Science Enabled by Specimen Data

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.

Akinlabi, F. M., M. D. Pirie, and A. A. Oskolski. 2023. Fire, frost, and drought constrain the structural diversity of wood within southern African Erica (Ericaceae). Botanical Journal of the Linnean Society.

Erica comprises ~860 species of evergreen shrubs and trees ranged from Europe to southern Africa and Madagascar. Wood structure of the around 20 European species is well studied, but despite its relevance to adaptation across the wider geographic range, it has not yet been explored across the much greater diversity, particularly of southern African lineages. In this study, we examine wood structure of 28 Erica species from southern Africa. In the African Erica clade, loss of scalariform perforation plates could be driven by increased aridity and seasonality in the mid-Miocene, and its re-gain can represent an adaptation to freezing in the high elevation species E. nubigena. As vessels in Erica are mostly solitary, imperforate tracheary elements probably form a subsidiary conduit network instead of vessel groups. Increase of ray frequency in habitats with a prominent dry and hot season probably facilitates refilling of vessels after embolism caused by water stress. Wider rays are ancestral for the lineage comprising African Erica and the Mediterranean E. australis. The negative correlation between ray width and expression of summer drought is consistent with Ojeda’s model explaining the diversification of seeders and resprouters among southern African Erica.

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.

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.

Hamer, M., M. Kgatla, and B. Petersen. 2023. An assessment of collection specimen data for South African mountain plants and invertebrates. Transactions of the Royal Society of South Africa: 1–19.

South Africa is considered a megadiverse country, with exceptionally high plant and relatively high animal species richness and endemism. The country’s species have been surveyed and studied for over 200 years, resulting in extensive natural science collections and a vast number of scientific papers and books. This study assessed whether existing data portals provide access to occurrence data and investigated the extent of the data in Global Biodiversity Information Facility and its completeness for plants and selected invertebrate taxa. The main focus was preserved specimen data, but some observation data from iNaturalist were also considered for selected analyses. Records that include species-level identification and co-ordinates were mapped in QGIS to show the coverage of collection localities across the country. The records that fall within the mountain range spatial layer were then extracted and counted to identify density of records per mountain range for various taxa. Forty percent of plant records are from mountain localities, and the Atlantic Cape Fold Mountains had the highest density of records. Table Mountain has been extensively collected for plants and invertebrates. A large proportion of the records for invertebrates lacked species-level identification and co-ordinates, resulting in a low number of records for analyses. The accessible data are only a relatively small subset of existing collections, and digitisation and data upgrading is considered a high priority before collecting gaps can be addressed by targeted surveys.

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.

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.

Ripley, B. S., S. L. Raubenheimer, L. Perumal, M. Anderson, E. Mostert, B. S. Kgope, G. F. Midgley, and K. J. Simpson. 2022. CO 2 ‐fertilisation enhances resilience to browsing in the recruitment phase of an encroaching savanna tree. Functional Ecology.

CO2‐fertilisation is implicated in the widespread and significant woody encroachment of savannas due to CO2‐stimulated increases in belowground reserves that enhance sapling regrowth after fire. However, the effect of CO2 concentration ([CO2]) on tree responses to the other major disturbance in savannas, herbivory, is poorly understood. Herbivory‐responses cannot be predicted from fire‐responses, as herbivore effects occur earlier during establishment and are moderated by plant palatability and defence rather than belowground carbon accumulation.

Williams, C. J. R., D. J. Lunt, U. Salzmann, T. Reichgelt, G. N. Inglis, D. R. Greenwood, W. Chan, et al. 2022. African Hydroclimate During the Early Eocene From the DeepMIP Simulations. Paleoceanography and Paleoclimatology 37.

The early Eocene (∼56‐48 million years ago) is characterised by high CO2 estimates (1200‐2500 ppmv) and elevated global temperatures (∼10 to 16°C higher than modern). However, the response of the hydrological cycle during the early Eocene is poorly constrained, especially in regions with sparse data coverage (e.g. Africa). Here we present a study of African hydroclimate during the early Eocene, as simulated by an ensemble of state‐of‐the‐art climate models in the Deep‐time Model Intercomparison Project (DeepMIP). A comparison between the DeepMIP pre‐industrial simulations and modern observations suggests that model biases are model‐ and geographically dependent, however these biases are reduced in the model ensemble mean. A comparison between the Eocene simulations and the pre‐industrial suggests that there is no obvious wetting or drying trend as the CO2 increases. The results suggest that changes to the land sea mask (relative to modern) in the models may be responsible for the simulated increases in precipitation to the north of Eocene Africa. There is an increase in precipitation over equatorial and West Africa and associated drying over northern Africa as CO2 rises. There are also important dynamical changes, with evidence that anticyclonic low‐level circulation is replaced by increased south‐westerly flow at high CO2 levels. Lastly, a model‐data comparison using newly‐compiled quantitative climate estimates from palaeobotanical proxy data suggests a marginally better fit with the reconstructions at lower levels of CO2.

Reichgelt, T., D. R. Greenwood, S. Steinig, J. G. Conran, D. K. Hutchinson, D. J. Lunt, L. J. Scriven, and J. Zhu. 2022. Plant Proxy Evidence for High Rainfall and Productivity in the Eocene of Australia. Paleoceanography and Paleoclimatology 37.

During the early to middle Eocene, a mid‐to‐high latitudinal position and enhanced hydrological cycle in Australia would have contributed to a wetter and “greener” Australian continent where today arid to semi‐arid climates dominate. Here, we revisit 12 southern Australian plant megafossil sites from the early to middle Eocene to generate temperature, precipitation and seasonality paleoclimate estimates, net primary productivity (NPP) and vegetation type, based on paleobotanical proxies and compare to early Eocene global climate models. Temperature reconstructions are uniformly subtropical (mean annual, summer, and winter mean temperatures 19–21 °C, 25–27 °C and 14–16 °C, respectively), indicating that southern Australia was ∼5 °C warmer than today, despite a >20° poleward shift from its modern geographic location. Precipitation was less homogeneous than temperature, with mean annual precipitation of ∼60 cm over inland sites and >100 cm over coastal sites. Precipitation may have been seasonal with the driest month receiving 2–7× less than mean monthly precipitation. Proxy‐model comparison is favorable with an 1680 ppm CO2 concentration. However, individual proxy reconstructions can disagree with models as well as with each other. In particular, seasonality reconstructions have systemic offsets. NPP estimates were higher than modern, implying a more homogenously “green” southern Australia in the early to middle Eocene, when this part of Australia was at 48–64 °S, and larger carbon fluxes to and from the Australian biosphere. The most similar modern vegetation type is modern‐day eastern Australian subtropical forest, although distance from coast and latitude may have led to vegetation heterogeneity.

Camacho, F., and G. Peyre. 2022. Red List and Vulnerability Assessment of the Páramo Vascular Flora in the Nevados Natural National Park (Colombia). Tropical Conservation Science 15: 194008292210869.

Background and research aims. The Andean páramo is renowned for its unique biodiversity and sensitivity to environmental threats. However, vulnerability assessments remain scarce, which hinders our capacity to prioritize and apply efficient conservation measures. To this end, we established the Red List of the páramo vascular flora from the Nevados National Natural Park and proposed conservation strategies for its threatened species. Methods. We performed International Union for Conservation of Nature (IUCN) Red List assessments by evaluating Criterion B, including sub-criteria B1–Extent of Occurrence and B2–Area of Occupancy, and using a systematic geographic-ecological approach for conditions a (Location analysis) and b (Continuing decline). We then executed a Conservation Gap Analysis to prioritize species for in- situ and/or ex-situ conservation. Results. Summing our 233 evaluated species with previous assessments, we completed the Red List of 262 páramo species and encountered 3% Threatened (7 VU, one EN), 44% Not Threatened (65 LC, 50 NT), and 53% Data Deficient. We acknowledged Lupinus ruizensis as Endangered and Aequatorium jamesonii, Carex jamesonii, Elaphoglossum cuspidatum, Miconia latifolia, Miconia alborosea, Pentacalia gelida, and Themistoclesia mucronata as Vulnerable. Conclusion. The eight threatened species should be included as target species in the PNN Nevados management plan 2023–2028 and regarded as national conservation priorities. Implications for Conservation. We recommend in-situ conservation for Medium-Priority species A. jamesonii, E. cuspidatum, and T. mucronata with thorough monitoring, paired with sub-population transfers for High-Priority species C. jamesonii. For the endemic L. ruizensis and P. gelida, we suggest combined in-situ/ex-situ strategies taking advantage of national germoplasm collections, like the seed bank of the Bogotá Botanical Garden José Celestino Mutis.