Unraveling the Pontocaspian biodiversity crisis
Systematics and Morphology (Zoology)
Final Report Abstract
We are currently experiencing the "sixth mass extinction event." This is especially apparent in the Pontocaspian region, which includes the brackish waters of the Caspian, Black, and Aral seas. Many Pontocaspian species are in sharp decline or threatened with extinction ("Pontocaspian biodiversity crisis)". Mollusks (Gastropoda and Bivalvia) are especially impacted due to their benthic lifestyle and high level of endemism. However, there are indications that the number of endemic mollusk species in the region is inflated. Additionally, field research in the region declined after the collapse of the former Soviet Union. Therefore, it is unclear whether 80% of the region's endemic mollusk species have actually been lost in the last 30 years, as suspected by some scientists. This proposal aimed to use mollusks as a model taxon to disentangle the effects of the taxonomic, sampling, and biodiversity crises using state-of-the-art "museomics," targeted fieldwork, and species delimitation approaches. The goal was to explain the sharp decline in reported endemic species in the Pontocaspian region. Specifically, we aimed to 1) assess the relationships between Pontocaspian mollusks at the species level using machine learning approaches that incorporate (historical) DNA, proteomics, 3D morphometric, and ecological information, 2) identify potential refugia in the Pontocaspian region based on predictive models and targeted fieldwork, 3) assess the adequacy of biodiversity data by examining the impact of sampling on the number of endemic species reported over time using sampling abundance analyses and radiocarbon dating, and 4) quantify the different contributions of the taxonomic crisis and the sampling crisis to the loss of endemic Pontocaspian mollusk species in order to understand the extent of the current biodiversity crisis. By combining genetic, genomic, proteomic, morphological, and sampling analyses with machine learning methods, we were able to answer all the questions raised in the original proposal. In the absence of fresh or freshly preserved materials of endemic Pontocaspian mollusks, we found that museomics approaches (including historical DNA, proteomics, and/or 3D morphometric analyses) are crucial for assessing species-level relationships. We also developed a machine learning pipeline for classifying hydrobiid snails. This system uses shell images, DNA sequence data and shell measurements, and is based on a convolutional neural network (CNN). Using predictive modeling, we demonstrated that refugia and hotspot areas for bivalves and gastropods in the Caspian Sea exhibit differential spatial and bathymetric distributions. These patterns are likely driven by the complex interplay of community assembly processes, such as environmental filtering and biotic interactions. However, with projected declines in Caspian Sea water levels of up to 21 m by 2100 driven by Global warming, we expect a critical disruption of key ecosystems and a massive reduction of existing marine protected area coverage. Replacing traditional static conservation planning with a pre-emptive, dynamic approach that allows protected areas to track shifting ecosystems is recommended to help endemic Caspian Sea biodiversity adapt to these changes. To evaluate the potential impact of a collection crisis on biodiversity assessments in the Caspian Sea, we examined sampling days for mollusk biodiversity studies from 1825 to 2020. We found a significant decrease in sampling efforts over time, especially following the dissolution of the Soviet Union. Furthermore, 14C analyses of "fresh-looking" shells from four endemic species collected in the Caspian Sea over the last 150 years revealed that all examined specimens had a calibrated age ranging from 1624 cal BC to 1888 cal AD. Two of the four species clearly predate the onset of the “Anthropocene”; one species may have been alive during the early Anthropocene; and one species likely existed during much of the Anthropocene. These findings suggest a taxonomic bias because at least some of the "recent" endemic gastropod specimens were long dead at the time of collection. While the results of our project clearly show taxonomic and sampling biases in current estimates of endemic mollusk biodiversity in the Caspian Sea, it contributes to the notion of a severe biodiversity crisis in the Caspian Sea. We show that between the beginning of the Anthropocene (late 18th century) and the 1950s there was a considerable loss of species, which cannot be attributed solely to taxonomic uncertainties. This extinction timeline coincides roughly with the period of increasing industrialization and chemical pollution in the Caspian Sea region. Unfortunately, the severe loss of endemic mollusk species is not yet reflected in the current IUCN assessments. In conclusion, our research project provides overwhelming evidence of a considerable loss of endemic species over the last 150 years, supporting the notion of a Caspian Sea biodiversity crisis. The project resulted in 13 scientific publications, 4 contributions to international conferences, and a comprehensive press coverage.
Publications
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Current extinction rate in European freshwater gastropods greatly exceeds that of the late Cretaceous mass extinction. Communications Earth & Environment, 2(1).
Neubauer, Thomas A.; Hauffe, Torsten; Silvestro, Daniele; Schauer, Jens; Kadolsky, Dietrich; Wesselingh, Frank P.; Harzhauser, Mathias & Wilke, Thomas
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Decline of unique Pontocaspian biodiversity in the Black Sea Basin: A review. Ecology and Evolution, 11(19), 12923-12947.
Gogaladze, Aleksandre; Son, Mikhail O.; Lattuada, Matteo; Anistratenko, Vitaliy V.; Syomin, Vitaly L.; Pavel, Ana Bianca; Popa, Oana P.; Popa, Luis O.; ter Poorten, Jan‐Johan; Biesmeijer, Jacobus C.; Raes, Niels; Wilke, Thomas; Sands, Arthur F.; Trichkova, Teodora; Hubenov, Zdravko K.; Vinarski, Maxim V.; Anistratenko, Olga Yu; Alexenko, Tatiana L. & Wesselingh, Frank P.
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Keyhole into a Lost World: The First Purely Freshwater Species of the Ponto-Caspian Genus Clathrocaspia (Caenogastropoda: Hydrobiidae). Diversity, 14(4), 232.
Anistratenko, Vitaliy V.; Palatov, Dmitry M.; Chertoprud, Elizaveta M.; Sitnikova, Tatyana Y.; Anistratenko, Olga Y.; Clewing, Catharina & Vinarski, Maxim V.
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Poor hDNA-Derived NGS Data May Provide Sufficient Phylogenetic Information of Potentially Extinct Taxa. Frontiers in Ecology and Evolution, 10.
Clewing, Catharina; Kehlmaier, Christian; Stelbrink, Björn; Albrecht, Christian & Wilke, Thomas
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Rapid spread of a new alien and potentially invasive species, Clathrocaspia knipowitschii (Makarov, 1938) (Gastropoda: Hydrobiidae), in the Danube River. Archives of Biological Sciences, 74(1), 81-89.
Szekeres, József; Beermann, Arne; Neubauer, Thomas; Ocadlik, Miroslav; Paunovic, Momir; Rakovic, Maja; Csányi, Béla; Varga, András; Weigand, Alexander; Wilke, Thomas & Fehér, Zoltán
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Fifth mass extinction event triggered the diversification of the largest family of freshwater gastropods (Caenogastropoda: Truncatelloidea: Hydrobiidae). Cladistics, 40(1), 82-96.
Delicado, Diana; Hauffe, Torsten & Wilke, Thomas
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Classification of freshwater snails of the genus Radomaniola with multimodal triplet networks
Vetter, D.; Ahsan, M.; Delicado, D.; Neubauer, T.A.; Wilke, T. & Roig, G.
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To be alive or not to be alive: Radiocarbon data provide new perspective on species diversity in the Caspian Sea. Aquatic Conservation: Marine and Freshwater Ecosystems, 34(2).
Clewing, Catharina; Albrecht, Christian; Anistratenko, Vitaliy V.; Anistratenko, Olga Yu. & Wilke, Thomas
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Rapid decline of Caspian Sea level threatens ecosystem integrity, biodiversity protection, and human infrastructure. Communications Earth & Environment, 6(1).
Court, Rebecca; Lattuada, Matteo; Shumeyko, Nataliya; Baimukanov, Mirgaliy; Eybatov, Tariyel; Kaidarova, Altynay; Mamedov, Elchin V.; Rustamov, Eldar; Tasmagambetova, Aselle; Prange, Matthias; Wilke, Thomas; Hassall, Christopher & Goodman, Simon J.
