Capturing arthropod diversity in complex cave systems

Aim

Identify the optimal combination of sampling techniques to maximize the detection of diversity of cave‐dwelling arthropods.

Location

Central‐western New Mexico; north‐western Arizona; Rapa Nui, Chile.

Methods

From 26 caves across three geographically distinct areas in the Western Hemisphere, arthropods were sampled using opportunistic collecting, timed searches, and baited pitfall trapping in all caves, and direct intuitive searches and bait sampling at select caves. To elucidate the techniques or combination of techniques for maximizing sampling completeness and efficiency, we examined our sampling results using nonmetric multidimensional scaling (NMDS), analysis of similarity (ANOSIM), Wilcoxon signed‐rank tests, species richness estimators and species accumulation curves.

Results

To maximize the detection of cave‐dwelling arthropod species, one must apply multiple sampling techniques and specifically sample unique microhabitats. For example, by sampling cave deep zones and nutrient resource sites, we identified several undescribed cave‐adapted and/or cave‐restricted taxa in the south‐western United States and eight new species of presumed cave‐restricted arthropods on Rapa Nui that would otherwise have been missed. Sampling techniques differed in their detection of both management concern species (e.g., newly discovered cave‐adapted/restricted species, range expansions of cave‐restricted species and newly confirmed alien species) and specific taxonomic groups. Spiders were detected primarily with visual search techniques (direct intuitive searches, opportunistic collecting and timed searches), while most beetles were detected using pitfall traps. Each sampling technique uniquely identified species of management concern further strengthening the importance of a multi‐technique sampling approach.

Main conclusions

Multiple sampling techniques were required to best characterize cave arthropod diversity. For techniques applied uniformly across all caves, each technique uniquely detected between ~40% and 67% of the total species observed. Also, sampling cave deep zones and nutrient resource sites was critical for both increasing the number of species detected and maximizing the likelihood of detecting management concern species.

     

Evolution of cave living in Hawaiian Schrankia (Lepidoptera: Noctuidae) with description of a remarkable new cave species

Although temperate cave‐adapted fauna may evolve as a result of climatic change, tropical cave dwellers probably colonize caves through adaptive shifts to exploit new resources. The founding populations may have traits that make colonization of underground spaces even more likely. To investigate the process of cave adaptation and the number of times that flightlessness has evolved in a group of reportedly flightless Hawaiian cave moths, we tested the flight ability of 54 Schrankia individuals from seven caves on two islands. Several caves on one island were sampled because separate caves could have been colonized by underground connections after flightlessness had already evolved. A phylogeny based on approximately 1500 bp of mtDNA and nDNA showed that Schrankia howarthi sp. nov. invaded caves on two islands, Maui and Hawaii. Cave‐adapted adults are not consistently flightless but instead are polymorphic for flight ability. Although the new species appears well suited to underground living, some individuals were found living above ground as well. These individuals, which are capable of flight, suggest that this normally cave‐limited species is able to colonize other, geographically separated caves via above‐ground dispersal. This is the first example of an apparently cave‐adapted species that occurs in caves on two separate Hawaiian islands. A revision of the other Hawaiian Schrankia is presented, revealing that Schrankia simplex, Schrankia oxygramma, Schrankia sarothrura, and Schrankia arrhecta are all junior synonyms of Schrankia altivolans. © 2009 The Linnean Society of London, Zoological Journal of the Linnean Society, 2009, 156 , 114–139.     

The hypogean invertebrate fauna of Georgia (Caucasus)

Information about the cave invertebrates of Georgia, Caucasus, is summarised, resulting in 43 troglo- and 43 stygobiont taxa reported from 64 caves. Species distribution analyses were conducted for 61 caves harbouring 58 invertebrate taxa, with the majority of caves (39) located in Apkhazeti (north-western Georgia). In 22 caves from central-west Georgia (Samegrelo, Imereti and Racha-Lechkhumi regions of west Georgia) 31 taxa are reported. Composition of cave fauna differed strongly between the caves in Apkhazeti and the central-west of Georgia. Only two taxa of the total 86 were shared, resulting in negligible similarity (Sørensen-Dice coefficient S_s=4.8%). Rarefaction indicated an increase in number of species with additional sampling could increase species richness from 58 to 76 for caves in Apkhazeti and from 31 to 69 for caves in central-west Georgia. These findings suggest that the low invertebrate species richness observed in caves of western Georgia is the result of insufficient sampling. A pairwise approach to analysing species co-occurrence showed ten positive spatial associations in 7 out of 86 cave species, all from Kveda Shakurani and Tsebelda caves. The species co-occurring in the same microhabitat require further study to understand their relationships.     

Spatial segregation among age classes in cave salamanders: habitat selection or social interactions?

Within species, individuals with different sexes, morphs and age classes often show spatial segregation. Both habitat selection and social processes have been proposed to explain intraspecific spatial segregation, but their relative importance is difficult to assess. We investigated spatial segregation between age classes in the cave salamander Hydromantes (Speleomantes) strinatii, and used a hypothetico-deductive approach to evaluate whether social or ecological processes explain segregation pattern. We recorded the location and age class of salamanders along multiple caves; we measured multiple microhabitat features of different sectors of caves that may determine salamander distribution. We assessed age-class segregation, and used generalized mixed models and an information-theoretic framework, to test if segregation is explained by social processes or by differences in habitat selection. We found significant age-class segregation, juveniles living in more external cave sectors than adults. Multiple environmental features varied along caves. Juveniles and adults showed contrasting habitat selection patterns: juveniles were associated with sectors having high invertebrate abundance, while adults were associated with scarce invertebrates and low temperature. When the effect of environmental features was taken into account, the relationship between juveniles and adults was non negative. This suggests that different habitat preferences, related to distinct risk-taking strategies of age classes, can explain the spatial segregation. Juveniles require more food and select more external sectors, even if they may be risky. Conversely, adults may trade off food availability in favour of safe areas with stable micro-climate.     

Milyeringa Veritas (Eleotridae), a remarkably versatile Cave Fish from the Arid Tropics of Northwestern Australia

The blind cave gudgeon Milyeringa veritas is restricted to groundwaters of Cape Range and Barrow Island, northwestern Australia. It occurs in freshwater caves and in seawater in anchialine systems. It is associated with the only other stygobitic cave vertebrate in Australia, the blind cave eel, Ophisternon candidum, the world's longest cave fish, and a diverse stygofauna comprising lineages with tethyan tracks and widely disjunct distributions, often from North Atlantic caves. The cave gudgeon inhabits a karst wetland developed in Miocene limestones in an arid area. There is an almost complete lack of information on the basic biology of this cave fish, despite it being listed as threatened under the Western Australian Wildlife Conservation Act. Allozyme frequencies and distributions indicate significant population sub-structuring on the Cape Range peninsula such that the populations are essentially isolated genetically suggesting that more than one biological species is present. Further, they suggest that the vicariant events may have been associated with a series of eustatic low sealevels. Analysis of intestinal contents indicates that they are opportunistic feeders, preying on stygofauna and accidentals trapped in the water, at least at the sites sampled which were open to the surface, a conclusion supported by the results of stable isotope ratio analysis. The gudgeons are found in freshwater caves and throughout deep anchialine systems in which they occur in vertically stratified water columns in which there is a polymodal distribution of water chemistries (temperature, pH, salinity, dissolved oxygen, redox, dissolved inorganic nitrogen series, hydrogen sulphide).     

Regional species richness in an obligate subterranean dwelling fauna – epikarst copepods

Aim  The diversity of the obligate cave-dwelling fauna has proved difficult to measure because of the highly localized distributions of most species. We investigated: (1) the local and regional diversity patterns of a major component of the obligate cave-dwelling fauna living in the epikarst zone, the karst layer closest to the surface; (2) variations in local and regional patterns of species richness; and (3) sampling sufficiency at multiple scales.
Location  Caves in the Dinaric Mountains of Slovenia.
Methods  We sampled continuously the abundance of 37 species of copepods dislodged from the epikarst from 35 ceiling drips in six caves for a period of one year. Copepods were collected in a specially designed net that allowed continuous collection.
Results  Based on species accumulation curves and Chao estimates of total diversity, we determined that 3–4 months of continuous sampling were sufficient to find 90% of the species in a drip, that five drips were sufficient to find 90% of the species in a cave, and that five caves were sufficient to find 90% of the species in a region.
Main conclusions  The epikarst copepod fauna is a significant part of the aquatic cave fauna, contributing about 20% at the regional level. Because of the scale of variation, much of which occurs within a cave, and because of the availability of continuous sampling devices, the epikarst component of subterranean diversity seems to be more thoroughly and accurately measured than do other components.     

Airborne fungi as indicators of ecosystem disturbance: an example from selected Tatra Mountains caves (Poland)

We report on the determination of the spore concentration and the species composition of the airborne fungi in selected caves of the Tatra Mountains, Poland. The following caves were surveyed: Mylna, Ob?azkowa, Mro?na, Zimna and Naciekowa. The sampling was carried out in July 2015 and in January 2016. The aeromycological analyses were performed with the impact method, using the Air Ideal 3P apparatus and potato dextrose agar (PDA, Biocorp) culture medium. In the course of the July 2015 analysis, 17 species of fungi were isolated and 11 species were isolated in January 2016. In Mylna and Naciekowa caves, the dominant species were Cladosporium cladosporioides and Stachybotrys cylindrospora. In Ob?azkowa cave, Rhizoctonia predominated and in Zimna cave—the colonies of the yeast-like fungi, along with S. cylindrospora. In Mro?na cave, Penicillium notatum was the most abundant taxon. In the winter time, in the majority of the caves Penicillium spp. predominated, with the exception of Mro?na and Naciekowa caves where Aspergillus niger was dominant. We propose that aeromycological monitoring be performed regularly in the following caves: Mro?na, Naciekowa and Zimna.     

Patterns of endemism of the eastern North American cave fauna

Aim Over 250 species of obligate terrestrial cave‐dwelling animals (troglobionts) are known from single caves in the eastern United States. We investigate their geographical distribution, especially in relation to other troglobionts. We relate these patterns to taxonomic group, opportunities for dispersal and geographical location. Location Caves of the United States east of the Mississippi River. Methods We associated over 3000 records of more than 450 troglobiotic species and subspecies with hexagons of 1000, 5000 and 10,000 km² in size. We calculated Moran's I, black–white joins and cubic regression of endemics on non‐endemics at all three spatial scales. For 5000 km² hexagons, we modelled the spatial autocorrelation of the residuals of the cubic regression of endemics on non‐endemics. Results Differences among orders in percentage single‐cave endemism were not significant, except for Pseudoscorpionida, which was higher (69%) than any other order. At all three scales, Moran's I and black–white joins were significant, indicating a clumped distribution of both single‐cave endemics and other troglobionts. Spatial patterns were similar at all three scales and Moran's I was highest at 5000 km². The cubic fit of endemics to non‐endemics was consistently better, with less systematic error or residuals, than were linear or quadratic models. Residuals showed a significant geographical pattern with excess endemics in more southerly locations. Main conclusions There was both a non‐spatial and spatial component to the pattern of single‐cave endemism. The non‐spatial component was the association of high levels of single‐cave endemism with areas of high diversity of non‐endemics. It may be that both are high because of high secondary productivity. Spatially, single‐cave endemism is high in central rather than peripheral areas and in the southern part of the range. It is not higher in areas of more dissected limestone, which would reduce migration rates; if anything endemism is lower. Regional spatial effects are important, indicating that cave communities cannot be understood (or protected) in isolation.     

Multi-spatial analysis on cave ecosystems to predict the diversity of subterranean invertebrates

Subterranean habitats around the world can shelter diversified and threatened faunal communities. However, issues related to alterations in the landscape and structure of subterranean habitats still need to be better understood. Therefore, we used a multi-spatial scale analysis of land cover, land use, and cave habitats to predict the diversity of communities of subterranean invertebrates. We hypothesized that changes in land cover promote alterations in both faunal richness and composition and microhabitat diversity and that microhabitat features determined subterranean biodiversity. Sixteen limestone caves were sampled in Brazil at micro, meso, and macro scales using quadrats (1m²), transects (100 meters) as sample units inside caves and buffers with the radius of 100 and 250 meters in the surroundings of the cave entrances. Models performed showed that land cover and land use influenced cave environments, regarding both microhabitats traits and terrestrial invertebrate richness and composition. We also observed a relationship between microhabitat structure and terrestrial invertebrate richness and composition. Our results showed that deforested areas had negative effects on species richness and changed their composition, while natural areas had positive effects on microhabitat diversity. The same effects were observed for both 100 and 250 meters buffers. Invertebrate richness was negatively predicted by deforested areas while positively predicted by natural areas. Richness was also positively predicted by the combination of all microhabitat traits, and dissimilarity of fauna was influenced by microhabitat diversity in mesoscale and microscale by all microhabitat elements. The results highlight the importance of the landscape surrounding the caves to conserve the subterranean habitats and their fauna. Due to the spatial and temporal changes in the global environmental scenario, we argue the urgency of further detailed studies in fragmented landscapes to define minimum areas of protection for cave environments.     

Emergence of Coleoptera from deadwood in a managed broadleaved forest in central Europe

We studied Coleoptera emerging from deadwood in a broadleaved forest that has been managed with nature-oriented forestry since 1990 and in which an accumulation of 10m³ deadwood/ha has been achieved. We sampled a total of 11m³ of deadwood from oak and beech trees and yielded 32,477 individuals pertaining to 342 species. The number of species emerging from oak deadwood was significantly higher than that from beech. Significantly more species emerged from deadwood with medium size (15–21cm) diameter than from smaller (5–7cm) or larger (40–60cm) diameters. The stage of decay did not influence the number of species during the first 6 years of decomposition. Species richness strongly increased with the amount of deadwood sampled. Species–area regressions yielded z-values of 0.81 for oak and 0.87 for beech deadwood. The beetle assemblage was characterized by a low number of xylophagous species and a high number of mobile zoophagous species. However, two-thirds of the individuals sampled pertained to nine species of Scolytidae. This is why Shannon–Wiener diversity (H) and evenness-indices (E) greatly decreased with increasing number of scolytids. The species and individuals yielded from the sun-exposed deadwood outnumbered those from shaded areas. Namely the scolytid Taphrorychus bicolor reached remarkably high densities in the sun-exposed beech deadwood (>800 individuals/m²). In contrast, oak deadwood never harboured such high numbers of scolytids. Felling of moribund trees had decreased the number of scolytids but it had also considerably reduced the number of rare and endangered species.     

Decrease in allochthonous organic inputs in dark submarine caves,connection with lowering in benthic community richness

Ten sediment trap arrays were deployed over two years for periods of 3 to 40 days in three different sampling points along a 50 m long Mediterranean submarine cave. Mean total particulate matter flux decreased strongly from the semi-dark area (3.3 g m^–2 d^–1) to the dark area (0.8 and 0.6 g m^–2 d^–1). Carbon represented 3.3% to 3.5% and nitrogen 0.34% to 0.38% of settling dry matter. The decrease in organic input from the entrance to the terminal part of the cave results in increasingly oligotrophic conditions with distance from the cave entrance. Horizontal resource limitation can be connected with a strong zonal decrease in fauna richness. Biomass declines both in hard substrate and soft bottom communities. Despite major differences, some similarities are noticed between oligotrophic conditions that may occur in the dark cave and those in around 1000 m depth ecosystems. Dark oligotrophic submarine caves can be considered to be good scale models for the study of some aspects of general trophic pathways.     

Hickmania Troglodytes, the Tasmanian Cave Spider, and its Potential Role in Cave Management

Cave faunas – which often contain a high representation of spiders – are subject to increasing pressure from the effects of epigean habitat degradation and recreational caving activities. Hickmania troglodytes is a prominent member of the Tasmanian cave fauna, a spider of phylogenetic, zoogeographic and ecological importance, but about which little has previously been known. Long-term monitoring has revealed many unusual life-cycle characteristics in this species, most of which occur over long periods of time and are dependent upon environmental stability. The species presents a potentially useful tool in the management and monitoring of cave fauna and karst, as it is large, conspicuous, numerous, ubiquitous, sedentary, functionally significant and potentially sensitive to various sources of disturbance. H. troglodytes may provide a visible and obvious measure of disturbance in and around cave entrances, and may also prove useful in detecting broader scale impacts affecting the entire cave. Many promising developments are being made in terms of cave management in Tasmania, but other issues are less well addressed and still need to be resolved. With further research, the use of indicator or sentinel species may prove to be well suited to the less complex and often sparsely populated subterranean environment, and may play an important role within larger management strategies for cave fauna and karst.     

Vicariance, dispersal and scale in the aquatic subterranean fauna of karst regions

1. The causes of distribution patterns of stygobionts (obligate subterranean-dwelling aquatic species) were examined with special emphasis on vicariance and dispersal.
2. Dispersal was investigated on the premise that if migration is important, then migration at small scales should predict patterns at larger scales. Data on the copepod fauna of epikarst in Slovenia were especially useful for the study of migration, because data on habitat occupancy could be collected at scales of individual drips located metres apart to the scale of individual caves to entire karst regions. Occupancy of drips in one cave was a remarkably good predictor of occupancy of caves in a region, although not of the overall range of a given species. These results were also supported by occupancy patterns of the general stygobiotic fauna of West Virginia caves, compared at different scales.
3. Vicariance was investigated by noting that proximity to marine embayments increases the likelihood of vicariant speciation. In the U.S.A., only the fauna of the Edwards Aquifer of Texas has a significant component of marine-derived species. Differences in shape of the relationship between species number and number of caves in a county indicated that the marine-derived component represented an addition to rather than a replacement of the other stygobiotic species.
4. Thus, we found evidence for the importance of both vicariance and dispersal. The techniques employed could be used to study these patterns more generally, as more data become available.     

The distribution of cave twilight‐zone spiders depends on microclimatic features and trophic supply

Caves are not closed systems. Trophic dynamics in these habitats are driven by resource availability, and species that move between cave and outdoor environments may play a major role in resource availability. Spiders are among the most abundant invertebrates in caves; however, very few studies have tested factors hypothesized to affect the distribution of spiders among caves, and it is not known whether the trophic features of caves play a role in determining the occurrence, abundance, or breeding success of spiders. We assessed the distribution of the cave‐dwelling orb‐weaver spider Meta menardi in Italy, in a Mediterranean and in a Pre‐alpine area during summer and winter. We analyzed the relationships between spider distribution and multiple cave features, describing both the abiotic and the biotic environment. Using visual encounter surveys, the detection probability of this species was high, indicating that this technique provides reliable information on spider distribution. In Mediterranean caves, spider presence was more likely in cold and wet caves with abundant dipterans. In Pre‐alpine caves, spider presence was more likely in deep caves with abundant dipterans. Dipteran abundance was the variable best explaining spider distribution when pooling all sampled caves. This study shows that adults of M. menardi do not occur randomly among caves, but select caves with specific features. Prey availability and abiotic features are major determinants of habitat suitability for cave spiders. The strong relationship between spider distribution and prey availability suggests that the distribution of these spiders might be an indicator of the resources available in the twilight zones of caves.     

High β diversity in the flora of Californian serpentine 'islands'

Identification of global biodiversity hotspots is a leading conservationpriority ( Hotspots.Conservation International, Washington, DC; Precious Heritage: The Statusof Biodiversity in the United States. Oxford University Press, Oxford, UK), but weknow little about the nature and structure of such hotspots. Botanical richnessin one recently identified hotspot, the California Floristic Province, has longbeen attributed by evolutionists to edaphic and climatic heterogeneity. Here we demonstrate that the flora restricted (endemic) toserpentine soil, the state's most botanically distinctive substrate, showsunusually high ' diversity' – i.e., spatial variation inspecies composition – among regions, although ''diversity within any given region is low. Conservation of an endemic-rich florarequires a network of sites to capture this among-region or spatial component ofdiversity.     

Organochlorine and mercury residues in fish from Lake Simcoe,Ontario 1970–76

Synopsis Lake Simcoe located in the central Ontario plain has four major streams draining the watershed. Persistent organochlorine insecticides were used in the basin for mosquito control and agricultural production until restricted. Methyl mercury compounds have been phased out and a voluntary restriction occurred for PCB.Ten species of fish were collected between 1970 and 1976 for organochlorine and mercury analysis. DDT residues significantly declined between 1970 and 1975–76 in all species except small Stizostedion vitreum vitreum and large Salvelinus namaycush. Eggs taken 1975–76 from small S. namaycush had DDT residues below the critical level reported for the production of viable offspring, but this was not so for large members.HEOD residues between 1970 and 1975–76 significantly declined in five species, showed no change in two, whereas in two species the Larger members of one had Lower residues and the smaller members of the other showed no change.PCB residues declined.in all species except the larger Perca flavescens. Chlordane and heptachlor-epoxide were identified in S. namaycush for the first time in 1975–76. Mercury residues showed no change between 1970 and 1975–76 in five species, it declined in two species and increased in small S. v. vitreum.Correlations existed between Levels of organic contaminant and Lipid content of fish especially in the immediate post period of their use. Where the increasing Lipid content was associated with an increasing trophic level a preypredator relationship existed for contaminant accumulations. However, where Lipid contents were Low, no correlation appeared to exist in the prey-predator.     

Cave lithology determining the structure of the invertebrate communities in the Brazilian Atlantic Rain Forest

In Brazil, only limestone caves and a few caves in sandstone, iron ore and granite rocks had their invertebrate communities evaluated. Being such, the present study aimed to promote a comparative analysis of the structure of the invertebrate communities in caves associated to carbonatic, magmatic, siliciclastic and ferruginous rocks of the Brazilian Atlantic forest. Significant differences in the relative richness, abundance and diversity were observed between lithologies. The average relative richness was higher in the ferruginous caves (0.53 spp). The total number of troglomorphic species was significantly different among caves and the highest average richness occurred at ferruginous caves (5.79 spp/cave). Siliciclastic, carbonatic and magmatic caves presented a higher quantitative similarity of the fauna. Ferruginous caves revealed communities with a fauna composition different from the other lithologies. The total richness of invertebrates correlated significantly and positively with the linear development in the siliciclastic caves (R_s = 0.67, P < 0.05), carbonatic (R_s = 0.71, P < 0.05) and ferruginous (R_s = 0.74, P < 0.05). The rock type in which the cave is inserted can determine differences in the richness of invertebrate troglophyles and troglobites. Therefore, on creating value attributes, the size of the caves should always come related to their lithology by the fact that same sized caves associated to different lithologies, possess communities with quite diverse structures.     

Troglomorphic Sculpins of the Cottus Carolinae Species Group in Perry County, Missouri: Distribution, External Morphology, and Conservation Status

The existence of cavernicolous sculpin (here allocated to Cottus carolinae, banded sculpin, and referred to as grotto sculpin), in the karst regions of Perry County, Missouri, first came to our attention in 1991. Examination of 35 caves in Missouri, 96 in Illinois, 17 in Tennessee, two in Indiana, and 11 in Arkansas revealed that banded sculpin are common in cave habitats; however, grotto sculpin are limited to two karst areas of Perry County, Missouri, where they are known from only six cave systems. These caves and their streams are extensive and apparently provide a unique habitat compared to other karst systems; this may be a critical factor in the present restricted distribution of the grotto sculpin. Grotto sculpin occupy pools and riffles of cave streams, and occur over a variety of substrates, from sediment to breakdown. Density estimates in Mystery and Running Bull caves were 0.29 and 0.63 individuals m^-2, respectively. Grotto sculpin have small eyes (1–6% SL vs. 6–10% SL in epigean samples), significantly reduced pigmentation (including nearly complete loss of dorsal saddles), a reduction in pelvic fin ray number (from 4+4 elements to often 4+3 , or 3+3), and enlarged cephalic lateralis pores (e.g., mandibular pores of cavernicolous samples are 2–3 times those of epigean stream samples). Multivariate analyses of body shape revealed statistically significant separation of epigean and hypogean samples, with eye size highly variable, but smallest in the Running Bull Cave population. We interpret these results as representative of losses associated with long-term cave habitation. Caves of Perry County provide ample habitat for grotto sculpin, but because the caves are located downgradient of the city of Perryville and an intensively farmed landscape, point and non-point source pollution threaten their continued existence. Escape of farm-pond fishes through the extensive sinkhole network in Perry County has increased potential predation pressure on grotto sculpin by channel catfish, Ictalurus punctatus, and other species normally excluded from cave environments.