprint interplay determine multiple facets of terrestrial mammal diversity patterns in Kenya. Accordingly, curbing human activities degrading long-term climatic regimes is vital to ensuring the ecological integrity of terrestrial mammal communities and should be integrated into biodiversity management frameworks. For a holistic representation of critical conservation areas, biodiversity managements should also prioritize terrestrial mammal phylogenetic and functional attributes besides species richness.

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.

Benson, C. W., M. R. Sheltra, P. J. Maughan, E. N. Jellen, M. D. Robbins, B. S. Bushman, E. L. Patterson, et al. 2023. Homoeologous evolution of the allotetraploid genome of Poa annua L. BMC Genomics 24.

Background Poa annua (annual bluegrass) is an allotetraploid turfgrass, an agronomically significant weed, and one of the most widely dispersed plant species on earth. Here, we report the chromosome-scale genome assemblies of P. annua’s diploid progenitors, P. infirma and P. supina, and use multi-omic analyses spanning all three species to better understand P. annua’s evolutionary novelty. Results We find that the diploids diverged from their common ancestor 5.5 – 6.3 million years ago and hybridized to form P. annua  ≤ 50,000 years ago. The diploid genomes are similar in chromosome structure and most notably distinguished by the divergent evolutionary histories of their transposable elements, leading to a 1.7 × difference in genome size. In allotetraploid P. annua, we find biased movement of retrotransposons from the larger (A) subgenome to the smaller (B) subgenome. We show that P. annua’s B subgenome is preferentially accumulating genes and that its genes are more highly expressed. Whole-genome resequencing of several additional P. annua accessions revealed large-scale chromosomal rearrangements characterized by extensive TE-downsizing and evidence to support the Genome Balance Hypothesis. Conclusions The divergent evolutions of the diploid progenitors played a central role in conferring onto P. annua its remarkable phenotypic plasticity. We find that plant genes (guided by selection and drift) and transposable elements (mostly guided by host immunity) each respond to polyploidy in unique ways and that P. annua uses whole-genome duplication to purge highly parasitized heterochromatic sequences. The findings and genomic resources presented here will enable the development of homoeolog-specific markers for accelerated weed science and turfgrass breeding .

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.

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.

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.

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.