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

Federal University of 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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Biodiversity decline in aquatic ecosystems - is groundwater fauna at particular risk?

Article

Full-text available

Aug 2024

The terrestrial subsurface harbours the largest available freshwater reserves on our planet: In particular, shallow aquifers are home to a vast but insufficiently explored biodiversity. Whilst biodiversity research gained a strong momentum in the past decades, threats to groundwater ecosystems increased as well and we may lose species before their discovery and formal description. Negative impacts to groundwater fauna mainly encompass groundwater pollution, warming, and habitat loss. Given their peculiar adaptation to the usually dark and energy poor environment including a slow metabolism and low reproduction rates, as well as further special characteristics of groundwater fauna like their fragmented distribution, and high number of endemic species, groundwater invertebrates seem to be specifically at risk. We firmly propose to establish ecological measures in routine groundwater monitoring and to take action in the development of biodiversity conservation strategies and groundwater ecosystem protection.

Systematic and highly resolved modelling of biodiversity in inherently rare groundwater amphipods

Article

Full-text available

Jul 2024

Aim Groundwater ecosystems harbour a unique biodiversity, but remain poorly studied, mainly due to difficulties in accessibility and imperfect species detection. Consequently, knowledge on the state and change of groundwater biodiversity remains highly deficient. In the context of global warming and excessive groundwater extraction, understanding groundwater from an ecosystem‐perspective, including organism diversity and distribution, is essential. This study presents the largest ever systematic assessment of groundwater amphipods, which are a key component of European groundwater biodiversity. Location Switzerland (41,285 km ² ), including data from 906 sampling sites. Taxon Groundwater amphipods, genera Niphargus and Crangonyx (Crustacea, Amphipoda). Methods We applied a highly standardized citizen science approach to collect repeated groundwater fauna samples in collaboration with municipal drinking water providers. Using detection–nondetection data of the genetically identified groundwater amphipod species, we assessed the overall species diversity of both rare and common species. The distribution of commonly found species was predicted using multispecies occupancy modelling. Results We retrieved 3882 samples from 906 sites, yielding 2350 groundwater amphipod individuals. We identified a remarkable species diversity, comprising few commonly and many rarely found species. Considering commonly found species, we identified distinct distribution ranges, low local species richness and a predominance of negative co‐occurrences. In contrast, a major portion of species were found rarely (generally at just one or two sites each), distributed uniformly throughout the study area and unrelated to common species' recognized hotspots. Many of these rarely found species are not yet formally described. Main Conclusions Our results give robust emphasis on the rare occurrence and narrow distribution of many groundwater dwellers. Our systematic and standardized sampling data of groundwater amphipods suggest that rarity is particularly prominent and inherent to groundwater organisms. We emphasize the need of systematic data to integrate rare groundwater species in biodiversity assessments, especially in times of global change.

From the front door to the basement: Invertebrate communities' structure as a proxy for determining cave zonation in Neotropics

Article

Full-text available

Jun 2024
BIOTROPICA

In caves, the absence of natural light in deeper regions starkly contrasts with the entrance areas, which still exhibit a light gradient extending into the cave interior. This interplay with the structural gradient of the environment potentially exerts distinct influences on invertebrate communities residing in different cave light zones. To investigate this, we formulated a hypothesis positing that communities within distinct cave light zones respond differently to habitat structure and microclimatic conditions. Our approach involved a spatial multi‐scale sampling of invertebrates and the application of statistical analyses to contrast the responses of communities inhabiting photic and aphotic zones. Photic zone richness is influenced by factors such as air moisture, resource availability, root presence, and shelter diversity. In contrast, the richness of communities in aphotic zones is shaped by resource availability, the presence of roots, branches, and distance from the cave entrance. As expected, the richness in the photic zone surpasses that of the deeper regions, highlighting the challenges faced by invertebrates attempting to establish themselves in the aphotic zone. The species composition of faunal communities varied predictably from the entrance to the aphotic zone, and the three most important factors driving this variation were geographic distance, humidity, and distance from the entrance. The composition between these cave zones differs significantly, primarily due to the high number of obligate cave species predominantly inhabiting the aphotic region. Indeed, communities associated with different cave zones exhibit distinct responses to resource, microclimatic, and structural variables. Abstract in Portuguese is available with online material.

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.

Cryptic diversity patterns of subterranean estuaries

Article

Full-text available

Nov 2024
Proc Biol Sci

Subterranean estuaries are coastal ecosystems characterized by vertically stratified groundwater. The biota within these ecosystems is relatively understudied due to the inherent difficulty of accessing such extreme environments. The fauna inhabiting these ecosystems is considered vulnerable to extinction, and the presence of cryptic species has major implications for research and conservation efforts. Most species lack molecular data; however, the evaluation of genetic data for some taxa has revealed that undocumented species are common. This study employs molecular species delimitation methods and DNA barcoding through the analysis of publicly and newly generated sequences, including individuals from type localities and non-crustacean phyla; the latter are typically overlooked in biodiversity assessments of subterranean estuaries. We analysed 376 cytochrome c oxidase subunit I (COI) gene sequences and 154 16S rRNA gene sequences. The COI sequences represented 32% of previously described species and 50% of stygobiont species from the Yucatan Peninsula and Cozumel Island, while sequences of the 16S rRNA represented 14% of described species and 22% of stygobionts. Our results revealed cryptic genetic lineages and taxonomic misidentification of species. As several species from these ecosystems are recognized as endangered, the use of molecular approaches will improve biodiversity estimates and highlight overlooked cryptic lineages in need of evaluation of conservation status.

Integrating historical and recent data to measure long-term trends of endangered subterranean species

Article

Full-text available

Jul 2024
BIOL CONSERV

Documenting population trends is pivotal to identify the underlying drivers of biodiversity changes and setting conservation priorities. Ascertaining trends often requires long-term, standardized, monitoring data that are not always available. Historical data provide important information on past species distribution, but their integration with recent data to obtain trend estimates is challenging. Here we show how site occupancy-detection models (SODMs) can allow combining data from recent monitoring with historical ones from the gray literature. Using data on the endangered cave salamander, Speleomantes strinatii, we tested whether SODMs can provide reliable trend estimates if i) historical data include repeated within-season surveys enabling the estimation of past detectability, or if ii) information on detection/non-detection is not available. We conducted repeated surveys across 40 caves covering the species range, for which historical (1940-1982) biospeleological data were available. We then developed Bayesian SODMs i) estimating species detectability from both recent and past surveys, and then assessing trends; ii) in absence of estimates of past detectability, assessing trends by comparing scenarios on the potential misdetection rate during historical surveys. Salamanders were widespread in the study sites. SODM estimated high detectability for both recent and historical surveys and suggested a growing occupancy. Changes in occupancy were unrelated to landscape modifications. Even without historical detection/non-detection data, realistic scenarios of past misdetection consistently suggested an increasing or stable trend. The application of tailored analytical approaches is fundamental to exploit the vault of information available in historical data, and can be linked to adaptive management to promote efficient conservation actions.

Towards invasion ecology for subterranean ecosystems

Article

Full-text available

Mar 2024
BIODIVERS CONSERV

Invasive alien species (IAS) are widely recognized as a major threat to ecosystems globally. Despite the growing interest and research effort on biological invasions, the impact of IAS on both terrestrial and aquatic subterranean habitats remains considerably under-studied in comparison to other environments. The Convention on Biological Diversity (CBD) has established global targets to mitigate the impacts of IAS, emphasizing the need for countries, organizations, and the scientific community to identify gaps in knowledge, monitoring, and management strategies for IAS. To this end, we mapped knowledge gaps in biological invasions of subterranean habitats that emerged from the first systematic surveys of the available information. We suggest that there are five main gaps restricting our ability to understand and tackle biological invasions in subterranean ecosystems. Given the vulnerability of subterranean ecosystems and the lack of attention they have received in conservation policies, it is crucial to increase research emphasis on IAS. This opinion paper aims to stimulate such efforts and contribute to the preservation of these ecosystems.

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.

Linking Surface and Subsurface: The Biogeochemical Basis of Cave Microbial Ecosystem Services

Article

Full-text available

Dec 2024

Terrestrial land use signals on groundwater fauna beyond current protection buffers

Article

Full-text available

Oct 2024
ECOL APPL

Terrestrial and aquatic ecosystems are tightly linked, with direct implications for applied resource management and conservation. It is well known that human land use change and intensification of terrestrial systems can have large impacts on surface freshwater ecosystems. Contrastingly, the study and understanding of such land use impacts on groundwater communities is lagging behind. Both the impact strength of land use on groundwater communities and the spatial extents at which such interlinkages are operating are largely unknown, despite our reliance on groundwater for drinking water extraction as a key ecosystem service. Here, we analyzed groundwater amphipod occurrence from several hundred shallow groundwater aquifers used for drinking water extraction across a region of varying agricultural intensity and human population density in Switzerland. Despite drinking water extraction sites being generally built at locations with expected minimal aboveground impacts on water quality, we found a direct correlation between land use type and intensity within the surrounding catchment area and the locally measured nitrate concentrations, which is a direct proxy for drinking water quality. Furthermore, groundwater amphipods were more likely to be found at sites with higher forest coverage than at sites with higher crop and intensive pasture coverages, clearly indicating a tight connection between aboveground land use and groundwater biodiversity. Our results indicate that land use type effects on groundwater communities are most relevant and pronounced to spatial scales of about 400–1000 m around the groundwater sampling site. Importantly, the here identified spatial scale is 1.2‐ to 3‐fold exceeding the average extent of currently defined groundwater protection zones. We postulate that incorporating an ecosystem perspective into groundwater management strategies is needed for effective protection of groundwater quality and biodiversity.

Long-term monitoring of the hypogeal Etruscan Tomba degli Scudi, Tarquinia, Italy. Early detection of black spots, investigation of fungal community and evaluation of their biodeterioration potential

Article

Oct 2024
J APPL MICROBIOL

Aims Hypogeal environments with Cultural Heritage interest pose a real challenge for their preservation and conservation. The ancient Etruscan Necropolis of Tarquinia, Italy, consists of 200 tombs decorated with extraordinary mural paintings, of great artistic and historical value. Since the beginning of the restoration campaign in 2016, a regular microbiological survey has been performed in the Tomba degli Scudi. The aim of this study was to investigate the nature of an expansion of black spots on the pictorial layers recently observed. Methods and Results To determine the origin of the black spots in the atrium chamber of the Tomba degli Scudi, the fungal community was sampled using various techniques: cellulose discs, swabs and nylon membranes and investigated by a multi-analytical approach. The obtained results suggest that the identified fungal strains (e.g. Gliomastix murorum and Pseudogymnoascus pannorum) are common to many subterranean environments around the world, such as Lascaux cave. Conclusions The continuous and long-term monitoring made it possible to detect alterations at an early stage and assess the harmfulness of different fungal strains. This work is a demonstration of the effectiveness of prevention and monitoring actions within these fragile and valuable environments.

Are haloclines distributional barriers in anchialine ecosystems? Physiological response of cave shrimps to salinity

Article

Full-text available

Jul 2024
PLOS ONE

Anchialine systems are coastal groundwater habitats around the world which host a unique community of cave adapted species (stygobionts). Such communities are expected to be separated by haloclines into either fresh or saline groundwater communities, hence climate changes (e.g., eustatic sea level shifts) and anthropic driven changes (e.g., salinization) may have a great impact on these stygobiont communities. Here we used cave-restricted species of Typhlatya from the Yucatan Peninsula as models to identify physiological capacities that enable the different species to thrive in marine groundwater (T. dzilamensis) or fresh groundwater (T. mitchelli and T. pearsei), and test if their distribution is limited by their salinity tolerance capacity. We used behavior, metabolic rates, indicators of the antioxidant system and cellular damage, and lactate content to evaluate the response of individuals to acute changes in salinity, as a recreation of crossing a halocline in the anchialine systems of the Yucatan Peninsula. Our results show that despite being sister species, some are restricted to the freshwater portion of the groundwater, while others appear to be euryhaline.

Efectos del cambio climático en la biodiversidad subterránea ibérica: estado del conocimiento y perspectivas_Material Suplementario

Article

Jun 2024

Datos recopilados en los artículos examinados sobre la región de estudio, especies estudiadas (información taxonómica y especificidad por el medio subterráneo), metodología y resultados. Los resultados cuantitativos se muestran como un único valor (ej.: temperatura letal), como una tasa de cambio porcentual entre dos tratamientos de temperatura (%/ºC) o entre dos escenarios climáticos (presente/futuro).

BIASES IN THE KNOWLEDGE OF THE GEOGRAPHICAL DISTRIBUTION OF CAVES IN BRAZIL

Article

Full-text available

Apr 2024

Many caves have yet to be discovered and/or mapped in Brazil. Various socio-economic and accessibility factors may be responsible for biasing the knowledge of Brazilian caves geographical distribution. In this study, using Bayesian modeling techniques, it was predicted that knowledge about the Brazilian caves geographic distribution is strongly biased towards locations close to urban centers and mining activities. More caves are known near mining environments and/or more accessible locations than far from them for instance. The models were built by associating the known occurrence data of digitally accessible caves in the Speleological Information National Register (Cadastro Nacional de Informações Espeleológicas (CANIE) with different accessibility and infrastructure variables. The findings suggest that the regions with the highest occurrence of known caves are mainly concentrated within the states of Minas Gerais, São Paulo, Goiás, Pará and Piauí. Meanwhile some Brazilian states, such as Amazonas, Roraima, Mato Grosso, Mato Grosso do Sul, Paraná and Maranhão are still under-explored. They have large gaps and high potential for the discovery of new caves. In conclusion, the economic exploitation has generated biased knowledge about the distribution of caves. This may be linked to the historical clashes between exploitation and conservation legislation, making it essential that new policies on the conservation of Brazil's speleological heritage consider the entire speleological landscape, its biases (better studied sites), Racovitzan shortfalls (less studied or possibly neglected sites), and the socio-economic processes that imply these.

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

Article

Full-text available

May 2024
GLOBAL ECOL BIOGEOGR

Aim Quantifying the relative contribution of environmental filtering versus limiting similarity in shaping communities is challenging because these processes often act simultaneously and their effect is scale‐dependent. Focusing on caves, island‐like natural laboratories with limited environmental variability and species diversity, we tested: (i) the relative contribution of environmental filtering and limiting similarity in determining community assembly in caves; (ii) how the relative contribution of these driving forces changes along environmental gradients. Location Europe. Time period Present. Major taxa studied Subterranean spiders. Methods We used data on distribution and traits for European cave spiders ( n = 475 communities). We estimated the trait space of each community using probabilistic hypervolumes, and obtained estimations of functional richness independent of the species richness of each community via null modelling. We model functional diversity change along environmental gradients using generalized dissimilarity modelling. Results Sixty‐three percent of subterranean spider communities exhibited a prevalence of trait underdispersion. However, most communities displayed trait dispersion that did not depart significantly from random, suggesting that environmental filtering and limiting similarity were both exerting equally weak or strong, yet opposing influences. Overdispersed communities were primarily concentrated in southern latitudes, particularly in the Dinaric karst, where there is greater subterranean habitat availability. Pairwise comparisons of functional richness across caves revealed these effects to be strongly scale‐dependent, largely varying across gradients of cave development, elevation, precipitation, entrance size and annual temperature range. Conversely, geographical distance weakly affected trait composition, suggesting convergence in traits among communities that are far apart. Main conclusions Even systems with stringent environmental conditions maintain the potential for trait differentiation, especially in areas of greater habitat availability. Yet, the relative influence of environmental filtering and limiting similarity change with scale, along clear environmental gradients. The interplay of these processes may explain the assembly of species‐poor subterranean communities displaying high functional specialization.

Advancing tourism sustainability in show caves

Article

Full-text available

Mar 2024

Gross morphology of the brain and some sense organs of subterranean pencil catfishes of the genus Ituglanis Costa and Bockmann, 1993 (Siluriformes, Trichomycteridae), with a discussion on sensory compensation versus preadaptation in subterranean fishes

Article

Full-text available

Feb 2024
J FISH BIOL

Subterranean organisms provide excellent opportunities to investigate morphological evolution, especially of sensory organs and structures and their processing areas in the central nervous system. We describe the gross morphology of the brain and some cephalic sensory organs (olfactory organ, eye, semicircular canals of the inner ear) and the swim bladder (a non‐sensory accessory structure) of subterranean species of pencil catfishes of the genus Ituglanis Costa and Bockmann, 1993 (Siluriformes, Trichomycteridae) and compare them with an epigean species of the genus, Ituglanis goya Datovo, Aquino and Langeani, 2016. We compared qualitatively the size of the different brain regions and sense organs of the subterranean species with those of the epigean one, searching for modifications possibly associated with living in the subterranean environment. Our findings suggest that species of Ituglanis exhibit sensory characteristics that are preadaptive for the subterranean life, as only slight modifications were observed in the brains and sense organs of the subterranean species of the genus when compared with the epigean one. Because most subterranean fish species belong to lineages putatively preadapted for subterranean life, our results, discussed in the context of available information on the brain and sense organs of other subterranean species, help identify general trends for the evolution of the brain and sensory organs of subterranean fishes in general.

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

Full-text available

Dec 2023
ANIM BEHAV

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

Simple Summary Recently, the study of amphibian behavioral ecology has received increased interest from ethologists and evolutionary biologists. In fact, plethodontid salamanders (family Plethodontidae) are often used as model organisms to better understand different aspects of behavioral adaptation. We reviewed the recent scientific literature published on the behavioral ecology of European cave salamanders belonging to the genus Speleomantes, to highlight recent advancements and possible future directions for successful research. We found that, in recent years, several aspects of Speleomantes behavior were investigated, such as trophic strategies and parental care, while others were neglected, in particular, chemical communication at the intraspecfic level. Finally, we propose European cave salamanders as useful models to understand the gradual adaptation of behaviors that facilitate the permanent colonization of subterranean habitats. Abstract 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

Subterranean fauna is an important contributor to the global fauna, but it is still understudied, and a large part of its taxonomy is not yet resolved. One species complex with unresolved taxonomy is the groundwater amphipod Niphargus ruffoi, endemic to the Alpine chain. Here, we used new samples from across the Alpine arc to review the taxonomic status of the entire clade, including the species N. ruffoi and N. arolaensis. We sequenced four genetic markers from the collected specimens, assessed the phylogenetic position of N. ruffoi within the genus, and studied the structure of this species complex using four molecular species delimitation methods. We tested for recombination using the alignments of the concatenated nuclear rDNA genes. The phylogenetic analyses revealed high support for the monophyly of the studied species complex, defining two lineages (i.e., N. arolaensis and N. ruffoi) within the clade. Molecular species delimitation methods suggested that N. arolaensis is a single species, while N. ruffoi should be considered as a species complex of three (using ITS) up to nine (using COI) putative species. Apart from mitonuclear discordance, we found a discrepancy between the different nuclear ribosomal DNA markers, indicating a possible recombination with fragments of 28S DNA of N. ruffoi s. lat. present in the genome of N. arolaensis. For the above-mentioned reasons, the internal phylogenetic structure of N. ruffoi s. lat could not be fully resolved. Moreover, no clear morphological evidence supported the molecular species delimitation. Consequently, no taxonomic changes were proposed. We postulate that this complex scenario was influenced by Pleistocene climate oscillations with subsequent fragmentation events and secondary contacts; this is an interesting study system to investigate the evolution and biogeography of Alpine clades.

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.

Independent Transitions to Freshwater Environments Promote Phenotypic Divergence, Not Convergence, in Stingrays

Article

Apr 2024
INTEGR COMP BIOL

Synopsis Instances of convergent or parallel evolution provide a potent model system for exploring contingency and determinism in evolutionary biology. Likewise, the multiple, independent habitat transitions from saltwater to freshwater biomes offer opportunities for studying convergent evolution within and among different vertebrate lineages. For example, stingrays have invaded freshwater habitats multiple times across different continents, sometimes even several times within the same clade (e.g., Dasyatidae). We evaluated the frequency of saltwater–freshwater invasions in stingrays, compared ecological and phenotypic diversification among freshwater and saltwater lineages, and assessed the degree of convergence among freshwater species. Despite not being morphologically distinct from saltwater stingrays, freshwater stingrays do expand the margins of stingray morphological diversity. According to our data, trophic specialists occupied non-overlapping regions of morphospace, with piscivores and molluscivores being distinct from other diet guilds. Freshwater stingrays as a group did not strongly converge morphologically, neither did freshwater rays from different lineages, which shared similar niches. These findings could be explained by there not being enough time for convergence to occur among more ancient and more recent freshwater lineages. Alternatively, the different ancestral bauplans of various freshwater ray lineages and weak selection on optimal phenotypes could promote contingency in the form of evolution along paths of least resistance.

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

Oct 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.

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

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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

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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

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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

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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

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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

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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

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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.

Environmental filtering and convergent evolution determine the ecological specialization of subterranean spiders

Article

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Jan 2020
FUNCT ECOL

Ecological specialization is an important mechanism enhancing species coexistence within a given community. Yet, unravelling the effect of multiple selective evolutionary and ecological factors leading the process of specialization remains a key challenge in ecology. Subterranean habitats provide highly replicated experimental arenas in which to disentangle the relative contribution of evolutionary history (convergent evolution vs. character displacement) and ecological setting (environmental filtering vs. competitive exclusion) in driving community assembly. We tested alternative hypotheses about the emergence of ecological specialization using the radiation of a lineage of sheet‐weaver cave‐dwelling spiders as model system. We observed that at the local scale, a differential specialization to cave microhabitats generally parallels moderate levels of morphological similarity and close phylogenetic relatedness among species. Conversely, geographic distance contributed little in explaining microhabitat occupation, possibly mirroring a limited role of competitive exclusion. Yet, compared to non‐coexisting species, co‐occurring species adapted to different microhabitats showed lower morphological niche overlap (i.e. higher dissimilarity) and deeper genetic distance. The framework here developed suggests that in the subterranean domain, habitat specialization is primarily driven by environmental filtering, secondarily by convergent evolution, and only marginally by character displacement or competitive exclusion. This pattern results in the establishment of replicated communities across geographical space, composed by ecologically equivalent species. Such process of community assembly well explains the numerous adaptive radiations observed in subterranean habitats, an eco‐evolutionary pattern well documented in oceanic islands or mountain summit communities. A free Plain Language Summary can be found within the Supporting Information of this article.

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

Full-text available

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

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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

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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

Full-text available

Aug 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.

Fundamental research questions in subterranean biology

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