In light of recent alarming trends in human population growth, climate change, and other environmental modifications, a “Warning to humanity” manifesto was published in BioScience in 2017. This call reiterated most of the ideas originally expressed by the Union of Concerned Scientists in 1992, including the fear that we are “pushing Earth's ecosystems beyond their capacities to support the web of life.” As subterranean biologists, we take this opportunity to emphasize the global importance and the conservation challenges associated with subterranean ecosystems. They likely represent the most widespread nonmarine environments on Earth, but specialized subterranean organisms remain among the least documented and studied. Largely overlooked in conservation policies, subterranean habitats play a critical role in the function of the web of life and provide important ecosystem services. We highlight the main threats to subterranean ecosystems and propose a set of effective actions to protect this globally important natural heritage.
The use of semi-isolated habitats such as oceanic islands, lakes and mountain summits as model systems has played a crucial role in the development of evolutionary and ecological theory. Soon after the discovery of life in caves, different pioneering authors similarly recognized the great potential of these peculiar habitats as biological model systems. In their 1969 paper in Science, 'The cave environment', Poulson and White discussed how caves can be used as natural laboratories in which to study the underlying principles governing the dynamics of more complex environments. Together with other seminal syntheses published at the time, this work contributed to establishing the conceptual foundation for expanding the scope and relevance of cave-based studies. Fifty years after, the aim of this review is to show why and how caves and other subterranean habitats can be used as eco-evolutionary laboratories. Recent advances and directions in different areas are provided, encompassing community ecology, trophicwebs and ecological networks, conservation biology, macroecology and climate change biology. Special emphasis is given to discuss how caves are only part of the extended network of fissures and cracks that permeate most substrates and, thus, their ecological role as habitat islands is critically discussed. Numerous studies have quantified the relative contribution of abiotic, biotic and historical factors in driving species distributions and community turnovers in space and time, from local to regional scales. Conversely, knowledge of macroecological patterns of subterranean organisms at a global scale remains largely elusive, due to major geographical and taxonomical biases. Also, knowledge regarding subterranean trophic webs and the effect of anthropogenic climate change on deep subterranean ecosystems is still limited. In these research fields, the extensive use of novel molecular and statistical tools may hold promise for quickly producing relevant information not accessible hitherto.
The term Milieu Souterrain Superficiel (MSS) has been used since the early 1980s in subterranean biology to categorize an array of different hypogean habitats. In general terms, a MSS habitat represents the underground network of empty air-filled voids and cracks developing within multiple layers of rock fragments. Its origins can be diverse and is generally covered by topsoil. The MSS habitat is often connected both with the deep hypogean domain-caves and deep rock cracks-and the superficial soil horizon. A MSS is usually characterized by peculiar microclimatic conditions, and it can harbor specialized hypogean, endogean, and surface-dwelling species. In light of the many interpretations given by different authors, we reviewed 235 papers regarding the MSS in order to provide a state-of-the-art description of these habitats and facilitate their study. We have briefly described the different types of MSS mentioned in the scientific literature (alluvial, bedrock, colluvial, volcanic, and other types) and synthesized the advances in the study of the physical and ecological factors affecting this habitat-i.e., microclimate, energy flows, animal communities, and trophic interactions. We finally described and reviewed the available sampling methods used to investigate MSS fauna.
Scientists of different disciplines have recognized the valuable role of terrestrial caves as ideal natural laboratories in which to study multiple eco-evolutionary processes, from genes to ecosystems. Because caves and other subterranean habitats are semi-closed systems characterized by a remarkable thermal stability, they should also represent insightful systems for understanding the effects of climate change on biodiversity in situ. Whilst a number of recent advances have demonstrated how promising this fast-moving field of research could be, a lack of synthesis is possibly holding back the adoption of caves as standard models for the study of the recent climatic alteration. By linking literature focusing on physics, geology, biology and ecology, we illustrate the rationale supporting the use of subterranean habitats as laboratories for studies of global change biology. We initially discuss the direct relationship between external and internal temperature, the stability of the subterranean climate and the dynamics of its alteration in an anthropogenic climate change perspective. Owing to their evolution in a stable environment, subterranean species are expected to exhibit low tolerance to climatic perturbations and could theoretically cope with such changes only by shifting their distributional range or by adapting to the new environmental conditions. However, they should have more obstacles to overcome than surface species in such shifts, and therefore could be more prone to local extinction. In the face of rapid climate change, subterranean habitats can be seen as refugia for some surface species, but at the same time they may turn into dead-end traps for some of their current obligate inhabitants. Together with other species living in confined habitats, we argue that subterranean species are particularly sensitive to climate change, and we stress the urgent need for future research, monitoring programs and conservation measures.
1. The use of n-dimensional hypervolumes in trait-based ecology is rapidly increasing.By representing the functional space of a species or community as a Hutchinsonian niche, the abstract Euclidean space defined by a set of independent axes corresponding to individuals or species traits, these multidimensional techniques show great potential for the advance of functional ecology theory.2. In the panorama of existing methods for delineating multidimensional spaces, the r package hypervolume (Global Ecology and Biogeography, 23, 2014, 595-609) is currently the most used. However, functions for calculating the standard set of functional diversity (FD) indices-richness, divergence and regularity-have not been developed within the hypervolume framework yet. This gap is delaying its full exploitation in functional ecology, meanwhile preventing the possibility to compare its performance with that of other methods.3. We develop a set of functions to calculate FD indices based on n-dimensional hypervolumes, including alpha (richness), beta (and respective components), dispersion, evenness, contribution and originality. Altogether, these indices provide a coherent framework to explore the primary mathematical components of FD within a multidimensional setting. These new functions can work either with hypervolume objects or with raw data (species presence or abundance and their traits) as input data, and are versatile in terms of input parameters and options. 4. These functions are implemented within bat (Biodiversity Assessment Tools), an r package for biodiversity assessments. As a coherent corpus of functional indices based on a common algorithm, it opens the possibility to fully explore the strengths of the Hutchinsonian niche concept in community ecology research.
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