Fluctuating asymmetry as a bio-marker to account for in conservation and management of cave-dwelling species

The applicability of fluctuating asymmetry (FA) in conservation biology as a bio-marker and an early warning system have been examined in various groups of animals. However, cave-dwelling invertebrates have gotten little attention and yet caves have no biological management. Thus, developing a bio-marker to identify early responses of cave-dwelling species to stress provides a valuable tool to account for in future conservation and management programs. We examined whether FA can be used as a bio-marker of relaxed selection for cave-dwelling invertebrates. Specifically, we compared FA levels of pedipalps and two segments of chelicerae (chelicel1 and chelicel2) between cave and surface habitats and among populations in a troglophilic harvestman specie, Paranemastoma sillii sillii (Herman, 1871). Under the assumption that cave environment exerts relaxed selection we hypothesised that cave-dwelling harvestmen express higher degree of FA than surface-dwelling harvestmen. Because female and male harvestmen use the pediplaps differently, we assumed sex-specific selective pressures and further examined the effect of sex and habitat (cave vs surface) and sex interaction on FA levels. We hypothesised no differences in the levels of FA among harvestman cave populations, because of the idea that relaxed selection is responsible for higher levels of FA in cave-dwelling harvestmen rather than environmental stress. We found significant habitat sex interactions in the FA of the pedipalp. Interactions of population and sex had a significant effect on pedipalp and chelicel2 FA. These results partially support the idea that FA responds to differences in the strength of selection. Although we cannot fully disentangle the mechanisms of natural selection affecting FA and the study of trait asymmetry should be combined with studies of other sources of stress (i.e. genetic stress, predation, prey availability) we conclude that FA could be a bioindicator to be used as a tool in conservation and management of cave.     

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.     

Anophthalmia and elongation of body appendages in cave scale worms (Annelida: Aphroditiformia)

This study addresses whether cave dwelling annelids exhibited similar reductive and constructive traits equally as strong as those of arthropods and vertebrates inhabiting caves. Known as troglomorphism, these adaptations bring about striking morphologies across invertebrates and vertebrates from both aquatic and terrestrial cave habitats, and include varying degrees of eye and pigmentation loss, as well as hypertrophy of body appendages and sensorial structures. Employing phylogenetic comparative methods and ancestral character reconstructions on a worldwide data set of a group of annelids, the scale worms (Aphroditiformia), we investigate the behavioural and morphological traits of species living in marine caves in comparison with those species living outside caves. Our work demonstrated that cave scale worms respond similar to arthropods in cave environments, showing a significant elongation of sensory parapodial cirri, while lacking eyes and pigmentation. However, whereas elongation of sensory appendages likely occurred in correlation to cave colonization, eyes were plausibly lost in correlation with specialization and colonization of deep‐sea habitats.     

Diet and body condition of cave‐dwelling dwarf crocodiles (Osteolaemus tetraspis,Cope 1861) in Gabon

We present the first ever observations of dwarf crocodiles (Osteolaemus tetraspis) selectively utilizing a cave ecosystem. We analysed crocodile diet to preliminarily assess the degree of ecological isolation of cave‐dwelling crocodiles from their forest‐dwelling conspecifics despite their physical proximity. We additionally conducted the first study of body condition of dwarf crocodiles and compared cave‐dwelling individuals to surface‐dwelling individuals from a variety of alternative habitats and sites as a means to better understand the implications of a semihypogean life on this species. Crocodiles captured in the caves appeared to forage exclusively in the caves and ate mostly cave crickets and bats, whereas crocodiles captured in the surrounding forest habitat consumed primarily freshwater crustaceans and insects and were not found to consume cave‐dwelling prey. Juvenile cave crocodiles had significantly higher body condition compared to juvenile forest crocodiles, which did not vary amongst forest locations. The difference in body condition between adult cave and forest crocodiles was not statistically significant despite also being higher; we suspect this is an artefact of the low sample size rather than a real nondifference. Forest adult crocodiles generally had significantly higher body condition than juveniles, but did not vary by site or habitat. This lack of variation suggests that habitat type is not the most important factor influencing dwarf crocodile body condition. Our results provide a unique insight into facultative cave use by a principally surface‐dwelling species and reinforce the necessity for further research into this unique system to better understand the evolutionary‐scale implications of cave habitat use by dwarf crocodiles.     

Ecological characteristics of a cave‐dwelling moth species,Triphosa dubitata (Lepidoptera: Geometridae), in Baram and Ssang caves in Gangwon Province,Korea

This study was performed to clarify the ecological characteristics of a cave‐dwelling moth species, Triphosa dubitata Linnaeus (Lepidoptera: Geometridae), at Baram cave and at Ssang cave within Pyeongchang‐gun of Gangwon province in south Korea. We investigated T. dubitata population for 3 days from March 2013 to October 2013 (except September) and in January 2014. We used a section investigation method in the caves every month to determine their ecological characteristic. A nocturnal investigation using a high intensity discharge lamp adjacent to the entrance of the cave was conducted in parallel with a diurnal investigation using butterfly traps to investigate the movement of T. dubitata. In order to investigate the range of habitat temperature of moths, we used a dual laser targeting infrared thermometer to measure the cave temperatures. We caught individuals of T. dubitata L.: 8,574 individuals in Baram cave and 828 individuals in Ssang cave. As 9,095 individuals (97 %) appeared at a temperature of ?3°C ~ 8°C, it was verified that the adults were living at specific temperatures. In addition, T. dubitata adults were not active outside the caves; they entered the cave as soon as they developed from pupa into adults. These results showed that T. dubitata depended on food plants outside of the cave during the egg–larva–pupa stages, and they used the cave as a habitat for long‐term survival when they develop into adults.     

Tracking the ice: Subterranean harvestmen distribution matches ancient glacier margins

Biogeographic studies often underline the role of glacial dynamism during Pleistocene (1.806–0.011 Mya) in shaping the distribution of subterranean species. Accordingly, it is presumed that present‐day distribution of most specialized cold‐adapted (cryophilic) cave‐dwelling species should bear the signatures of past climatic events. To test this idea, we modelled the distribution of specialized cold‐adapted subterranean alpine harvestmen (Arachnida: Opiliones: Ischyropsalididae: Ischyropsalis). We found that the distance from the glacier margins during Last Glacial Maximum (LGM; about 22,000 years ago) was the most important predictor of their present‐day distribution. In particular, the peak in the probability of occurrence of alpine subterranean Ischyropsalis was found to be in close proximity to the LGM glacier, with a sharp drop at a distance of 30 km from the ice margin. In light of the role played by past climatic events in determining the species current range, we briefly discuss their biogeographic history and the role played by glacial refugia dynamics in determining the current distribution of these species. We argue that low dispersal harvestmen such as our model species can be used as biological indicators for tracking past glaciations and other similar biogeographic events.     

Population ecology ofGoniosoma spelaeum, a cavernicolous harvestman from south-eastern Brazil (Arachnida: Opiliones: Gonyleptidae)

Goniosoma spelaeum (Mello-Leitão) is a widespread trogloxene harvestman in caves of the Ribeira Valley in São Paulo State. It inhabits walls and ceilings near cave entrances. Populations inhabiting six selected caves of the region were analysed during this study. Mark-recapture techniques were used to estimate population sizes. Populations vary from tens to hundreds of individuals in each cave, and vary throughout the year. Barra Bonita cave had the largest population and was used to identify other ecological features of the species. These harvestmen show a high degree of philopartry, and recapture rate was high. They remain motionless inside the caves during the day, leaving them after dark to forage, and return just after dawn. They always feed outside the caves and do not carry food into the caves. Soft-bodied insects were the main food observed in the field. In the laboratory, they accepted plant and animal items and industrial foods. Their main predators are the spider Ctenus fasciatus , the heteropteran Zelurus travassosi , and the marsupial Philander opossum , and their main parasites are dipteran larvae (probably Phoridae).     

Ecological preferences of neotropical cave bats in roost site selection and their implications for conservation

Bats frequently use caves as roosts due to higher environmental stability and protection. However, species-specific ecological and physiological requirements and conditions of roosts and their surroundings can influence species presence. Little is known on cave choice by bats in the Neotropics, a species- and cave-rich region. Understanding how bats, cave characteristics and the surrounding landscape are related with each other helps the management and conservation of bats and caves. Based on sampling 19 caves using both diurnal observations and captures, we tested (1) whether bat richness was positively related to cave temperature, humidity, size, stability, and heterogeneity of microhabitats, and the preservation and heterogeneity of the surrounding landscape in central Brazil; (2) whether cave and landscape characteristics influenced on species composition; (3) how species responded to cave and landscape variables; and (4) whether these relationships changed between seasons. Temperature was a limiting factor, whereas environmental stability, humidity, and structural attributes of caves favored the occurrence of more species. Larger caves, rich in microhabitats – but more stable than the external environment – supported more species, especially in the dry season. Landscape context did not influence species richness and composition in the caves, but the percentage of vegetation around caves was important for certain species. Our results highlight the influence of environmental variables in the process of cave selection by Neotropical bat species. Moreover, we emphasize the importance of cave protection for bats and provide useful information for decision-making in processes of environmental licensing.     

Phylogenetic evidence from freshwater crayfishes that cave adaptation is not an evolutionary dead‐end

Caves are perceived as isolated, extreme habitats with a uniquely specialized biota, which long ago led to the idea that caves are “evolutionary dead‐ends.” This implies that cave‐adapted taxa may be doomed for extinction before they can diversify or transition to a more stable state. However, this hypothesis has not been explicitly tested in a phylogenetic framework with multiple independently evolved cave‐dwelling groups. Here, we use the freshwater crayfish, a group with dozens of cave‐dwelling species in multiple lineages, as a system to test this hypothesis. We consider historical patterns of lineage diversification and habitat transition as well as current patterns of geographic range size. We find that while cave‐dwelling lineages have small relative range sizes and rarely transition back to the surface, they exhibit remarkably similar diversification patterns to those of other habitat types and appear to be able to maintain a diversity of lineages through time. This suggests that cave adaptation is not a “dead‐end” for freshwater crayfish, which has positive implications for our understanding of biodiversity and conservation in cave habitats.     

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.

     

Leveraging multidimensional heterogeneity in resource selection to define movement tactics of animals

Increasing interest in the complexity, variation and drivers of movement‐related behaviours promise new insight into fundamental components of ecology. Resolving the multidimensionality of spatially explicit behaviour remains a challenge for investigating tactics and their relation to niche construction, but high‐resolution movement data are providing unprecedented understanding of the diversity of spatially explicit behaviours. We introduce a framework for investigating individual variation in movement‐defined resource selection that integrates the behavioural and ecological niche concepts. We apply it to long‐term tracking data of 115 African elephants (Loxodonta africana), illustrating how a behavioural hypervolume can be defined based on differences between individuals and their ecological settings, and applied to explore population heterogeneity. While normative movement behaviour is frequently used to characterise population behaviour, we demonstrate the value of leveraging heterogeneity in the behaviour to gain greater insight into population structure and the mechanisms driving space‐use tactics.     

Cave invertebrate assemblages differ between native and exotic leaf litter

Abstract Allochtonous leaf litter is an important source of energy and nutrients for invertebrates in cave ecosystems. A change to the quality or quantity of litter entering caves has the potential to disrupt the structure and function of cave communities. In this study, we adopted an experimental approach to examine rates of leaf litter decomposition and the invertebrate assemblages colonizing native and exotic leaf litter in limestone caves in the Jenolan Caves Karst Conservation Reserve, New South Wales, Australia. We deployed traps containing leaf litter from exotic sycamore (Acer pseudoplatanus) and radiata pine (Pinus radiata) trees and native eucalypts (Eucalyptus spp.) in twilight zones (near the cave entrance) and areas deep within the caves for 3 months. Thirty‐two invertebrate morphospecies were recorded from the litter traps, with greater richness and abundance evident in the samples from the twilight zone compared with areas deep within the cave. Sycamore litter had significantly greater richness and abundance of invertebrates compared with eucalypt and pine litter in samples from the twilight zone, but there was no difference in richness or abundance among litter samples placed deep within the cave. Relative rates of decay of the three litters were sycamore > eucalypt > pine. We discuss the potential for the higher decomposition rates and specific leaf area in sycamores to explain their higher invertebrate diversity and abundance. Our findings have important implications for the management of exotic plants and the contribution of their leaf litter to subterranean ecosystems.     

Effects of an aerial 1080 possum poison operation using carrot baits on invertebrates in artificial refuges at Whirinaki Forest Park, 1999– 2002

The effects of an aerial 1080 possum poison operation using carrot baits on invertebrates in Whirinaki Forest Park are described from an un-replicated study of artificial refuges attached to tree trunks. Auckland tree weta (Hemideina thoracica), cave weta (Pharmacus sp. and Isoplectron sp.), cockroaches, spiders and harvestmen, and leaf-veined slugs (Athoracophorus bitentaculatus) were the most frequent occupants, but snails, millipedes, centipedes, flatworms, lepidopteran larvae, glowworm larvae (Arachnocampa luminosa), peripatus, slaters and beetles were also present occasionally. Invertebrate numbers were monitored every second or third month for a year before the poison operation, and for two years afterwards. Numbers of tree weta, cave weta, cockroaches, spiders and harvestmen, and leaf-veined slugs did not decline substantially in refuges in the treatment area relative to those in the non-treatment area immediately after the poison operation. Our results, and those from two other similar studies, suggest that aerial 1080 poison operations are unlikely to have a detrimental effect on invertebrates that occupy cavities above ground.     

Energy and speleogenesis: Key determinants of terrestrial species richness in caves

The aim of this study was to unravel the relative role played by speleogenesis (i.e., the process in which a cave is formed), landscape‐scale variables, and geophysical factors in the determination of species richness in caves. Biological inventories from 21 caves located in the southeastern Iberian Peninsula along with partial least square (PLS) regression analysis were used to assess the relative importance of the different explanatory variables. The caves were grouped according to the similarity in their species composition; the effect that spatial distance could have on similarity was also studied using correlation between matrices. The energy and speleogenesis of caves accounted for 44.3% of the variation in species richness. The trophic level of each cave was the most significant factor in PLS regression analysis, and epigenic caves (i.e., those formed by the action of percolating water) had significantly more species than hypogenic ones (i.e., those formed by the action of upward flows in confined aquifers). Dissimilarity among the caves was very high (multiple‐site β_sim = 0.92). Two main groups of caves were revealed through the cluster analysis, one formed by the western caves and the other by the eastern ones. The significant—but low—correlation found between faunistic dissimilarity and geographical distance (r = .16) disappeared once the caves were split into the two groups. The extreme beta‐diversity suggests a very low connection among the caves and/or a very low dispersal capacity of the species. In the region under study, two main factors are intimately related to the richness of terrestrial subterranean species in caves: the amount of organic material (trophic level) and the formation process (genesis). This is the first time that the history of a cave genesis has been quantitatively considered to assess its importance in explaining richness patterns in comparison with other factors more widely recognized.     

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.     

Trophic niche, age structure and seasonality in Dolichopoda cave crickets

Shifts in feeding habits are expected to occur during adaptation to cave life Doltchopoda cave crickets inhabit both natural and artificial caves showing differences in population size, fecundity, phenology and age structure Compared to artificial caves, typically holding a seasonal age structure, populations from natural caves maintain a constantly heterogeneous age structure Faecal content analysis of 605 individuals from 24 natural and artificial cave populations, enabled us to characterize their trophic niche and to investigate its variation The results of multivariate analyses and measures of niche breadth and niche overlap outlined differences in trophic resource exploitation between natural and artificial cave populations Seasonal variation in diet occurred in both types of caves, and it was greater in artificial cave populations However, within any season, differences in feeding habits between individuals were much greater in natural caves resulting in a wider heterogeneity in trophic resources exploitation. Such heterogeneity appears to be mainly due to differences in diet between individuals of different developmental stages In fact, in a sample of 15 populations we found a positive, statistical significant correlation between niche breadth and heterogeneity in age structure These data are discussed in a broader evolutionary context in order to understand the role of limited resources availability in shaping and maintaining heterogeneity in age structure of Dolichopoda populations     

The effects of overwintering and habitat type on body condition and locomotion of the wolf spider Pardosa alacris

Overwintering in temperate regions is a prominent mortality risk for invertebrates and may affect their behaviour and body condition. Pardosa alacris is a common ground dwelling spider in central European native and plantation forests, and habitat type and prey availability may play important roles in their overwintering. The effect of overwintering on body condition and behaviour of spiders in semi natural and exotic habitats is relatively unknown. Here we assess the effects of winter on spiders from native poplar and exotic pine plantations. The locomotory behaviour of P. alacris (distance covered and speed) was assessed by tracking their movement in a white circular plastic arena. We assessed body condition, body size, and total fat content. Forest type and sex had significant effects on body length. Fat content was significantly higher in the spring than in autumn, and spiders covered larger distances and were faster in autumn than in spring. Fat content had a significant negative effect on average speed. Spiders in native forests were smaller but grew more during the winter than in exotic plantations, possibly due to higher prey availability in native forests. Visually-hunting predators may significantly affect spiders. Fat spiders with better body condition moved less, and were thus less detectable by predators. However the low movement rate may result in a low rate of encountering prey items, thus lowering feeding efficiency.     

Buthid scorpions found in caves; a new species of Isometrus Ehrenberg, 1828 (Scorpiones,Buthidae) from southern Vietnam

A new species, Isometrus (Reddyanus) deharvengi sp. n., is described from caves of the region of Hon Chong, Kien Giang in southern Vietnam. Comments are also added about the scorpion fauna of Southeast Asia and cave dwelling buthid scorpions.     

Ancient DNA reveals differences in behaviour and sociality between brown bears and extinct cave bears

Ancient DNA studies have revolutionized the study of extinct species and populations, providing insights on phylogeny, phylogeography, admixture and demographic history. However, inferences on behaviour and sociality have been far less frequent. Here, we investigate the complete mitochondrial genomes of extinct Late Pleistocene cave bears and middle Holocene brown bears that each inhabited multiple geographically proximate caves in northern Spain. In cave bears, we find that, although most caves were occupied simultaneously, each cave almost exclusively contains a unique lineage of closely related haplotypes. This remarkable pattern suggests extreme fidelity to their birth site in cave bears, best described as homing behaviour, and that cave bears formed stable maternal social groups at least for hibernation. In contrast, brown bears do not show any strong association of mitochondrial lineage and cave, suggesting that these two closely related species differed in aspects of their behaviour and sociality. This difference is likely to have contributed to cave bear extinction, which occurred at a time in which competition for caves between bears and humans was likely intense and the ability to rapidly colonize new hibernation sites would have been crucial for the survival of a species so dependent on caves for hibernation as cave bears. Our study demonstrates the potential of ancient DNA to uncover patterns of behaviour and sociality in ancient species and populations, even those that went extinct many tens of thousands of years ago.