Shallow Subterranean Habitats Research Articles

Arthropod diversity in shallow subterranean habitats of the Appalachian Mountains

Subterranean arthropods are important components of soils and contribute essential food-web functions and other ecosystem services, however, their diversity and community composition has scarcely been assessed. Subterranean pitfall traps are a commonly used method for sampling soil habitats in Europe but have never been widely implemented in the Americas. We used subterranean pitfall traps to sample previously unsurveyed arthropod communities in southwestern Virginia, U.S. Traps were placed in shallow subterranean habitats (SSHs), underground habitats close to the surface where light does not penetrate, and more specifically at the interface between the soil and underlying “milieu souterrain superficiel”—a microhabitat consisting of the air-filled interstitial spaces between rocks (abbreviated MSS). In total, 2,260 arthropod specimens were collected constituting 345 morphospecies from 8 classes, 33 orders, and 94 families. A region of the mitochondrial cytochrome c oxidase subunit I (COI) gene was amplified and sequenced, and objective sequence clustering of 3% was used to establish molecular operational taxonomic units (mOTUs) to infer observed species richness. In all, 272 COI barcodes representing 256 mOTUs were documented for rare soil-dwelling arthropod taxa and are published to build a molecular library for future research in this system. This work is the first taxonomically extensive survey of North American soil-dwelling arthropods greater than 10 cm below the soil surface.

Sexual dimorphism in subterranean amphipod crustaceans covaries with subterranean habitat type.

Sexual dimorphism can evolve in response to sex-specific selection pressures that vary across habitats. We studied sexual differences in subterranean amphipods Niphargus living in shallow subterranean habitats (close to the surface), cave streams (intermediate), and cave lakes (deepest and most isolated). These three habitats differ because at greater depths there is lower food availability, reduced predation, and weaker seasonality. Additionally, species near the surface have a near-even adult sex ratio (ASR), whereas species from cave lakes have a female-biased ASR. We hypothesized (a) a decrease in sexual dimorphism from shallow subterranean habitats to cave lake species because of weaker sexual selection derived from changes in the ASR and (b) an increase in female body size in cave lakes because of stronger fecundity selection on account of oligotrophy, reduced predation, and weaker seasonality. We measured body size and two sexually dimorphic abdominal appendages for all 31 species and several behaviours related to male competition (activity, risk-taking, exploration) for 12 species. Species with an equal ASR that live close to the surface exhibited sexual dimorphism in all three morphological traits, but not in behaviour. The body size of females increased from the surface to cave lakes, but no such trend was observed in males. In cave lake species, males and females differed neither morphologically nor behaviourally. Our results are consistent with the possibility that sexual and fecundity selection covary across the three habitats, which indirectly and directly, respectively, shape the degree of sexual dimorphism in Niphargus species.

New Caledonia's enigmatic terrestrial diving beetle Typhlodessus monteithi is a derived species of Paroster

AbstractThe classification of highly adapted species in well‐studied clades may be obscured by convergent character evolution. This is for example the case in aquatic lineages adapted to subterranean (and shallow subterranean) habitats, in which species usually possess reduced eyes and wings as well as translucent cuticles. In 1985, the terrestrial diving beetle genus and species Typhlodessus monteithi Brancucci (Coleoptera: Dytiscidae) was described from a shallow subterranean habitat in New Caledonia. Until now, the systematic classification of Typhlodessus remains unclear, as it could not be assigned to any of the known tribes of the subfamily Hydroporinae. Here, we reveal this species' phylogenetic position and evolutionary history. We obtained molecular data from an almost 30 years old museum specimen and performed phylogenetic analyses using complete mitochondrial genomes and nuclear markers, which resulted in the placement of Typhlodessus monteithi within the subtribe Sternopriscina, as a junior synonym of the genus Paroster. The genus Paroster contains epigean, stygobitic as well as two other terrestrial Australian species. Our finding extends the geographical distribution of Paroster to New Caledonia. Adaptation to terrestrial habitats in Paroster species may be a way to survive in hyper humid environments that however might lack suitable lentic habitats.

Vertical distribution of spiders (Araneae) in Central European shallow subterranean habitats

Shallow subterranean habitats are among the last habitats in Central Europe to be arachnologically researched. Using stratified pipe traps, we studied the vertical distribution of spiders in soil and interspaces in bedrock (shallow subterranean habitats). Specifically, we sampled fauna in different substrates, including limestone, sandy marlstone, sandy marl, claystone, loess, and artificial gravel accumulation. Employing stratified pipe traps allowed us to identify the depth at which particular species occurred. Across multiple years and sampling sites, we collected 76 spider species, 21 of which showed an affinity for subterranean microhabitats. Some of these species occurred in interspaces in soil and bedrock, whereas others have been previously found in subterranean ant nests and animal burrows. We collected five species (Iberina microphthalma, Centromerus cf. piccolo, Porrhomma cambridgei, P. microcavense, and P. microps) almost exclusively at depths over half a meter, suggesting the strong affinity of these species for a subterranean lifestyle. We provide diagrams of these species’ vertical distribution and photo-document eye reduction. Our study demonstrates that poorly studied shallow subterranean habitats harbor diverse subterranean spider fauna, including several previously considered rare species in Central Europe.

Hotspot in ferruginous rock may have serious implications in Brazilian conservation policy

A hotspot of subterranean Collembola in ferruginous rock caves and Mesovoid Shallow Substratum is revealed by the analysis of pseudocryptic diversity. The diversity is accessed by detailed description of chaetotaxy and slight variation in morphology of 11 new species of Trogolaphysa Mills, 1938 (Collembola, Paronellidae, Paronellinae) and the 50 previously recorded species of springtails from caves, using optical and electronic microscopy. When combined with recent subterranean surveys, our results show an important reservoir of cave diversity in the Mesovoid Shallow Substratum. Contrastingly the conservation policy for subterranean fauna in metallogenic areas in Brazil prioritizes the caves instead the cave species, which may be extremely detrimental to the fauna in the shallow subterranean habitats not accessible to humans.

Cave lithology effect on subterranean biodiversity: A case study in quartzite and granitoid caves

Physical features and lithology variations contribute to promoting changes in faunal composition and richness between caves in Neotropics. Cave lithology effects on biodiversity were reported to iron ore caves in Brazil, however, it is less clear to granitoid and quartzite caves. Hence, based on these two kinds of rocks we correlate invertebrates species richness and composition with some cave features (lithology, the distance between caves, cave extension, number of entrances, entrance size, environmental stability, and altitude). Overall, 1,027 invertebrate species were recorded in 50 sampled caves. From this total, 11 obligate cave species were found. Invertebrate assemblages showed considerable turnover between caves and rock types with a strong contribution of replacement component of beta diversity. Replacement influence was greatest in quartzite caves mainly because of altitude and distance among caves. Furthermore, richness was determined by cave extension in both lithotypes, although this relationship was much more pronounced for the granitoid caves, which contradicts previous studies. The granitoid caves studied here are predominantly structured by stacked blocks with macro and meso anastomosed subterranean spaces that provide an extensive network of interstices with structural characteristics similar to shallow subterranean habitats that may increase in habitat availability and species richness. The study highlight that the lithology-mediated effects of cave extension on richness must be considered for quartzite and granitoid in the ecological and conservational proposal. Furthermore, altitude and distance among caves were important elements determining invertebrate composition.

Distributional dynamics of a specialized subterranean community oppose the classical understanding of the preferred subterranean habitats

AbstractTroglobionts are organisms that are specialized for living in a subterranean environment. These organisms reside prevalently in the deepest zones of caves and in shallow subterranean habitats, and complete their entire life cycles therein. Because troglobionts in most caves depend on organic matter resources from the surface, we hypothesized that they would also select the sections of caves nearest the surface, as long as environmental conditions were favorable. Over 1 year, we analyzed, in monthly intervals, the annual distributional dynamics of a subterranean community consisting of 17 troglobiont species, in relation to multiple environmental factors. Cumulative standardized annual species richness and diversity clearly indicated the existence of two ecotones within the cave: between soil and shallow subterranean habitats, inhabited by soil and shallow troglobionts; and between the transition and inner cave zones, where the spatial niches of shallow and deep troglobionts overlap. The mean standardized annual species richness and diversity showed inverse relationships, but both contributed to a better insight into the dynamics of subterranean fauna. Regression analyses revealed that temperatures in the range 7–10°C, high moisture content of substrate, large cross section of the cave, and high pH of substrate were the most important ecological drivers governing the spatiotemporal dynamics of troglobionts. Overall, this study shows general trends in the annual distributional dynamics of troglobionts in shallow caves and reveals that the distribution patterns of troglobionts within subterranean habitats may be more complex than commonly assumed.

Response of shallow subterranean freshwater amphipods to habitat drying

The ability of three amphipods that occupy shallow subterranean habitats in the lower Potomac Basin of the US (hypotelminorheic), which often dry out seasonally, to withstand desiccation by burrowing in clay was investigated. Both Crangonyxshoemakeri, a wetland species, and Stygobromustenuis, a subterranean species, burrowed in clay in the laboratory after surface water was removed. Gammarusminus, a spring species, did not. All three species exhibited behavioral changes as the habitat dried out.

Seven new species of the spider genus Ochyrocera from caves in Floresta Nacional de Carajás, PA, Brazil (Araneae, Ochyroceratidae).

Seven new species of the spider genus Ochyrocera from cave areas in Floresta Nacional de Carajás (state of Pará, northern Brazil) are described: Ochyrocera varys sp. n., Ochyrocera atlachnacha sp. n., Ochyrocera laracna sp. n., Ochyrocera aragogue sp. n., Ochyrocera misspider sp. n., Ochyrocera charlotte sp. n., and Ochyrocera ungoliant sp. n. Two groups of the species are discussed, the quinquivittata group that include specimens with an apparently bifid retrolateral apophysis in the cymbium of the male palp and the arietina group, here proposed, that include those specimens with an entire cymbium, with no retrolateral apophysis, in the male palp. Although these species were abundant inside caves, the examined specimens do not have troglomorphic characteristics and can be classified as edaphic troglophile species, capable of completing its life cycle in soil, shallow subterranean habitats, or caves.

Aquatic Shallow Subterranean Habitats: General Features

Shallow (superficial) subterranean habitats, or SSHs are very close to the surface, but are aphotic. Some of these habitats are large cavities, especially lava tubes, while others are small cavity habitats, especially the underflow of streams and rivers (interstitial aquifers), and the soil. But, there is an especially interesting set of SSHs that do not fit into either category, with intermediate sized space with many close connections with the surface. These habitats include talus and scree slopes, milieu souterrain superficiel (MSS), in both carbonate (soluble) and non-carbonate rocks, including volcanic rocks. Epikarst, the uppermost layer of karst formed largely by solutional processes that may be air or water filled, occupies a similar vertical position to that of the MSS, but perhaps with smaller spaces. The most superficial of SSHs are the miniature perched aquifers (isolated wetlands) given the name hypotelminorheic that exit through seepage springs, diffuse discharges when the flow cannot be immediately observed but the land surface is wet compared to the surrounding area. These two SSHs (epikarst and hypotelminorheic), which do not extend beyond a few meters in depth are called strict sense shallow subterranean habitats and will be presented in more detail.

Catching of spiders in shallow subterranean habitats in the Czech Republic

Catching of spiders in shallow subterranean habitats in the Czech Republic

Land snails from subterranean traps exposed in a forested scree slope (Western Carpathians, Slovakia)

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Organic Carbon in Shallow Subterranean Habitats

subterranean habitatsOrganic carbon is likely to be a limiting factor in shallow subterranean habitats (SSHs). Data on dissolved organic carbon (DOC) in three SSHs are reviewed: (1) hypotelminorheic and associated seepage springs (Nanos Mountain, Slovenia), (2) hyporheic zones (Rhône River, France and seepage streams on Nanos Mountain, Slovenia), and (3) epikarst (China, Slovenia, and USA). Hypotelminorheic habitats are superficial groundwater sites less than 1 m below the surface that exit from seepage springs. Hyporheic habitats are the underflow of streams and rivers. Epikarst is the uppermost zone of karst with extensive small cavities and channels. Nanos hypotelminorheic sites that harbored stygobiotic species had organic carbon values averaging 3.4 mg C L−1, and temporal variability was high. For hypoheic sites in the Rhône River basin and on Nanos Mountain, mean values ranged from 1.4 to 3.5 mg C L−1. In the more extensively studied Rhône River basin sites, temporal variability was low. Epikarst DOC ranged from 0.70 to 1.10 mg C L−1 in three caves in China (Shihua Cave), Slovenia (Postojna Planina Cave System) and United States (Organ Cave, West Virginia). These results suggest that organic carbon in aquatic SSHs is lowest in epikarst.Keywords: dissolved organic carbon, epikarst, hyporheic, hypotelminorheic, seepage spring.DOI: 10.3986/ac.v42i2.603

The Fauna of Seepage Springs and Other Shallow Subterranean Habitats in the Mid-Atlantic Piedmont and Coastal Plain

A number of shallow groundwater habitats that occur in the Coastal Plain and Piedmont of the mid-Atlantic region are documented and described. These isolated tiny aquifers are underlain by clay (hypotelminorheic habitats) and exit at seepage springs, springs, tiled fields and tile drains, and shallow wells. These shallow groundwater habitats harbor species with reduced eyes and pigment that are limited to these habitats. The distribution of 23 such species—four planarians (Sphalloplana and Phagocata), one snail (Fontigens), 13 amphipods (Stygobromus), and five isopods (Caecidotea)—is documented, based on over 450 records. More species (16) were found in hypotelminorheic habitats than in other shallow groundwater habitats. Also, more species were found exclusively in either the Piedmont or Coastal Plain, but seven species were found along the boundary (Fall Line) between these physiographic provinces. Compared to surface waters in nearby habitats, hypotelminorheic water had higher conductivity, higher dissolved oxygen, and slightly lower pH.

Duality of terrestrial subterranean fauna

Terrestrial animals in subterranean habitats are often classified according to their degree of morphological or ecological specialization to the subterranean environment. The commonly held view is that, as distance into a cave increases, the frequency of morphologically specialized, i.e., troglomorphic, species or ecological specialization will increase. We tested this hypothesis for the fauna in 54 caves in Slovenia–the classical land for subterranean biology. We found that there exist two ecologically well separated terrestrial subsurface faunas: one shallow and one deep. 1) The shallow subterranean fauna, adapted to the terrestrial shallow subterranean habitats (SSHs) in the upper 10 m of subsurface strata, is most diverse. It consists of randomly distributed non-troglobionts and a major group of troglobionts adapted to the soil root zone. 2) The deep subterranean fauna is represented by a minor group of troglobionts, adapted to caves. Troglobionts are strictly divided between the two faunas. There is strong evidence that in karstic ecosystems with deep-rooted vegetation this might be a global pattern, or that in these locations only the shallow subterranean fauna exist.

Ecological studies of an epikarst community in Snežna jama na planini Arto – an ice cave in north central Slovenia

Epikarst biodiversity in relation to environmental conditions was studied for the first time in an ice cave, Snežna jama na planini Arto on Mt. Raduha in north central Slovenia. In this alpine cave five sampling sites were monitored for fauna in percolation water in the period of one year. Temperature, conductivity, discharge, pH, total hardness and concentrations of various ions (calcium, chloride, nitrite, sulphate and phosphate) of water were measured. At the entrance of the cave ice is present all year round and the temperature inside the cave rises to a maximum of 4°C. These circumstances are reflected in the fauna found in percolating water. The first sampling site in the permanent ice was without fauna, as did the sampling site in an area with moonmilk. In the other three sampling sites, individuals of ten invertebrate taxa were found, Copepoda being the most abundant. Their abundance was positively correlated with discharge, pH and temperature of percolation water and additionally in the most abundant drip also with conductivity and total hardness. High proportion of immature copepods in drips shows that epikarst is their primary (i.e. source) habitat. Investigations of the alpine epikarst fauna can help to understand better the ecology of the epikarst fauna and its roles within the large range of different shallow subterranean habitats.

Tasmanian Trechinae and Psydrinae (Coleoptera, Carabidae): a taxonomic and biogeographic synthesis, with description of new species and evaluation of the impact of Quaternary climate changes on evolution of the subterranean fauna(3)

This paper provides taxonomic, distributional and ecological data for 59 species in 17 genera of Trechinae and Psydrinae from Tasmania, and describes 18 new species in six existing genera (Pterocyrtus, Tasmanorites, Sloanella, Trechistus, Goedetrechus, Tasmanotrechus) collected from caves, forest and montane habitats: Pterocyrtus grayi sp. nov., P. meridionalis sp. nov., Tasmanorites beatricis sp. nov., T. daccordii sp. nov., T. lynceorum sp. nov., T. microphthalmus sp. nov., Sloanella gordoni sp. nov., Trechistus gordoni sp. nov., Goedetrechus minutus sp. nov., G. rolani sp. nov., G. florentinus sp. nov., G. damperi sp. nov., Tasmanotrechus gordoni sp. nov., T. alticola sp. nov., T. montisfieldi sp. nov., T. osbornianus sp. nov., T. moorei sp. nov., T. rolani sp. nov. Forty-one (41) previously described species have been re-examined and illustrated with supplementary descriptions. New collection records combined with the published literature revealed 196 records of 83 species in 21 genera, collected from 41 localities (including 11 karst areas). Regional-scale survey coverage has been patchy and three biogeographic regions stand out as poorly surveyed: Flinders, South East, and Northern Midlands. Local-scale survey efforts have been intensive at just a few localities, the richest being 18 species recorded at Cradle Mountain. Seventeen (17) described species of Zolini and Trechini are troglobites with distribution ranges restricted to individual karst areas. Some karst areas and caves harbour multiple congeneric species which differ in their degree of troglomorphic specialization suggesting heterochronic colonisations, possibly linked to multiple Quaternary glacial / inter-glacial cycles. Palaeo-climatic and palaeo-vegetation evidence is examined to test the ‘Climatic Relict Hypothesis’ as a mechanism driving evolution of the subterranean fauna. It is proposed that present-day troglobitic Trechinae in Tasmania are derived from troglophilic progenitors that colonised subterranean habitats from adjacent forest ground litter habitats during Pleistocene inter-glacial periods, while retreat of forests during glacial periods isolated subterranean populations from surface populations facilitating troglogenesis. It is predicted that future collecting efforts will reveal many additional new subteranean species, including in non-karstic Shallow Subterranean Habitats (SSH).

Vertical distribution of spiders in soil

Research studies of the shallow subterranean habitats as environments for arthropods have been sparse up to this point. Using subterranean traps, we studied the distribution of spiders in soil profile over a depth span of 5-95 cm at six sites. Although almost 40% of individual specimens (1088 in total) were obtained from the epigeon (5 cm depth), spiders colonized all parts of the soil profiles examined. Beside ground-dwelling species with significant preferences for the upper layers, some species (Porrhomma microphthalmum (O. Pickard-Cambridge 1871), Centromerus cavernarum (L. Koch 1872), Cicurina cicur (Fabricius 1793), Dysdera lantosquensis Simon 1882, and Nesticus cellulanus (Clerck 1757)) commonly inhabited the whole range of the profiles studied, without any depth preference. In contrast, depigmented and microphthalmous Porrhomma microps (Roewer 1931) and Maro sp. exclusively inhabited deep soil layers adjoining void systems in bedrock.

Redefining the extent of the aquatic subterranean biotope—shallow subterranean habitats

AbstractCaves are the best known subterranean habitats, harbouring animals with a convergent morphology of reduced eyes and pigment and elongated appendages (troglomorphy). We have identified a group of aphotic aquatic habitats close to the surface [shallow subterranean habitats (SSHs)] that also harbour troglomorphic species, but with intimate surface connections, typically small in size but very abundant, with high levels of organic matter compared to caves. SSHs are hypotelminorheic, hyporheic, and epikarstic habitats. All SSHs show a pattern of environmental variation intermediate between that of surface and deep subterranean habitats, and all show seasonal and sometimes daily fluctuations in temperature but with truncated extremes. Initial colonization of these habitats was likely the result of environmental changes, especially increasing aridity, perhaps during the Pleistocene and the Messinian salinity crisis. The evolution of the troglomorphic morphology of reduced eyes and pigment and elaborated extra‐sensory structures likely occurred in situ rather than by dispersal from other habitats. SSHs may be a stepping stone to colonization of deeper subterranean habitats. Copyright © 2011 John Wiley & Sons, Ltd.

PSEUDOCRANGONYХ ELENAE, SP. N. (CRUSTACEA: AMPHIPODA: PSEUDOCRANGONYCTIDAE) ИЗ СУБПОВЕРХНОСТНЫХ ПОДЗЕМНЫХ МЕСТООБИТАНИЙ (СППМ) ВОСТОЧНОГО СИХОТЭ-АЛИНЯ

The new stygobiont amphipod species, Pseudocrangonyх elenae, sampled in shallow subterranean habitats (SSHs) of Eastern Sikhote-Alin Mountain Ridge, the Serebryanka River basin (Russia, Primorskii Krai) is described.