Science Enabled by Specimen Data

Cortese, M. R., and A. L. Freestone. 2024. When species don’t move together: Non-concurrent range shifts in Eastern Pacific kelp forest communities G. M. Martins [ed.],. PLOS ONE 19: e0303536. https://doi.org/10.1371/journal.pone.0303536

Species range shifts due to changing ocean conditions are occurring around the world. As species move, they build new interaction networks as they shift from or into new ecological communities. Typically, species ranges are modeled individually, but biotic interactions have been shown to be important to creating more realistic modeling outputs for species. To understand the importance of consumer interactions in Eastern Pacific kelp forest species distributions, we used a Maxent framework to model a key foundation species, giant kelp (Macrocystis pyrifera), and a dominant herbivore, purple sea urchins (Strongylocentrotus purpuratus). With neither species having previously been modeled in the Eastern Pacific, we found evidence for M. pyrifera expansion in the northern section of its range, with no projected contraction at the southern range edge. Despite its known co-occurrence with M. pyrifera, models of S. purpuratus showed a non-concurrent southern range contraction and a co-occurring northern range expansion. While the co-occurring shifts may lead to increased spatial competition for suitable substrate, this non-concurrent contraction could result in community wide impacts such as herbivore release, tropicalization, or ecosystem restructuring.

Zhao, Y., G. A. O’Neill, N. C. Coops, and T. Wang. 2024. Predicting the site productivity of forest tree species using climate niche models. Forest Ecology and Management 562: 121936. https://doi.org/10.1016/j.foreco.2024.121936

Species occurrence-based climate niche models (CNMs) serve as valuable tools for predicting the future ranges of species’ suitable habitats, aiding the development of climate change adaptation strategies. However, these models do not address an essential aspect - productivity, which holds economic significance for timber production and ecological importance for carbon sequestration and ecosystem services. In this study, we investigated the potential to extend the CNMs to predict species productivity under various climate conditions. Lodgepole pine (Pinus contorta Dougl. ex Loud.) and Douglas-fir (Pseudotsuga menziesii Franco.) were selected as our model species due to their comprehensive range-wide occurrence data and measurement of site productivity. To achieve this, we compared and optimized the performance of four individual modeling algorithms (Random Forest (RF), Maxent, Generalized Boosted Models (GBM), and Generalized Additive Model (GAM)) in reflecting site productivity by evaluating the effect of spatial filtering, and the ratio of presence to absence (p/a ratio) observations. Additionally, we applied a binning process to capture the overarching trend of climatic effects while minimizing the impact of other factors. We observed consistency in optimal performance across both species when using the unfiltered data and a 1:1.5 p/a ratio, which could potentially be extended to other species. Among the modeling algorithms explored, we selected the ensemble model combining RF and Maxent as the final model to predict the range-wide site productivity for both species. The predicted range-wide site productivity was validated with an independent dataset for each species and yielded promising results (R2 above 0.7), affirming our model’s credibility. Our model introduced an innovative approach for predicting species productivity with high accuracy using only species occurrence data, and significantly advanced the application of CNMs. It provided crucial tools and insights for evaluating climate change's impact on productivity and holds a better potential for informed forest management and conservation decisions.

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.

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. https://doi.org/10.1186/s12864-023-09456-5

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 .

Wang, Y., J. Wang, T. A. Garran, H. Liu, H. Lin, J. Luo, Q. Yuan, et al. 2023. Genetic diversity and population divergence of Leonurus japonicus and its distribution dynamic changes from the last interglacial to the present in China. BMC Plant Biology 23. https://doi.org/10.1186/s12870-023-04284-x

Background Leonurus japonicus , a significant medicinal plant known for its therapeutic effects on gynecological and cardiovascular diseases, has genetic diversity that forms the basis for germplasm preservation and utilization in medicine. Despite its economic value, limited research has focused on its genetic diversity and divergence. Results The avg. nucleotide diversity of 59 accessions from China were 0.00029 and hotspot regions in petN-psbM and rpl32-trnL (UAG) spacers, which can be used for genotype discrimination. These accessions divided into four clades with significant divergence. The four subclades, which split at approximately 7.36 Ma, were likely influenced by the Hengduan Mountains uplift and global temperature drop. The initial divergence gave rise to Clade D, with a crown age estimated at 4.27 Ma, followed by Clade C, with a crown age estimated at 3.39 Ma. The four clades were not showed a clear spatial distribution. Suitable climatic conditions for the species were identified, including warmest quarter precipitation 433.20 mm ~ 1,524.07 mm, driest month precipitation > 12.06 mm, and coldest month min temp > -4.34 °C. The high suitability distribution showed contraction in LIG to LGM, followed by expansion from LGM to present. The Hengduan Mountains acted as a glacial refuge for the species during climate changes. Conclusions Our findings reflected a clear phylogenetic relationships and divergence within species L. japonicus and the identified hotspot regions could facilitate the genotype discrimination. The divergence time estimation and suitable area simulation revealed evolution dynamics of this species and may propose conservation suggestions and exploitation approaches in the future.

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.

Zhao, Y., G. A. O’Neill, and T. Wang. 2023. Predicting fundamental climate niches of forest trees based on species occurrence data. Ecological Indicators 148: 110072. https://doi.org/10.1016/j.ecolind.2023.110072

Species climate niche models (CNMs) have been widely used for assessing climate change impact, developing conservation strategies and guiding assisted migration for adaptation to future climates. However, the CNMs built based on species occurrence data only reflect the species’ realized niche, which can overestimate the potential loss of suitable habitat of existing forests and underestimate the potential of assisted migration to mitigate climate change. In this study, we explored building a fundamental climate niche model using widely available species occurrence data with two important forest tree species, lodgepole pine (Pinus contorta Dougl. ex Loud.) and Douglas-fir (Pseudotsuga menziesii Franco.), which were introduced to many countries worldwide. We first compared and optimized three individual modeling techniques and their ensemble by adjusting the ratio of presence to absence (p/a) observations using an innovative approach to predict the realized climate niche of the two species. We then extended the realized climate niches to their fundamental niches by determining a new cut-off threshold based on species occurrence data beyond the native distributions. We found that the ensemble model comprising Random Forest and Maxent had the best performance and identified a common cut-off threshold of 0.3 for predicting the fundamental climate niches of the two species, which is likely applicable to other species. We then predicted the fundamental climate niches of the two species under current and future climate conditions. Our study demonstrated a novel approach for predicting species’ fundamental climate niche with high accuracy using only species occurrence data, including both presence and absence data points. It provided a new tool for assessing climate change impact on the future loss of existing forests and implementing assisted migration for better adapting to future climates.

Reichgelt, T., A. Baumgartner, R. Feng, and D. A. Willard. 2023. Poleward amplification, seasonal rainfall and forest heterogeneity in the Miocene of the eastern USA. Global and Planetary Change 222: 104073. https://doi.org/10.1016/j.gloplacha.2023.104073

Paleoclimate reconstructions can provide a window into the environmental conditions in Earth history when atmospheric carbon dioxide concentrations were higher than today. In the eastern USA, paleoclimate reconstructions are sparse, because terrestrial sedimentary deposits are rare. Despite this, the eastern USA has the largest population and population density in North America, and understanding the effects of current and future climate change is of vital importance. Here, we provide terrestrial paleoclimate reconstructions of the eastern USA from Miocene fossil floras. Additionally, we compare proxy paleoclimate reconstructions from the warmest period in the Miocene, the Miocene Climatic Optimum (MCO), to those of an MCO Earth System Model. Reconstructed Miocene temperatures and precipitation north of 35°N are higher than modern. In contrast, south of 35°N, temperatures and precipitation are similar to today, suggesting a poleward amplification effect in eastern North America. Reconstructed Miocene rainfall seasonality was predominantly higher than modern, regardless of latitude, indicating greater variability in intra-annual moisture transport. Reconstructed climates are almost uniformly in the temperate seasonal forest biome, but heterogeneity of specific forest types is evident. Reconstructed Miocene terrestrial temperatures from the eastern USA are lower than modeled temperatures and coeval Atlantic sea surface temperatures. However, reconstructed rainfall is consistent with modeled rainfall. Our results show that during the Miocene, climate was most different from modern in the northeastern states, and may suggest a drastic reduction in the meridional temperature gradient along the North American east coast compared to today.

Baltensperger, A., J. Hagelin, P. Schuette, A. Droghini, and K. Ott. 2022. High dietary and habitat diversity indicate generalist behaviors of northern bog lemmings Synaptomys borealis in Alaska, USA. Endangered Species Research 49: 145–158. https://doi.org/10.3354/esr01211

The northern bog lemming Synaptomys borealis (NBL) is a rare small mammal that is undergoing a federal Species Status Assessment (SSA) under the US Endangered Species Act. Despite a wide North American distribution, very little is known about NBL dietary or habitat needs, both of which are germane to the resiliency of this species to climate change. To quantify diet composition of NBL in Alaska, we used DNA metabarcoding from 59 archived specimens to describe the taxonomic richness and relative abundance of foods in recent diets. DNA analyses revealed a broad diet composed of at least 110 families and 92 genera of bryophytes (mosses and liverworts), graminoids, fungi, forbs, and woody shrubs. Nine bryophyte genera and Carex sedges composed the largest portions of NBL diets. To quantify habitat preference, we intersected 467 georeferenced occurrence records of NBL in Alaska with remotely sensed land cover classes and used a compositional analysis framework that accounts for the relative abundance of land cover types. We did not detect significant habitat preferences for specific land cover types, although NBL frequently occurred in evergreen forest, woody wetlands, and adjacent to water. Our research highlights the importance of bryophytes, among a high diversity of dietary components, and describes NBL as boreal habitat generalists. Results will inform the current federal SSA by quantifying the extent to which ecological constraints are likely to affect NBL in a rapidly changing boreal environment.