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.     

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.     

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.     

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.     

Global diversity of amphipods (Amphipoda; Crustacea) in freshwater

Amphipods are brooding peracaridan crustaceans whose young undergo direct development, with no independent larval dispersal stage. Most species are epibenthic, benthic, or subterranean. There are some 1,870 amphipod species and subspecies recognized from fresh or inland waters worldwide at the end of 2005. This accounts for 20% of the total known amphipod diversity. The actual diversity may still be several-fold. Amphipods are most abundant in cool and temperate environments; they are particularly diversified in subterranean environments and in running waters (fragmented habitats), and in temperate ancient lakes, but are notably rare in the tropics. Of the described freshwater taxa 70% are Palearctic, 13% Nearctic, 7% Neotropical, 6% Australasian and 3% Afrotropical. Approximately 45% of the taxa are subterranean; subterranean diversity is highest in the karst landscapes of Central and Southern Europe (e.g., Niphargidae), North America (Crangonyctidae), and Australia (Paramelitidae). The majority of Palearctic epigean amphipods are in the superfamily Gammaroidea, whereas talitroid amphipods (Hyalella) account for all Neotropic and much of the Nearctic epigean fauna. Major concentrations of endemic species diversity occur in Southern Europe, Lake Baikal, the Ponto-Caspian basin, Southern Australia (including Tasmania), and the south-eastern USA. Endemic family diversity is similarly centered in the Western Palearctic and Lake Baikal. Freshwater amphipods are greatly polyphyletic, continental invasions have taken place repeatedly in different time frames and regions of the world. In the recent decades, human mediated invasions of Ponto-Caspian amphipods have had great impacts on European fluvial ecosystems. Guest editors: E. V. Balian, C. Lévêque, H. Segers and K. Martens Freshwater Animal Diversity Assessment     

A synthesis on cave‐dwelling spiders in Europe

We provide the first overview on spiders living in subterranean habitats in Europe, including the first European subterranean spider checklist. In Europe, there are 486 spider species known to dwell in caves and other subterranean habitats, distributed across 22 families. Despite a few species being able to colonize caves across the whole continent, approximately 90% of the species show a restricted distribution, occurring exclusively in one or two countries. From a biogeographic perspective, southern Europe emerges as the main hot spot of subterranean spider diversity, showing the highest richness of endemic species. Compared to other temperate regions of the world, some families appear to be well represented and other poorly represented (or lacking) in European subterranean habitats. Overall, it appears that the taxonomical knowledge on subterranean spiders in Europe is sufficient, but not evenly distributed. As this checklist represents a useful baseline for advances in this field, we point out specific areas of interest for future research.     

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

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

Priority caves for biodiversity conservation in a key karst area of Brazil: comparing the applicability of cave conservation indices

Landscapes in tropical regions have been greatly altered by human activities, as a product of growing demands for mineral and agricultural production, as well as those related to the generation of energy (e.g., hydroelectric, wind). In this scenario, caves have suffered several impacts, sometimes irreversible, as they are generally associated with rocks of high economic value and are closely related to epigean systems. Several indices have been proposed to guide conservation policies for the world’s speleological heritage, although few of them consider cave biodiversity as a criterion. To address this knowledge gap, we tested the applicability of four newly proposed indices to assist researchers and policy-makers select priority areas for global cave biodiversity conservation. To compare indices, we used data from 48 caves of the largest carbonate region of South America (Bambui geological group), all found within the Cerrado, a global biodiversity hotspot. Each of the four indices considered cave biodiversity as a criterion, although only three adequately evaluated this attribute. Based on results of Simões index and CCPi, which were the most appropriate in relation to indicate priority caves for biodiversity conservation in regions where the fauna and its distribution are not fully known, 15 of the 48 caves were identified as conservation priorities.     

Functional Resilience against Climate-Driven Extinctions – Comparing the Functional Diversity of European and North American Tree Floras

Future global change scenarios predict a dramatic loss of biodiversity for many regions in the world, potentially reducing the resistance and resilience of ecosystem functions. Once before, during Plio-Pleistocene glaciations, harsher climatic conditions in Europe as compared to North America led to a more depauperate tree flora. Here we hypothesize that this climate driven species loss has also reduced functional diversity in Europe as compared to North America. We used variation in 26 traits for 154 North American and 66 European tree species and grid-based co-occurrences derived from distribution maps to compare functional diversity patterns of the two continents. First, we identified similar regions with respect to contemporary climate in the temperate zone of North America and Europe. Second, we compared the functional diversity of both continents and for the climatically similar sub-regions using the functional dispersion-index (FDis) and the functional richness index (FRic). Third, we accounted in these comparisons for grid-scale differences in species richness, and, fourth, investigated the associated trait spaces using dimensionality reduction. For gymnosperms we find similar functional diversity on both continents, whereas for angiosperms functional diversity is significantly greater in Europe than in North America. These results are consistent across different scales, for climatically similar regions and considering species richness patterns. We decomposed these differences in trait space occupation into differences in functional diversity vs. differences in functional identity. We show that climate-driven species loss on a continental scale might be decoupled from or at least not linearly related to changes in functional diversity. This might be important when analyzing the effects of climate-driven biodiversity change on ecosystem functioning.     

The North American obligate cave fauna: regional patterns

The obligate cave faunas of nine regions of the United States –Florida Lime Sinks, Appalachians, Interior Low Plateaus, Ozarks, Driftless Area,Edwards Aquifer/Balcones Escarpment, Guadalupe Mountains, Black Hills, andMother Lode – are described and compared. The number of aquatic(stygobitic) species ranged from zero (Black Hills) to 82 (Appalachians), andthe number of terrestrial (troglobitic) species ranged from zero (Florida LimeSinks) to 256 (Interior Low Plateau). Even at the level of genus, overlapbetween regions is low. Several predictor variables (karst area, number ofcaves, number of long caves, number of deep caves, distance from the Pleistoceneice margin, distance from the late Cretaceous Sea, and vegetation type – asurrogate for productivity) were assessed using rank order statistics,especially rank order multiple regression with a backward elimination procedure.For both stygobites and troglobites, only number of caves was a significantpredictor. The absence of a karst area effect suggested that the degree of karstdevelopment is better described by the number of caves rather than area ofkarst. There was no evidence that distance to Pleistocene glacial boundaries wasimportant, but there was some support for the importance of distance from late Cretaceous sea margins, a potential source of aquatic subterranean colonists. Finally,there was no indication that surface productivity had an effect on speciesrichness. Analysis was complicated by correlations among predictor variables.     

贵州荔波玉屏洞穴陆生动物食物来源及营养级

洞穴是“极端地下生物多样性”的聚集地, 为了揭示洞穴陆生动物的食物来源以及营养级关系, 本文于2016年10月对贵州荔波玉屏镇的3个代表性洞穴内的陆生动物进行调查, 应用¹³C和¹⁵N稳定同位素方法, 分析了洞内陆生动物和基础碳源的δ¹³C、δ¹⁵N值变化特征, 探究了各动物类群的营养级位置以及不同的基础碳源对动物的食物源的贡献率。结果表明: 洞穴植物的δ¹³C值范围为-38.25‰ ± 0.95‰至-29.44‰ ± 0.49‰, 土壤有机质δ¹³C值范围为-32.73‰ ± 0.03‰至-24.68‰ ± 0.41‰, 大部分不在洞穴植物的δ¹³C变化范围内。洞穴动物δ¹³C、δ¹⁵N值范围分别为-34.22‰ ± 0.39‰至-14.83‰ ± 0.78‰、1.86‰ ± 0.20‰至16.43‰ ± 0.05‰, 表现出较大的种(或类群)间差异。IsoSource软件估算结果表明, 洞穴土壤有机质对78.3%动物类群的食物源的贡献率高于植物。荔波玉屏洞穴消费者的营养级范围为1.01-5.32, 其中, 巨蚓科、螺类、潮虫科、马陆、大蚊科、夜蛾科主要处于第2营养层次; 蚰蜒科、蚁蛉科(幼虫)、蝙蝠处于第3营养层次; 蜚蠊科处于第2-3营养层次; 驼螽科、蠼螋科处于第2-4营养层次; 蜘蛛处于第2-5营养层次, 跨3个营养级。综上认为, 洞穴土壤有机质是洞穴消费者的主要食物基础。大部分同一类群的动物在洞穴中所处的营养级位置较稳定, 少部分同属于一个类群的动物在不同洞穴或同一洞穴不同光带所处的营养级位置有差异。     

EFFECTS OF CLIMATIC AND GEOLOGICAL PROCESSES DURING THE PLEISTOCENE ON THE EVOLUTIONARY HISTORY OF THE NORTHERN CAVEFISH,AMBLYOPSIS SPELAEA (TELEOSTEI: AMBLYOPSIDAE)

Climatic and geological processes associated with glaciation cycles during the Pleistocene have been implicated in influencing patterns of genetic variation and promoting speciation of temperate flora and fauna. However, determining the factors promoting divergence and speciation is often difficult in many groups because of our limited understanding of potential vicariant barriers and connectivity between populations. Pleistocene glacial cycles are thought to have significantly influenced the distribution and diversity of subterranean invertebrates; however, impacts on subterranean aquatic vertebrates are less clear. We employed several hypothesis‐driven approaches to assess the impacts of Pleistocene climatic and geological changes on the Northern Cavefish, Amblyopsis spelaea, whose current distribution occurs near the southern extent of glacial advances in North America. Our results show that the modern Ohio River has been a significant barrier to dispersal and is correlated with patterns of genetic divergence. We infer that populations were isolated in two refugia located north and south of the Ohio River during the most recent two glacial cycles with evidence of demographic expansion in the northern isolate. Finally, we conclude that climatic and geological processes have resulted in the formation of cryptic forms and advocate recognition of two distinct phylogenetic lineages currently recognized as A. spelaea.     

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.     

Responses to light in two blind cave fishes (Amblyopsis spelaea and Typhlichthys subterraneus) (Pisces: Amblyopsidae)

Explanations for the phenotypical features resulting from colonization of subterranean environments have always been a source of controversy. Although a great number of cave organisms are blind, they nevertheless display responses to light. The interpretation of this phototactic responsiveness in cave-dwelling animals may provide clues on the general issue of evolution of behavior in parallel with specialized structures. We studied the phototactic responses in two amblyopsid fishes of North America and found responses to light only in the species reported to have a functional pineal organ. Our findings are consistent with the hypotheses that (1) adaptation to the cave environment is a gradual process and (2) responsiveness to light in cave fishes may best be understood as a relict character, one that exists in an environment where it may never be expressed.     

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.     

Distribution pattern and radiation of the European subterranean genus Verhoeffiella (Collembola,Entomobryidae)

One of the most striking features of obligate subterranean species is their narrow distribution ranges. These prevail not only at specific, but often also at generic level. However, some subterranean genera have continental scale and disjunct distribution, which challenges their monophyly and questions the scenarios of their origin and colonization. In our study, we investigated the subterranean collembolan genus Verhoeffiella, currently known from five remote karst regions of Europe. Four nuclear and one mitochondrial genes were assembled to reveal the evolutionary history of the genus. We tested the monophyly of the genus, explored its relationship with putative surface relatives, and its temporal patterns of molecular diversification. The phylogeny revealed a complex relationship of Verhoeffiella with surface species Heteromurus nitidus and partially disentangled the biogeographical question of its disjunct distribution. Further on, several lineages of Verhoeffiella were recognized in the Dinarides, showing highly underestimated diversity and, compared with the number of described species, a sevenfold increase in the number of MOTUs. The radiation is relatively recent, with the events triggering the diversification linked to the Messinian salinity crisis and Pleistocene climatic shifts. The combination of this extensive subterranean radiation and close evolutionary links with epigean relatives makes Verhoeffiella an exceptional case within the subterranean fauna of temperate areas, which significantly contributes to our understanding of subterranean colonization and diversification patterns.     

A new Stygonitocrella Petkovski (Copepoda: Harpacticoida) from a cave in Northern Mexico with comments on the taxonomy of the genus

The cave-dwelling harpacticoid copepod fauna of Mexico is still yet to be known. There are only a few records related to karstic caves, but most refer to epigean forms. The analysis of samples collected in a cave system in Northern Mexico yielded two female specimens of an unknown harpacticoid copepod species which is described herein. It was assigned to the genus Stygonitocrella Petkovski, 1976 mainly because of the presence of a single endopodal segment on legs 1–4; the new species, S. mexicana n. sp. differs from its congeners by a combination of characters related to the segmentation and armature of the swimming legs 1–4, the fifth leg of the female, and the strcture of the antennae. Based on the current limits of Stygonitocrella, two new subgenera are proposed to recognize different morphological patterns based on the presence or absence of an inner baseoendopodal lobe in the female fifth leg, a character not evaluated before. This lobe is absent in the new species and in other five species now contained in the subgenus Eustygonitocrella. A lobe is present in the new subgenus Fiersiella, also with six species. This is the second record of Stygonitocrella in North America, after S. (Fiersiella) sequoyahi Reid, Hunt & Stanley, 2003; it is the only North American cave-dwelling species of the genus. It is suggested that the influence of marine transgressions in Northern Mexico was related to the origin of the new species as part of a group of troglobitic forms originated from marine interstitial ancestors that colonized the freshwater caves. A key for the identification of all the known species of Stygonitocrellais also provided.     

氮沉降对森林生物多样性的影响

从3个方面论述了氮沉降对森林生物多样性影响：（1）森林植物多样性,包括乔木层植物、林下层植物和隐花植物;（2）土壤微生物多样性,主要是细菌和真菌;（3）森林动物多样性：主要包括地下土壤动物和地上草食动物。综合来看,氮沉降改变了物种组成,过量氮沉降降低了生物多样性。同时,也对氮沉降影响生物多样性的机理进行了分析。最后,还探讨了当前在氮沉降对森林生物多样性影响的研究方面存在的问题以及今后研究的方向。     

Exploring the homogeneity of terrestrial subterranean communities at a local spatial scale

1. Although caves are generally perceived as isolated habitats, at the local scale, they are often interconnected via a network of fissures in the bedrock. Accordingly, caves in close proximity are expected to host the same, or very similar, animal communities. 2. We explored the extent to which subterranean arthropod communities are homogenous at a local spatial scale of less than 1 km², along with which cave-specific environmental features result in a departure from the expected homogeneous pattern. We approached this question by studying richness and turnover in terrestrial invertebrate communities of 27 caves in a small karst massif in the Western Italian Alps. 3. Specialised subterranean species were homogeneously distributed among caves and were not influenced by seasonality. The only factor driving their distribution was the distance from the cave entrance, with deeper caves yielding a greater diversity of species. 4. Significant spatio-temporal turnover in species not specialised to subterranean life was observed. In summer, there was a significant homogenisation of the community and a more even distribution of species among sites; in winter, these species were missing or found exclusively at greater depths, where environmental conditions were more stable. Furthermore, caves at lower elevations yielded, on average, a greater diversity and abundance of these species. 5. This study demonstrated that the theoretical expectation of no turnover in community composition in caves in close proximity is not always met. Turnover can be mostly attributed to seasonal patterns and sampling depth; thus, our findings have implications for planning sampling and monitoring activities in caves.     

森林生态系统碳循环对全球氮沉降的响应

森林土壤和植被储存着全球陆地生态系统大约46%的碳,在全球碳平衡中起着非常重要的作用。过去几十年来,森林生态系统的碳循环和碳吸存受到了全球氮沉降的深刻影响,因为氮沉降改变了陆地生态系统的生产力和生物量积累。以欧洲和北美温带森林区域开展的研究为基础,综述了氮沉降对植物光合作用、土壤呼吸、土壤DOM及林木生长的影响特征和机理,探讨了森林生态系统碳动态对氮沉降响应的不确定性因素。热带森林C、N循环与大部分温带森林不同,人为输入的氮对热带生态系统过程的影响也可能不同,因此指出了在热带地区开展碳氮循环耦合研究的必要性和紧迫性。