Collecting eco-evolutionary data in the dark: Impediments to subterranean research and how to overcome them

Abstract

Caves and other subterranean habitats fulfill the requirements of experimental model systems to address general questions in ecology and evolution. Yet, the harsh working conditions of these environments and the uniqueness of the subterranean organisms have challenged most attempts to pursuit standardized research.Two main obstacles have synergistically hampered previous attempts. First, there is a habitat impediment related to the objective difficulties of exploring subterranean habitats and our inability to access the network of fissures that represents the elective habitat for the so-called "cave species." Second, there is a biological impediment illustrated by the rarity of most subterranean species and their low physiological tolerance, often limiting sample size and complicating laboratory experiments.We explore the advantages and disadvantages of four general experimental setups (in situ, quasi in situ, ex situ, and in silico) in the light of habitat and biological impediments. We also discuss the potential of indirect approaches to research. Furthermore, using bibliometric data, we provide a quantitative overview of the model organisms that scientists have exploited in the study of subterranean life.Our over-arching goal is to promote caves as model systems where one can perform standardized scientific research. This is important not only to achieve an in-depth understanding of the functioning of subterranean ecosystems but also to fully exploit their long-discussed potential in addressing general scientific questions with implications beyond the boundaries of this discipline.

Keywords: Asellus aquaticus; Astyanax; anchialine; cave laboratory; computer simulations; experimental design; groundwater; model system; natural laboratory; nonmodel organisms; sampling strategy; stygobite; troglobite.

FIGURE 1

Challenges of subterranean research and experimental designs to avoid these. Schematic representation of the main challenges of subterranean research (coded with capital letters), and main experimental approaches that can be adopted to overcome these

FIGURE 2

A theoretical trade‐off between the ease of study and biological realism of the observations in different experimental setups. On the one hand, exploring a cave is physically demanding and requires specific speleological equipment, whereas it is possible to run a simulation sitting at home in front of a computer in a pyjama—and even during a COVID‐19 pandemic! Running a simulation or conducting an experiment in the laboratory also allows us to control for a number of confounding factors. On the other hand, the result obtained in the field is often less artefactual, requiring no abstraction or formulation of a priori assumptions. At some point, when studying phenomena in the laboratory or with simulations, one will want to get back to the field to corroborate results using real‐world observations

FIGURE 3

Diversity of model organisms in subterranean biology across the animal Tree of Life. The branch Cambaridae refers to the genera Cambarus, Orconectes, Procambarus, and Troglocambarus. Atyidae refers to the exclusively subterranean genera Speleocaris, Stygiocaris, Troglocaris, and Typhlatya. Dytiscidae indicates the Australian diving beetles of the genera Limbodesus, Nirridesus, Nirripirti, and Paroster. Amblyopsidae indicates the North American cave fish in the genera Amblyopsis, Chologaster, Forbesichthys, Speleoplatyrhinus, and Typhichthys. WoS entries: Number of papers focusing on the species in Web of Science (accessed on 25 November 2020). (1–3): The information refers to the genera (1) Speleocaris, Stygiocaris, Troglocaris, and Typhlatya; (2) Cambarus, Orconectes, Procambarus, and Troglocambarus; (3) Paroster, Limbodesus, Nirridesus, and Nirripirti