Science Enabled by Specimen Data

Metreveli, V., H. Kreft, I. Akobia, Z. Janiashvili, Z. Nonashvili, L. Dzadzamia, Z. Javakhishvili, and A. Gavashelishvili. 2023. Potential Distribution and Suitable Habitat for Chestnut (Castanea sativa). Forests 14: 2076.

Chestnut, Castanea sativa Miller (Fagales: Fagaceae), is an ecologically and economically important tree species of the forest ecosystem in Southern Europe, North-Western Europe, Western Asia, North Africa, and the Caucasus. The distributional range of chestnut in Europe has been highly modified by humans since ancient times. Biotic and abiotic factors have dramatically changed its distribution. Historic anthropogenic range expansion makes it difficult to identify habitat requirements for natural stands of chestnut. In the Caucasus, natural stands of chestnut survived in glacial forest refugia and landscapes that have been difficult for humans to colonize. To identify the species reliable habitat requirements, we estimated the relationship between climatic variables and 620 occurrence locations of natural chestnut stands from the Caucasus and validated the model using GBIF data from outside the Caucasus. We found that our best model is reasonably accurate and the data from the Caucasus characterize chestnut stands throughout the species range well.

Rodriguez, C. S., M. B. Rose, S. J. E. Velazco, J. Franklin, and L. Larios. 2023. High potential for Brassica tournefortii spread in North American introduced range, despite highly conserved niche. Biological Invasions.

Identifying areas vulnerable to the spread of invasive species is critical for designing effective management plans. Species distribution modeling is commonly used to predict species suitable habitat. However, invasive species may not be in equilibrium with environmental conditions within the introduced range, leading to inaccurate predictions. We focused on Brassica tournefortii to (1) assess the role of niche dynamics, (2) identify environmental drivers facilitating spread, and (3) identify suitable habitat within currently un-invaded areas in North America (introduced range) by quantifying the realized niche in its home range (Mediterranean basin and Middle East) and introduced range. Brassica tournefortii continues to expand its distribution within North America, threatening native species and altering ecosystem dynamics through invasion. We found that Brassica tournefortii has a highly conserved environmental niche, driven primarily by warm and dry climates with resource-limited soils. Despite high niche stability, we detected environmental non-equilibrium between the ranges, with 55% niche unfilling and 1% expansion into more arid and resource-limited environments within the introduced range. Our distribution models also highlighted invadable regions in the introduced range where this species is not found currently, indicating opportunities for this species to continue to spread within North America, and suggesting that previous estimates may underestimate areas at risk for invasion. To improve spatial predictions of the potential spread of invasive species, we must consider the role that niche dynamics and environmental equilibrium play during biological invasions.

Yim, C., E. S. Bellis, V. L. DeLeo, D. Gamba, R. Muscarella, and J. R. Lasky. 2023. Climate biogeography of Arabidopsis thaliana: Linking distribution models and individual variation. Journal of Biogeography.

Aim Patterns of individual variation are key to testing hypotheses about the mechanisms underlying biogeographic patterns. If species distributions are determined by environmental constraints, then populations near range margins may have reduced performance and be adapted to harsher environments. Model organisms are potentially important systems for biogeographical studies, given the available range‐wide natural history collections, and the importance of providing biogeographical context to their genetic and phenotypic diversity.LocationGlobal.TaxonArabidopsis thaliana (‘Arabidopsis’).MethodsWe fit occurrence records to climate data, and then projected the distribution of Arabidopsis under last glacial maximum, current and future climates. We confronted model predictions with individual performance measured on 2194 herbarium specimens, and we asked whether predicted suitability was associated with life history and genomic variation measured on ~900 natural accessions.ResultsThe most important climate variables constraining the Arabidopsis distribution were winter cold in northern and high elevation regions and summer heat in southern regions. Herbarium specimens from regions with lower habitat suitability in both northern and southern regions were smaller, supporting the hypothesis that the distribution of Arabidopsis is constrained by climate‐associated factors. Climate anomalies partly explained interannual variation in herbarium specimen size, but these did not closely correspond to local limiting factors identified in the distribution model. Late‐flowering genotypes were absent from the lowest suitability regions, suggesting slower life histories are only viable closer to the centre of the realized niche. We identified glacial refugia farther north than previously recognized, as well as refugia concordant with previous population genetic findings. Lower latitude populations, known to be genetically distinct, are most threatened by future climate change. The recently colonized range of Arabidopsis was well‐predicted by our native‐range model applied to certain regions but not others, suggesting it has colonized novel climates.Main ConclusionsIntegration of distribution models with performance data from vast natural history collections is a route forward for testing biogeographical hypotheses about species distributions and their relationship with evolutionary fitness across large scales.

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.

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.

Van der Meersch, V., and I. Chuine. 2023. Estimating process‐based model parameters from species distribution data using the evolutionary algorithm CMA‐ES. Methods in Ecology and Evolution.

Two main types of species distribution models are used to project species range shifts in future climatic conditions: correlative and process‐based models. Although there is some continuity between these two types of models, they are fundamentally different in their hypotheses (statistical relationships vs. mechanistic relationships) and their calibration methods (SDMs tend to be occurrence data driven while PBMs tend to be prior driven).One of the limitations to the use of process‐based models is the difficulty to parameterize them for a large number of species compared to correlative SDMs. We investigated the feasibility of using an evolutionary algorithm (called covariance matrix adaptation evolution strategy, CMA‐ES) to calibrate process‐based models using species distribution data. This method is well established in some fields (robotics, aerodynamics, etc.), but has never been used, to our knowledge, in ecology, despite its ability to deal with very large space dimensions. Using tree species occurrence data across Europe, we adapted the CMA‐ES algorithm to find appropriate values of model parameters. We estimated simultaneously 27–77 parameters of two process‐based models simulating forest tree's ecophysiology for three species with varying range sizes and geographical distributions.CMA‐ES provided parameter estimates leading to better prediction of species distribution than parameter estimates based on expert knowledge. Our results also revealed that some model parameters and processes were strongly dependent, and different parameter combinations could therefore lead to high model accuracy.We conclude that CMA‐ES is an efficient state‐of‐the‐art method to calibrate process‐based models with a large number of parameters using species occurrence data. Inverse modelling using CMA‐ES is a powerful method to calibrate process‐based parameters which can hardly be measured. However, the method does not warranty that parameter estimates are correct because of several sources of bias, similarly to correlative models, and expert knowledge is required to validate results.

Kolanowska, M. 2023. Loss of fungal symbionts and changes in pollinator availability caused by climate change will affect the distribution and survival chances of myco-heterotrophic orchid species. Scientific Reports 13.

The first comprehensive species distribution models for orchid, its fungal symbionts and pollinator are presented. To evaluate impact of global warming on these organisms three different projections and four various climate change scenarios were analysed. The niche modelling was based on presence-only records of Limodorum abortivum , two species of Russula and three insects pollinating orchid ( Anthophora affinis, Bombus terrestris, Rhodanthidium septemdentatum ). Two sets of orchid predictions were examined—the first one included only climatic data and the second one was based on climate data and data on future distribution of orchid fungal symbionts. Overall, a poleward range shift is predicted to occur as a result of climate change and apparently global warming will be favorable for L. abortivum and its potential geographical range will expand. However, due to the negative effect of global warming on fungal symbionts of L. abortivum , the actual extension of the suitable niches of the orchid will be much limited. Considering future possibility of cross-pollination, the availability of A. affinis for L. abortivum will decrease and this bee will be available in the worst case scenarios only for 21% of orchid populations. On the other hand, the overlap of orchid and the buff-tailed bumblebee will increase and as much as 86.5% of plant populations will be located within B. terrestris potential range. Also the availability of R. septemdentatum will be higher than currently observed in almost all analysed climate change projections. This study showed the importance of inclusion of ecological factors in species distribution models as the climate data itself are not enough to estimate the future distribution of plant species. Moreover, the availability of pollen vectors which is crucial for long-term survival of orchid populations should be analysed in context of climate changes.

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.

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.