Science Enabled by Specimen Data

Kolanowska, M. 2023. Future distribution of the epiphytic leafless orchid (Dendrophylax lindenii), its pollinators and phorophytes evaluated using niche modelling and three different climate change projections. Scientific Reports 13. https://doi.org/10.1038/s41598-023-42573-5

The identification of future refugia for endangered species from the effects of global warming is crucial for improving their conservation. Because climate-driven shifts in ranges and local extinctions can result in a spatial mismatch with their symbiotic organisms, however, it is important to incorporate in niche modelling the ecological partners of the species studied. The aim of this study was to evaluate the effect of climate change on the distribution of suitable niches for the ghost orchid ( Dendrophylax lindenii ) and its phorophytes and pollinators. Thus, its five species of host trees and three pollen vectors were included in the analysis. Climatic preferences of all the species studied were evaluated. The modelling was based on three different climate change projections and four Shared Socio-economic Pathway trajectories. All the species analysed are characterized by narrow temperature tolerances, which with global warming are likely to result in local extinctions and range shifts. D. lindenii is likely to be subjected to a significant loss of suitable niches, but within a reduced geographical range, both host trees and pollen vectors will be available in the future. Future conservation of this orchid should focus on areas that are likely be suitable for it and its ecological partners.

Thongsangtum, N., J. Huang, S.-F. Li, Y. Thasod, and T. Su. 2023. Calophyllum (Calophyllaceae) from late Oligocene–Early Miocene of Li Basin, northern Thailand and its biogeographic and paleoclimatic implications. Palaeoworld. https://doi.org/10.1016/j.palwor.2023.09.002

Fossils from tropical Asia, which are far from fully investigated, are important for understanding the evolution of plant diversity and the associated surrounding environment there. In this study, we report, as the first record in Thailand, the well-preserved leaf fossils of Calophyllum Linnaeus (Calophyllaceae) from the upper Oligocene–Lower Miocene lacustrine deposits in Li Basin, northern Thailand. The fossils were identified through detailed comparison with leaves of extant and fossil species. These leaf fossils are assigned to Calophyllum based on several key leaf characteristics such as oblanceolate or oblong in shape and parallel secondary veins, nearly perpendicular to the midvein, as well as secondary veins alternate, closely placed, craspedodromous, parallel, dense, and distinct on surface, forming marginal veins. Based on detailed morphological comparison, these fossil leaves are assigned to C. suraikholaensis Awasthi and Prasad, 1990 and Calophyllum sp. The discovery of Calophyllum indicates a montane subtropical to tropical climate in northern Thailand during the Oligocene–Miocene. Together with previous fossil records, these results suggest that this genus probably originated in India during the Paleogene, and spread from India to Indochina during the Neogene, leading to its modern distribution, which currently prefers tropical climates.

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.

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. https://doi.org/10.1093/botlinnean/boad047

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.

Freire-Fierro, A., F. Forest, D. S. Devey, J. F. B. Pastore, J. W. Horn, X.-J. Ge, Z. Wang, et al. 2023. Monnina (Polygalaceae), a New World monophyletic genus full of contrasts. Botanical Journal of the Linnean Society. https://doi.org/10.1093/botlinnean/boad026

Endemic to the Neotropics, Monnina is the second largest genus of Polygalaceae, yet little is known about its phylogenetic history, biogeography, and morphological character evolution. To address these knowledge gaps, we conducted Bayesian and maximum likelihood (ML) analyses of nuclear ITS and plastid trnL–F regions to test the monophyly of Monnina s.l. We used this phylogenetic framework to (i) infer divergence time estimates of lineages within the genus and reconstruct their historical biogeography; (ii) reconstruct the evolution of morphological characters of putative ecological and evolutionary importance in Monnina; and (iii) test for correlations between our phylogenetic hypothesis and environmental data. Our results reveal that Monnina is monophyletic with an indehiscent, 1–2-seeded fruit as a synapomorphy for the genus. We identify six clades within Monnina based on our combined phylogenetic results: Clades A, B, and D are primarily distributed in southern and eastern South America, Clades C and E are primarily Central Andean, and Clade F is chiefly distributed in the Northern Andes and Central America. The ancestor of the Monnina stem lineage dispersed from Australia/Africa to South America during the late Eocene to early Oligocene. The divergences of major lineages within the genus began in the early Miocene. We inferred the most recent common ancestor of Monnina to be an herbaceous plant with one-seeded samaroid fruits. The origins of fleshy fruits and shrubby habits are phylogenetically correlated within Monnina, and their concerted convergent evolution may have promoted increased net diversification rates in the two most species-rich subclades of the genus.

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. https://doi.org/10.1093/evolut/qpad140

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.

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.

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.

Lima, V. P., R. A. Ferreira de Lima, F. Joner, L. D’Orangeville, N. Raes, I. Siddique, and H. ter Steege. 2023. Integrating climate change into agroforestry conservation: A case study on native plant species in the Brazilian Atlantic Forest. Journal of Applied Ecology. https://doi.org/10.1111/1365-2664.14464

Designing multispecies systems with suitable climatic affinity and identifying species' vulnerability under human‐driven climate change are current challenges to achieve successful adaptation of natural systems. To address this problem, we need to (1) identify groups of species with climatic similarity under climate scenarios and (2) identify areas with high conservation value under predicted climate change.To recognize species with similar climatic niche requirements that can be grouped for mixed cropping in Brazil, we employed ecological niche models (ENMs) and Spearman's ρ for overlap. We also used prioritization algorithms to map areas of high conservation value using two Shared Socioeconomic Pathways (SSP2‐4.5 and SSP5‐8.5) to assess mid‐term (2041–2060) and long‐term (2061–2080) climate change impacts.We identified 15 species groups with finer climatic affinities at different times depicted on hierarchical clustering dendrograms, which can be combined into agroecological agroforestry systems. Furthermore, we highlight the climatically suitable areas for these groups of species, thus providing an outlook of where different species will need to be planted over time to be conserved. In addition, we observed that climate change is predicted to modify the spatial association of these groups under different future climate scenarios, causing a mean negative change in species climatic similarity of 9.5% to 13.7% under SSP2‐4.5 scenario and 9.5% to 10.5% under SSP5‐8.5, for 2041–2060 and 2061–2080, respectively.Synthesis and applications. Our findings provide a framework for agroforestry conservation. The groups of species with finer climatic affinities identified and the climatically suitable areas can be combined into agroecological productive systems, and provide an outlook of where different species may be planted over time. In addition, the conservation priority zones displaying high climate stability for each species individually and all at once can be incorporated into Brazil's conservation plans by policymakers to prioritize specific sites. Lastly, we urge policymakers, conservation organizations and donors to promote interventions involving farmers and local communities, since the species' evaluated have proven to maintain landscapes with productive forest fragments and can be conserved in different Brazilian ecosystems.

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.