Science Enabled by Specimen Data

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.

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.

Kanmaz, O., T. Şenel, and H. N. Dalfes. 2023. A Modeling Framework to Frame a Biological Invasion: Impatiens glandulifera in North America. Plants 12: 1433. https://doi.org/10.3390/plants12071433

Biological invasions are a major component of global environmental change with severe ecological and economic consequences. Since eradicating biological invaders is costly and even futile in many cases, predicting the areas under risk to take preventive measures is crucial. Impatiens glandulifera is a very aggressive and prolific invasive species and has been expanding its invasive range all across the Northern hemisphere, primarily in Europe. Although it is currently spread in the east and west of North America (in Canada and USA), studies on its fate under climate change are quite limited compared to the vast literature in Europe. Hybrid models, which integrate multiple modeling approaches, are promising tools for making projections to identify the areas under invasion risk. We developed a hybrid and spatially explicit framework by utilizing MaxEnt, one of the most preferred species distribution modeling (SDM) methods, and we developed an agent-based model (ABM) with the statistical language R. We projected the I. glandulifera invasion in North America, for the 2020–2050 period, under the RCP 4.5 scenario. Our results showed a predominant northward progression of the invasive range alongside an aggressive expansion in both currently invaded areas and interior regions. Our projections will provide valuable insights for risk assessment before the potentially irreversible outcomes emerge, considering the severity of the current state of the invasion in Europe.

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.

Pérez, G., M. Vilà, and B. Gallardo. 2022. Potential impact of four invasive alien plants on the provision of ecosystem services in Europe under present and future climatic scenarios. Ecosystem Services 56: 101459. https://doi.org/10.1016/j.ecoser.2022.101459

Invasive alien species (IAS) are one of the main threats to biodiversity conservation, with significant socio-economic and ecological impacts as they disrupt ecosystem services and compromise human well-being. Global change may exacerbate the impacts of IAS, since rising temperatures and human activities favour their introduction and range expansion. Therefore, anticipating the impacts of biological invasions is crucial to support decision-making for their management. In this work, the potential impacts of four invasive alien plant species: Ailanthus altissima, Baccharis halimifolia, Impatiens glandulifera and Pueraria montana, on the provision of three ecosystem services in Europe were evaluated under current and future climate change scenarios. Using a risk analysis protocol, we determined that the most affected services are food provisioning, soil erosion regulation and the maintenance of biological diversity. To evaluate future impacts, species distribution models were calibrated using bioclimatic, environmental and human impact variables. We found that most of continental Europe is suitable for the establishment of A. altissima, B. halimifolia and I. glandulifera, while the potential distribution of P. montana is more limited. Models anticipate a shift in the distribution range for the species towards the north and east of Europe under future scenarios. Bivariate analysis allowed the identification of trends for future impacts in ecosystem services by simultaneously visualising the potential distribution of invasive species and the provision of ecosystem services. Our models project an increase in critical and high impact areas on the analysed ecosystem services, with Western Europe and the British Isles as the most affected regions. In comparison, lower impacts are projected for the Mediterranean region, likely as a consequence of the northwards expansion of invaders. Measures need to be taken to mitigate the expansion and impact of invasive species as our work shows that it can jeopardise the provision of three key services in Europe.

Willems, F. M., J. F. Scheepens, and O. Bossdorf. 2022. Forest wildflowers bloom earlier as Europe warms: lessons from herbaria and spatial modelling. New Phytologist 235: 52–65. https://doi.org/10.1111/nph.18124

Today plants often flower earlier due to climate warming. Herbarium specimens are excellent witnesses of such long‐term changes. However, the magnitude of phenological shifts may vary geographically, and the data are often clustered. Therefore, large‐scale analyses of herbarium data are prone to pseudoreplication and geographical biases.We studied over 6000 herbarium specimens of 20 spring‐flowering forest understory herbs from Europe to understand how their phenology had changed during the last century. We estimated phenology trends with or without taking spatial autocorrelation into account.On average plants now flowered over 6 d earlier than at the beginning of the last century. These changes were strongly associated with warmer spring temperatures. Flowering time advanced 3.6 d per 1°C warming. Spatial modelling showed that, in some parts of Europe, plants flowered earlier or later than expected. Without accounting for this, the estimates of phenological shifts were biased and model fits were poor.Our study indicates that forest wildflowers in Europe strongly advanced their phenology in response to climate change. However, these phenological shifts differ geographically. This shows that it is crucial to combine the analysis of herbarium data with spatial modelling when testing for long‐term phenology trends across large spatial scales.

Chevalier, M. 2022. <i>crestr</i>: an R package to perform probabilistic climate reconstructions from palaeoecological datasets. Climate of the Past 18: 821–844. https://doi.org/10.5194/cp-18-821-2022

Abstract. Statistical climate reconstruction techniques are fundamental tools to study past climate variability from fossil proxy data. In particular, the methods based on probability density functions (or PDFs) can be used in various environments and with different climate proxies because they rely on elementary calibration data (i.e. modern geolocalised presence data). However, the difficulty of accessing and curating these calibration data and the complexity of interpreting probabilistic results have often limited their use in palaeoclimatological studies. Here, I introduce a new R package (crestr) to apply the PDF-based method CREST (Climate REconstruction SofTware) on diverse palaeoecological datasets and address these problems. crestr includes a globally curated calibration dataset for six common climate proxies (i.e. plants, beetles, chironomids, rodents, foraminifera, and dinoflagellate cysts) associated with an extensive range of climate variables (20 terrestrial and 19 marine variables) that enables its use in most terrestrial and marine environments. Private data collections can also be used instead of, or in combination with, the provided calibration dataset. The package includes a suite of graphical diagnostic tools to represent the data at each step of the reconstruction process and provide insights into the effect of the different modelling assumptions and external factors that underlie a reconstruction. With this R package, the CREST method can now be used in a scriptable environment and thus be more easily integrated with existing workflows. It is hoped that crestr will be used to produce the much-needed quantified climate reconstructions from the many regions where they are currently lacking, despite the availability of suitable fossil records. To support this development, the use of the package is illustrated with a step-by-step replication of a 790 000-year-long mean annual temperature reconstruction based on a pollen record from southeastern Africa.

Charitonidou, M., K. Kougioumoutzis, M. C. Karypidou, and J. M. Halley. 2022. ‘Fly to a Safer North’: Distributional Shifts of the Orchid Ophrys insectifera L. Due to Climate Change. Biology 11: 497. https://doi.org/10.3390/biology11040497

Numerous orchid species around the world have already been affected by the ongoing climate change, displaying phenological alterations and considerable changes to their distributions. The fly orchid (Ophrys insectifera L.) is a well-known and distinctive Ophrys species in Europe, with a broad distribution across the continent. This study explores the effects of climate change on the range of O. insectifera, using a species distribution models (SDMs) framework that encompasses different climatic models and scenarios for the near- and long-term future. The species’ environmentally suitable area is projected to shift northwards (as expected) but downhill (contrary to usual expectations) in the future. In addition, an overall range contraction is predicted under all investigated combinations of climatic models and scenarios. While this is moderate overall, it includes some regions of severe loss and other areas with major gains. Specifically, O. insectifera is projected to experience major area loss in its southern reaches (the Balkans, Italy and Spain), while it will expand its northern limits to North Europe, with the UK, Scandinavia, and the Baltic countries exhibiting the largest gains.View Full-Text

Filartiga, A. L., A. Klimeš, J. Altman, M. P. Nobis, A. Crivellaro, F. Schweingruber, and J. Doležal. 2022. Comparative anatomy of leaf petioles in temperate trees and shrubs: the role of plant size, environment and phylogeny. Annals of Botany 129: 567–582. https://doi.org/10.1093/aob/mcac014

Background and Aims Petioles are important plant organs connecting stems with leaf blades and affecting light-harvesting ability of the leaf as well as transport of water, nutrients and biochemical signals. Despite the high diversity in petiole size, shape and anatomy, little information is availabl…

Campbell, C., G. Granath, and H. Rydin. 2021. Climatic drivers of Sphagnum species distributions. Frontiers of Biogeography 13. https://doi.org/10.21425/f5fbg51146

Peatmosses(genus Sphagnum) dominate most Northern mires and show distinct distributional limits in Europe despite having efficient dispersal and few dispersal barriers. This pattern indicates that Sphagnum species distributions are strongly linked to climate. Sphagnumdominated mires have been the la…