Marine caves of the Mediterranean Sea: a sponge biodiversity reservoir within a biodiversity hotspot

Marine caves are widely acknowledged for their unique biodiversity and constitute a typical feature of the Mediterranean coastline. Herein an attempt was made to evaluate the ecological significance of this particular ecosystem in the Mediterranean Sea, which is considered a biodiversity hotspot. This was accomplished by using Porifera, which dominate the rocky sublittoral substrata, as a reference group in a meta-analytical approach, combining primary research data from the Aegean Sea (eastern Mediterranean) with data derived from the literature. In total 311 species from all poriferan classes were recorded, representing 45.7% of the Mediterranean Porifera. Demospongiae and Homoscleromorpha are highly represented in marine caves at the family (88%), generic (70%), and species level (47.5%), the latter being the most favored group along with Dictyoceratida and Lithistida. Several rare and cave-exclusive species were reported from only one or few caves, indicating the fragmentation and peculiarity of this unique ecosystem. Species richness and phylogenetic diversity varied among Mediterranean areas; the former was positively correlated with research effort, being higher in the northern Mediterranean, while the latter was generally higher in caves than in the overall sponge assemblages of each area. Resemblance analysis among areas revealed that cavernicolous sponge assemblages followed a pattern quite similar to that of the overall Mediterranean assemblages. The same pattern was exhibited by the zoogeographic affinities of cave sponges: species with Atlanto-Mediterranean distribution and Mediterranean endemics prevailed (more than 40% each), 70% of them having warm-water affinities, since most caves were studied in shallow waters. According to our findings, Mediterranean marine caves appear to be important sponge biodiversity reservoirs of high representativeness and great scientific interest, deserving further detailed study and protection.     

Cave Fauna of Bermuda

Sea-level pools are found in most of Bermuda's known caves. Although the terrestrial fauna of the caves is sparse, a rich aquatic fauna inhabits the pools. While many of the marine cave animals are more or less regular immigrants from open littoral habitats, a number of new species have been discovered, including blind and probably subterranean ones. Zoogeographical connections exist between Bermuda's cave fauna and those of the West Indies and the Mediterranean.     

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.     

贵州部分洞穴裸灶螽的鉴定及其遗传多样性分析

贵州是中国具有丰富喀斯特洞穴生态系统的省份之一,裸灶螽作为洞穴中的优势物种又为生态环境指示种,其遗传多样性能够反应洞穴生物多样性.为评估洞穴开发对洞穴生物多样性的影响,本研究通过形态鉴定和分子辅助鉴定的方式对来自贵州省毕节、黔西南、铜仁和黔南4个地区8个洞穴97号裸灶螽标本进行鉴定,并对其遗传多样性进行分析.结果共鉴定...     

Anthropization level of Lascaux Cave microbiome shown by regional‐scale comparisons of pristine and anthropized caves

Limestone areas across the world develop karstic caves, which are populated by a wide range of macro‐ and microorganisms. Many of these caves display Paleolithic art or outstanding speleothems, and in the last century they have been subjected to anthropization due to touristic management and intense human frequentation. Despite their cultural importance and associated conservation issues, the impact of anthropization on cave biodiversity is not known. Here, we show that anthropization is associated with specific cave biota modifications. We compared diversity in four pristine caves, four anthropized show caves, and the iconic Lascaux Cave with even stronger anthropization. The predominant microbial higher taxa were the same in all caves, but the most anthropized cave (Lascaux) was unique as it differed from the eight others by a higher proportion of Bacteroidetes bacteria and the absence of Euryarchaeota and Woesearchaeota archaea. Anthropization resulted in lower diversity and altered community structure for bacteria and archaea on cave walls, especially in Lascaux, but with a more limited effect on microeukaryotes and arthropods. Our findings fill a key gap in our understanding of the response of karstic communities to anthropization, by revealing that tourism‐related anthropization impacts on the prokaryotic microbiome rather than on eukaryotic residents, and that it shapes cave biota irrespective of cave natural features.     

Diversity and ecology of the bryophytes in the cave environment: a study on the volcanic and karstic caves of Sicily

The results of a long investigation (20 years) on bryophyte diversity of 28 Sicilian caves are reported; the study regarded both karstic and volcanic caves, located at altitudes ranging from 15 to 2030 m a.s.l. The bryophyte diversity consists of a total of 136 taxa, 20 liverworts, 3 hornworts and 113 mosses. The ecological analysis was performed using the Ellenberg indicator values for moisture, light and soil reaction to the substrate. On the whole, mesophytic and meso-hygrophytic, sciophytic and photo-sciophytic species strongly prevail independently from the geological nature of the caves; the values of the soil reaction to the substrate well reflect the characteristics of the substrate. The phytogeographical analysis shows the prevalence of the Mediterranean species, followed by the temperate and southern-temperate species. It is remarkable the occurrence of boreo-arctic-montane species, which find refuge for their survival in some high-altitude caves. Some typical species well adapted to the cave environment are reported, including Amphidium mougeotii, Isopterygiopsis pulchella, Thamnobryum alopecurum and Rhynchostegiella tenella, showing a troglophilous character. The occurrence of species of phytogeographical significance, as well as of conservation interest, e.g. Ptychostomum cernuum, Tortula bolanderi, Rhabdoweisia fugax, Grimmia torquata, Brachytheciastrum collinum, very rare in Italy, is emphasized too.     

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。     

Regional warming-induced species shift in north-west Mediterranean marine caves

The north‐western Mediterranean Sea's high biodiversity originates from a mixture of temperate and subtropical species. Large‐scale warming has been detected through northward range shifts of ‘warm‐water’ species, and mass‐mortality events for ‘cold‐water’ invertebrates. Marine caves are affected in a more subtle way. By monitoring endemic species of cave mysids (Crustacea) and comparing our results with data in the literature, we observed a strong decline in one species, coupled with the success of another. Near Marseille (France), this phenomenon began while two major thermal anomalies were reported. Different tolerances to temperature were demonstrated by both the species distribution ranges and laboratory experimentation. We provide a possible physiological explanation for populations of cold stenothermal species of endemic cave mysids being replaced by congeners of warmer affinities, with a high risk of extinction. We also found strong support for the view that Mediterranean marine biodiversity is already under the threat of global warming.     

Microbial Diversity in Caves

Relatively stable physical conditions in caves allow for the examination of the relationship between geochemical processes and the activity of microorganisms, reflected in substantial rock alterations, formation of new structures, surface deterioration and cave expansion. Although caves are considered as extreme environments, they are inhabited by microbial communities with unexpected diversity. While Proteobacteria and Actinobacteria are the most ubiquitous groups, also the presence of Archaea has been frequently noted recently. Here, we present a summary of results on diversity of cave microorganisms in the context of taxon distribution as well as the contribution and role of individual taxa in cave ecosystems.     

Ammonia oxidation (amoA) and nitrogen fixation (nifH) genes along metasandstone and limestone caves of Brazil

Abstract

Many cave-dwelling microorganisms have been studied, but little is known about whether genes related to the nitrogen cycle are present in this environment, particularly in sandstone caves. The profiles of nitrogen fixation (nifH) and archaeal and bacterial ammonia oxidation (amoA) genes were analyzed along a cave of metasandstone and limestone lithologies. Using polymerase chain reaction (PCR)-denaturing gradient gel electrophoresis and quantitative PCR to evaluate these genes, we analyzed the variations in the microorganisms and frequency of these genes along the caves. In both caves analyzed for nifH, different community profiles were observed, particularly in entrance samples. Quantitative PCR of the genes showed that samples from the entrance of the caves contained a larger number of copies of amoA. In addition, archaeal amoA was predominant compared to bacterial amoA. The present study demonstrated that the genes for nitrogen fixation and ammonia oxidation are present in both cave lithologies and that their frequency and the organisms present along the caves vary with factors such as the characteristics of the cave itself.     

Molecular genetic variation and population structure in morphologically differentiated cave and surface populations of the freshwater amphipod Gammarus minus

Gammarus minus is an important component of surface spring and cave ecosystems throughout Appalachia, and is a useful indicator of the hydrology and gene flow in freshwater communities. Gammarus minus populations occupying large cave passages (> 2 km) are usually troglomorphic, having reduced eyes, fewer ommatidia, larger body size, longer antennae, and reduced pigmentation relative to surface populations. We surveyed five cave stream and 10 surface spring populations for DNA sequence variation in the cytochrome c oxidase I (COI) and internal transcribed spacer 1 (ITS-1) genes with an aim towards characterizing phylogeographical structure and comparing the nature of genetic variation in cave vs. surface populations. Although standing variation at both loci was rather low within populations, a significant degree of divergence and spatial structuring of populations was observed. Levels of genetic variation within cave and spring populations differed substantially, with caves harbouring significantly less variation at the COI locus than surface springs. Codon usage bias was significantly lower in caves, indicating that cave streams harbour smaller and/or more recently colonized populations. Overall these data indicate limited gene flow among populations and suggest that the cave populations sampled in this study are prone to bottlenecks, possibly due to larger temperature fluctuations and more frequent incidence of drought conditions associated with these particular cave habitats.     

Big family,warm home,and lots of friends: Pteronotus large colonies affect species richness and occupation inside caves

Roosts are essential for the survival of most animals. Due to homothermic requirements, mammals are particularly dependent on roost quality and availability. Bats select their roosts in a species-specific way, likely related to species´ different physiological and adaptive needs. Unlike species whose individuals roost solitarily, roost selection is critical for bats forming large colonies due to the requirements for maintaining thousands of individuals in a single shelter. This is the case of Pteronotus (Mormoopidae), whose colonies reach hundreds of thousands of bats. Using captures, bioacoustics, and automated censuses, we evaluated how cave size, ceiling characteristics, environmental stability, temperature, and humidity influence the formation of exceptionally large colonies, species richness and composition in caves in north-eastern Brazil. We expected that colonies would be positively related to cave size and stability, internal cave selection would be species-specific, but larger and more environmentally stable caves would have higher richness. Pteronotus colonies were positively related to cave size, stability, and ceiling characteristics, and their presence strongly influenced cave temperature variation. Species richness was positively correlated to a cave stability index. Species other than Pteronotus preferred different climatic and ceiling characteristics. We detected an indirect influence of the large colonies of Pteronotus on the species richness and occupation inside caves. On the other hand, such caves favor species coexistence, as they offer a range of microenvironments, reducing niche overlap in their interior. Pteronotus gymnonotus and Pteronotus personatus are both key- and umbrella-species for cave ecosystems, stressing the need for specific conservation strategies in Brazil. Abstract in Portuguese is available with online material.     

贵州仙家洞和忆苦洞洞穴动物群落多样性及其环境因子的影响

为了解矿区洞穴动物群落多样性特征及其影响因素,于2019年3月对贵州松桃锰矿区仙家洞和忆苦洞的动物进行了调查,运用主成分(PCA)综合分析了环境因子对洞穴动物群落多样性的影响,并利用潜在生态危害指数对洞穴内土壤重金属的生态风险水平进行了评价.结果 表明:共获动物标本445号,隶属4门8纲18目32科,其中仙家洞178号...     

Identification of roots in lava tube caves using molecular techniques: implications for conservation of cave arthropod faunas

Lava tube cave ecosystems on the volcanic islands of Hawai‘i support communities of rare and highly specialized cave arthropods. In these cave ecosystems, plant roots, both living and dead, provide the main energy source for cave animals. Loss of deep-rooted plants over caves will affect populations of cave-adapted animals living below. Furthermore, the loss of native plant species will likely eliminate host specific cave animals. Thus, identification of plant roots currently found in caves is necessary for the development of effective management actions that encourage the growth of appropriate deep-rooted plant species, thereby protecting the underlying cave ecosystem. We used molecular techniques to identify plant roots found within cave ecosystems on the islands of Maui and Hawai‘i. Sequences of the internal transcribed spacer (ITS) regions and the 5.8S gene of nuclear ribosomal DNA from cave roots were compared to sequences of known plant species either collected on the surface over the footprint of each cave or to sequences accessioned in GenBank. Roots in the cave ecosystem studied on Maui belonged to two alien tree species: Eucalyptus tereticornis and Grevillea robusta. Within the Hawai‘i cave ecosystem, roots of two plant species were identified: the alien tree G. robusta and the native vine Cocculus orbiculatus. The Maui cave ecosystem supports populations of at least 28 species of arthropods, including eight that are blind obligate cave inhabitants. The Hawai‘i cave ecosystem supports 18 arthropod species, of which three are cave-adapted. Creating protected reserves around biologically significant caves, controlling, and preventing the introduction of harmful invasive plant species within the cave footprint, and encouraging the establishment of deep-rooted native plant species is essential for the continued survival of the unique ecosystems found within Hawaiian lava tube cave systems.     

PUPPING HABITAT USE IN THE MEDITERRANEAN MONK SEAL: A LONG-TERM STUDY

The Mediterranean monk seal gives birth almost exclusively in coastal caves. Given its critical conservation status, the identification and protection of such sites is important for the survival of the species. From 1990 to 2004 we collected data on physical and environmental variables and monitored pupping events in thirty-four coastal caves in Greece. We modeled the probability of cave occupancy as a function of the properties of each cave. Model selection and model averaging enabled us to rank the variables that influenced use of potential pupping sites. Environmental variables related to cave seclusion, substrate, and degree of protection from wind and wave action were the most important among them. The relative importance and directions of these relationships confirm the long-standing assumption that Mediterranean monk seals require sheltered pupping sites, far from sources of human disturbance and thus are progressively limited to isolated parts of the country's coastline. We used cross-validation to examine the predictive ability of our analysis and quantified the sensitivity of our predictions to the degree of extrapolation. We conclude that, although more data are required, the model is capable of predicting occupancy for caves close to the middle of the environmental space examined in this study.     

英格兰洞穴苔藓植物区系特征及其岩溶沉积研究

根据作者1998－2000年采自英格兰7个岩溶洞穴452份苔藓植物标本研究,英格兰岩溶洞穴苔藓植物区系具有下列特征：（1）区系种类由20科41属65种（含变种亚种）组成;（2）区系地理成分含北温带分布（52．30％）、温带欧洲分布（15．38％）、欧洲－亚洲分布（1．54％）、欧洲－北美分布（12．31％）、旧世界温带分布（4．62％）、英国特有（1．54％）和世界广泛分布（12．31％）等7种成分;（3）生活型含高丛集型（9．22％）、矮丛集型（20％）、交织型（61．54％）、扇型（4．08％）和平铺型（4．08％）5种类型。14种洞穴苔藓植物参与了洞穴洞口钙华沉积,沉积形态包括钟乳石、洞壁钙华、洞底泉华和洞底滴水钙华4种类型。     

Natural-trap ursid mortality and the Kurtén Response

Ursid mortality data have long been used to evaluate associations between cave-bear remains (Ursus deningeri and U. spelaeus) and hominin (Homo sp.) remains. Typically, such ursid assemblages produce mortality patterns that indicate that juvenile and old bears died during hibernation, a pattern that is used to suggest that humans and bears occupied the same caves at different times. However, a different kind of mortality pattern can also be used to suggest human influence on cave bears, particularly under circumstances when bears and humans compete for habitat. In particular, data from Lawson Cave and Jerry Long Cave, Missouri indicate that young-adult North American black bears (Ursus americanus) are prone to capture in natural-trap caves. Similar faunal data from Sima de los Huesos in Spain, where cave-bear and hominin remains are found in the same deposit, might also suggest that the bears died from falling into a natural trap. It is concluded that mortality analysis of ursid remains from caves is a useful tool with which to evaluate accumulation histories of cave deposits and relations between humans, artifacts, and cave-bear remains. In particular, ursid mortality data are relevant to the Kurtén Response, a hypothesis reiterated in the recent literature that implicates human encroachment on ursid habitat (e.g., cave den sites) as a potential cause in cave-bear extinction.