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Understanding the role of environmental and climatic changes in shaping subterranean diversity to preserve Europe’s unique hidden biodiversity

Periodic Reporting for period 1 - HiddenLife (Understanding the role of environmental and climatic changes in shaping subterranean diversity to preserve Europe’s unique hidden biodiversity)

Reporting period: 2017-06-05 to 2019-06-04

What is the problem/issue being addressed?
HIDDENLIFE project aims to improve our understanding of one of the top biodiversity hotspots in Europe–the Dinarides, and its unique cave fauna, to ensure its conservation and future well-being. Through a multidisciplinary approach that combines state of the art molecular and statistical tools, I investigated the systematics, phylogeography, and environmental preferences of three independent lineages of cave spiders. This will contribute to understanding the mechanisms that shaped their origin and present-day diversity and distribution. By projecting potential distributions under predicted scenarios of global warming, I predicted future habitat suitability and assessed the vulnerability of this unique and fragile fauna.

Why is it important for society?
Climate warming and other anthropogenic perturbations are affecting ecosystems worldwide, contributing to the sixth mass extinction. Documenting and explaining vanishing biodiversity are major challenges today. Understanding biodiversity is an essential step towards halting its loss and in preventing the degradation of ecosystem services. Caves are isolated and extreme habitats. Their stable climatic conditions, scarcity of food and absence of light drive the evolution of highly adapted fauna. Despite their stable climatic conditions, recent studies show that global warming may impact subterranean habitats by rising temperatures and, consequently, threatening troglobionts (animals adapted to caves life), which have a low tolerance to temperature variations, causing the reduction of optimal habitat and driving narrowly distributed species to extinction.

Through the HIDDENLIFE project I discovered 41 new species, most of them indistinguishable by morphology, I evaluated sensitivity to climatic changes for all the species and identified regions with high species richness – hotspots within a hotspot. All of this is prerequisite for sustainable management and protection of this species and areas with high biodiversity.


What are the overall objectives?
Several objectives have been set at the beginning of this action:
1. To infer the phylogenies of three independent lineages Dinaric of cave spiders, families Dysderidae and Leptonetidae and genus Troglohyphantes, to estimate divergence times and to identify drivers of cave diversification.
2. To delimit species, describe new species and to reveal population structure of studied groups.
3. To infer past, present and future potential distributions of cave spider species and to evaluate their sensitivity of to global warming, especially of endangered ones.

Conclusions of the action
- inferred phylogenies of the three groups of cave-dwelling spiders in the Dinarides are an essential tool for conducting comparative analyses to identify the main drivers of diversification
- most of the cave-adapted lineages are of Miocene origin (23 to 5 million years ago) and most diversification events happened in Pleistocene (2.5 million years ago) supporting the hypothesis that the onset of seasonality and glacial cycles are one of the main drivers of cave diversification
- number of species of all three groups is almost double what was known before, confirming Dinarides as a World’s hotspot for cave fauna
- in the case of predicted climate warming scenario almost all species will suffer geographical shift in suitable habitat, and given low mobility of these species and fragmentation of karst systems it is highly improbable that they will be able to move and colonize new areas
- in the case of highest predicted temperature increase, several species will completely lose suitable habitats, probably causing their extinction
A large collection of the Dinaric cave spiders from the families Dysderidae and Leptonetidae and genus Troglohyphantes has been assembled and georeferenced data on all the caves have been collected.
All samples have been sequenced and phylogenetic trees for the three groups have been inferred.
Applying several species delimitation methods resulted in a major increase in a number of recognized species for these three groups: from 74 previously known to as much as 115 different species.
Potential present, past and future distributions were modeled for each species using ecological niche modeling approach. Also, the sensitivity of cave spider populations to global warming was evaluated. In the case of a high emission scenario (the highest predicted temperature increase), several species will lose suitable habitats and will potentially be threatened with extinction.

RESULTS, EXPLOITATION, AND DISSEMINATION
Currently, 3 research papers are being prepared for publishing. I attended 6 international conferences during the action and on all of them I presented the results of the project. I attended: IV Iberian Congress of Biological Systematics, 31st European Congress of Arachnology, 24th International Conference on Subterranean Biology (the biggest event in the field of subterranean biology), XXXVII Annual Meeting of the Willi Hennig Society, 9th Biennial Conference of the International Biogeography Society and XXI International Congress of Arachnology (the main event in the field of arachnology). Besides transmitting my results to the scientific community, I designed actions to reach wider audiences. I particularly focused on disseminating my research to young people by organizing the exhibition on cave spiders at the Faculty of Biology at the University of Barcelona, by organizing a series of scientific talks (SEMBIO) held at the Natural History Museum in Barcelona.
Although Dinarides are well known as a World’s hotspot for highly adapted cave fauna, very little is known about it and knowledge on most groups originates from the middle of 20th century. This project for the first time combines several state-of-the-art approaches to understand current diversity, historical reasons for it and potential threats caused by anthropogenic global climate change to one of the most abundant groups on the Dinarides- cave spiders.
Discovery of new species has a major impact on nature conservation efforts. For example, the discovery that one species that was known from 300 km long distribution range is in fact a complex of 5 different species, each with much smaller distribution areas, has a large impact on their protection, especially if they inhabit regions with high touristic and development pressure. On the other hand, touristic caves can be an economic boost for the local society and a great instrument to raise awareness of rich a fragile ecosystem surrounding us, but it is necessary to know the cave ecosystem well to protect it and display it in the best possible manner.
On of the biggest spiders in Dinaric caves, adult male of Parastalita stygia
A male of a new species from genus Troglohyphantes from Croatia
A male of Leptonetid Sulcia orientalis, feeding on a cave Pseudoscorpion caught in it's web
Collecting in a small but rich cave Pecina kod Krstaca in Montenegro