Article

Fundamental research questions in subterranean biology

November 2020
Biological reviews of the Cambridge Philosophical Society 95:1855–1872

DOI:10.1111/brv.12642

Authors:

Stefano Mammola

Italian National Research Council

Isabel R. Amorim

University of the Azores, Terceira, Portugal

Maria Elina Bichuette

Universidade Federal de São Carlos

Paulo A.V. Borges

University of the Azores

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Five decades ago, a landmark paper in Science titled The Cave Environment heralded caves as ideal natural experimental laboratories in which to develop and address general questions in geology, ecology, biogeography, and evolutionary biology. Although the 'caves as laboratory' paradigm has since been advocated by subterranean biologists, there are few examples of studies that successfully translated their results into general principles. The contemporary era of big data, modelling tools, and revolutionary advances in genetics and (meta)genomics provides an opportunity to revisit unresolved questions and challenges, as well as examine promising new avenues of research in subterranean biology. Accordingly, we have developed a roadmap to guide future research endeavours in subterranean biology by adapting a well-established methodology of 'horizon scanning' to identify the highest priority research questions across six subject areas. Based on the expert opinion of 30 scientists from around the globe with complementary expertise and of different academic ages, we assembled an initial list of 258 fundamental questions concentrating on macroecology and microbial ecology, adaptation , evolution, and conservation. Subsequently, through online surveys, 130 subterranean biologists with various backgrounds assisted us in reducing our list to 50 top-priority questions. These research questions are broad in scope and ready to be addressed in the next decade. We believe this exercise will stimulate research towards a deeper understanding of subterranean biology and foster hypothesis-driven studies likely to resonate broadly from the traditional boundaries of this field.

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Freshwater Meiofauna—A Biota with Different Rules?

Chapter

Mar 2023

Great divergences arise when comparing the ecology of meiofauna in freshwater and marine ecosystems. Emphasizing the main differences between freshwater meiofauna and their marine counterparts, we will go on a stepwise journey through three major frontiers in freshwater research, which in turn are hierarchically interrelated: biodiversity, community organization (e.g. food webs structure), and ecosystem processes (e.g. metabolism and organic carbon breakdown). The starting point of this chapter is one of the utmost frontiers, both in marine and freshwater research: meiofaunal diversity. Especially in freshwater ecosystems diversity becomes evident since, here, habitats extend as highly disconnected biotopes, each characterized by an often fundamentally different biocenosis. From the biodiversity level, we move up the theoretical hierarchy to assess the role of meiofauna as an integral part of benthic food webs. Recent research underlines the role of freshwater meiofauna as highly connected nodes and shows their pivotal role in the transfer of energy and carbon along food chains. Distributed over all trophic levels, this structure contrasts with the prevailing conception of meiofauna in food webs, where meiofauna often are considered rather marginal units. Finally, we apply allometric principles from the metabolic theory of ecology in order to assess the role of freshwater meiofauna in the functioning of the benthic systems. With a novel modelling framework we develop an analytical perspective, showing that secondary production of micro- and meiobenthic communities can predict microbial decomposition rates within the benthic interface. Our results demonstrate that productive micro- and meiobenthos act as catalysers in the system of organic carbon breakdown and recycling. These findings underline the relevance of freshwater meiofauna within the biogeochemical carbon cycle. The mechanistic forces behind the processes involved require future experimental research.

Cave Meiofauna—Models for Ecology and Evolution

Chapter

Mar 2023

Alejandro Martínez

Caves can be used as model systems for developing and understanding evolutionary and ecological theory. Yet, most scientists have paid little attention to cave meiofaunal communities, thereby potentially underestimating subterranean biodiversity. To date, meiofauna has been recorded in only 2026 caves, totalling 31% of caves for which information on aquatic fauna is available around the world. However, these records primarily originate from Europe and the Western Mediterranean and focus on target species, rather than on describing entire communities. Of the 1856 meiofaunal species recorded in caves, 699 might be regarded as restricted to subterranean habitats. Most of those species belong to Arthropoda, with Copepoda the richest species group, both in terms of the number of species recorded and the number of taxa restricted to the subterranean world. Different models have been proposed to explain the origin of meiofaunal cave lineages, but testing them is hampered by the lack of phylogenetic information for most taxa. Although the current lack of diversity data renders studies at a community level challenging, studies to date suggest that cave meiofauna might play a central role in carbon cycling and crucially affect the composition of the groundwater in inland and coastal aquifers. The fundamental ecosystem services that aquifers provide and the pivotal role groundwater discharge attains in the chemical balance of the ocean offer new horizons for future research on cave meiofauna. Cave meiofauna might affect our everyday life much more than we have so far imagined.

Fundamental Science and Engineering Questions in Planetary Cave Exploration

Article

Full-text available

Nov 2022

Nearly half a century ago, two papers postulated the likelihood of lunar lava tube caves using mathematical models. Today, armed with an array of orbiting and fly-by satellites and survey instrumentation, we have now acquired cave data across our solar system—including the identification of potential cave entrances on the Moon, Mars, and at least nine other planetary bodies. These discoveries gave rise to the study of planetary caves. To help advance this field, we leveraged the expertise of an interdisciplinary group to identify a strategy to explore caves beyond Earth. Focusing primarily on astrobiology, the cave environment, geology, robotics, instrumentation, and human exploration, our goal was to produce a framework to guide this subdiscipline through at least the next decade. To do this, we first assembled a list of 198 science and engineering questions. Then, through a series of social surveys, 114 scientists and engineers winnowed down the list to the top 53 highest priority questions. This exercise resulted in identifying emerging and crucial research areas that require robust development to ultimately support a robotic mission to a planetary cave—principally the Moon and/or Mars. With the necessary financial investment and institutional support, the research and technological development required to achieve these necessary advancements over the next decade are attainable. Subsequently, we will be positioned to robotically examine lunar caves and search for evidence of life within martian caves; in turn, this will set the stage for human exploration and potential habitation of both the lunar and martian subsurface.

Unveiling the nature of a miniature world: a horizon scan of fundamental questions in bryology

Article

Full-text available

Apr 2022
J BRYOL

Introduction Half a century since the creation of the International Association of Bryologists, we carried out a review to identify outstanding challenges and future perspectives in bryology. Specifically, we have identified 50 fundamental questions that are critical in advancing the discipline. Methods We have adapted a deep-rooted methodology of horizon scanning to identify key research foci. An initial pool of 258 questions was prepared by a multidisciplinary and international working group of 32 bryologists. A series of online surveys completed by a broader community of researchers in bryology, followed by quality-control steps implemented by the working group, were used to create a list of top-priority questions. This final list was restricted to 50 questions with a broad conceptual scope and answerable through realistic research approaches. Key results The top list of 50 fundamental questions was organised into four general topics: Bryophyte Biodiversity and Biogeography; Bryophyte Ecology, Physiology and Reproductive Biology; Bryophyte Conservation and Management; and Bryophyte Evolution and Systematics. These topics included 9, 19, 14 and 8 questions, respectively. Conclusions Although many of the research challenges identified are not newly conceived, our horizon-scanning exercise has established a significant foundation for future bryological research. We suggest analytical and conceptual strategies and novel developments for potential use in advancing the research agenda for bryology.

Photoreceptor genes in a trechine beetle, Trechiama kuznetsovi, living in the upper hypogean zone

Article

Full-text available

May 2023

To address how organisms adapt to a new environment, subterranean organisms whose ancestors colonized subterranean habitats from surface habitats have been studied. Photoreception abilities have been shown to have degenerated in organisms living in caves and calcrete aquifers. Meanwhile, the organisms living in a shallow subterranean environment, which are inferred to reflect an intermediate stage in an evolutionary pathway to colonization of a deeper subterranean environment, have not been studied well. In the present study, we examined the photoreception ability in a trechine beetle, Trechiama kuznetsovi, which inhabits the upper hypogean zone and has a vestigial compound eye. By de novo assembly of genome and transcript sequences, we were able to identify photoreceptor genes and phototransduction genes. Specifically, we focused on opsin genes, where one long wavelength opsin gene and one ultraviolet opsin gene were identified. The encoded amino acid sequences had neither a premature stop codon nor a frameshift mutation, and appeared to be subject to purifying selection. Subsequently, we examined the internal structure of the compound eye and nerve tissue in the adult head, and found potential photoreceptor cells in the compound eye and nerve bundle connected to the brain. The present findings suggest that T. kuznetsovi has retained the ability of photoreception. This species represents a transitional stage of vision, in which the compound eye regresses, but it may retain the ability of photoreception using the vestigial eye. Supplementary Information The online version contains supplementary material available at 10.1186/s40851-023-00208-7.

Life-History Traits and Acclimation Ability of a Copepod Species from the Dripping Waters of the Corchia Cave (Apuan Alps, Tuscany, Italy)

Article

Full-text available

Apr 2023

Copepods are the dominant crustacean group in groundwater, where they perform valuable ecosystem services related to carbon recycling. The life-history traits of stygobitic (groundwater-obligate dweller) copepods, however, have only been casually studied in the past. In addition, next to nothing is known about the responses of stygobitic copepods to climate change. In this study, we investigated the life-history traits and respiratory metabolism of a species of harpacticoid copepods, Moraria sp., endemic to the Corchia Cave in the Apuan Alps (Italy). We collected the specimens of Moraria sp. from the dripping waters of the cave and observed their development, survival, and reproduction rates in the laboratory for one year. We also evaluated the acclimation ability of adult females of Moraria sp. by measuring their oxygen consumption in a temperature range from 8 °C (average annual temperature of the dripping water in the Stalactites Gallery of the Corchia Cave) to 12.5 °C (maximum temperature of the dripping water of the cave expected according to climate change scenarios in 2100). Our results indicate that Moraria sp. Is a stenothermal species showing remarkable stygobitic traits (long life span, low metabolic rates). We noted that the metabolism of this species is significantly affected by small (+1.5 °C) thermal changes. Our results showed no metabolic compensation occurring in this species over two weeks of exposure to temperatures higher than 8 °C. The outcomes of this study suggest that Moraria sp. May not be able to tolerate thermal changes brought on by climate change.

Aliens in caves: the global dimension of biological invasions in subterranean ecosystems

Article

Full-text available

May 2023

Alien species are a significant threat to natural ecosystems and human economies. Despite global efforts to address this challenge, the documented number of alien species is rapidly increasing worldwide. However, the magnitude of the impact of alien species may vary significantly across habitats. For example, some habitats are naturally less prone to biological invasions due to stringent abiotic and biotic characteristics, selecting for a limited number of introduced species possessing traits closely related to the native organisms. Subterranean ecosystems are quintessential examples of habitats with strong environmental filters (e.g. lack of light and scarcity of food), driving convergent adaptations in species that have successfully adapted to life in darkness. Despite these stringent environmental constraints, the number of records of alien species in subterranean ecosystems has increased in recent decades, but the relevant literature remains largely fragmented and mostly anecdotal. Therefore, even though caves are generally considered very fragile ecosystems, their susceptibility to impacts by alien species remains untested other than for some very specific cases. We provide the first systematic literature survey to synthesise available knowledge on alien species in subterranean ecosystems globally. This review is supported by a database summarising the available literature, aiming to identify gaps in the distribution and spread of alien invertebrate species in subterranean habitats, and laying the foundations for future management practices and interventions. First, we quantitatively assessed the current knowledge of alien species in subterranean ecosystems to shed light on broader questions about taxonomic biases, geographical patterns, modes of dispersal, pathways for introductions and potential impacts. Secondly, we collected species-specific traits for each recorded alien species and tested whether subterranean habitats act as ecological filters for their establishment, favouring organisms with pre-adaptive traits suitable for subterranean life. We found information on the presence of 246 subterranean alien species belonging to 18 different classes. The dominant alien species were invertebrates, especially insects and arachnids. Most species were reported in terrestrial subterranean habitats from all continents except Antarctica. Palaearctic and Nearctic biogeographic regions represented the main source of alien species. The main routes of introductions into the recipient country are linked to commercial activities (84.3% of cases for which there was information available). Negative impacts have been documented for a small number of case studies (22.7%), mostly related to increased competition with native species. For a limited number of case studies (6.1%), management strategies were reported but the effectiveness of these interventions has rarely been quantified. Accordingly, information on costs is very limited. Approximately half of the species in our database can be considered established in subterranean habitats. According to our results, the presence of suitable traits grants access to the stringent environmental filter posed by subterranean environments, facilitating establishment in the new habitat. We recommend that future studies deepen the understanding of invasiveness into subterranean habitats, raising public and scientific community awareness of preserving these fragile ecosystems.

Cave-dwelling fauna of Costa Rica: current state of knowledge and future research perspectives

Article

Full-text available

Dec 2023

This study focused on the cave fauna of Costa Rica, which has remained relatively understudied despite the presence of more than 435 recorded natural caves and artificial subterranean sites. We collected and reviewed all available literature data on cave fauna in Costa Rica and created the first comprehensive review of the existing information. In addition, we report new records from field surveys conducted between 2015 and 2018. This study reported approximately 123 animal species, whereas the remaining records (n = 82) represented taxa that could not be identified at the species level. Data were collected from 127 locations throughout the country, with new cave fauna records from 41 sites. Notably, we reported the first occurrence of the true bug Amnestus subferrugineus (Westwood 1837) within Costa Rican caves, which represents an addition to the country's faunal inventory. As this study highlights the knowledge gaps in the subterranean fauna, it will serve as an important stepping stone for future research and conservation efforts related to caves in Costa Rica.

Sit-and-wait foraging is not enough in food-deprived environments: evidence from groundwater and salamanders

Article

Dec 2023

Raoul Manenti

Keywords: activity ambush freshwater interaction optimal foraging predatoreprey sit-and-wait wide active foraging Foraging strategies are fundamental traits that characterize predators, with strong differences between sit-and-wait predators and active-searching predators. Optimal foraging theory predicts that environmental conditions affect the efficiency of these strategies, with active predators being favoured when prey are scarce and difficult to detect. Subterranean habitats are ideal models to study the effectiveness of foraging strategies. Laboratory studies on fish and salamander predators showed that active foraging often characterizes cave-adapted species, but field studies demonstrating the advantages of active foraging for growth and survival are lacking. In this study, we assessed how predators displaying a sit-and-wait strategy can cope with the variable costs of foraging under different ecological contexts, such as cave and surface environments. We performed a cross-environment experiment that was repeated in 3 years by rearing salamander, Salamandra salamandra, larvae from caves and surface streams in cages placed in both surface and cave environments. We measured larval growth (weight and total length) repeatedly every 10e20 days, from March to July, and assessed water temperature variation, prey availability and metamorphosis achievement in the rearing sites. Larvae in stream cages grew larger than larvae in subterranean cages, which showed negative growth. Our results suggest that the sit-and-wait strategy does not provide enough prey for development in cave environments, irrespective of larvae origin. In food-deprived environments, active foraging is necessary to obtain the energy required for the basic functions of the organisms exploiting them.

Recent Advances in the Behavioral Ecology of European Plethodontid Salamanders

Article

Full-text available

Nov 2023

There is a recent growing interest in the study of evolutionary and behavioral ecology of amphibians. Among salamanders, Plethodontidae is the most speciose family, with more than 500 species, while in Europe, there are only 8 species, all belonging to the genus Speleomantes. European plethodontids recently received increasing attention with regard to the study of their natural history, ecology and behavior; however, the lack of standardized data, especially for the latter, hampers comparative analysis with the species from the New World. We here synthetized the recent advances in Speleomantes behavioral ecology, considering as a starting point the comprehensive monography of Lanza and colleagues published in 2006. We identified the behavioral categories that were investigated the most, but we also highlighted knowledge gaps and provided directions for future studies. By reviewing the scientific literature published within the period 2006–2022, we observed a significant increase in the number of published articles on Speleomantes behavior, overall obtaining 36 articles. Behavioral studies on Speleomantes focused mainly on trophic behavior (42%), and on intraspecific behavior (33%), while studies on pheromonal communication and interspecific behavioral interactions were lacking. In addition, most of the studies were observational (83%), while the experimental method was rarely used. After providing a synthesis of the current knowledge, we suggest some relevant topics that need to be considered in future research on the behavioral ecology of European plethodontids, highlighting the importance of a more integrative approach in which both field observations and planned experiments are used.

Temperature variation in caves and its significance for subterranean ecosystems

Article

Full-text available

Nov 2023

Climate change affects all ecosystems, but subterranean ecosystems are repeatedly neglected from political and public agendas. Cave habitats are home to unknown and endangered species, with low trait variability and intrinsic vulnerability to recover from human-induced disturbances. We studied the annual variability and cyclicity of temperatures in caves vis-à-vis surface in different climatic areas. We hypothesize that cave temperatures follow the average temperature pattern at the surface for each location with a slight delay in the signal, but we found three different thermal patterns occurring in caves: (1) high positive correlation and a similar thermal pattern to the surface, (2) low correlation and a slight thermal delay of the signal from the surface, and (3) high negative correlation with an extreme delay from the surface. We found daily thermal cycles in some caves, which may potentially control the circadian rhythms of cave organisms. Our results show that caves had lower thermal amplitude than the surface, and that thermal averages within caves approximately correspond to the to the annual average of surface temperature. Caves buffer external temperature and act as refugia for biota in extreme climatic events. Likewise, temperature increases at surface will lead to increment in caves, threatening subterranean biota and ecosystem services.

Assessment of occurrence, diversity, and biomass of macroinvertebrates in Swiss groundwater systems using citizen science data

Article

Full-text available

Nov 2023

Groundwater is a vast ecosystem harboring a high diversity of specialized taxa. Despite its diversity, groundwater is a still relatively unexplored and threatened ecosystem. Especially the linkage of groundwater with other ecosystems remains largely unknown from the perspective of groundwater fauna. Here, we used citizen science data to get a first baseline knowledge of the occurrence, diversity, and biomass of major macroinvertebrate groups found in shallow groundwater systems of Switzerland. We investigated all organisms collected from the groundwater in 346 spring catchment boxes of municipal drinking water providers. We morphologically identified the organisms on a broad taxonomic level and estimated their biomass and pigmentation using automated image processing. Crustaceans, particularly Niphargus and groundwater isopods, were the most common taxa of obligate groundwater organisms. We also found a surprisingly high number of macroinvertebrates associated with surface and subsurface ecosystems. These taxa might be accidentally entering the groundwater or use it as temporary habitat. In both cases they possibly contribute essential allochthonous energy imports from the surface. We found a positive relationship between the estimated biomass of macroinvertebrates in the samples and the occurrence and abundance of Niphargus . Owing to the widespread occurrences of surface and subsurface macroinvertebrates in our groundwater samples, our study provides evidence for common interactions between groundwater, soil, and surface ecosystems.

Species richness, occurrence and rarity of bats in Brazilian caves

Article

Full-text available

Oct 2023
AUSTRAL ECOL

Caves are among the most important roosts of hundreds of bat species worldwide. However, caves can be formed in different lithologies. Cave structure and characteristics, which are shaped by lithology, can, in turn, influence roost preferences for different bat species. Therefore, cave lithology and characteristics can help us to better understand why some bat species may be rare in some caves and common in others. Brazil is a continental country, rich in bat species (181 spp.), lithologies and caves (>23 000). However, only a small fraction of the known caves has been sampled for bats so far, with no emphasis on the role lithology may have. Based on a literature review and using data on bat occurrence, in this study, we investigated the influence of lithology on bat species richness and rarity in Brazilian caves. We evaluated 117 studies, including data from 552 caves, and updated the number of bat species occurring in Brazilian caves to 81. Species richness differed between lithologies: carbonate caves had higher species richness, whereas iron caves had lower species richness. Richness was positively related to carbonate caves and with cave size: the bigger the cave, the more species‐rich it tends to be. Overall, caves in the Cerrado had the highest species richness, followed by Atlantic Forest, Caatinga caves and Amazonian caves. Thirteen species can be considered as primarily cave‐dwelling species, recorded in 10%–20% of the caves. Rarity was common among primarily cave‐dwelling species. Nearly 22% of the sampled caves harboured endangered species, reaching 53% of the species‐richest caves. Our analysis provides a comprehensive baseline for bat fauna in different types of caves in Brazil. Even so, we strongly recommend the establishment of long‐term monitoring of population trends for bats in Brazilian caves, which is necessary information but almost non‐existing for the country.

Behavioural adjustments enable the colonization of subterranean environments

Article

Full-text available

Oct 2023

Specialized subterranean species are iconic examples of convergent evolution driven by environmental constraints, representing an ideal model system for eco-evolutionary studies. However, scientific research on the behavioural adaptations of subterranean organisms has lagged and is biased mostly towards a few model species. Through a systematic literature review, we aimed to assess quantitatively whether a congruent evolution of behavioural traits among subterranean species exists. We considered four types of behaviours (exploratory, feeding, social and anti-predator) and tested predictions about their occurrence among species with different degrees of adaptation to subterranean environments. We argue that these behaviours constitute the earliest adaptations to three main ecological factors characterizing subterranean habitats, namely the constant darkness, the limited food resources and the reduced predator pressure. Darkness selects for individuals that rely on non-visual cues to explore their surroundings, track food resources and locate potential sexual partners. The reduced availability of food promotes high foraging plasticity and deters species from adopting aggressive behaviours towards conspecifics. The reduced predator pressure allows species to abandon specific anti-predator behaviours and permits safer execution of their biological activities. Our analyses show that these four behaviours are likely to represent the result of an early convergent adaptation to the subterranean realm.

Hypogeal fauna of the military subterranean fortification Forte di Vernante Opera 11 "Tetto Ruinas" (Piedmont, Italy)

Conference Paper

Full-text available

Sep 2023

The military subterranean fortification Forte di Vernante Opera 11 "Tetto Ruinas" is not mentioned in the extensive specific literature about the NW Alps underground works. Only the project in the Military Engineers Corps archives is known, however, the survey recently detected by our research association Biologia Sotterranea Piemonte – Gruppo di Ricerca highlights differences from the original map. On the contrary, pubblications about the hypogeal fauna in this artificial cavity are numerous. Two new species of spiders with remarkable adaptations to the underground environment were discovered by Angelo Morisi (1943-2016): the Linyphiidae Troglohyphantes konradi Brignoli, 1975 and the Nesticidae Typhlonesticus morisii (Brignoli, 1975). Subsequently, other adapted to this particular environment spiders were observed, such as Kryptonesticus eremita (Simon, 1880) and Leptoneta crypticola Simon, 1907. Spiders with less evident adaptations were reported for this cavity, such as Tegenaria silvestris L. Koch, 1872, Pimoa rupicola (Simon, 1884), Meta menardi (Latreille, 1804), Metellina merianae (Scopoli, 1763). Terrestrial Crustacean adapted to underground environment are present in this fort: Buddelundiella zimmeri Verhoeff, 1930 and Trichoniscus voltai Arcangeli, 1948. Among the Miriapods were observed the Chilopoda Eupolybothrus longicornis (Risso, 1826) and Lithobius microps Meinert, 1868, and the Diplopoda Plectogona vignai draco (Strasser, 1975), a very specialized organism, and the larger and less adapted Callipus foetidissimus (Savi, 1819). The troglophile grasshopper Dolichopoda azami Saulcy, 1893 is very common in the cavity. Of considerable interest are the anophthalmous beetle Duvalius carantii (Sella, 1874), and the very rare Staphylinidae Blepharhymenus mirandus Fauvel, 1899. Moreover, it is possible to observe the cave salamander Speleomantes strinatii (Aellen, 1958) and different Chiroptera species. The association Biologia Sotterranea Piemonte - Gruppo di Ricerca deals mainly the study of subterranean species and environments and their conservation. Our last twenty years research in this subterranean military cavity have allowed to observe and monitor the presence of all the mentioned in the bibliography organisms, and to document the presence of other 20 species. Our studies in this and other artificial cavities of Piedmont highlight the presence of different extremely adapted to the hypogeal environment species, reiterating the importance of the subterranean fauna monitoring in the artificial cavities too, and the presence of these organisms due to some biotic and abiotic environmental factors, regardless of the natural or artificial origin of the cavity.

A new troglobitic species of the genus Troglocoelotes Zhao & S. Li, 2019 (Araneae, Agelenidae, Coelotinae) from Guizhou, China

Article

Full-text available

Jul 2023

Troglocoelotes Zhao & S. Li, 2019 is the only known genus of Coelotinae of which all species have deep morphological adaptations to the subterranean environment, such as depigmentation of body, degenerated or absent eyes and, frequently, with attenuated bodies and/or appendages. Four species of Troglocoelotes have been reported from Guizhou Province, China. A new funnel-web spider of the genus Troglocoelotes is described and illustrated on the basis of a single female specimen from Tongren City, Guizhou: Troglocoelotes sinanensis sp. nov. Additionally, photos of the collection site and a distribution map are also provided.

Phylogenetic structure and molecular species delimitation hint a complex evolutionary history in an Alpine endemic Niphargus clade (Crustacea, Amphipoda)

Article

Full-text available

Jul 2023
ZOOL ANZ

How to map potential mesovoid shallow substratum (MSS) habitats? A case study in colluvial MSS

Article

Full-text available

Apr 2023

Understanding habitat extension that limits species distribution is a crucial tool for management and conservation, in which habitat mapping plays a pivotal role. The mesovoid shallow substratum (MSS) is a type of shallow subterranean habitat with an important conservation value for invertebrate communities, functioning as climatic/reproductive refuge, biogeographic corridor and/or permanent habitat. Methodologies to map the mesovoid shallow substratum (MSS) are currently lacking. We propose a novel method for colluvial MSS habitat mapping, combining geographic information systems, geological maps, and geological knowledge on the habitat genesis. We tested and validated the efficiency of the method using the Arrábida karst area (Portugal) as a model. The method allowed the remote detection of MSS habitats suitable for invertebrate communities ex situ within the study area, and enabled the estimation of habitat extent. The faunal communities sampled in the selected location were dominated by arthropods, especially insects, showcasing the efficacy of this mapping method to detect suitable MSS habitats. The use of this method considerably reduces the in situ scouting area, providing a more efficient way of locating these habitats. The MSS is protected under EU legislation concerning floral communities and geological features, completely neglecting its faunal communities. This method also allows to estimate potential MSS habitat extension in several lithologies, facilitating the implementation of invertebrate prospections, and the establishment of more effective conservation measures.

Functional convergence underground? The scale-dependency of community assembly processes in European cave spiders

Preprint

Full-text available

Mar 2023

Understanding how species assemble into communities is a central tenet in ecology. One of the most elusive questions is the relative contribution of environmental filtering versus limiting similarity. Important advances in this area have been achieved by looking at communities through a functional lens (i.e., the traits they express), so as to derive principles valid across species pools. Yet, even using traits in lieu of taxonomy, the issue remains controversial because i) environmental filtering and limiting similarity often act simultaneously in shaping communities; and ii) their effect is scale-dependent. We exploited the experimental arena offered by caves, island-like natural laboratories characterized by largely constant environmental gradients and a limited diversity of species and interactions. Leveraging uniquely available data on distribution and traits for European cave spiders, we tested explicit hypotheses about variations in community assembly rules across ecological gradients and scales. We demonstrate that environmental filtering and limiting similarity shape cave communities acting on trait evolution in opposing directions. These effects are strongly scale dependent, varying along multiple environmental gradients. Conversely, the effect of geography on trait composition is weak, indicating that trait turnover in space happens primarily by substitution of species pursuing similar functions due to strong environmental filters. Our findings reconcile contrasted views about the relative importance of the two main mechanisms shaping patterns of biodiversity, and provide a conceptual foundation to account for scaling effects in the study of community assembly.

Coastal karst aquifers and submarine springs: what future for their water resources?

Article

Dec 2022

This paper is intended to be a reminder of a series of scientific works whose origin is largely attributable to G. de Marsily, without attempting to make an exhaustive overview of submarine springs and coastal karst aquifers. The main results show that coastal karst aquifers with their submarine outlets and the possibility of natural seawater intrusion are particularly fragile and must be studied and managed with appropriate tools. For the coming decades, the evolution of the climate as results from the IPCC scenarios leads us to question the effects of the increase of sea level on this coastal resource, and the effects of frequent and severe droughts, added to an increase in withdrawals from aquifers caused by the coastalisation of the population.

Lithology and disturbance drive cavefish and cave crayfish occurrence in the Ozark Highlands ecoregion

Article

Full-text available

Nov 2022

Diverse communities of groundwater-dwelling organisms (i.e., stygobionts) are important for human wellbeing; however, we lack an understanding of the factors driving their distributions, making it difficult to protect many at-risk species. Therefore, our study objective was to determine the landscape factors related to the occurrence of cavefishes and cave crayfishes in the Ozark Highlands ecoregion, USA. We sampled cavefishes and cave crayfishes at 61 sampling units using both visual and environmental DNA surveys. We then modeled occurrence probability in relation to lithology and human disturbance while accounting for imperfect detection. Our results indicated that occurrence probability of cave crayfishes was negatively associated with human disturbance, whereas there was a weak positive relationship between cavefish occurrence and disturbance. Both cavefishes and cave crayfishes were more likely to occur in limestone rather than dolostone lithology. Our results indicate structuring factors are related to the distribution of these taxa, but with human disturbance as a prevalent modifier of distributions for cave crayfishes. Limiting human alteration near karst features may be warranted to promote the persistence of some stygobionts. Moreover, our results indicate current sampling efforts are inadequate to detect cryptic species; therefore, expanding sampling may be needed to develop effective conservation actions.

Approches analytiques en biogéographie : progrès et défis

Chapter

Sep 2022

Isabel Sanmartin

Les progrès récents des méthodes d’analyse en biologie, impliquant différentes disciplines, ouvrent un large panel d’études qui fait aujourd’hui de la biogéographie une approche intégrative de l’évolution du vivant. En tant que telle, la biogéographie va bien au-delà d’une simple description de la répartition des espèces vivantes sur Terre.La biogéographie est une discipline où écologistes et évolutionnistes cherchent à comprendre la manière dont les espèces vivantes s’organisent en relation avec leur environnement. Face aux défis majeurs tels que le réchauffement climatique, l’extinction massive d’espèces ou les pandémies, la biogéographie fournit les éléments indispensables à l’élaboration des solutions.La biogéographie présente un large aperçu des différents domaines de cette discipline. Les auteurs internationaux y développent différentes analyses sur la base de leurs connaissances et de leur expérience, illustrant les vastes domaines couverts par la biogéographie.

Caves as simplified settings for testing ecological theory

Conference Paper

Full-text available

Jul 2022

Community assembly, how it changes in space and time, and how it will be affected by global threats, is one of the most pressing issues in ecology, evolution, and conservation biology. To fully understand assembly rules and future community change, one has to delve into multiple interrelated factors, such as the history of environmental and habitat changes in the past, current biotic and abiotic factors, spatial constraints, and future scenarios for all these. Yet, two factors have prevented us from obtaining a complete picture for any organism or system. First, communities are utterly complex, typically encompassing thousands of species and millions of interspecific interactions. Second, future scenarios are overwhelming to model without the challenge of dealing with chaotic systems, where even small changes can lead to large, unpredictable, consequences. We propose to use cave communities as the simplest and easiest setting to model assembly rules and future change across space and time. Caves offer unique opportunities for eco evolutionary studies because they are characterized by a low abundance and diversity of organisms and interactions, they receive limited external inputs, and are easily modelled. The potential of subterranean systems as "natural laboratories" for exploring general, non cave specific agendas has emerged in recent years, with many cave based studies starting to resonate outside caves.

Microbial roles in cave biogeochemical cycling

Article

Full-text available

Sep 2022

Among fundamental research questions in subterranean biology, the role of subterranean microbiomes playing in key elements cycling is a top-priority one. Karst caves are widely distributed subsurface ecosystems, and cave microbes get more and more attention as they could drive cave evolution and biogeochemical cycling. Research have demonstrated the existence of diverse microbes and their participance in biogeochemical cycling of elements in cave environments. However, there are still gaps in how these microbes sustain in caves with limited nutrients and interact with cave environment. Cultivation of novel cave bacteria with certain functions is still a challenging assignment. This review summarized the role of microbes in cave evolution and mineral deposition, and intended to inspire further exploration of microbial performances on C/N/S biogeocycles.

Differential transcriptomic responses to heat stress in surface and subterranean diving beetles

Article

Full-text available

Sep 2022

Subterranean habitats are generally very stable environments, and as such evolutionary transitions of organisms from surface to subterranean lifestyles may cause considerable shifts in physiology, particularly with respect to thermal tolerance. In this study we compared responses to heat shock at the molecular level in a geographically widespread, surface-dwelling water beetle to a congeneric subterranean species restricted to a single aquifer (Dytiscidae: Hydroporinae). The obligate subterranean beetle Paroster macrosturtensis is known to have a lower thermal tolerance compared to surface lineages (CTmax 38 °C cf. 42–46 °C), but the genetic basis of this physiological difference has not been characterized. We experimentally manipulated the thermal environment of 24 individuals to demonstrate that both species can mount a heat shock response at high temperatures (35 °C), as determined by comparative transcriptomics. However, genes involved in these responses differ between species and a far greater number were differentially expressed in the surface taxon, suggesting it can mount a more robust heat shock response; these data may underpin its higher thermal tolerance compared to subterranean relatives. In contrast, the subterranean species examined not only differentially expressed fewer genes in response to increasing temperatures, but also in the presence of the experimental setup employed here alone. Our results suggest P. macrosturtensis may be comparatively poorly equipped to respond to both thermally induced stress and environmental disturbances more broadly. The molecular findings presented here have conservation implications for P. macrosturtensis and contribute to a growing narrative concerning weakened thermal tolerances in obligate subterranean organisms at the molecular level.

Stygofaunal diversity and ecological sustainability of coastal groundwater ecosystems in a changing climate: The Australian paradigm

Article

Full-text available

Sep 2022
FRESHWATER BIOL

1. Coastal aquifers are vital water sources for humanity. Their quality and the ecosystem services they provide depend on the integrity of their subterranean biota. However, current anthropogenic impacts such as climate change effects and coastal population growth place enormous pressure on the sustainability of these environments. 2. Despite the significance of subterranean biota to ecosystem function and the delivery of ecosystem services, stygofauna-groundwater-dwelling aquatic animals-have until recently been largely ignored in aquifer monitoring and management. This issue is of importance in both coastal and inland zones. Common threats in inland and coastal areas are water extraction, reduced recharge caused by aridification, and pollution, while, in coastal zones, additional complications arise from sea-level change and salt water ingress. 3. This review examines stygofaunal diversity, impacts, and future conservation challenges in coastal aquifers. Focussing on Australia, we provide a summary of the available data on stygofaunal communities and distributions; identify and describe potential threats to these communities across the diverse coastal regions of the continent; and propose future research priorities with the goal of facilitating the long-term preservation of these ecosystems on the Australian continent. While we focus this review on Australia, the threats and management issues discussed are relevant globally. 4. Recent subterranean studies in Australia have been primarily undertaken in inland areas, and while coastal data exist, ecological assessment of coastal subterranean ecosystems is incomplete, compromising the efficacy of conservation plans. This review indicates that the Australian continent hosts five major coastal stygofaunal biodiversity areas characterised by heterogeneous community assemblages, involving a total of 17 taxonomic groups spanning microscopic.

A Plea for Considering Processes That Take Place on the Micrometer Scale in Modelling the Groundwater Ecosystems’ Functions

Article

Full-text available

Jun 2022

Susanne I Schmidt

The largest freshwater ecosystem on earth is in the subsurface: the groundwater. It is populated by animals of almost all phyla and by bacteria, archaea, and fungi. Processes on the macro-, meso-, and micro-scale shape this ecosystem. Bioremediation, i.e., the degradation of contaminants, is steered on the scale of micrometers. However, processes that take place on the micrometer scale are still poorly understood and have not been studied extensively. They are usually lacking from models. In this communication, the plea for studying and making models for the processes that take place on the micrometer scale is based on the conceptual model of bottom-up effects of the pore scale environment. Such conceptual models may influence how quantitative models are built by structuring them.

A trait database and updated checklist for European subterranean spiders

Article

Full-text available

May 2022

Species traits are an essential currency in ecology, evolution, biogeography, and conservation biology. However, trait databases are unavailable for most organisms, especially those living in difficult-to- access habitats such as caves and other subterranean ecosystems. We compiled an expert-curated trait database for subterranean spiders in Europe using both literature data (including grey literature published in many different languages) and direct morphological measurements whenever specimens were available to us. We started by updating the checklist of European subterranean spiders, now including 512 species across 20 families, of which at least 192 have been found uniquely in subterranean habitats. For each of these species, we compiled 64 traits. The trait database encompasses morphological measures, including several traits related to subterranean adaptation, and ecological traits referring to habitat preference, dispersal, and feeding strategies. By making these data freely available, we open up opportunities for exploring different research questions, from the quantification of functional dimensions of subterranean adaptation to the study of spatial patterns in functional diversity across European caves.

Towards evidence-based conservation of subterranean ecosystems

Article

Full-text available

Jul 2022
BIOL REV

Subterranean ecosystems are among the most widespread environments on Earth, yet we still have poor knowledge of their biodiversity. To raise awareness of subterranean ecosystems, the essential services they provide, and their unique conservation challenges, 2021 and 2022 were designated International Years of Caves and Karst. As these ecosystems have traditionally been overlooked in global conservation agendas and multilateral agreements, a quantitative assessment of solution-based approaches to safeguard subterranean biota and associated habitats is timely. This assessment allows researchers and practitioners to understand the progress made and research needs in subterranean ecology and management. We conducted a systematic review of peer-reviewed and grey literature focused on subterranean ecosystems globally (terrestrial, freshwater, and saltwater systems), to quantify the available evidence-base for the effectiveness of conservation interventions. We selected 708 publications from the years 1964 to 2021 that discussed, recommended, or implemented 1,954 conservation interventions in subterranean ecosystems. We noted a steep increase in the number of studies from the 2000s while, surprisingly, the proportion of studies quantifying the impact of conservation interventions has steadily and significantly decreased in recent years. The effectiveness of 31% of conservation interventions has been tested statistically. We further highlight that 64% of the reported research occurred in the Palearctic and Nearctic biogeographic regions. Assessments of the effectiveness of conservation interventions were heavily biased towards indirect measures (monitoring and risk assessment), a limited sample of organisms (mostly arthropods and bats), and more accessible systems (terrestrial caves). Our results indicate that most conservation science in the field of subterranean biology does not apply a rigorous quantitative approach, resulting in sparse evidence for the effectiveness of interventions. This raises the important question of how to make conservation efforts more feasible to implement, cost-effective, and long-lasting. Although there is no single remedy, we propose a suite of potential solutions to focus our efforts better towards increasing statistical testing and stress the importance of standardising study reporting to facilitate meta-analytical exercises. We also provide a database summarising the available literature, which will help to build quantitative knowledge about interventions likely to yield the greatest impacts depending upon the subterranean species and habitats of interest. We view this as a starting point to shift away from the widespread tendency of recommending conservation interventions based on anecdotal and expert-based information rather than scientific evidence, without quantitatively testing their effectiveness.

Geologia, Grutas e Fauna Subterrânea do Planalto das Cesaredas, Portugal

Article

Full-text available

Mar 2022

O Planalto das Cesaredas é formado por calcários marinhos do Jurássico Inferior a Superior (Toarciano ao Titoniano, ~180 a 144 milhões de anos) e alberga várias cavidades naturais com condições propícias à vida subterrânea. Localizado a baixa altitude na transição entre o maciço de Montejunto e vale Tifónico das Caldas da Rainha, este afloramento cársico inclui-se no distrito bioespeleológico Lusitânico, unidade biogeográfica que inclui os maciços da Arrábida, Estremenho, Sicó-Condeixa-Alvaiázere, Outil-Cantanhede e os afloramentos calcários da Península de Lisboa. O interesse científico sobre a biologia das grutas das Cesaredas teve o seu despertar há sete décadas e investigações recentes revelaram que a sua fauna estritamente subterrânea é composta sobretudo por invertebrados: moluscos, aracnídeos, miriápodes, crustáceos e insectos. A descoberta de espécies endémicas, i.e., cuja única área de distribuição mundial se encontra confinada ao Planalto das Cesaredas, lança grandes desafios em termos de conservação e urge estabelecer medidas de proteção para salvaguardar a sua biodiversidade subterrânea. Este artigo oferece uma perspectiva sobre a geologia, composição faunística e a ecologia das grutas das Cesaredas.

A collaborative backbone resource for comparative studies of subterranean evolution: The World Asellidae database

Article

Oct 2023

Transition to novel environments, such as groundwater colonization by surface organisms, provides an excellent research ground to study phenotypic evolution. However, interspecific comparative studies on evolution to groundwater life are few because of the challenge in assembling large ecological and molecular resources for species‐rich taxa comprised of surface and subterranean species. Here, we make available to the scientific community an operational set of working tools and resources for the Asellidae, a family of freshwater isopods containing hundreds of surface and subterranean species. First, we release the World Asellidae database (WAD) and its web application, a sustainable and FAIR solution to producing and sharing data and biological material. WAD provides access to thousands of species occurrences, specimens, DNA extracts and DNA sequences with rich metadata ensuring full scientific traceability. Second, we perform a large‐scale dated phylogenetic reconstruction of Asellidae to support phylogenetic comparative analyses. Of 424 terminal branches, we identify 34 pairs of surface and subterranean species representing independent replicates of the transition from surface water to groundwater. Third, we exemplify the usefulness of WAD for documenting phenotypic shifts associated with colonization of subterranean habitats. We provide the first phylogenetically controlled evidence that body size of males decreases relative to that of females upon groundwater colonization, suggesting competition for rare receptive females selects for smaller, more agile males in groundwater. By making these tools and resources widely accessible, we open up new opportunities for exploring how phenotypic traits evolve in response to changes in selective pressures and trade‐offs during groundwater colonization.

The biomimetic potential of novel adaptations in subterranean animals

Article

Full-text available

Oct 2023

Thomas Hesselberg

Subterranean habitats can be considered harsh conditions with lack of light, low nutrients levels and constant high humidity. To thrive under such conditions, cave-adapted species have evolved a range of novel morphological, physiological and behavioural adaptations. These adaptations might have significant biomimetic potential. Biomimetics or biologically inspired design is a relatively new interdisciplinary field that aims to harness the processes and mechanisms in nature that have been optimised over millions of years’ evolution to improve our own technology. There are two main approaches to biologically inspired design—the problem-driven approach starting with an engineering problem and searching through biological equivalents and the solution-driven approach, which starts with a biological example or solution followed by the identification of a suitable engineering application. While the former approach is the most popular and is favoured by engineers, the latter remains the most successful and is typically driven by fundamental biological research. However, few biomimetic solutions or concepts have so far been described from subterranean habitats despite the rich potential. In this review paper, I first outline the theory behind biologically inspired design before I review the few biomimetic related studies of cave adapted organisms mainly based on the exceptional lateral line systems in blind cave fish. However, the main body of the review focuses on identifying and discussing subterranean adaptations with a particular strong potential including biomimetics sensors, adhesion in high humidity and wet conditions and biomaterials

Considerable gene flow in troglomorphic cockroach species across a vast subterranean landscape

Article

Full-text available

Aug 2023

Aim There has been growing interest in non‐cave subterranean habitats and their influence on the evolution of troglomorphic (i.e. ‘subterranean adapted’) species. Studies on the diversification of aquatic subterranean organisms in these habitats generally support the ‘subterranean island’ hypothesis, whereby isolated subterranean refuges lead to patterns of short‐range endemism. However, their terrestrial counterparts have received less attention. We aimed to elucidate the applicability of the ‘subterranean island’ hypothesis to terrestrial subterranean fauna through genetic analyses of two widespread troglomorphic cockroach species. To investigate the influence of subterranean biogeography, we also analysed a closely related species that inhabits ‘classic’ cave environments to represent a contrasting biogeographic comparison. Location Pilbara region, Western Australia, and the Chillagoe‐Mungana Caves, Queensland (Australia). Taxa Cave cockroach species: Nocticola cockingi , Nocticola quartermainei and Nocticola australiensis. Methods We used DArTseq to generate genome‐wide SNPs in 78 samples, and Sanger sequencing to generate 16S mtDNA data. We then applied various population genomic analyses to characterize the distribution of genetic diversity within the three study species. Results We identified distinct genetic clusters within the two Pilbara species; however, there appeared to be a notable lack of discernible population differentiation across large parts of their range (>135 km), opposing the subterranean island hypothesis. The highest level of population differentiation in the three study species was between the two caves in Queensland, ~3 km apart. Main Conclusions The Pilbara subterranean habitat appeared to be conducive to gene flow across relatively large distances, contrasting high levels of endemism observed in other subterranean taxa within the region. The disparate patterns of gene flow among the Pilbara and Queensland study species emphasize the significance of differing subterranean habitats on patterns of dispersal and vicariance. These inferences will inform conservation genetic management of these species, and may help elucidate the evolutionary paradox of widespread subterranean fauna.

First insight into molecular diversity and DNA barcode library of epikarst-dwelling invertebrates in the Western Carpathians

Article

Full-text available

Jul 2023

DNA barcoding represents a handy tool for species identification. In addition, it serves as a complementary approach that improves the characterisation of evolutionary lineages and facilitates the detection of potentially undescribed and cryptic species. Based on the case study in the Western Carpathians, which belong to the Carpathian biodiversity hotspot, we have compiled the first DNA barcode reference library for molecular identification of invertebrates associated with epikarst, a unique, yet understudied, shallow subterranean aquatic habitat that extends at the interface between the soil and carbonate rocks. We analysed invertebrates collected between 2019 and 2020 from epikarst water that continuously seeps into four caves of the Demänovský Cave System in northern Slovakia. The standard barcode marker of the mitochondrial COI gene was amplified in more than 920 individuals of aquatic, semi-aquatic, and terrestrial invertebrates. The final data set consisted of 784 barcode sequences representing 36 morphospecies, the majority (98.3%) belonged to Arthropoda. Automated cluster delineation using the Barcode of Life Data System (BOLD) revealed 60 Barcode Index Numbers (BINs), of which 43 BINs were new to BOLD, representing mostly typical subterranean species. Almost 20% of the morphospecies displayed high intraspecific variation (>2.2%), suggesting the need for further investigation to assess potential taxonomic problems or cryptic diversity. Our results also indicated the existence of several yet undescribed invertebrate species and possible heteroplasmy or COI numts in the collembolan Megalothorax sp. (incertus species group). The resulting DNA barcode library represents a significant advance not only in the characterisation of epikarst biodiversity but also in the understanding of subterranean biodiversity in general, paving the way for future complex evolutionary and biogeographical studies.

Groundwater ecology and evolution: an introduction

Chapter

Jan 2023

Groundwater ecosystems are very diverse in respect to biodiversity and physical environment. These open systems are strongly connected to the open water as well as adjacent terrestrial and atmospheric ecosystems. Groundwater taxa represent a large array of biota including viruses, prokaryotes (bacteria and archaea), microeukaryotes (fungi and protists) and metazoans. Their activities sustain groundwater ecosystem functions (e.g., cycling of material and flow of energy), and the resulting ecosystem services (e.g. purification of water) significantly contribute to human well-being. Research on the ecology and evolution of groundwater organisms dates back to the early 1900s. Our current understanding ranges from biodiversity to biogeography, from genes to mechanisms involved in adaptation and development of specific biological traits, from the inter- and intraspecific interactions to carbon and energy flow through food webs, and from physical–chemical and structural drivers to the role of individual organisms in groundwater ecosystem functioning and services. This research has been providing the basis for integrating ecosystem functions and resulting services into the governance and management of groundwater, thereby generating joint benefits to society and biodiversity. The second edition of “Groundwater Ecology and Evolution” is composed of 24 chapters grouped into six sections that portray the diversity of groundwater research conducted by ecologists and evolutionary biologists. This includes, but is not restricted to, the hydrogeological and hydrochemical attributes of groundwater habitats, the controls and patterns of groundwater biodiversity, the role of organisms in groundwater systems, the evolutionary processes and forces for acquisition of subterranean biological traits, and the way these traits are differently expressed among organisms. Finally, it discusses the challenges and opportunities for conservation of groundwater biodiversity and management of groundwater ecosystems.

Dissolving morphological and behavioral traits of groundwater animals into a functional phenotype

Chapter

Mar 2023

Organismal fitness depends on performance of functional traits. In subterranean biology, function has usually been inferred from either morphology or behavior, but rarely from both. Here we introduce a well-known principle, the “many-to-one relationship of form and function”, stating that enhancement of functional performance is possible in diverse ways, either through morphological, physiological, behavioral or joint morphological-behavioral change. We present general aspects of the functional phenotype (sensory input, locomotion, feeding, reproduction, habitat choice and antipredation mechanisms) and discuss how the selective environment of different subterranean habitats shaped them. Darkness is the only shared property of all subterranean habitats and can explain the most ubiquitous morphological characteristics related to sensory input, reductions of eyes and pigments as well as sensory compensations using other modalities. Other functional traits such as elongated appendages seem to depend on more specific parameters (e.g., low fluid motions), not associated with all subterranean habitats. Therefore, the patterns of morphological and behavioral variation in these functional traits are less predictable. We find fragmented evidence for the “many-to-one relationship”, but also deep gaps in knowledge of basic biology of subterranean species. We conclude that “many-to-one relationship” in morphology and behavior could also be elaborated using physiological and life-history traits, and holds a promise to explain functional phenotypes in variable subterranean environments accounting for different trade-offs.

Life histories in groundwater organisms

Chapter

Jan 2023

Groundwater food webs

Chapter

Jan 2023

Phylogenies reveal speciation dynamics

Chapter

Jan 2023

Ecological and evolutionary jargon in subterranean biology

Chapter

Mar 2023

Subterranean biology has a rich history of a special terminology used to describe the ecological distribution of subterranean species, their mode of colonization and speciation, and their morphology. This special terminology has several sources, including the exotic nature of the habitats, the often bizarre morphology of their inhabitants, as well as the range of evolutionary explanations put forward. While the ecological classifications, especially the Schiner-Racovitza terminology (troglobite, troglophile, etc.), colonization scenarios, and evolutionary classifications (troglomorphy of Christiansen) have been very useful, the time has come to at least minimize their use, if not outright retire them. In the case of ecological classifications, exceptions threaten to overwhelm the categories and rather we recommend to treat species as specialists or generalists. In the case of colonization and speciation, the Climatic Relict and Adaptive Shift hypotheses are easily subsumed in general concepts, especially ecological speciation. In the case of evolutionary classifications, there is little evidence of universality of troglomorphy. We propose that the standard terms of convergence and divergence be used instead.

Classifying groundwater ecosystems

Chapter

Jan 2023

Photoreceptor genes in a trechine beetle, Trechiama kuznetsovi , living in the upper hypogean zone

Preprint

Full-text available

Mar 2023

To address how organisms adapt to a new environment, subterranean organisms whose ancestors colonized subterranean habitats from surface habitats have been studied. Photoreception abilities have been shown to have degenerated in organisms living in caves and calcrete aquifers. Meanwhile, the organisms living in a shallow subterranean environment, which are inferred to reflect an intermediate stage in an evolutionary pathway to colonization of a deeper subterranean environment, have not been studied well. In the present study, we examined the photoreception ability in a trechine beetle, Trechiama kuznetsovi , which inhabits the upper hypogean zone and has a vestigial compound eye. By de novo assembly of genome and transcript sequences, we were able to identify photoreceptor genes and phototransduction genes. Specifically, we focused on opsin genes, where one long wavelength opsin gene and one ultraviolet opsin gene were identified. The encoded amino acid sequences had neither a premature stop codon nor a frameshift mutation, and appeared to be subject to purifying selection. Subsequently, we examined the internal structure of the compound eye and nerve tissue in the adult head, and found potential photoreceptor cells in the compound eye and nerve bundle connected to the brain. The present findings suggest that T. kuznetsovi has retained the ability of photoreception. This species represents a transitional stage of vision, in which the compound eye regresses, but it may retains the ability of photoreception using the vestigial eye.

Environmental factors shaping copepod distributions in cave waters of the Lessinian unsaturated karst (NE-Italy)

Article

Full-text available

Mar 2023

The unsaturated karst represents a transitional zone connecting the land surface to the water table of the underlying saturated zone through percolating water and small perched aquifers. It constitutes a significant groundwater reservoir and hosts a high biodiversity of specialized and endemic species. Whereas investigating this ecotone can shed light on the invertebrate diversity of the whole karst system, ecological studies in the unsaturated karst have been hampered by access, mapping, and sampling challenges. We studied the unsaturated zone of 52 caves in the Lessinian Massif (NE-Italy), which is dominated by carbonate rocks interspersed with spot areas composed mainly of igneous rocks. Our aim was to understand which ecological and historical factors may have shaped the distribution of the groundwater crustacean copepods at a regional spatial scale in the Lessinian unsaturated karst. We collected 33 species belonging to the orders Harpacticoida and Cyclopoida. Species richness estimators and related species accumulation curves suggest an exhaustive sampling effort. A hydrologic analysis performed in a Geographic Information System environment divided the study area in three distinct drainage basins: Eastern Lessini, Lessinian Core, and Western Lessini. Regression analyses indicated that richness of non-stygobitic copepods (i.e., surface-water species which exploit groundwater for different purposes) was mainly driven by inter-basin differences. Richness of stygobitic copepods (i.e., obligate groundwater dwellers) was instead strongly related to lithological features and responded negatively to surface thermal variability. Next, we used a kernel density estimation to spatially explore diversity patterns in the area. The highest density of stygobitic harpacticoids was identified in the Eastern Lessinian basin, which is lithologically more heterogeneous and surrounded by practically non-aquiferous igneous rocks that may limit dispersal. Conversely, the Western Lessinian basin hosted a high density of stygobitic cyclopoid species. This spatial pattern suggests different colonization pathways for the two taxa, with a strong effect of igneous rocks in hampering dispersal of most harpacticoids. Lithological barriers seemingly did not affect non-stygobitic copepods, which were found across the whole area. Altogether, these results emphasize the key role played by the interaction of hydrological features, climate, and lithology in determining different copepod biodiversity patterns in the unsaturated karst.

The Unique Australian Subterranean Dytiscidae: Diversity, Biology, and Evolution

Chapter

Jan 2023

The western half of the Australian arid zone harbours the richest diversity of obligate subterranean dytiscids in the world, which are found in isolated calcrete (carbonate) aquifers. Each calcrete usually supports from one to three beetle species that are locally endemic to a specific calcrete, and display the full array of adaptations to living in a permanently dark, aquatic environment. The origin of this dytiscid diversity likely dates back to the late Miocene to Pliocene when central and western Australia was dominated by a more benign, mesic environment. Subsequent aridification led to relictualisation of the fauna to the calcrete aquifers which, because of their physical isolation from each other, have been described as ‘islands under the desert’. Here we provide an overview of this remarkable fauna of dytiscids, and outline what is currently known about their diversity, life history, respiratory physiology, modes of speciation, population biology, and outline their conservation issues and areas for future research.

Multi-spatial analysis on cave ecosystems to predict the diversity of subterranean invertebrates

Article

Full-text available

Nov 2022
BASIC APPL ECOL

Subterranean habitats around the world can shelter diversified and threatened faunal communities. However, issues related to alterations in the landscape and structure of subterranean habitats still need to be better understood. Therefore, we used a multi-spatial scale analysis of land cover, land use, and cave habitats to predict the diversity of communities of subterranean invertebrates. We hypothesized that changes in land cover promote alterations in both faunal richness and composition and microhabitat diversity and that microhabitat features determined subterranean biodiversity. Sixteen limestone caves were sampled in Brazil at micro, meso, and macro scales using quadrats (1m²), transects (100 meters) as sample units inside caves and buffers with the radius of 100 and 250 meters in the surroundings of the cave entrances. Models performed showed that land cover and land use influenced cave environments, regarding both microhabitats traits and terrestrial invertebrate richness and composition. We also observed a relationship between microhabitat structure and terrestrial invertebrate richness and composition. Our results showed that deforested areas had negative effects on species richness and changed their composition, while natural areas had positive effects on microhabitat diversity. The same effects were observed for both 100 and 250 meters buffers. Invertebrate richness was negatively predicted by deforested areas while positively predicted by natural areas. Richness was also positively predicted by the combination of all microhabitat traits, and dissimilarity of fauna was influenced by microhabitat diversity in mesoscale and microscale by all microhabitat elements. The results highlight the importance of the landscape surrounding the caves to conserve the subterranean habitats and their fauna. Due to the spatial and temporal changes in the global environmental scenario, we argue the urgency of further detailed studies in fragmented landscapes to define minimum areas of protection for cave environments.

High genetic connectivity among large populations of Pteronotus gymnonotus in bat caves in Brazil and its implications for conservation

Article

Full-text available

Oct 2022

Bat caves in the Neotropical region harbor exceptional bat populations (> 100,000 individuals). These populations play a wider role in ecological interactions, are vulnerable due to their restriction to caves, and have a disproportionate conservation value. Current knowledge of bat caves in Brazil is still small. However, systematic monitoring of some bat caves in northeastern Brazil shows that they experience strong population fluctuations over short periods of time, suggesting large-scale movements between roosts and a much broader use of the landscape than previously considered. Spatio-temporal reproductive connectivity between distant populations would change our understanding of the use of roosts among bat species in Brazil, and important gaps in knowledge of long-distance bat movements in the country would be filled. Here, we used ddRADseq data to analyze the genetic structure of Pteronotus gymnonotus across nine bat caves over 700 km. Our results indicate the lack of a clear geographic structure with gene flow among all the caves analyzed, suggesting that P. gymnonotus uses a network of bat caves geographically segregated hundreds of kilometers apart. Facing strong anthropogenic impacts and an underrepresentation of caves in conservation action plans worldwide, the genetic connectivity demonstrated here confirms that bat caves are priority sites for bat and speleological conservation in Brazil and elsewhere. Moreover, our results demonstrate a warning call: the applied aspects of the environmental licensing process of the mining sector and its impact must be reviewed, not only in Brazil, but wherever this licensing process affects caves having exceptional bat populations.

Overcoming shortfalls and impediments in subterranean biology: a challenge for the future

Article

Full-text available

Jul 2022

Since the discovery and description of the first specialized cave species, subterranean fauna stimulated the scientific research of several generations of speleobiologists especially after the publication of Racovitza's classification of cave species, which is still used today, amended for non-karstic areas and groundwaters. More than 28,000 obligate subterranean species are known worldwide; however, these figures are likely to be underestimated since species richness is highly correlated with research effort (Stoch and Galassi 2010). Subterranean ecosystems are very rich in strict endemic species and taxonomic efforts are still quite low (i.e., the so-called "taxonomic impediment"), while several environments are very difficult to be explored (i.e., the "Racovitzan impediment: Ficetola et al. 2018). Furthermore, several paradigms were debated for years. Albeit constrasting hypotheses were conceived to explain the colonization of subsurface habitats, their importance is still debated (i.e., climate relicts vs. adaptive shift in colonization and speciation, dispersal vs. vicariance in shaping distributional patterns, and selective vs. neutral hypotheses in explaining regressive evolution). Moreover, the paradigm of a "truncated functional diversity" of subterranean ecosystems (Gibert and Deharveng 2002) lasted for years but was recently challenged by the discovery of chemoautotrophic ecosystems in hypogenic and anchialine caves, and the recognition that caves are not isolated environments, but they are highly interconnected with surface ecosystems. The increased importance of their conservation (like in the case of GDEs, Groundwater Dependent Ecosystems) was recently recognized, together with their provision of important ecosystem services (Boulton 2020). A deeper knowledge is required to assess biodiversity hotspots as well as to plan efficient monitoring surveys (Mammola et al. 2020). In the last decades, a growing amount of molecular data has been obtained for subterranean species, allowing some of the classical debates on colonization, evolution, and dispersal to be revisited (Bauzà-Ribot et al. 2012); moreover, novel promising techniques like metabarcoding and environmental DNA were applied in field surveys and monitoring efforts. Unfortunately, after more than one century of research in subterranean biology, large gaps remain in our knowledge of phylogeny, richness, and distribution of subterranean fauna (formalized in the so-called Darwinian, Linnean and Wallacean shortfalls), preventing the definition of large-scale sound management and protection plans. It is proposed that data from recent biomolecular techniques coupled with remotely sensed data may enhance biodiversity mapping and conservation and are promising approaches to fill our knowledge gaps. Perhaps this is the greatest challenge that tomorrow's subterranean biologists will face.

Recreational caving impacts of visitors in a high-altitude cave in Bolivian Andes: Main effects on microhabitat structure and faunal distribution

Article

Full-text available

Jul 2022

The cave's physical environment can be affected by tourism activities but only a few studies evaluated how recreational use may affect the cave fauna, mainly in caves with a low number of visitors per year. To test the hypothesis that recreational use led to changes in habitat structure and invertebrate diversity, distinct scales along a cave were analyzed. Distinct areas with and without human visitation were analyzed and transects (10 x 3 m) and quadrats (1 x 1 m) were used to access the invertebrate communities and environmental traits. Thirty-two invertebrate species were recorded, among which six are troglobitic. The similarity of non-troglobitic species differed between the visited and non-visited areas. Substrate composition inside transects differed between the two areas and the differences were higher in the percentage of matrix rock and fine sediments. The distance from the entrance influenced the similarity of non-troglobitic species while troglobitic fauna responded to the proportion of sandy sediment. Inside quadrats, both matrix rock and fine sediments influenced the similarity of non-troglobitic species. Similarity of non-troglobitic species in the visited area was explained by the proportion of matrix rock in transects and quadrats. The proportion of cobbles influenced the similarity of non-troglobitic species in quadrats in the non-visited area. The non-troglobitic species richness inside quadrants was positively related to the amount of guano, wood, fine sediment, boulders, cobbles, matrix rock, sand sediment, and plant debris. Differentiation in habitat structure and faunal composition between the two areas seems to be an effect of distance from the entrance and spatial heterogeneity, but not recreational activities. cave management, impacts, cave conservation, Andes

A Global Perspective on Sustainable Show Cave Tourism

Article

Full-text available

Jun 2022

Caves are among the most visited geological features in the world, attracting over 70 million people every year in more than 1,200 caves worldwide, and amounting up to 800 million Euros in entrance fees alone. The global business of show caves employs roughly 25,000 people directly (management, guides), and at least 100 times more people if we consider the connected tourist activities (souvenir shops, local transport, travel agencies, restaurants, and bars). It is estimated that the whole show cave business has a global commercial value of roughly 2 billion Euros, a number that is increasing constantly. Show caves are generally fragile ecosystems, and care should be taken in their management to safeguard their value for future generations. The international scientific (speleological) community has issued international guidelines for the sustainable development and management of show caves eight years ago, but their application is still far from being applied globally, especially in developing and least developed countries. Cave tourism is expected to increase, especially in countries where caves are abundant but not yet considered as tourist attractions, and where economic and political instability slow down the development of tourism. There are still a lot of possibilities for the opening of new show caves, especially in countries with low Gross Domestic Income (GDI), but their management needs to be sustainable, so that caves become a means of sustaining local economies, educating people on these fragile geo- and ecosystems, and protecting contemporarily their scientific and cultural heritage for future generations.

Life in the Darkness of Caves

Article

Full-text available

Apr 2022

For humans, caves are dark, moist, and often dangerous places. However, caves are also home to many animals that live strange lives: blind beetles that eat bat poop and appreciate it; tiny spiders that spin webs to catch insects, also known as flying food; and white salamanders that swim in cave ponds without getting lost, at least not all the time. Most of these animals do not have eyes—why would you need eyes when you live in the dark? Instead, they have developed other special senses to “see” in the dark. These animals look nothing like the ones you know, and many of them are endangered because they can only live in caves. Mining, pollution, and climate change are threatening cave animals and all their weirdness. Anyone can study and help them, even you!

The role of selection in the evolution of blindness in cave fish

Article

Full-text available

Jun 2020

Horst Wilkens

The forces driving regression of biologically functionless traits remain disputed. There is ongoing debate regarding whether selection, as opposed to disuse and neutral mutations, is involved in this process. Cave species are of particular relevance for study in this regard because in continuous darkness all traits that depend on information from light, such as eyes, dark pigmentation and certain behaviours, abruptly lose their function. Recently, strong selection driving reduction has again been proposed, which relied on modelling analyses based on assumptions such as immigration of surface alleles into the cave forms or no fitness difference existing between Astyanax surface and cave fish. The validity of these assumptions, often applied to reject neutral processes in functionless traits, is questioned in this review. Morphological variation in a trait resulting from genetic variability is typical of biologically functionless traits and is particularly notable in phylogenetically young cave species. It is the most evident indicator of loss of selection, which normally enforces uniformity to guarantee optimal functionality. Phenotypic and genotypic variability in Astyanax cave fish eyes does not derive from genetic introgression by the surface form, but from regressive mutations not being eliminated by selection. This matches well with the principles of Kimura’s neutral theory of molecular evolution.

World Scientists' Warning of a Climate Emergency

Article

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Jul 2020
BIOSCIENCE

We scientists have a moral obligation to clearly warn humanity of any catastrophic threat. In this paper, we present a suite of graphical vital signs of climate change over the last 40 years. Results show greenhouse gas emissions are still rising, with increasingly damaging effects. With few exceptions, we are largely failing to address this predicament. The climate crisis has arrived and is accelerating faster than many scientists expected. It is more severe than anticipated, threatening natural ecosystems and the fate of humanity. We suggest six critical and interrelated steps that governments and the rest of humanity can take to lessen the worst effects of climate change, covering 1) Energy, 2) Short-lived pollutants, 3) Nature, 4) Food, 5) Economy, and 6) Population. Mitigating and adapting to climate change entails transformations in the ways we govern, manage, feed, and fulfill material and energy requirements. We are encouraged by a recent global surge of concern. Governmental bodies are making climate emergency declarations. The Pope issued an encyclical on climate change. Schoolchildren are striking. Ecocide lawsuits are proceeding in the courts. Grassroots citizen movements are demanding change. As scientists, we urge widespread use of our vital signs and anticipate that graphical indicators will better allow policymakers and the public to understand the magnitude of this crisis, track progress, and realign priorities to alleviate climate change. The good news is that such transformative change, with social and ecological justice, promises greater human wellbeing in the long-run than business as usual. We believe that prospects will be greatest if policy makers and the rest of humanity promptly respond to our warning and declaration of a climate emergency, and act to sustain life on planet Earth, our only home.

Scientists' warning on invasive alien species

Article

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Jun 2020

Biological invasions are a global consequence of an increasingly connected world and the rise in human population size. The numbers of invasive alien species – the subset of alien species that spread widely in areas where they are not native, affecting the environment or human livelihoods – are increasing. Synergies with other global changes are exacerbating current invasions and facilitating new ones, thereby escalating the extent and impacts of invaders. Invasions have complex and often immense long‐term direct and indirect impacts. In many cases, such impacts become apparent or problematic only when invaders are well established and have large ranges. Invasive alien species break down biogeographic realms, affect native species richness and abundance, increase the risk of native species extinction, affect the genetic composition of native populations, change native animal behaviour, alter phylogenetic diversity across communities, and modify trophic networks. Many invasive alien species also change ecosystem functioning and the delivery of ecosystem services by altering nutrient and contaminant cycling, hydrology, habitat structure, and disturbance regimes. These biodiversity and ecosystem impacts are accelerating and will increase further in the future. Scientific evidence has identified policy strategies to reduce future invasions, but these strategies are often insufficiently implemented. For some nations, notably Australia and New Zealand, biosecurity has become a national priority. There have been long‐term successes, such as eradication of rats and cats on increasingly large islands and biological control of weeds across continental areas. However, in many countries, invasions receive little attention. Improved international cooperation is crucial to reduce the impacts of invasive alien species on biodiversity, ecosystem services, and human livelihoods. Countries can strengthen their biosecurity regulations to implement and enforce more effective management strategies that should also address other global changes that interact with invasions.

Phenotypic plasticity as a mechanism of cave colonization and adaptation

Article

Full-text available

Apr 2020
eLife

A widely accepted model for the evolution of cave animals posits colonization by surface ancestors followed by the acquisition of adaptations over many generations. However, the speed of cave adaptation in some species suggests mechanisms operating over shorter timescales. To address these mechanisms, we used Astyanax mexicanus, a teleost with ancestral surface morphs (surface fish, SF) and derived cave morphs (cavefish, CF). We exposed SF to completely dark conditions and identified numerous altered traits at both the gene expression and phenotypic levels. Remarkably, most of these alterations mimicked CF phenotypes. Our results indicate that many cave-related traits can appear within a single generation by phenotypic plasticity. In the next generation, plasticity can be further refined. The initial plastic responses are random in adaptive outcome but may determine the subsequent course of evolution. Our study suggests that phenotypic plasticity contributes to the rapid evolution of cave-related traits in A. mexicanus.

iEcology: Harnessing Large Online Resources to Generate Ecological Insights

Article

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Apr 2020
TRENDS ECOL EVOL

Digital data are accumulating at unprecedented rates. These contain a lot of information about the natural world, some of which can be used to answer key ecological questions. Here, we introduce iEcology (i.e., internet ecology), an emerging research approach that uses diverse online data sources and methods to generate insights about species distribution over space and time, interactions and dynamics of organisms and their environment, and anthropogenic impacts. We review iEcology data sources and methods, and provide examples of potential research applications. We also outline approaches to reduce potential biases and improve reliability and applicability. As technologies and expertise improve, and costs diminish, iEcology will become an increasingly important means to gain novel insights into the natural world.

Solutions for humanity on how to conserve insects

Article

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Feb 2020
BIOL CONSERV

The fate of humans and insects intertwine, especially through the medium of plants. Global environmental change, including land transformation and contamination, is causing concerning insect diversity loss, articulated in the companion review Scientists' warning to humanity on insect extinctions. Yet, despite a sound philosophical foundation, recognized ethical values, and scientific evidence, globally we are performing poorly at instigating effective insect conservation. As insects are a major component of the tapestry of life, insect conservation would do well to integrate better with overall biodiversity conservation and climate change mitigation. This also involves popularizing insects, especially through use of iconic species, through more media coverage, and more inclusive education. Insect conservationists need to liaise better with decision makers, stakeholders, and land managers, especially at the conceptually familiar scale of the landscape. Enough evidence is now available, and synthesized here, which illustrates that multiple strategies work at local levels towards saving insects. We now need to expand these locally-crafted strategies globally. Tangible actions include ensuring maintenance of biotic complexity, especially through improving temporal and spatial heterogeneity, functional connectivity, and metapopulation dynamics, while maintaining unique habitats, across landscape mosaics, as well as instigating better communication. Key is to have more expansive sustainable agriculture and forestry, improved regulation and prevention of environmental risks, and greater recognition of protected areas alongside agro-ecology in novel landscapes. Future-proofing insect diversity is now critical, with the benefits far reaching, including continued provision of valuable ecosystem services and the conservation of a rich and impressive component of Earth's biodiversity.

Scientists' warning to humanity on insect extinctions

Article

Full-text available

Feb 2020
BIOL CONSERV

Here we build on the manifesto 'World Scientists' Warning to Humanity, issued by the Alliance of World Scientists. As a group of conservation biologists deeply concerned about the decline of insect populations, we here review what we know about the drivers of insect extinctions, their consequences, and how extinctions can negatively impact humanity. We are causing insect extinctions by driving habitat loss, degradation, and fragmentation, use of polluting and harmful substances, the spread of invasive species, global climate change, direct overexploitation, and co-extinction of species dependent on other species. With insect extinctions, we lose much more than species. We lose abundance and biomass of insects, diversity across space and time with consequent homogenization, large parts of the tree of life, unique ecological functions and traits, and fundamental parts of extensive networks of biotic interactions. Such losses lead to the decline of key ecosystem services on which humanity depends. From pollination and decomposition, to being resources for new medicines, habitat quality indication and many others, insects provide essential and irreplaceable services. We appeal for urgent action to close key knowledge gaps and curb insect extinctions. An investment in research

Comparing Adaptive Radiations Across Space, Time, and Taxa

Article

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Jan 2020

Adaptive radiation plays a fundamental role in our understanding of the evolutionary process. However, the concept has provoked strong and differing opinions concerning its definition and nature among researchers studying a wide diversity of systems. Here, we take a broad view of what constitutes an adaptive radiation, and seek to find commonalities among disparate examples, ranging from plants to invertebrate and vertebrate animals, and remote islands to lakes and continents, to better understand processes shared across adaptive radiations. We surveyed many groups to evaluate factors considered important in a large variety of species radiations. In each of these studies, ecological opportunity of some form is identified as a prerequisite for adaptive radiation. However, evolvability, which can be enhanced by hybridization between distantly related species, may play a role in seeding entire radiations. Within radiations, the processes that lead to speciation depend largely on (1) whether the primary drivers of ecological shifts are (a) external to the membership of the radiation itself (mostly divergent or disruptive ecological selection) or (b) due to competition within the radiation membership (interactions among members) subsequent to reproductive isolation in similar environments, and (2) the extent and timing of admixture. These differences translate into different patterns of species accumulation and subsequent patterns of diversity across an adaptive radiation. Adaptive radiations occur in an extraordinary diversity of different ways, and continue to provide rich data for a better understanding of the diversification of life.

AQUALIFE Software: A New Tool for a Standardized Ecological Assessment of Groundwater Dependent Ecosystems

Article

Full-text available

Dec 2019

We introduce a suite of software tools aimed at investigating multiple bio-ecological facets of aquatic Groundwater Dependent Ecosystems (GDEs). The suite focuses on: (1) threats posed by pollutants to GDE invertebrates (Ecological Risk, ER); (2) threats posed by hydrological and hydromorphological alterations on the subsurface zone of lotic systems and groundwater-fed springs (Hydrological-Hydromorphological Risk, HHR); and (3) the conservation priority of GDE communities (Groundwater Biodiversity Concern index, GBC). The ER is assessed by comparing tolerance limits of invertebrate species to specific pollutants with the maximum observed concentration of the same pollutants at the target site(s). Comparison is based on an original, comprehensive dataset including the most updated information on tolerance to 116 pollutants for 474 freshwater invertebrate species. The HHR is assessed by accounting for the main direct and indirect effects on both the hyporheic zone of lotic systems and groundwater-fed springs, and by scoring each impact according to the potential effect on subsurface invertebrates. Finally, the GBC index is computed on the basis of the taxonomical composition of a target community, and allows the evaluation of its conservation priority in comparison to others. The software suite is freely available at: http://app.aqualifeproject.eu by registered users.

World Scientists' Warning of a Climate Emergency

Article

Full-text available

Dec 2019

World Scientists' Warning of a Climate Emergency

Article

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Jan 2020

Scientists have a moral obligation to clearly warn humanity of any catastrophic threat and to “tell it like it is.” On the basis of this obligation and the graphical indicators presented below, we declare, with more than 11,000 scientist signatories from around the world, clearly and unequivocally that planet Earth is facing a climate emergency.

World scientists' warning to humanity: a second notice

Article

Full-text available

Nov 2017

Local- versus broad-scale environmental drivers of continental β-diversity patterns in subterranean spider communities across Europe

Article

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Oct 2019

Macroecologists seek to identify drivers of community turnover (β-diversity) through broad spatial scales. However, the influence of local habitat features in driving broad-scale β-diversity patterns remains largely untested, owing to the objective challenges of associating local-scale variables to continental-framed datasets. We examined the relative contribution of local- versus broad-scale drivers of conti- nental β-diversity patterns, using a uniquely suited dataset of cave-dwelling spider communities across Europe (35–70° latitude). Generalized dissimilarity model- ling showed that geographical distance, mean annual temperature and size of the karst area in which caves occurred drove most of β-diversity, with differential contributions of each factor according to the level of subter- ranean specialization. Highly specialized communities were mostly influenced by geographical distance, while less specialized communities were mostly driven by mean annual temperature. Conversely, local-scale habitat features turned out to be meaningless predictors of community change, which emphasizes the idea of caves as the human accessible fraction of the extended network of fissures that more properly represents the elective habitat of the subterra- nean fauna. To the extent that the effect of local features turned to be inconspicuous, caves emerge as experimental model systems in which to study broad biological patterns without the confounding effect of local habitat features.

Testing the uniqueness of deep terrestrial life

Article

Full-text available

Oct 2019

Terrestrial life typically does not occur at depths greater than a few meters. Notable exceptions are massifs of fissured rock with caves and hollow spaces reaching depths of two kilometres and more. Recent biological discoveries from extremely deep caves have been reported as sensations analogous to wondrous deep sea creatures. However, the existence of unique deep terrestrial communities is questionable when caves are understood as integral parts of a bedrock fissure network (BFN) interconnecting all parts of a massif horizontally and vertically. We tested these two opposing hypotheses – unique deep cave fauna vs. BFN – by sampling subterranean communities within the 3D matrix of a typical karst massif. There was no distinction between deep core and shallow upper zone communities. Beta diversity patterns analysed against null models of random distribution were generally congruent with the BFN hypothesis, but suggested gravity-assisted concentration of fauna in deep caves and temperature-dependent horizontal distribution. We propose that the idea of a unique deep terrestrial fauna akin to deep oceanic life is unsupported by data and unwarranted by ecological considerations. Instead, the BFN hypothesis and local ecological and structural factors sufficiently explain the distribution of subterranean terrestrial life even in the deepest karst massifs.

Contribution of rare and common species to subterranean species richness patterns

Article

Full-text available

Sep 2019

Aim: Common species contribute more to species richness patterns (SRPs) than rare species in most studies. Our aim was to test this hypothesis using a novel model system, species living exclusively in subterranean habitats. They consist of mainly rare species (small ranges), only a few of them being common (large ranges), and challenge whether rare species are less important for the development of SRPs in this environment. We separately analyzed aquatic and terrestrial species. Location: Western Balkans in southeastern Europe. Methods: We assembled two datasets comprising 431 beetle and 145 amphipod species, representing the model groups of subterranean terrestrial and aquatic diversity, respectively. We assessed the importance of rare and common species using the stepwise reconstruction of SRPs and subsequent correlation analyses, corrected also for the cumulative information content of the subsets based on species prevalence. We applied generalized linear regression models to evaluate the importance of rare and common species in forming SRPs. Additionally, we analyzed the contribution of rare and common species in species-rich cells. Results: Patterns of subterranean aquatic and terrestrial species richness overlapped only weakly, with aquatic species having larger ranges than terrestrial ones. Our analyses supported higher importance of common species for forming overall SRPs in both beetles and amphipods. However, in stepwise analysis corrected for information content, results were ambiguous. Common species presented a higher proportion of species than rare species in species-rich cells. Main conclusion: We have shown that even in habitats with the domination of rare species, it is still common species that drive SRPs. This may be due to an even spatial distribution of rare species or spatial mismatch in hotspots of rare and common species. SRPs of aquatic and terrestrial subterranean organisms overlap very little, so the conservation approaches need to be habitat specific.

Evolution of acoustic communication in blind cavefish

Article

Full-text available

Sep 2019

Acoustic communication allows the exchange of information within specific contexts and during specific behaviors. The blind, cave-adapted and the sighted, river-dwelling morphs of the species Astyanax mexicanus have evolved in markedly different environments. During their evolution in darkness, cavefish underwent a series of morphological, physiological and behavioral changes, allowing the study of adaptation to drastic environmental change. Here we discover that Astyanax is a sonic species, in the laboratory and in the wild, with sound production depending on the social contexts and the type of morph. We characterize one sound, the "Sharp Click", as a visually-triggered sound produced by dominant surface fish during agonistic behaviors and as a chemosensory-, food odor-triggered sound produced by cavefish during foraging. Sharp Clicks also elicit different reactions in the two morphs in play-back experiments. Our results demonstrate that acoustic communication does exist and has evolved in cavefish, accompanying the evolution of its behaviors.

Knowledge in the dark: scientific challenges and ways forward

Article

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Jun 2019

A key dimension of our current era is Big Data, the rapid rise in produced data and information; a key frustration is that we are nonetheless living in an age of ignorance, as the real knowledge and understanding of people does not seem to be substantially increasing. This development has critical consequences, for example it limits the ability to find and apply effective solutions to pressing environmental and socioeconomic challenges. Here, we propose the concept of “knowledge in the dark”—or short: dark knowledge—and outline how it can help clarify key reasons for this development: (i) production of biased, erroneous, or fabricated data and information; (ii) inaccessibility and (iii) incomprehensibility of data and information; and (iv) loss of previous knowledge. Even in the academic realm, where financial interests are less pronounced than in the private sector, several factors lead to dark knowledge, that is they inhibit a more substantial increase in knowledge and understanding. We highlight four of these factors—loss of academic freedom, research biases, lack of reproducibility, and the Scientific tower of Babel—and offer ways to tackle them, for example establishing an international court of arbitration for research and developing advanced tools for research synthesis.

A review of the relation between species traits and extinction risk

Article

Full-text available

Sep 2019
BIOL CONSERV

Biodiversity is shrinking rapidly, and despite our efforts only a small part of it has been assessed for extinction risk. Identifying the traits that make species vulnerable might help us to predict the status for those less known. We gathered information on the relationships between traits and extinction risk from 173 publications, across all taxa, spatial scales and biogeographical regions, in what we think it is the most comprehensive compilation to date. We aimed to identify (1) taxonomical and spatial biases, and (2) statistically robust and generalizable predictors of extinction risk through the use of meta-analyses. Vertebrates and the Palaearctic are the most studied taxon and region because of higher accumulation of data in these groups. Among the many traits that have been suggested to be predictors, only three had enough data for meta-analyses. Two of them are potentially useful in assessing risk for the lesser-known species: regardless of the taxon, species with small range and narrow habitat breadth are more vulnerable to extinction. Contrastingly, body size (the most studied trait) did not present a consistently positive or negative response. We hypothesize that the relationship between body size and extinction risk is shaped by different aspects, namely the phenomena represented by body size depending on the taxonomic group. To increase our understanding of the drivers of extinction, further studies should focus on understudied groups such as invertebrates and fungi and regions such as the tropics and expand the number of traits in comparative analyses that should avoid current biases.

The multifaceted effects induced by floods on the macroinvertebrate communities inhabiting a sinking cave stream

Article

Full-text available

May 2019

First-order sinking cave streams experience considerable hydrological variability, including spates and periods of base-flow during dry seasons. Early-summer flooding on a first-order stream sinking in Ciur-Ponor Cave (Romania) represented a suitable opportunity to test the response of the macroinvertebrate community and of basal food resources quantity and diversity to such a disturbance event. The invertebrate community and basal resources (i.e., woody debris, leaves, fine particulate organic matter and epilithon) were collected from three sampling sites, before and after the flood. The sampling strategy followed an up-downstream gradient of both species diversity and quantity of allochtonous organic matter decrease as the stream flows through the cave. From each sampling site, ten replicates of both the benthic community and basal resources (detritus and epilithon) were taken. Outside the cave, the spate reduced the invertebrate community density, instant secondary production, complexity and stability (measured as eco-exergy and specific eco-exergy). The epigean section of the stream is populated mainly by taxa characteristic of karst headwaters prone to floods that usually recolonize the streambed rapidly from adjacent habitats. This effect was corroborated with a subsequent increase of both the mass of fine particulate organic matter and of invertebrate density within the cave, following the aftermath of the flood. In the river stretch situated close to the entrance (100 m), where the flood carried both live and dead organic matter, the stability index showed that the complexity of the community was not severely disturbed, despite the high influx of surface-dwelling taxa and temporary increase in species richness. Further downstream, in the third sampling site (400 m from entrance), all measured endpoints indicated a change in community stability, suggesting that local spates can act as rejuvenating drivers in shaping the invertebrate community structure and functioning.

Pancrustacean Evolution Illuminated by Taxon-Rich Genomic-Scale Data Sets with an Expanded Remipede Sampling

Article

Full-text available

Jul 2019

The relationships of crustaceans and hexapods (Pancrustacea) have been much discussed and partially elucidated following the emergence of phylogenomic data sets. However, major uncertainties still remain regarding the position of iconic taxa such as Branchiopoda, Copepoda, Remipedia, and Cephalocarida, and the sister group relationship of hexapods. We assembled the most taxon-rich phylogenomic pancrustacean data set to date and analyzed it using a variety of methodological approaches. We prioritised low levels of missing data and found that some clades were consistently recovered independently of the analytical approach used. These include, for example, Oligostraca and Altocrustacea. Substantial support was also found for Allotriocarida, with Remipedia as the sister of Hexapoda (i.e., Labiocarida), and Branchiopoda as the sister of Labiocarida, a clade that we name Athalassocarida (="non-marine shrimps"). Within Allotriocarida, Cephalocarida was found as the sister of Athalassocarida. Finally, moderate support was found for Hexanauplia (Copepoda as sister to Thecostraca) in alliance with Malacostraca. Mapping key crustacean tagmosis patterns and developmental characters across the revised phylogeny suggests that the ancestral pancrustacean was relatively short-bodied, with extreme body elongation and anamorphic development emerging later in pancrustacean evolution.

Scientists’ warning to humanity: microorganisms and climate change

Article

Full-text available

Jun 2019

In the Anthropocene, in which we now live, climate change is impacting most life on Earth. Microorganisms support the existence of all higher trophic life forms. To understand how humans and other life forms on Earth (including those we are yet to discover) can withstand anthropogenic climate change, it is vital to incorporate knowledge of the microbial ‘unseen majority’. We must learn not just how microorganisms affect climate change (including production and consumption of greenhouse gases) but also how they will be affected by climate change and other human activities. This Consensus Statement documents the central role and global importance of microorganisms in climate change biology. It also puts humanity on notice that the impact of climate change will depend heavily on responses of microorganisms, which are essential for achieving an environmentally sustainable future.

Over-optimization of academic publishing metrics: Observing Goodhart's Law in action

Article

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Jun 2019

Background The academic publishing world is changing significantly, with ever-growing numbers of publications each year and shifting publishing patterns. However, the metrics used to measure academic success, such as the number of publications, citation number, and impact factor, have not changed for decades. Moreover, recent studies indicate that these metrics have become targets and follow Goodhart’s Law, according to which, “when a measure becomes a target, it ceases to be a good measure.” Results In this study, we analyzed >120 million papers to examine how the academic publishing world has evolved over the last century, with a deeper look into the specific field of biology. Our study shows that the validity of citation-based measures is being compromised and their usefulness is lessening. In particular, the number of publications has ceased to be a good metric as a result of longer author lists, shorter papers, and surging publication numbers. Citation-based metrics, such citation number and h-index, are likewise affected by the flood of papers, self-citations, and lengthy reference lists. Measures such as a journal’s impact factor have also ceased to be good metrics due to the soaring numbers of papers that are published in top journals, particularly from the same pool of authors. Moreover, by analyzing properties of >2,600 research fields, we observed that citation-based metrics are not beneficial for comparing researchers in different fields, or even in the same department. Conclusions Academic publishing has changed considerably; now we need to reconsider how we measure success.

Fifty years of cave arthropod sampling: techniques and best practices

Article

Full-text available

Feb 2019
INT J SPELEOL

Ever-increasing human pressures on cave biodiversity have amplified the need for systematic, repeatable, and intensive surveys of cave-dwelling arthropods to formulate evidence-based management decisions. We examined 110 papers (from 1967 to 2018) to: (i) understand how cave-dwelling invertebrates have been sampled; (ii) provide a summary of techniques most commonly applied and appropriateness of these techniques, and; (iii) make recommendations for sampling design improvement. Of the studies reviewed, over half (56) were biological inventories, 43 ecologically focused, seven were techniques papers, and four were conservation studies. Nearly one-half (48) of the papers applied systematic techniques. Few papers (24) provided enough information to repeat the study; of these, only 11 studies included cave maps. Most studies (56) used two or more techniques for sampling cave-dwelling invertebrates. Ten studies conducted ≥10 site visits per cave. The use of quantitative techniques was applied in 43 of the studies assessed. More than one-third (42) included some level of discussion on management. Future studies should employ a systematic study design, describe their methods in sufficient detail as to be repeatable, and apply multiple techniques and site visits. This level of effort and detail is required to obtain the most complete inventories, facilitate monitoring of sensitive cave arthropod populations, and make informed decisions regarding the management of cave habitats. We also identified naming inconsistencies of sampling techniques and provide recommendations towards standardization.

Niches within a niche: ecological differentiation of subterranean amphipods across Europe's interstitial Waters

Fundamental research questions in subterranean biology

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