Using simplified settings to advance ecological theory: a lesson from the subterranean world

Submitted by editor on 27 September 2018. Get the paper!

by Stefano Mammola

E4 award

A wise man named Socrates once stated a famous aphorism: "I know that I know nothing". Some thousands years later, in the era of internet, satellites and artificial intelligence, our knowledge of this world has certainly improved, but actually not that much. The world around us is characterised by an overwhelming complexity, and our perception of it, being filtered by our human senses, is ephemeral and subjective. On top of that, our lifespan is dramatically short. Therefore, even most basic questions about life in this universe are very likely to remain unanswered, even in the long run – but see 42. Yet, the awareness of human limitations poses to many of us a stimulating challenge to keep expanding knowledge.

                      Ecological systems are notoriously among the most difficult systems to describe and understand. Ecology, as a discipline, involves by definition the study of the complexity, which arises from the interaction amongst different features of the biotic and abiotic components of the environment. From the one hand, biological communities are extremely diverse, typically encompassing thousands of species and millions of interspecific interactions. From the other hand, ecological systems are stochastic and chaotic, meaning that even small changes in the conditions of the systems can lead to large, unpredictable, consequences. As such, how can we discern general principles from the study of highly unpredictable ecological systems?

                      By looking at the history of the ecological thinking, it appears that most fundamental principles and theories were discovered by taking advantage of specific model organisms or systems, i.e. simplified natural experimental setting in which to minimize confounding effects and reduce the number of parameters needed to develop representations of key eco-evolutionary processes. Over the years, scientists have agreed upon several convenient and simplified models, spanning from small midgets in the genus Drosophila to highly diversified Anolis lizards, from secluded oceanic islands to oceanic thermal vents.

                      Among the variety of possible eco-evolutionary models, it appears that ecologists have preferentially focused their attention on several types of insular systems (mountain summit, lakes, islands, etc.), given that these systems often have known histories and a relatively low richness of species and interactions. Therefore, insular systems allows ecologists to more easily quantify community assembly process, rates of immigration and extinction, processes of speciation and diversification, and multi-species interactions. Considering this general framework, in a recent Ecography review and synthesis paper  I discussed the potential role of caves and other deep subterranean ecosystems as one of the most promising nature’s eco-evolutionary model systems. Of course, this is not a new paradigm, nor a particularly original idea. Back in 1969, Thomas L. Poulson and William B. White formalised this concept in a highly cited paper published in Science, writing that "[...] the most important use of caves is their use as limited and simple natural laboratories in which we can study the principles governing evolution in more complex stable environments"

                      But why is that so? Several characteristics make caves and other deep subterranean habitats strategic natural laboratories for eco-evolutionary studies. Foremost, subterranean habitats are semi-closed systems that are extensively replicated across the Earth. Second, subterranean environments often display an extremely reduced variability in their environmental conditions. Notably, the thermal stability of deep subterranean habitats – in most caves the internal temperature varies by few tenths of degrees over a year – makes them particularly suitable systems in which to shed light on the effects of climate change on biodiversity. Third, due to limited food resources underground, subterranean communities generally exhibit lower diversity and abundance of organisms than surface ones, and are characterised by a reduced functional diversity and by shorter trophic webs. Finally, subterranean species are among the most astonishing and bizarre outcomes of the Darwinian evolution, making caves an ideal setting for the study of tempo and mode of speciation and biological diversification.

                      In spite of all these premises, the use of caves as model systems in ecology appears to be still in its infancy, especially if compared with other island-like systems. This is partially a problem related to the objective difficulties of working in caves – not the most human-friendly environments one can think of! – and partly a methodological problem connected to the inaccessibility of most subterranean spaces and to the general lack of large-scale dataset of subterranean species distribution. At the 50th anniversary of the landmark publication by Poulson and White, I took the long view of these promising nature’s laboratories, summarizing fifty years of ecological research in caves and highlighting modern trends in subterranean biological studies. Given that in the last twenty years there have been recent revolutionary advances in molecular techniques, remote sensing techniques, spatial statistics, as well as caving techniques, there is today a concrete possibility of fully exploit the potential of these model systems for unlocking some of the unresolved questions in ecology, biogeography and evolutionary biology. Besides the enjoyable part of working in caves – for some crazy people, caving can be really entertaining! – humans can really learn a lot by studying these systems and their unique inhabitants. We just need to wear a speleological helmet, turn the light on and enjoy the show.