Stefano Mammola

Alpine endemic spiders shed light on the origin and evolution of subterranean species

We designed a comparative study to unravel the phylogeography of two Alpine endemic spiders characterized by a different degree of adaptation to subterranean life: Troglohyphantes vignai (Araneae, Linyphiidae) and Pimoa rupicola (Araneae, Pimoidae), the latter showing minor adaptation to hypogean life. We sampled populations of the model species in caves and other subterranean habitats across their known geographical range in the Western Alps. By combining phylogeographic inferences and Ecological Niche Modeling techniques, we inferred the biogeographic scenario that led to the present day population structure of the two species. According to our divergent time estimates and relative uncertainties, the isolation of T. vignai and P. rupicola from their northern sister groups was tracked back to Middle–Late Miocene. Furthermore, the fingerprint left by Pleistocene glaciations on the population structure revealed by the genetic data, led to the hypothesis that a progressive adaptation to subterranean habitats occurred in T. vignai, followed by strong population isolation. On the other hand, P. rupicola underwent a remarkable genetic bottleneck during the Pleistocene glaciations, that shaped its present population structure. It seems likely that such shallow population structure is both the result of the minor degree of specialization to hypogean life and the higher dispersal ability characterizing this species. The simultaneous study of overlapping spider species showing different levels of adaptation to hypogean life, disclosed a new way to clarify patterns of biological diversification and to understand the effects of past climatic shift on the subterranean biodiversity.

Niche differentiation in Meta bourneti and M. menardi (Araneae, Tetragnathidae) with notes on the life history

Meta menardi and M. bourneti are two species of spiders inhabiting caves and other subterranean habitats. The occurrence of both species within the same cave has never been proved convincingly and several authors hypothesized a complete niche differentiation mainly based on microclimatic conditions. In order to study the apparent niche differentiation of the two species, we studied several populations of M. menardi and M. bourneti occurring in six caves in the Western Italian Alps (NW Italy). A series of squared plots were monitored monthly from March 2012 to February 2013. At each survey, we counted individuals and we collected the main environmental variables at each plot, namely distance from cave entrance, structural typology (wall, floor, or ceiling), light intensity, wind speed and counts of potential prey. Moreover, temperature and relative humidity were continuously logged in each cave. We run several statistical models (GLMMs) in order to relate the counts of individuals to the environmental parameters. The distance from the cave entrance, structural typology and prey availability resulted most important factors driving the abundance of both species within the cave. On the other hand, despite life cycles appeared very similar, the two species seems to exhibit different tolerance to the microclimatic variations within the cave, which emerged as the main factors determining the differentiation of their niche. At least in our study area, M. bourneti tolerates broad microclimatic fluctuations and is potentially able to colonize a wide variety of caves. On the other hand, when the climatic conditions in a cave are suitable for M. menardi (narrow ranges of relatively low temperature and high humidity), M. bourneti is excluded.

Ecology and sampling techniques of an understudied subterranean habitat: the Milieu Souterrain Superficiel (MSS)

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.

Climate change may drive cave spiders to extinction

Subterranean ecosystems present ideal opportunities to study mechanisms underlying responses to changes in climate because species within them are often adapted to a largely constant temperature. We have characterized the thermal conditions of caves in the western Alps, and related these hypogean climate data to the occurrence of Troglohyphantes spiders (Araneae, Linyphiidae). Our data indicated that present distributions reflect Pleistocene glaciation events and also pointed to specific responses as a consequence of changes in temperature. Constant temperatures recorded inside caves provide an approximation of the mean annual temperature outside, thus we extended the results to a regional scale. We used ecological niche modeling to predict habitat suitability both in the Pleistocene and under future global warming scenarios. These analyses pointed toward a future decline in habitat suitability for subterranean spiders and the potential extinction of the most restricted endemic species. When compared with other species that live in confined habitats such as islands and mountains, we expect cave species to be as much, if not more, vulnerable to climate change.

Spiders in caves

World experts of different disciplines, from molecular biology to macro-ecology, recognize the value of cave ecosystems as ideal ecological and evolutionary laboratories. Among other subterranean taxa, spiders stand out as intriguing model organisms for their ecological role of top predators, their unique adaptations to the hypogean medium and their sensitivity to anthropogenic disturbance. As the description of the first eyeless spider (Stalita taenaria), an array of papers on subterranean spider biology, ecology and evolution has been published, but a comprehensive review on these topics is still lacking. We provide a general overview of the spider families recorded in hypogean habitats worldwide, we review the different adaptations of hypogean spiders to subterranean life, and we summarize the information gathered so far about their origin, population structure, ecology and conservation status. Finally, we point out the limits of the knowledge we currently have regarding hypogean spiders, aiming to stimulate future research.

Seasonal dynamics and micro-climatic preference of two Alpine endemic hypogean beetles

The climatic conditions occurring underground have a profound influence on hypogean fauna (Culver & Pipan, 2010). As far as hypogean beetles are concerned, it is well known that they generally dwell in environments which are relatively stable from an environmental point of view, characterized by constant temperature and an atmosphere saturated with water vapor (Moldovan, 2005). Indeed several hypogean beetles are adapted to narrow ranges of temperature and relative humidity, and thus classified as stenothermic and stenohygric (Howarth, 1980). Hence, it has been observed that they are able to react quickly when significant changes in the microclimatic conditions occurs (Juberthie, 1969), migrating inside the inner parts of the cave (and through the network Citation:

Unexpected diversity in the relictual European spiders of the genus Pimoa (Araneae : Pimoidae)

Abstract. Pimoidae is a small family of araneoid spiders, hitherto represented in Europe by two species with disjunct distribution in the Alps and in the Cantabrian Mountains of northern Spain. Here we report the description of two additional European species of Pimoa, discovered within the range of the only former alpine species, P. rupicola: P. graphitica sp. nov. and P. delphinica sp. nov. The new species are distinguished from the latter by genitalic characters as well as by molecular characters. On the basis of the re-examination of old and recent abundant material collected in caves and other subterranean habitats, we revise the distribution patterns of the genus Pimoa in the Alps and outline the species distribution ranges. Molecular data suggest the existence of gene flow between populations of the two new species when in sympatry. The different species probably originated in the alpine region as a result of range contractions following dramatic climatic changes in the Alps since the mid Miocene. We interpreted the present-day overlapping distribution in light of a possible postglacial expansion. Finally, we provide insights on the natural history and life cycles of the new species and discuss their phylogenetic relationships within Pimoidae.

Cave spiders choose optimal environmental factors with respect to the generated entropy when laying their cocoon

The choice of a suitable area to spiders where to lay eggs is promoted in terms of Darwinian fitness. Despite its importance, the underlying factors behind this key decision are generally poorly understood. Here, we designed a multidisciplinary study based both on in-field data and laboratory experiments focusing on the European cave spider Meta menardi (Araneae, Tetragnathidae) and aiming at understanding the selective forces driving the female in the choice of the depositional area. Our in-field data analysis demonstrated a major role of air velocity and distance from the cave entrance within a particular cave in driving the female choice. This has been interpreted using a model based on the Entropy Generation Minimization - EGM - method, without invoking best fit parameters and thanks to independent lab experiments, thus demonstrating that the female chooses the depositional area according to minimal level of thermo-fluid-dynamic irreversibility. This methodology may pave the way to a novel approach in understanding evolutionary strategies for other living organisms.

Record breaking achievements by spiders and the scientists who study them

Organismal biology has been steadily losing fashion in both formal education and scientific research. Simultaneous with this is an observable decrease in the connection between humans, their environment, and the organisms with which they share the planet. Nonetheless, we propose that organismal biology can facilitate scientific observation, discovery, research, and engagement, especially when the organisms of focus are ubiquitous and charismatic animals such as spiders. Despite being often feared, spiders are mysterious and intriguing, offering a useful foundation for the effective teaching and learning of scientific concepts and processes. In order to provide an entryway for teachers and students—as well as scientists themselves—into the biology of spiders, we compiled a list of 99 record breaking achievements by spiders (the “Spider World Records”). We chose a world-record style format, as this is known to be an effective way to intrigue readers of all ages. We highlighted, for example, the largest and smallest spiders, the largest prey eaten, the fastest runners, the highest fliers, the species with the longest sperm, the most venomous species, and many more. We hope that our compilation will inspire science educators to embrace the biology of spiders as a resource that engages students in science learning. By making these achievements accessible to non-arachnologists and arachnologists alike, we suggest that they could be used: (i) by educators to draw in students for science education, (ii) to highlight gaps in current organismal knowledge, and (iii) to suggest novel avenues for future research efforts. Our contribution is not meant to be comprehensive, but aims to raise public awareness on spiders, while also providing an initial database of their record breaking achievements.

Advances in the systematics of the spider genus Troglohyphantes (Araneae, Linyphiidae)

With 128 described species and five subspecies, the spider genus Troglohyphantes (Araneae, Linyphiidae) is a remarkable example of species diversification in the subterranean environment. In this paper, we conducted a systematic revision of the Troglohyphantes species of the Italian Alps, with a special focus on the Lucifuga complex, including the description of two new species (T. lucifer sp. nov. and T. apenninicus n. sp.). In addition, we provided new diagnostic drawings of the holotype of T. henroti (Henroti complex) and established three new synonymies within the genus. The molecular analysis of the animal DNA barcode confirms the validity of this method of identification of the Alpine Troglohyphantes and provides additional support for the morphology based species complexes. Finally, we revised the known distribution range of additional Troglohyphantes species, as well as other poorly known alpine cave-dwelling spiders. Troglohyphantes lucifer http://www.zoobank.org/urn:lsid:zoobank.org:act:AB4B644A-D18A-4EB7-99E7-B5117AED5389 Troglohyphantes apenninicus http://www.zoobank.org/urn:lsid:zoobank.org:act:3C86E78E-7145-4F0C-803E-2A909201579C