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Science Enabled by Specimen Data

Ramírez-Barahona, S. 2024. Incorporating fossils into the joint inference of phylogeny and biogeography of the tree fern order Cyatheales R. Warnock, and M. Zelditch [eds.],. Evolution.

Present-day geographic and phylogenetic patterns often reflect the geological and climatic history of the planet. Neontological distribution data are often sufficient to unravel a lineage’s biogeographic history, yet ancestral range inferences can be at odds with fossil evidence. Here, I use the fossilized birth–death process and the dispersal–extinction cladogenesis model to jointly infer the dated phylogeny and range evolution of the tree fern order Cyatheales. I use data for 101 fossil and 442 extant tree ferns to reconstruct the biogeographic history of the group over the last 220 million years. Fossil-aware reconstructions evince a prolonged occupancy of Laurasia over the Triassic–Cretaceous by Cyathealean tree ferns, which is evident in the fossil record but hidden from analyses relying on neontological data alone. Nonetheless, fossil-aware reconstructions are affected by uncertainty in fossils’ phylogenetic placement, taphonomic biases, and specimen sampling and are sensitive to interpretation of paleodistributions and how these are scored. The present results highlight the need and challenges of incorporating fossils into joint inferences of phylogeny and biogeography to improve the reliability of ancestral geographic range estimation.

Souto, C. P., L. P. Zalazar, M. Tadey, and A. C. Premoli. 2024. Modeling past, present and future: Species-specific responses to climate changes in three shrub congeners from south American drylands. Journal of Arid Environments 221: 105139.

Drylands cover ca. 40% of the land global surface and deliver significant ecosystem services. These regions are the most sensitive, prone to suffer the effects of climate and distribution changes, so estimates on projected range shifts are crucial to complement traditional approaches to biodiversity conservation and sustainability. Shrubs of the Monte Desert dominate the largest temperate dryland in South America. Our goal is to assess the spatial distribution and niche overlap of three native shrubs (Larrea cuneifolia (LC), L. divaricata (LD), and L. nitida (LN)), under present climate conditions, to retrodict their potential past distribution, and anticipate their predicted range under future climate scenarios. We used ecological niche modeling that were projected to the past (LGM and Mid Holocene) and future (2050 and 2070) under two scenarios of greenhouse gas emissions and two model of global circulation. All species have high niche overlap (67–89%), but showed species-specific responses, highlighting the need to develop mitigation measures particularly for LD and LN in the face of climate change and land use pressures. Global South deserts are being highly degraded and information on future potential ranges of endemic species can support the development of sustainable conservation and management plans.

Anest, A., Y. Bouchenak-Khelladi, T. Charles-Dominique, F. Forest, Y. Caraglio, G. P. Hempson, O. Maurin, and K. W. Tomlinson. 2024. Blocking then stinging as a case of two-step evolution of defensive cage architectures in herbivore-driven ecosystems. Nature Plants.

Dense branching and spines are common features of plant species in ecosystems with high mammalian herbivory pressure. While dense branching and spines can inhibit herbivory independently, when combined, they form a powerful defensive cage architecture. However, how cage architecture evolved under mammalian pressure has remained unexplored. Here we show how dense branching and spines emerged during the age of mammalian radiation in the Combretaceae family and diversified in herbivore-driven ecosystems in the tropics. Phylogenetic comparative methods revealed that modern plant architectural strategies defending against large mammals evolved via a stepwise process. First, dense branching emerged under intermediate herbivory pressure, followed by the acquisition of spines that supported higher speciation rates under high herbivory pressure. Our study highlights the adaptive value of dense branching as part of a herbivore defence strategy and identifies large mammal herbivory as a major selective force shaping the whole plant architecture of woody plants. This study explores the evolution of two traits, branching density and spine presence, in the globally distributed plant family Combretaceae. These traits were found to have appeared in a two-step process in response to mammalian herbivory pressure, revealing the importance of large mammals in the evolution of plant architecture diversity.

Prochazka, L. S., S. Alcantara, J. G. Rando, T. Vasconcelos, R. C. Pizzardo, and A. Nogueira. 2024. Resource availability and disturbance frequency shape evolution of plant life forms in Neotropical habitats. New Phytologist.

Organisms use diverse strategies to thrive in varying habitats. While life history theory partly explains these relationships, the combined impact of resource availability and disturbance frequency on life form strategy evolution has received limited attention.We use Chamaecrista species, a legume plant lineage with a high diversity of plant life forms in the Neotropics, and employ ecological niche modeling and comparative phylogenetic methods to examine the correlated evolution of plant life forms and environmental niches.Chamaephytes and phanerophytes have optima in environments characterized by moderate water and nutrient availability coupled with infrequent fire disturbances. By contrast, annual plants thrive in environments with scarce water and nutrients, alongside frequent fire disturbances. Similarly, geophyte species also show increased resistance to frequent fire disturbances, although they thrive in resource‐rich environments.Our findings shed light on the evolution of plant strategies along environmental gradients, highlighting that annuals and geophytes respond differently to high incidences of fire disturbances, with one enduring it as seeds in a resource‐limited habitat and the other relying on reserves and root resprouting systems in resource‐abundant habitats. Furthermore, it deepens our understanding of how organisms evolve associated with their habitats, emphasizing a constraint posed by low‐resource and high‐disturbance environments.

Finegan, B., D. Delgado, A. L. Hernández Gordillo, N. Zamora Villalobos, R. Núñez Florez, F. Díaz Santos, and S. Vílchez Mendoza. 2024. Multi-dimensional temperature sensitivity of protected tropical mountain rain forests. Frontiers in Forests and Global Change 6.

Introduction Tropical mountain rain forests (TMRF, natural forests at > 300 m asl) are globally important for biodiversity and ecosystem services and are believed to be highly vulnerable to climate change. But there are no specific approaches for rigorous assessment of their vulnerability at the landscape and local scales necessary for management for adaptation. We address the challenge of evaluating the ecological sensitivity to temperature of TMRF, applying a multidimensional approach in protected areas over a 440–2,950 m asl altitudinal gradient in Costa Rica, synthesizing results of a long-term research programme (2012-present). We evaluate the sensitivity to the current spatial temperature gradient of eleven ecosystem properties in three categories: forest composition and diversity, thermal characteristics of forest stands and forest structure and dynamics.MethodsData are from 29 to 32 plots of 50 m x 50 m (0.25 ha) distributed over the gradient, in which all trees, palms and tree ferns ≥ 10 dbh are identified to species and measured for recruitment, growth and mortality. An experimental study of leaf litter decomposition rates was carried out in twelve plots. Current and future (SSP 585, 2070) values of mean annual temperatures MAT were obtained from online climate surfaces. Thermal characteristics of forest stands were determined using MATs of species occurrences in GBIF and include a new index, the Community Thermal Capital Index (CTCI), calculated as CTI-MAT.ResultsWe classified degrees of sensitivity to temperature as very weak, weak, moderate or substantial. All eleven ecosystem properties are substantially sensitive, so changes in their values are expected under rising temperatures. Species density, the community temperature index CTI, tree recruitment and mortality rates and leaf litter decomposition rates are positively related to temperature, while the community weighted mean thermal niche breadth, the CTCI, net basal area increments, stand basal area and carbon in aboveground biomass are negatively related. Results point to zones of vulnerability in the protected areas.DiscussionIn montane forests, positive values of the CTCI–climate credit– robust basal area growth and very low mortality and leaf litter decomposition rates suggest healthy ecosystems and no risk of mountaintop extinction. Lowland forests may be vulnerable to degradation and biotic attrition, showing current basal area loss, high mortality and climate debts. National and local actors are participating in a process of adoption of the sensitivity analysis and recommendations regarding zones of vulnerability.

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.

Rosas, M. R., R. A. Segovia, and P. C. Guerrero. 2023. Climatic Niche Dynamics of the Astereae Lineage and Haplopappus Species Distribution following Amphitropical Long-Distance Dispersal. Plants 12: 2721.

The tribe Astereae (Asteraceae) displays an American Amphitropical Disjunction. To understand the eco-evolutionary dynamics associated with a long-distance dispersal event and subsequent colonization of extratropical South America, we compared the climatic and geographic distributions of South American species with their closest North American relatives, focusing on the diverse South American Astereae genus, Haplopappus. Phylogenetic analysis revealed that two South American genera are closely related to seven North American genera. The climatic niche overlap (D = 0.5) between South and North America exhibits high stability (0.89), low expansion (0.12), and very low unfilling (0.04). The distribution of the North American species predicted the climatic and geographic space occupied by the South American species. In central Chile, Haplopappus showed a non-random latitudinal gradient in species richness, with Mediterranean climate variables mainly explaining the variation. Altitudinal patterns indicated peak richness at 600 m, declining at lower and higher elevations. These findings support climatic niche conservatism in shaping Haplopappus species distribution and diversity. Two major endemism zones were identified in central Chile and the southern region, with a transitional zone between Mediterranean and Temperate macro-bioclimates. Our results indicate strong niche conservatism following long-distance dispersal and slight niche expansion due to unique climatic variables in each hemisphere.

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.

Goolsby, J. A., P. J. Moran, M. Martínez Jiménez, C. Yang, K. Canavan, Q. Paynter, N. Ota, and D. J. Kriticos. 2023. Biology of Invasive Plants 4. Arundo donax L. Invasive Plant Science and Management 16: 81–109.