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.     

Ecology of Subterranean Fishes: An Overview

A synthesis of ecological data available for subterranean fishes throughout the world is presented, and comparatively analyzed in an evolutionary context. Methods of ecological research are described, and their potential and limitations for the study of hypogean fishes are discussed. Ecology of troglobitic (exclusively subterranean) fishes is discussed with focus on distribution areas, population densities and sizes, use of habitat and movements, life cycle and feeding. When data are available, these species are compared with their epigean relatives. Putative ecological autapomorphies of troglobitic fishes, including habitat change, adaptations to cope with food scarcity, and precocial lifestyles, are interpreted in ecological and evolutionary contexts. Species interactions among subterranean species, including cases of syntopy and predation are briefly analyzed. Non-troglobitic hypogean fishes, with their ecological importance and evolutionary role, are also addressed. Problems of classification of subterranean fishes according to the Schiner-Racovitza system (troglobites, troglophiles and trogloxenes) are discussed, and a scenario of evolution of subterranean populations is presented.     

Venom evolution widespread in fishes: a phylogenetic road map for the bioprospecting of piscine venoms

Knowledge of evolutionary relationships or phylogeny allows for effective predictions about the unstudied characteristics of species. These include the presence and biological activity of an organism's venoms. To date, most venom bioprospecting has focused on snakes, resulting in six stroke and cancer treatment drugs that are nearing U.S. Food and Drug Administration review. Fishes, however, with thousands of venoms, represent an untapped resource of natural products. The first step involved in the efficient bioprospecting of these compounds is a phylogeny of venomous fishes. Here, we show the results of such an analysis and provide the first explicit suborder-level phylogeny for spiny-rayed fishes. The results, based on approximately 1.1 million aligned base pairs, suggest that, in contrast to previous estimates of 200 venomous fishes, >1,200 fishes in 12 clades should be presumed venomous. This assertion was corroborated by a detailed anatomical study examining potentially venomous structures in >100 species. The results of these studies not only alter our view of the diversity of venomous fishes, now representing >50% of venomous vertebrates, but also provide the predictive phylogeny or "road map" for the efficient search for potential pharmacological agents or physiological tools from the unexplored fish venoms.     

Checklist of the helminth parasites of vertebrates in Costa Rica

Helminth parasites of vertebrates have been studied in Costa Rica for more than 50 years. Survey work on this group of parasites is far from complete. We assembled a database with all the records of helminth parasites of wild and domestic vertebrates in Costa Rica. Information was obtained from different sources such as literature search (all published accounts) and parasite collections. Here we present a checklist with a parasite-host list as well as a host-parasite list. Up to now, 303 species have been recorded, including 81 species of digeneans, 23 monogeneans, 63 cestodes, 12 acanthocephalans, and 124 nematodes. In total, 108 species of vertebrates have been studied for helminths in Costa Rica (31 species of fishes, 7 amphibians, 14 reptiles, 20 birds, and 36 mammals). This represents only 3.8% of the vertebrate fauna of Costa Rica since about 2,855 species of vertebrates occur in the country. Interestingly, 58 species (19.1 %) were recorded as new species from Costa Rica and most of them are endemic to particular regions. Considering the valuable information that parasites provide because it is synergistic with all the information about the natural history of the hosts, helminth parasites of vertebrates in Costa Rica should be considered within any initiatives to accomplish the national inventory of biological resources. Starting with this compilation work, the Colección de Helmintos de Costa Rica (CHCR), hosted at the Facultad de Microbiología, Universidad de Costa Rica, has re-emerged and it is our hope that it will have the standards of quality to assure that it will become the national depository of helminths in the country.     

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.     

Discovering Hidden Diversity of Characins (Teleostei: Characiformes) in Ecuador’s Yasuní National Park

Background

Management and conservation of biodiversity requires adequate species inventories. The Yasuní National Park is one of the most diverse regions on Earth and recent studies of terrestrial vertebrates, based on genetic evidence, have shown high levels of cryptic and undescribed diversity. Few genetic studies have been carried out in freshwater fishes from western Amazonia. Thus, in contrast with terrestrial vertebrates, their content of cryptic diversity remains unknown. In this study, we carried out genetic and morphological analyses on characin fishes at Yasuní National Park, in eastern Ecuador. Our goal was to identify cryptic diversity among one of the most speciose fish families in the Amazon region. This is the first time that genetic evidence has been used to assess the species content of the Napo Basin, one of the richest regions in vertebrate diversity.

Results

Phylogenetic analyses of partial mitochondrial 16S ribosomal RNA gene (∼600 pb) DNA sequences from 232 specimens of the family Characidae and its closest groups revealed eight candidate new species among 33 species sampled, representing a 24% increase in species number. Analyses of external morphology allowed us to confirm the species status of six of the candidate species.

Conclusions

Our results show high levels of cryptic diversity in Amazonian characins. If this group is representative of other Amazonian fish, our results would imply that the species richness of the Amazonian ichthyofauna is highly underestimated. Molecular methods are a necessary tool to obtain more realistic inventories of Neotropical freshwater fishes.     

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.     

The influence of translational selection on codon usage in fishes from the family Cyprinidae

In this paper, the main factors shaping codon usage in three species of fishes that belong to the family Cyprinidae (namely Brachidanio rerio, Cyprinus carpio, and Carassius auratus) are reported. Correspondence analysis (COA), a commonly used multivariate statistical approach, was used to analyze codon usage bias. Our results show that the main trend is strongly correlated with the GC(3) content at silent sites of each sequence. On the other hand, the second axis discriminates between presumed highly and lowly expressed genes, a result that is confirmed by the distribution of matching expressed sequence tags (ESTs) along that axis. Translational selection appears, therefore, to influence synonymous codon usage in these fishes. The comparison of codon usages of the sequences displaying the extreme values on the second axis indicates that several codons are significantly incremented among the heavily expressed sequences. Interestingly, several of these triplets are not only shared by the three fishes but also by Xenopus laevis, another cold-blooded vertebrate in which translational selection influences codon choices. We postulate that natural selection was operative for codon usage in the last common ancestor of these fishes and Xenopus, and will probably be detected in cold-blooded vertebrates in general. Finally, we raise the possibility that the same phenomena will be found among warm-blooded vertebrates.     

A novel sperm adaptation to evolutionary constraints on reproduction: Pre‐ejaculatory sperm activation in the beach spawning capelin (Osmeridae)

Reproduction of external fertilizing vertebrates is typically constrained to either fresh or salt water, not both. For all studied amphibians and fishes, this constraint includes immotile sperm that are activated after ejaculation only by the specific chemistry of the fertilizing medium in which the species evolved (fresh, brackish, or salt water). No amphibians can reproduce in the sea. Although diadromous fishes may migrate between salt and fresh water, they are shackled to their natal environment for spawning in part because of sperm activation. Here, we report for the first time among all documented external fertilizing vertebrates, that in the absence of any external media, sperm are motile at ejaculation in a marine spawning fish (Osmeridae, capelin, Mallotus villosus). To illuminate why, we evaluated sperm behavior at different salinities in M. villosus as well as the related freshwater spawning anadromous rainbow smelt (Osmerus mordax). Surprisingly, sperm performance was superior in fresh water for both species. M. villosus spend their entire life at sea but our results show that their sperm are deactivated by sea water, suggesting a freshwater ancestry. By circumventing constraining water chemistry, we interpret the unique pre‐ejaculatory sperm activation in this species as a novel adaptation that enables fertilization in the marine environment. These findings also contribute to understanding the persistence of anadromy, despite great energetic costs to adult fishes.     

Addendum to the checklist of the helminth parasites of vertebrates in Costa Rica

In this work, we present an addendum to the "Checklist of the helminth parasites of vertebrates in Costa Rica" with a parasite-host list as well as a host-parasite list. This addendum updates the available information on this group of parasites in Costa Rica, since very recently a new input has been made to describe the helminth fauna of vertebrates, particularly at the Area de Conservación de Guanacaste. In this paper, we add 33 records, representing 23 species. This raises the number of helminth species described in vertebrates from Costa Rica to 325, represented by 89 species of digeneans, 23 of monogeneans. 63 of cestodes, 13 of acanthocephalans, and 137 of nematodes. In total, 133 species of vertebrates have been studied for helminths in Costa Rica (31 species of fishes. 7 amphibians, 18 reptiles, 40 birds, and 37 mammals). Currently, 67 species (20.6 %) have been recorded as new species from Costa Rica and most of them are endemic to particular regions. The Colecci6n de Helmintos de Costa Rica, housed at the Universidad de Costa Rica (UCR), San José, is the depositary of only 23% of the species recorded so far; however this situation is changing and people recognizes.     

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.     

Have fishes had their chips? The dilemma of threatened fishes

Synopsis The conservation status and factors threatening fishes worldwide are reviewed in order to introduce a series of one-page articles on Threatened fishes of the world, and to encourage the incorporation of information on threatened fishes into international conservation programmes. Information on fish extinction and threat rates are compared with those of other animal groups, and the unique characteristics of fish conservation problems are highlighted. At present 979 species of fishes are listed as threatened in the IUCN Red List and at least 36 species and three subspecies are listed as recently extinct. It is argued that these figures are probably gross underestimates and that they may mislead conservation authorities and resource users about the seriousness of the situation. Freshwater fishes may be the most threatened group of vertebrates after the Amphibia. Urgent action is required to save many narrowly endemic, stenotopic species from extinction, especially in Africa, Asia and South America. The conservation of common species that drive essential ecological processes is also important. Anthropogenic pressures, especially habitat degradation, the introduction of invasive species and pollution, on inland and coastal waters are particularly severe and many major fish communities are threatened with elimination throughout the world. The conservation of marine fishes is complicated by the fact that it is difficult to ascertain their rarity. The importance of the retention of genetic variation is highlighted, and both orthodox and innovative conservation measures are encouraged. Further research on minimum viable populations, genetics, and the factors that cause fishes to become vulnerable to extinction, is urgently required.Invited editorial     

Neural and hormonal mechanisms of reproductive-related arousal in fishes

The major classes of chemicals and brain pathways involved in sexual arousal in mammals are well studied and are thought to be of an ancient, evolutionarily conserved origin. Here we discuss what is known of these neurochemicals and brain circuits in fishes, the oldest and most species-rich group of vertebrates from which tetrapods arose over 350 million years ago. Highlighted are case studies in vocal species where well-delineated sensory and motor pathways underlying reproductive-related behaviors illustrate the diversity and evolution of brain mechanisms driving sexual motivation between (and within) sexes. Also discussed are evolutionary insights from the neurobiology and reproductive behavior of elasmobranch fishes, the most ancient lineage of jawed vertebrates, which are remarkably similar in their reproductive biology to terrestrial mammals.     

新疆阿勒泰地区额尔齐斯河和乌伦古河流域鱼类多样性演变和流域健康评价

为了解阿勒泰地区额尔齐斯河和乌伦古河流域的鱼类多样性现状和历史演变, 本研究于2013-2016年间在该流域的鱼类多样性进行了连续调查, 并结合历史资料和标本, 以Margalef丰富度指数、Shannon-Wiener多样性指数、Pielou均匀度指数分析评估了流域内鱼类的多样性水平和时空变化。该流域历史上分布有土著鱼类23种, 当前记录到19种, 流域内还有外来鱼类15种。阿勒泰鱼类的区系组成以鲤科种类为主, 其中特有和珍稀濒危物种占比高, 具有重要的保护价值。多样性指数计算结果显示, 2013-2016年鱼类多样性情况整体稳定, 额尔齐斯河鱼类物种数多于乌伦古河。研究还基于鱼类生物完整性指数(Fish Index of Biological Integrity, F-IBI)对34个采集点的河流健康状况进行了评价, 结果显示额尔齐斯河流域大多数调查点的健康状况处于“亚健康”或“一般”水平, 乌伦古河流域多数调查点的健康状况处于“健康”水平。水利工程、外来物种、过度捕捞是影响阿勒泰地区鱼类多样性的重要因素。未来应通过水利工程的联合调度、下泄合理生态流量、布设鱼类通道、规范养殖渔业、严控外来物种、本地土著鱼类的人工增殖放流, 以及合理的就地保护措施对阿勒泰地区的鱼类多样性加以保护, 提升水体健康程度。     

Maximal thermogenic capacity and non-shivering thermogenesis in the South American subterranean rodent Ctenomys talarum

Subterranean rodents inhabit closed tunnel systems that are hypoxic and hypercapnic and buffer aboveground ambient temperature. In contrast to other strictly subterranean rodents, Ctenomys talarum exhibits activity on the surface during foraging and dispersion and hence, is exposed also to the aboveground environment. In this context, this species is a valuable model to explore how the interplay between underground and aboveground use affects the relationship among basal metabolic rate (BMR), cold-induced maximum metabolic rate (MMR), shivering (ST), and non-shivering thermogenesis (NST). In this work, we provide the first evidence of the presence of NST, including the expression of uncoupling proteins in brown adipose tissue (BAT), and shivering thermogenesis in Ctenomys talarum, a species belonging to the most numerous subterranean genus, endemic to South America. Our results show no differences in BMR, cold-induced MMR, and NST between cold- (15?°C) and warm- (25?°C) acclimated individuals. Furthermore, thermal acclimation had no effect on the expression of mitochondrial uncoupling protein 1 (UCP1) in BAT. Only cytochrome c oxidase (COX) content and activity increased during cold acclimation. When interscapular BAT was removed, NST decreased more than 30?%, whereas cold-induced MMR remained unchanged. All together, these data suggest that cold-induced MMR reaches a maximum in warm-acclimated individuals and so a probable ceiling in NST and UCP1 expression in BAT. Possible thermogenic mechanisms explaining the increase in the oxidative capacity, mediated by COX in BAT of cold-acclimated individuals and the role of ST in subterranean life habits are proposed.     

A subterranean generalist predator: diet of the soil-dwelling caecilian Gegeneophis ramaswamii (Amphibia; Gymnophiona; Caeciliidae) in southern India

Biologists have paid relatively little attention to subterranean predators, especially their ecology. Although diets of some subterranean lower vertebrates suggest specialisation, there remains a lack of quantitative data. The diet of the caecilian amphibian Gegeneophis ramaswamii was investigated through analyses of gut contents of 67 specimens collected in randomised surveys at three localities in Kerala, southern India, in early and mid-monsoon. Although termites were the most frequently ingested items in the mid-monsoon, the specialist predator hypothesis was rejected because of differences in diet found in early monsoon samples, when earthworms contributed the greatest mass. That guts of some G. ramaswamii contained many individuals of only a single dietary taxon was interpreted as feeding on patchily distributed prey rather than specialisation. No ontogenetic differences in diet were apparent, but more sampling is required to investigate this further. Subadults largely feed on fewer items of the same prey as adults, though there is an indication that subadult diet is less diverse. The data do not support differences between male and female diet. High densities of G. ramaswamii, and perhaps of other terrestrial caecilians and subterranean lower vertebrates feeding on soil-ecosystem engineers (termites, earthworms and ants), might substantially impact soil ecology.     

A compact cartilaginous fish model genome

The genomes of several vertebrates, including six mammals, the chicken, Xenopus and four ray-finned fishes have been sequenced or are currently being sequenced to provide a better understanding of the human genome through comparative analysis. However, this list does not include cartilaginous fishes, which are the most basal living jawed vertebrates [1]. The genomes of the current ‘popular’ cartilaginous fishes such as the nurse shark, dogfish, and horn shark are larger than the human genome (∼3800 Mb to 7000 Mb) [2], and are not attractive for whole-genome sequencing. Here, we report the characterization of the relatively small genome (1200 Mb) of a cartilaginous fish, the elephant fish (Callorhinchus milii), and propose it as a model for whole-genome sequencing.     

Ecological studies on crater lakes in West Cameroon Lakes Kotto and Mboandong

Lake Kotto is a shallow crater lake, sometimes weakly stratified, and with a dense phytoplankton dominated by blue-green algae. The ecology of Lake Kotto and the similar, smaller lake Mboandong is described in relation to the feeding biology of their fishes. Of the five species of cichlids in Lake Kotto only one is endemic. Two are phytoplankton-feeders, one takes invertebrates as well as phytoplankton, one feeds mainly on chironomid larvae, and one preys on vertebrates as well as on invertebrates. The three phytoplanktivores are the main species eaten by man. One species of Clarias and one of Barbus also occur in Lake Kotto; and in the associated streams are four species of cyprinodont fishes. The fish fauna of Mboandong consists of three species of cichlids and two cyprinodonts, all known from the Kotto system. We contrast Lake Kotto with the oligotrophic lake Barombi Mbo, and conclude that Lake Kotto would probably be less sensitive to human interference than would Barombi Mbo.