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 mid-latitude biodiversity ridge in terrestrial cave fauna

The world's obligate cave-dwelling fauna holds considerable promise for biogeographic analysis because it represents a large number of independent evolutionary experiments in isolation in caves and adaptation to subterranean life. We focus on seven north temperate regions of at least 2000 km², utilizing more than 4300 records of obligate cave-dwelling terrestrial invertebrates. In North America, highest diversity was found in northeast Alabama while in Europe highest diversity was found in Ariège, France, and in southeast Slovenia. Based on these regions as well as more qualitative data from 16 other regions, we hypothesize that a ridge (ca 42°–46° in Europe and 34° in North America) of high biodiversity occurs in temperate areas of high productivity and cave density. This may reflect a strong dependence of cave communities on long term surface productivity (as reflected in actual evapotranspiration), because the subterranean fauna relies almost entirely on resources produced outside caves. This dependence may explain the unique biodiversity pattern of terrestrial cave invertebrates.     

Multivariate Analysis of Copepod Assemblages in Epikarstic Waters of Some Slovenian Caves

A series of sampling sites in 6 caves was established in order to assess the importance of the epikarst as a habitat of high diversity of meiofauna. Special attention was given to the stygobiotic species of copepods (Crustacea), which was the most abundant group of animals in water percolating from the epikarst. In total, 37 species of Copepoda were identified from nearly 4000 individuals. To understand epikarst as a habitat, 14 structural and physico-chemical factors were analysed and compared for two types of habitats, i.e., trickles and pools filled with percolation water. Results of canonical correspondence analysis indicated that the significant factors influencing faunal composition in trickles were the thickness of the cave ceiling and the concentrations of sodium, nitrate, and potassium ions, while in pools correlations between individual species and pH, temperature, volume, conductivity and thickness of the cave ceiling were statistically significant. Aquatic copepod assemblages in epikarst encompass species of different taxonomic affinities, living in severe environmental conditions. The pattern of the system reflects both high taxonomic diversity and environmental severity.     

Do cave features affect underground habitat exploitation by non-troglobite species?

Many biospeleological studies focus on organisms that are exclusive inhabitants of the subterranean realm, but organisms that are not obligate cave-dwellers are frequent in caves, and may account for a substantial portion of biomass. Moreover, several taxa that are usually epigeous are regularly found inside caves, but for most of them it is unknown whether they accidentally enter them, or whether they actively select caves for specific environmental features. In this study we analysed the community of non-strict cave-dwelling organisms (amphibians, gastropods, spiders and orthopterans) in 33 caves from Central Italy, to assess how environmental factors determine community structure. Cave features strongly affected the distribution of the taxa considered. The combined effect of cave morphology and microclimate explained nearly 50% of the variation of community structure. Most of community variation occurred along a gradient from deep, dark and humid caves, to dry caves with wider entrances and extended photic areas. Most of species were associated with humid, deep and dark caves. Most of the non-troglobiont amphibians and invertebrates did not occur randomly in caves, but were associated to caves with specific environmental features. Analysing relationships between cave-dwelling species and environmental variables can allow a more ecological and objective classification of cave-dwelling organisms.     

Phylogeography of cave pseudoscorpions in southern Australia

Aim  To investigate molecular phylogenetic divergence and historical biogeography of the cave-dwelling pseudoscorpion genus Protochelifer.
Location  Caves and nearby epigean habitats in southern Australia were sampled from western Victoria, Naracoorte Caves, Flinders Ranges, Kangaroo Island, Nullarbor Plain and south-west Western Australia.
Methods  Allozyme electrophoresis (57 individuals) and a 569-base-pair section of the mtDNA COI gene (22 individuals) were used to reconstruct phylogenetic relationships among four cave species and three epigean species from 13 locations.
Results  Phylogenetic reconstruction using the allozyme and mtDNA sequence data revealed a similar topology, showing recent speciation of several Protochelifer populations in caves from Naracoorte to the Nullarbor Plain. Naracoorte Caves contained a single species, Protochelifer naracoortensis , found in four separate caves, while all other cave species appear to be restricted to single caves.
Main conclusions  At a local scale, as indicated by the four Naracoorte caves, dispersal is thought to occur via micro- and mesocaverns, and possibly by phoresy using insect or bat vectors. With current data we are unable to determine if cavernicolous species of Protochelifer have arisen from a single cave colonization event followed by phoretic dispersal on bats to other caves, or multiple cave-invasion events from independent epigean ancestors. Genetic heterogeneity among Protochelifer populations from Nullarbor caves suggest that P. cavernarum , the only species presently recorded from this region, is likely to constitute a species complex requiring further study to fully resolve its relationships.     

The first troglobitic species of freshwater flatworm of the suborder Continenticola (Platyhelminthes) from South America

Brazilian cave diversity, especially of invertebrates, is poorly known. The Bodoquena Plateau, which is located in the Cerrado Biome in central Brazil, has approximately 200 recorded caves with a rich system of subterranean water resources and high troglobitic diversity. Herein we describe a new troglobitic species of Girardia that represents the first obligate cave-dwelling species of the suborder Continenticola in South America. Specimens of the new species, which occur in a limestone cave in the Bodoquena Plateau, in the Cerrado biome, are unpigmented and eyeless. Species recognition in the genus Girardia is difficult, due to their great morphological resemblance. However, the new species can be easily recognized by a unique feature in its copulatory apparatus, namely a large, branched bulbar cavity with multiple diverticula.     

Six new cavernicolous cixiid planthoppers in the genus Solonaima from Australia (Homoptera: Fulgoroidea)

Abstract The monophyletic genus Solonaima , endemic to northern Queensland, is reviewed and six new species are described: S.sullivani sp.n., S.pholetor sp.n., S.stonei sp.n., S.halos sp.n., S.irvini sp.n. and S. baylissa sp.n. The previously known epigean species, S.solonaima Kirkaldy and S.pallesens (Distant) are illustrated and redescribed. The six new species represent four separate independent cave invasions and nearly double the number of known cavernicolous cixiids in the world. This is the first report of a closely related group of cave-dwelling Homoptera showing varying degrees of cave adaptation. One facultative cave species, S.sullivani , shows virtually no modification from surface relatives. Two species, S.pholetor and S.stonei , show some eye, colour, and wing-reduction, but they are still flighted and are considered facultative cave species. S.halos and S. irvini are nearly blind and have reduced, non-functional wings and are considered obligate cave species. S. baylissa , the most remarkable obligate cave species, is highly modified: eyeless, nearly wingless and colourless. The evolutionary trends displayed in cave adaptation are illustrated and discussed. These include reduction in body colour, eyes and wings, alteration of head and thorax shape, and possibly simplification of the male genitalia. The geology of the caves is complex and ranges from greater than 5-million-year-old caves in Silurian-aged metamorphosed limestone to 190,000-year-old lava tubes. The facultative species are generally found in the most open caves, the two intermediate obligate species are found in deeper caves, and the most highly modified species is restricted to damp cave passages with high CO₂ levels. There is no correlation between the ages of the caves and the degree of cave adaptation.     

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.     

Sampling adequacy in an extreme environment: species richness patterns in Slovenian caves

Caves harbor a rich fauna unique to subterranean environments. Although extensive records of cave animals are available, only a small fraction of known caves in any region have been biologically assessed. We investigated the impact of incomplete sampling using one of the richest, best documented cave faunas in the world – that of the Dinaric karst of Slovenia. We utilized time snapshots (1940, 1970, and 2000) of the caves and cave fauna to analyze stability of hotspots, spatial pattern, and relationship between number of species and number of caves. Using data aggregated into 100km² hexagons, the location of hotspots, black–white joins, Moran's I, and spatial autocorrelation all remained constant, at least from 1970 on. The linear regression coefficient of the relationship between number of caves and number of species declined with time. Most hexagons had been sampled, but there was no indication that any hexagon had been sampled intensively enough for the accumulation curve of number of caves versus number of species within a hexagon to reach an asymptote. This appeared to be the result of a highly skewed distribution of species richness among caves. Number and position of hotspots can be predicted from information on these few high diversity caves.     

中华菊头蝠的栖息生态特征及种群保护

中华菊头蝠(Rhinolophus sinicus)主要分布于我国境内,属于典型的洞栖食虫性蝙蝠,具有重要的研究意义与保护价值。近年,在湘西州境内的16个溶洞中对其栖息生态特征进行了观察,共记录到其个体12942只次,数据分析结果显示：该蝠是该区域溶洞中的居留型优势蝠种,具有集群冬眠的习性。每年的9月中下旬开始逐步聚群冬眠,翌年的3月底开始苏醒,其夏季的繁育场所非常隐蔽,通常位于人无法进入的洞段或人迹罕至的洞穴。总体上,其栖点主要集中于距洞口150—200 m(91.60%)的洞段,离地高度6—10 m(91.75%),多以“双足悬挂”的栖姿将身体悬空倒挂于洞道的顶壁。其体温与栖点温度之间不存在显著性差异(P>0.05),但具有明显的线性正相关关系(R~2=0.8886)。其栖点安全性春夏季高,秋冬季中等偏低。中华菊头蝠作为该区域洞栖性蝙蝠的优势种,在维持洞穴生态系统的稳定中发挥着至关重要的作用,加强对洞穴生态系统中蝙蝠伞护性的研究有助于洞穴生态保护教育及对蝙蝠种群的保护实践。     

The dispersal and colonisation behaviour of the marine polychaete <Emphasis Type="Italic">Nereis diversicolor</Emphasis> (O. F. Müller) in south-east England

Recent submarine caves are inhabited by endemic faunas adapted to oligotrophism, darkness and a tranquil environment. Many of their representatives are archaic types of animals resembling fossils from very early times in evolution. This article compares fossil fauna from Jurassic neptunian dykes (originally sea bed clefts) from the Western Carpathians with the Recent cave-dwelling fauna. The ostracods Pokornyopsis feifeli are particularly important. In the Western Carpathians, these were exclusively found in the Middle/Late Jurassic fissure fillings, but in the non-Tethyan Germanic Jurassic this species was found in deep-marine claystones. They are phylogenetic forerunners of the recent genus Danielopolina inhabiting both anchialine caves and deep seas. This indicates a Jurassic migration of deep-marine fauna to cryptic habitats. Other examples of cryptic communities include the Upper Jurassic cavity-dwelling fauna dominated by serpulids and scleractinian corals. Associated suspension feeders include thecideidine brachiopods, oysters, bryozoans, sponges, crinoids and sessile foraminifers. Serpulid-dominated bioconstructions have recent analogies in the Mediterranean and Carribean seas. Different type of dyke communities represent the Late Jurassic fauna of small sized ammonites which originated from both Tethyan and Boreal paleobioprovinces. It has not been established whether these amonites were juvenile, dwarfed specimens adapted to limited cave space or size-sorted adult specimens.     

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.

     

Climatic conditions, diapause and migration in a troglophile caddisfly

1. Factors explaining the end of diapause include environmental conditions such as daily photoperiod, temperature and humidity. However, because all these factors are almost constant inside deep caves, they would hardly affect diapause termination in many animal taxa that use such habitats in which to aestivate or hibernate (such as bats and some insects, snakes or frogs).
2. An innate biological signal, based on body reserves (mass), could determine the end of diapause in cave-dwelling animals. Another possibility is that the diapausing animals may use as a stimulus convective air circulation, produced by a fall in temperature outside the cave to a value below that inside (i.e. temperature inversions). Here, we explored these two non-exclusive hypotheses explaining the end of diapause and the start of migration in the caddis Mesophylax aspersus . This species aestivates as an adult in caves, as a physiological adaptation to seasonal drought and stream drying.
3. The variation in body mass of individuals entering and leaving the cave was similar, suggesting no role for the 'reserve level' hypothesis in breaking diapause. However, the onset of a temperature inversion in autumn coincided with the breaking of diapause followed after a few days by the migration of the caddisflies.
4. We conclude that the seasonal air currents, produced by thermal inversions, could be the migration stimulus for caddisflies and many other animals that spend a period of diapause in caves.     

中国喀斯特洞穴维管植物多样性

洞穴是喀斯特景观中普遍存在的地质地貌结构, 拥有丰富的植物资源。仅2001-2020年间, 就发表了中国喀斯特洞穴维管植物新属1个; 新种(含种下等级) 170个, 隶属于16科31属, 占近20年发表的中国维管植物新种的3.9%, 说明洞穴植物具有较高的物种多样性潜力。据统计, 中国喀斯特洞穴维管植物有110科339属871种, 主要分布于广西、广东、贵州、云南、重庆等地。物种数排名前5的科包括苦苣苔科、荨麻科、鳞毛蕨科、秋海棠科和茜草科, 其所含物种数共占整个洞穴植物种类的39.4%; 排名前5的属包括报春苣苔属(Primulina)、楼梯草属(Elatostema)、耳蕨属(Polystichum)、秋海棠属(Begonia)和凤尾蕨属(Pteris), 其所含物种数共占整个洞穴植物种类的25.1%。本名录的所有洞穴植物中, 草本习性的种类占一半以上。从洞内分布来看, 仅有10.7%的种类分布于弱光带, 其中石松类和蕨类植物占比远高于被子植物, 说明前者更能适应弱光带的极端环境。不仅如此, 洞穴维管植物也具有较高的特有性成分, 其中省级特有种占比25.8%, 分别包括非洞穴特有种(11.0%)、多洞穴特有种(3.3%)和单洞穴特有种(11.5%)。依据文献显示受威胁种类有115种(占13.0%)。受威胁种类占比较高的类群均是近年来发表新种较多的科, 包括鳞毛蕨科、苦苣苔科、荨麻科、秋海棠科、茜草科等。针对这些类群, 有待更详细地调查来完善对它们的评估。此外, 本名录中至少有36%的种类没有任何分子数据, 亟待补充。     

Predation of a cave fish (Poecilia mexicana, Poeciliidae) by a giant water-bug (Belostoma, Belostomatidae) in a Mexican sulphur cave

Abstract.  1. Caves are often assumed to be predator-free environments for cave fishes. This has been proposed to be a potential benefit of colonising these otherwise harsh environments. In order to test this hypothesis, the predator–prey interaction of a belostomatid (predator) and a cave fish (prey) occurring in the Cueva del Azufre (Tabasco, Mexico) was investigated with two separate experiments.
2. In one experiment, individual Belostoma were given a chance to prey on a cave fish, the cave form of the Atlantic molly ( Poecilia mexicana ), to estimate feeding rates and size-specific prey preferences of the predator. In the other experiment, population density of Belostoma was estimated using a mark–recapture analysis in one of the cave chambers.
3. Belostomatids were found to heavily prey on cave mollies and to exhibit a prey preference for large fish. The mark–recapture analysis revealed a high population density of the heteropterans in the cave.
4. The absence of predators in caves is not a general habitat feature for cave fishes. None the less predation regimes differ strikingly between epigean and hypogean habitats. The prey preference of Belostoma indicates that cave-dwelling P. mexicana experience size-specific predation pressure comparable with surface populations, which may have implications for life-history evolution in this cave fish.     

Assessing and conserving groundwater biodiversity: synthesis and perspectives

1. This paper is a synthesis of a special issue on groundwater biodiversity with a focus on obligate subterranean species, the stygobionts. The series of papers constitutes a great leap forward in assessing and understanding biodiversity patterns because of the use of large quantitative data sets obtained over a broad geographic scale. They also represent a conceptual shift, away from a purely taxonomic and phylogenetic focus to the analysis of whole groundwater assemblages.
2. The general patterns emerging for groundwater fauna are: very high levels of endemism, low local diversity relative to regional diversity, a limited number of lineages, occurrence of many relicts, and truncated food webs with very few predators.
3. β-Diversity is at least as important as α-diversity in determining total richness at different scales (aquifer, basin and region) and overall taxa richness increases across spatial scales.
4. Advances in understanding groundwater biodiversity patterns further include identification of several important factors related to geology and hydrology that determine the composition of European stygobiotic assemblages.
5. Important challenges for future research include improving sampling strategies, filling gaps in sampling coverage, intensifying research on theoretical and statistical models, and including functional and genetic diversity components in biodiversity assessments.
6. Strategies are proposed for protecting groundwater biodiversity and an argument is made to integrate biodiversity in groundwater management. Applying principles such as complementarity and flexibility for groundwater biodiversity conservation is a major step toward delineating a reserve network that maximise species representation at the European scale.     

Evaluating the sampling bias in pattern of subterranean species richness: combining approaches

We investigated the pattern of species richness of obligate subterranean (troglobiotic) beetles in caves in the northwestern Balkans, given unequal and biased sampling. On the regional scale, we modeled the relationship between species numbers and sampling intensity using an asymptotic Clench (Michaelis–Menten) function. On the local scale, we calculated Chao 2 species richness estimates for 20 × 20 km grid cells, and investigated the distribution of uniques, species found in only one cave within the grid cell. Cells having high positive residuals, those with above average species richness than expected according to the Clench function, can be considered true hotspots. They were nearly identical to the observed areas of highest species richness. As sampling intensity in a grid cell increases the expected number of uniques decreases for any fixed number of species in the grid cell. High positive residuals show above average species richness for a certain level of sampling intensity within a cell, so further sampling has the most potential for additional species. In some cells this was supported by high numbers of uniques, also indicating insufficient sampling. Cells with low negative residuals have fewer species than would be expected, and some of them also had a low number of uniques, both indicating sufficient sampling. By combining different analyses in a novel way we were able to evaluate observed species richness pattern as well as identify, where further sampling would be most beneficial. Approach we demonstrate is of broad interest to study of biota with high levels of endemism, small distribution ranges and low catchability.     

Distribution and underground habitats of cave-dwelling bats in China

To understand the distribution and relative abundance of cave-dwelling bats and to identify those sites that would be important for conservation of bat species, 25 underground sites that had not been previously surveyed were investigated in this 3-year study (from December 2003 to April 2006) in Funiu Mountain of Henan province, China. Approximately 80 000 bats were recorded, representing 12 species. The most abundant species were Rhinolophus affini s, Miniopterus schreibersi and Hipposideros pratti . The roosts were evaluated for their conservation importance. The most important sites in the area are Yunhua and Nanzhao caves, which serve as hibernaculums and nursery roosts to c . 13 740 and 11 803 bats, respectively, representing seven species. By means of cluster and correspondence analysis, the distribution of bat species was different between the two sides of the mountain and was highly dependent on the size of the cave. The underground sites in the south region hosted c . 80% of the total bats, representing 11 species. The sites in the north region hosted 20% of the total bats, representing seven species. Presently, none of the caves in the region has adequate protection and some bat populations are under serious threat. Many large caves that contained large bat populations and several species of concern had been developed as tourist sites, and so some advice on protecting the most important local habitats was sought based on the assessment of the conservation status of underground sites. This paper presents basic data concerning the distribution of cave-dwelling bats and the patterns of cave use on Funiu Mountain. The data will help local governments and policy-makers develop suitable strategies to promote local tourisms while protecting important habitats of animal species.     

The biology of Schizomus vinei (Chelicerata: Schizomida) in the caves of Cape Range, Western Australia

The chelicerate order Schizomida is represented in Western Australia by a single species, Schizomus vinei Harvey, from caves in the semi–arid Cape Range on the North West Cape peninsula. Schizomus vinei occurs in eight of 170 caves known from the range but is found only in areas where the relative humidity exceeds 92%. The schizomids are associated with a rich fauna (at least 11 species) mostly of detritivores, some of which show troglobitic adaptations. They prey on the cave animals that feed on detritus and are known to eat oniscoid isopods, millipedes, cockroaches, worms and S. vinei.
The size class structure of the population in cave C 118 was strongly skewed negatively suggesting that the smaller size classes occupy interstices of the infill of sumps. Schizomids in this cave were found to be distributed at random up to the third nearest neighbour. The minimum population size, with 95% confidence, was estimated to be 1323 individuals. Schizomus vinei grew very slowly in vivaria. One female produced nine eggs which did not survive.
Schizomus vinei has a high mean rate of water loss (470–4 mg g^-1 h^-1) and a low resistance to water loss (15–2 cm sec^-1); their resistance is about 10 x greater than that of a free water surface, but is about two orders of magnitude lower than that of some spiders and scorpions. Schizomus vinei excretes a clear fluid and may be ammonotelic.
Allozyme electrophoresis strongly suggests that individuals from the different caves are of the same species. Consideration of climate, age of separation of the caves and the general biology of the schizomids suggests that those caves containing schizomids may be linked.