洞穴鱼类:概念、多样性及研究进展

洞穴鱼类是淡水鱼类中一个特殊的生态类群,其生活史的自然完成离不开洞穴或地下水环境。洞穴鱼类可分为典型和非典型两种类型,前者具有易辨识的特殊适应性形态结构(如眼消失、身体透明等),后者此类特征不明显。目前世界典型洞穴鱼类共记录有107种,其中鲤形目和鲇形目的种类最多,分别占49.5%和24.3%;在科级水平上以鲤科和爬鳅科最为丰富。东南亚和中南美是洞穴鱼类多样性最高的地区,有着世界上75.0%的典型洞穴鱼类。中国的洞穴鱼类具有物种多样性高、但集中出现在个别类群(如金线鲃属(Sinocyclocheilus)和高原鳅属(Triplophysa))、物种分化强烈、分布范围狭窄、种群数量小等特点。洞穴鱼类学是一门交叉科学,研究涉及系统学、生态学、生理学、保护生物学等众多学科领域,但目前研究仍多围绕演化问题展开。中国洞穴鱼类研究还处于系统分类和区系研究水平,其他有关学科的研究有待开展。     

Out of sight out of mind: current knowledge of Chinese cave fishes

Caves and karsts are among the most threatened ecosystems in the world. They are very fragile, balanced habitats with high levels of endemic species that are extremely sensitive to environmental changes. In recent decades, however, threats from rapid economic growth have increased the need for conservation efforts for cave-dwelling communities. In addition, difficulties in accessing and sampling these habitats mean that they remain as one of the least known ecosystems in the world with modern studies of cave fishes only starting in China during the 1980s. Here, the current status of cave fishes in China is reviewed. China is host to the highest number of cave fish species in the world, with 48 troglobite species out of a total of 101 cave fish species. All of these cave fish species (one order and three families) and half of the genera are endemic to China with Sinocyclocheilus being the most speciose cave fish genus. Species from this genus possess horns and humpbacks resulting from processes of parallel evolution, but the function of these features remains unknown. With the exception of Onychostoma macrolepis distributed in north China, all other species are found in the karst environment of the Yunnan-Guizhou Plateau. Sympatric distribution is common, and sometimes several different cave fish species can be found in the same cave or subterranean river. For this reason, Chinese cave fishes represent an important evolutionary framework.     

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.     

Reaction to Alarm Substance in Cave Populations of Astyanax fasciatus (Characidae,Pisces)1

The effect of species-specific skin-extract containing alarm substance has been studied in two epigean and three hypogean populations of the Mexican-tetra Astyanax fasciatus. In all populations tested the feeding rate at the water surface decreased significantly after introducing the alarm substance and the fish avoided this surface area. Additionally epigean fish and some individuals from the Chica cave showed zigzag movements, rapid swimming and hiding. The fish did not respond to a skinextract of a species without alarm substance.     

The end of regressive evolution: examining and interpreting the evidence from cave fishes

The evolution of hypogean fauna in general and hypogean fishes in particular has been controversial. Explanations regarding the reduction or loss of phenotypic characters such as eyes and pigmentation range from neo‐Lamarckism to neutral mutations, with 'regressive evolution' being a catch‐all characterization for such processes. The assumptions required for special evolutionary mechanisms underlying the evolution of cave dwellers have been based on generalizations about the animals and their environments drawn from relatively few observations. The evidence offered for notions such as pre‐adaptation of colonizing fauna and the purported impoverished nutrients in all caves is examined and it appears that the generalizations cannot be supported. Some major accomplishments in field and laboratory studies of hypogean fishes are summarized, including work highlighting developmental phenotypic plasticity. At the end, it is argued that evolution of hypogean fauna can be explained by well‐known mechanisms within the current context of evolutionary biology.     

The Laterosensory Canal System in Epigean and Subterranean Ituglanis (Siluriformes: Trichomycteridae), With Comments About Troglomorphism and the Phylogeny of the Genus

The laterosensory system is a mechanosensory modality involved in many aspects of fish biology and behavior. Laterosensory perception may be crucial for individual survival, especially in habitats where other sensory modalities are generally useless, such as the permanently aphotic subterranean environment. In the present study, we describe the laterosensory canal system of epigean and subterranean species of the genus Ituglanis (Siluriformes: Trichomycteridae). With seven independent colonizations of the subterranean environment in a limited geographical range coupled with a high diversity of epigean forms, the genus is an excellent model for the study of morphological specialization to hypogean life. The comparison between epigean and subterranean species reveals a trend toward reduction of the laterosensory canal system in the subterranean species, coupled with higher intraspecific variability and asymmetry. This trend is mirrored in other subterranean fishes and in species living in different confined spaces, like the interstitial environment. Therefore, we propose that the reduction of the laterosensory canal system should be regarded as a troglomorphic (= cave‐related) character for subterranean fishes. We also comment about the patterns of the laterosensory canal system in trichomycterids and use the diversity of this system among species of Ituglanis to infer phylogenetic relationships within the genus. J. Morphol. 278:4–28, 2017. ©© 2016 Wiley Periodicals,Inc.     

Rediscovery of the “extinct” blind ground beetle (Coleoptera: Carabidae: Trechinae)

The blind ground beetle Ishikawatrechus intermedius (Coleoptera: Carabidae: Trechinae), called Kadota‐mekurachibigomimushi in Japanese, was first found in 1952 in the cave Ôchi‐dô, Kôchi Prefecture, Japan. However, this cave and a large part of the surrounding hill were destroyed by limestone mining in the 1970s. Because most species of blind ground beetles are restricted to specific caves or cave systems, I. intermedius has been considered endemic to very narrow areas of the cave Ôchi‐dô and the upper hypogean zone around the cave. Therefore, I. intermedius was considered to have become extinct. In this study, during 2011–2015, we collected ten individuals of a blind ground beetle, which appeared to be I. intermedius, from the upper hypogean zone, approximately 0.3–1.0 m below ground, in the southern part of the type locality. A comparison with type specimens indicated that the individuals were indeed I. intermedius. Therefore, we conclude that I. intermedius survives in the upper hypogean zone near the type locality. The results of this study will be useful for quickly establishing conservation measures for threatened or vulnerable species of Trechinae beetles.     

Sex recognition in surface- and cave-dwelling Atlantic molly females (<Emphasis Type="Italic">Poecilia mexicana</Emphasis>, Poeciliidae,Teleostei): influence of visual and non-visual cues

Cave fishes need to rely on non-visual senses, such as the sense of smell or the lateral line to communicate in darkness. In the present study, we investigated sex identification by females of a cave-dwelling livebearing fish, Poecilia mexicana (cave molly), as well as its surface-dwelling relatives. Unlike many other cave fishes, cave mollies still possess functional eyes. Three different modes of presentation of the stimulus fish (a male and an equally sized female) were used: (i) the stimulus fish were presented behind wire-mesh in light, allowing the focal female to perceive multiple cues, (ii) the experiment was carried out under infrared conditions, such that only non-visual cues could be perceived and (iii) the stimulus fish were presented in light behind transparent Plexiglas, allowing for the use of visual cues only. Females of all populations examined preferred to associate with the stimulus female in at least one of the treatments, but only when visible light was provided, suggesting that far-range sex recognition is limited or even absent in the cave molly under naturally dark conditions.     

Locomotory Responses of the Cave Cyprinid Phreatichthys Andruzzii Chemical Signals from Conspecifics and Related Species: New Findings

Previous research on chemical communication among hypogean fishes have suggested that these species are attracted, as are epigean species, by the odour of non-injured conspecifics. Considerations on the biological meaning of such responses and some doubts about the reliability of the experimental procedure previously utilised, have led us to reconsider the matter and verify the results already obtained in the cave cyprinid Phreatichthys andruzzii. Using a new methodological approach we ascertained not only the absence of positive chemotaxis to odour of known or unknown conspecifics, but also the presence of a strong negative chemotaxis towards the odour of unfamiliar conspecifics and of individuals belonging to the closely related species Barbus conchonius. The biological meaning and the adaptive value of these reactions are briefly discussed.     

Scientists Prefer them Blind: The History of Hypogean Fish Research

The history of hypogean fish research has been strongly influenced by neo-Lamarckism (including orthogenesis) and typological thinking. Only in the last few decades neo-Darwinism has made any inroads in the research approach to this subject. The majority of the most distinguished and productive hypogean fish researchers have used their research subjects to confirm their own views on evolution rather than to use those subjects as a spring of knowledge to enrich mainstream biological thought. Of these views, I found that the most perversive of all is the notion of evolutionary progress that has led many researchers to envision hypogean fishes as prime examples of regressive evolution. I propose that the utilization of hypogean fishes for the study of convergent evolution should catapult these subjects of research into prime objects of evolutionary ideas.     

Ecotone delimitation: Epigean–hypogean transition in cave ecosystems

Abstract The ecotone zone between epigean and hypogean environments has been delimited for two limestone caves using a new method proposed herein. The richness and the diversity of the ecotone, epigean and hypogean environments and their similarities have also been determined. The ecotones were delimited using a similarity matrix between the inner and outer sectors of each cave. The ecotone of Dona Rita's cave was estimated to be 12 m long and the ecotone of Retiro's cave 16 m. The richness (S) of arthropods in Dona Rita's cave was higher in the ecotone (S = 131), intermediate in the epigean environment (S = 75) and lower in the hypogean system (S = 45). The invertebrate diversity (H′) was lower in the hypogean environment (H′ = 2.89) and not statistically different between the epigean environment and the ecotone (H′ = 3.56 and H′ = 3.76, respectively). The richness in Retiro's cave was higher in the ecotone (S = 86), intermediate in the epigean environment (S = 39) and lower in the hypogean system (S = 12). The invertebrate diversity was lower in the hypogean environment (H′ = 0.48), intermediate in the ecotone (H′ = 3.02) and higher in the epigean region (H′ = 3.29). Species migration patterns, differential environmental barriers and determination of accidental versus trogloxenes/troglophylous species are topics that are primarily approached by establishing ecotone zones in caves. The aim of the present paper is to establish the delimitation of theses zones.     

Life on the edge: hydrogen sulfide and the fish communities of a Mexican cave and surrounding waters

Most eucaryotic organisms classified as living in an extreme habitat are invertebrates. Here we report of a fish living in a Mexican cave (Cueva del Azufre) that is rich in highly toxic H₂S. We compared the water chemistry and fish communities of the cave and several nearby surface streams. Our study revealed high concentrations of H₂S in the cave and its outflow (El Azufre). The concentrations of H₂S reach more than 300 μM inside the cave, which are acutely toxic for most fishes. In both sulfidic habitats, the diversity of fishes was heavily reduced, and Poecilia mexicana was the dominant species indicating that the presence of H₂S has an all-or-none effect, permitting only few species to survive in sulfidic habitats. Compared to habitats without H₂S, P. mexicana from the cave and the outflow have a significantly lower body condition. Although there are microhabitats with varying concentrations of H₂S within the cave, we could not find a higher fish density in areas with lower concentrations of H₂S. We discuss that P. mexicana is one of the few extremophile vertebrates. Our study supports the idea that extreme habitats lead to an impoverished species diversity.     

A review of conservation status of freshwater fish diversity in China

China harbors a high species diversity of freshwater fishes not shared with any of its neighboring nations. Freshwater fish diversity in the country has been under severe threat from human activities over the past decades, thus conservation freshwater fishes and ecosystems is urgently needed. To accumulate baseline data for guiding protection actions, the third red list assessment of Chinese freshwater fishes was carried out. Among Chinese freshwater fishes assessed, there are 355 at-risk species (22.3% of the total), including 69 ranked as Critically Endangered, 97 as Endangered, and 189 as Vulnerable. Two species are classified as Extinct and one as Regionally Extinct. China's threat level seems to be lower than the known average level found in the IUCN's global assessment of freshwater fishes, but this is an artifact of a high rate of species classified as Data Deficient. Conservation of freshwater fishes is presently facing a grim situation in China. Imperilment of Chinese freshwater fishes is primarily attributed to habitat loss and degradation arising from human perturbations, particularly river damming. Despite the adoption of protected areas setting up, captive breeding and release, and a fishing moratorium, conservation efforts for freshwater fishes are compromised by disproportional attention in China's biodiversity conservation, baseline data deficiency, insufficiently designed protection networks, and inefficient or inadequate implementation of conservation strategies. To achieve the objectives of Chinese freshwater fish conservation, it is proposed to conduct a national-scale survey of fish diversity and reassess their at-risk status, develop systematic conservation planning of freshwater fish diversity and ecosystems, prioritize strategies for protected areas development, perform genetic-based captive breeding for releasing in concert with other protection actions, and implement flexible fishing moratorium strategies in different water bodies.     

Parallel evolution leads to reduced shoaling behavior in two cave dwelling populations of Atlantic mollies (<Emphasis Type="Italic">Poecilia mexicana</Emphasis>, Poeciliidae,Teleostei)

Shoaling behavior protects fishes from avian and piscine predation, but at the same time costs of group living arise due to several mechanisms including increased food competition. Most cave fishes live in an environment in which avian and piscine predators are lacking, and cave environments are often characterized by low food availability, leading to increased food competition. Altogether, this should favor the reduction of shoaling in cave fishes. We compared shoaling behavior (i.e. the tendency to associate with a stimulus shoal) among surface dwelling populations of the Atlantic molly, Poecilia mexicana, and two cave forms of that species. The first cave population of P. mexicana originated from the Cueva del Azufre and was previously recognized as the only cave form of a poeciliid fish. The second cave population examined came from a cave that was discovered only recently (Cueva Luna Azufre). In both cave forms shoaling behavior was reduced compared with surface dwelling mollies.     

长江口中华鲟自然保护区底层鱼类的群落结构特征

根据2004年8月、11月和2005年2月(Ⅰ年度)、2005年8月、11月和2006年2月、5月(Ⅱ年度)、2007年8月、11月和2008年2月和5月(Ⅲ年度)对长江口中华鲟自然保护区15个站位点的底拖网调查数据,对该水域的底层鱼类群落结构特征及时间和空间变化规律进行了分析。结果表明,调查中捕获底层鱼类42种,隶属于13目24科39属。底层鱼类的种类组成和群落结构进行聚类分析,15个站位聚合成两大类群,类群A位于南支北港和北港北沙近东滩水域,共出现20种底层鱼类,主要以淡水性和河口性鱼类为主;类群B位于北支和北港北沙近外海水域,共出现鱼类39种,主要以河口性和海洋性鱼类为主。ANOSIM和SIMPER分析表明底层鱼类群落结构不同季节间差异显著,造成这种趋势的主要原因可能是与棘头梅童鱼(Collichthys lucidus)和凤鲚(Coilia mystus)的繁殖和索饵洄游有关。     

Phototactic response and light sensitivity in an epigean and a hypogean population of a barb (Garra barreimiae, Cyprinidae)

We investigated the response of two populations of the barb Garra barreimiae to different light intensities (0.5–2000 lx) from a light source. Adults of both the surface (epigean) and cave (hypogean) G. barreimiae populations show photophobic behavior. A photophobic response in the cave form was seen only at higher light intensities because the cavefish are eyeless and rely on extra-retinal light receptors to detect light. In contrast, juveniles (surface and cave) showed photophilic behavior, and their preference for the photic zone of the test tank decreased with increasing age. We discuss the potential role played by photophobic behavior for the colonization of caves by previously surface-dwelling fishes.     

贵州荔波发现弱须洞鳅

洞鳅属（Troglonectes Zhang, Zhao & Tang 2016）鱼类为中国特有的小型洞穴淡水鱼类,主要分布在贵州和广西喀斯特地区的地下河流中。2018至2019年在贵州省荔波县境内进行洞穴生物多样性调查时采集到4号洞鳅属标本,经过形态比较,与弱须洞鳅（Troglonectes barbatus）相似;基于线粒体16S rRNA和Cyt b重建的系统发育树及遗传距离分析显示,4号洞鳅属标本与来自模式产地的弱须洞鳅高度支持聚为一支;利用Kimura双参数模型计算基于16S rRNA和Cyt b的遗传距离,这些标本与弱须洞鳅之间的遗传距离分别为0.4%和0.2%,小于洞鳅属物种之间的遗传距离（16S rRNA遗传距离为2.4%,Cyt b遗传距离为6.1%）。本次研究使用16S rRNA和Cyt b分子标记研究洞鳅属部分物种的系统发育关系和遗传距离。综合形态和分子系统发育分析结果,确定采集自贵州省荔波县小七孔景区的4号标本为隶属于鲤形目条鳅科洞鳅属的弱须洞鳅,系贵州省洞穴鱼类新记录种。     

Fish Assemblages of Mediterranean Marine Caves

Fish assemblages associated with 14 marine caves and adjacent external rocky reefs were investigated at four Marine Protected Areas (MPAs) along the coasts of Italy. Within the caves sampling was carried out in different sub-habitats: walls, ceilings, bottoms and ends of caves. On the whole, 38 species were recorded inside the 14 caves investigated. Eighteen species were exclusively found inside the caves: they were mainly represented by speleophilic (i.e. species preferentially or exclusively inhabiting caves) gobids (e.g. Didogobius splechtnai) and nocturnal species (e.g. Conger conger). Forty-one species were censused outside, 20 of which were shared with cave habitats. Apogon imberbis was the most common fish found in all 14 caves investigated, followed by Thorogobius ephippiatus (recorded in 13 caves), and Diplodus vulgaris and Scorpaena notata (both censused in 12 caves). Distinct fish assemblages were found between external rocky reefs and the different cave sub-habitats. New data on the distribution of some speleophilic gobids were collected, showing the existence of a pool of species shared by marine caves on a large scale (i.e. hundreds of km). Considering the uniqueness of cave fishes (18 exclusive species and different assemblage structures), the inclusion of marine caves among the habitats routinely investigated for fish biodiversity monitoring could facilitate the achievement of more comprehensive inventories. Due to their contribution to local species diversity and the shelter they provide to species valuable for conservation, marine caves should be prioritized for their inclusion not only within future MPAs through the Mediterranean Sea, but also into larger management spatial planning.     

Neutrale Mutationen und evolutionäre Fortentwicklung

Neutral mutation and evolutionary progress The process and causes of regressive evolution are still under debate. Contrary to DARWIN'S original assumption, Neo-Darwinian proponents make selection responsible for reduction. Biologically functionless structures like eye and pigmentation in cave animals deliver excellent material to study this problem. Comparison of regressive (eye, pigmentation, aggression, dorsal light reaction) and constructive traits (gustatory equipment, egg yolk content, feeding behavior) in epigean and cave fish (Astyanax fasciatus, Characidae) reveal a high variability of the regressive features in the cave forms. Contrary to this, the constructive traits are characterized by a low variability in epigean and cave fish. This difference is attributed to the lack of selection on regressive structures. The existence of an intermediate cave population between epigean and true cave fish of A. fasciatus makes possible the study of evolutionary rates. It is shown that the regressive traits do not evolve more quickly than the constructive ones do. On the contrary, constructive traits like egg yolk content are even more rapid because they are of great biological value in the cave biotope. Especially energy economy is claimed by Neo-Darwinists to play a decisive role as a selective force. Comparison of the development of epi- and hypogean larvae of A. fasciatus shows that the formation of a smaller and less differentiated eye in the cave specimens has no effect on body growth. Furthermore, even behavioral traits like aggressiveness, schooling, dorsal light reaction, or negative phototaxis, which all are not performed in darkness by the epigean ancestor, become genetically reduced in the cave fish. The principles of regressive evolution, loss of selection and increase in variability, play a central role in evolution in general. When biota with empty niches are colonized, stabilizing selection relaxes from the special adaptations to the niche inhabited before by the invading species. Variability may arise in these and is permitted as long as fitness is guaranteed. Such processes characterize adaptive radiation. Examples are given by the species flocks on isolated islands or in chemically abnormal lakes like those of the East African Rift Valley. Only secondarily, on the basis of the arisen variability, does directional selection promote the newly developing species into different niches. The loss of stabilizing selection is an important factor for the evolutionary process to be open for evolutionary progress.