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.     

Locomotory,ventilatory and metabolic responses of the subterranean Stenasellus virei (Crustacea,Isopoda) to severe hypoxia and subsequent recovery

The locomotory and ventilatory activities and the intermediary and energy metabolism modifications of the hypogean aquatic isopod crustacean Stenasellus virei were investigated in severe hypoxia (Po₂ < 0.03 kPa) and subsequent recovery. The aims of this study were i) to determine why the subterranean species displayed a greater tolerance of hypoxia than numerous other epigean crustaceans, ii) to confirm previous results obtained with four hypogean and epigean crustaceans, iii) to compare the responses to severe hypoxia in hypogean amphipods and isopods, and iv) to better understand the ecological problems of the hypogean organisms survival in subterranean habitats. S. virei responded to experimental long-term, severe hypoxia with classical anaerobic metabolism mainly characterized by a decrease in adenosine triphosphate (ATP) and phosphagen, utilization of glycogen and glutamate, and accumulation of lactate and alanine. Lactate was also largely excreted by this organism, which is unusual for crustaceans in general. Compared to most other epigean crustaceans, the isopod S. virei showed high amounts of stored glycogen and arginine phosphate. These differences in glycogen and phosphagen stores, and the ability to reduce energetic expenditures linked to locomotion and ventilation, extended the survival of S. virei under experimental anaerobiosis. During recovery, the isopod S. virei showed a higher capacity for glyconeogenesis from lactate and a faster and total replenishment of ATP and arginine phosphate levels than epigean crustaceans. Data concerning responses to hypoxia and subsequent recovery in S. virei are similar to those previously obtained with two other hypogean amphipods, except that this isopod did not synthesize succinate in anaerobiosis.     

Selection of physiological and metabolic adaptations to food deprivation in the Pyrenean newt Calotriton asper during cave colonisation

Food restriction is one of the major and most common constraints that subterranean animals face in their biotope. Cave-dwelling organisms thus have to cope with fasting periods that can extend from a month to a year. However, adaptive fasting resistance previously found in subterranean fauna has only been highlighted by direct comparisons with phylogenetically distant epigean organisms, which could severely impact conclusions. Here we report physiological and metabolic responses to 42 days of fasting followed by 10 days of refeeding in two populations (one subterranean and one epigean) of Calotriton asper. In the fed state (control), the hypogean population exhibited a hypometabolism together with higher glycogen (+ 25% in liver and muscles) and triglyceride stores (+ 50% in muscles). During the fasting period, cave individuals exhibited a 20% decrease in VO₂ whereas epigean individuals experienced no significant change. In addition, the energetic reserves always remained higher in the hypogean population. According to phylogenic and biogeographic data, cave colonization by this species dates back to less than 10,000 years, suggesting a rapid selection of adaptive traits related to fasting. This study strongly suggests that cave colonization induces a decrease in metabolism together with a higher capacity to accumulate energy reserves and therefore to withstand unpredictable fasting periods.     

Effect of fasting on hypogean (<Emphasis Type="Italic">Niphargus stygius</Emphasis>) and epigean (<Emphasis Type="Italic">Gammarus fossarum</Emphasis>) amphipods: a laboratory study

Two amphipods, the hypogean Niphargus stygius and epigean Gammarus fossarum, were analyzed for fatty acid (FA) composition, electron transport system (ETS) activity and respiration (R) during a laboratory fasting experiment. In agreement with ETS and R measurements (and the ETS/R ratio), the hypogean N. stygius utilized FA more slowly than the epigean G. fossarum. Inter-specific differences in the utilization of certain FA during fasting were also revealed. While N. stygius tended to preserve all of its FA during the experimental fasting period, G. fossarum showed a tendency to utilize MUFA (monounsaturated FA) and SAFA (saturated FA) and preferentially retain PUFA (polyunsaturated FA). The significant correlations between ETS activity and composition of specific FA during fasting can be linked to R. During the fasting, both ETS activity and respiration rate of G. fossarum decreased, however, ETS/R ratio increased. In contrast, N. stygius did not show significant changes in these parameters. This is the first report, which connects ETS activity with changes in concentrations of specific FA during fasting. Such evolutionary adaptations of hypogean species enables them to better survive chronically low and/or discontinuous food supplies compared to epigean species, which live in environments where food shortages are much less frequent.     

Regional Risk Assessment of a Brazilian Rain Forest Reserve

The objective of this study was to identify subareas inside and near an Atlantic Rain Forest reserve, the Parque Estadual Turístico do Alto Ribeira (PETAR), most likely to be affected by land use in the vicinity of the area. In addition, the study aimed to compare risks per stressor source (agriculture, human settlements and mining) to both epigean (surface) and hypogean (subterranean) aquatic fauna. The methodological approach included the relative vulnerability of endpoints to the stressors (pesticides, metals, nutrients, and particles) and ranking of stressor sources and habitats (epigean and hypogean streams) based on their relative distribution in 14 subareas within the catchment areas of the main rivers that cross PETAR: Pilões, Betari and Iporanga. Four subareas presented high risk for both epigean and hypogean fauna. Three of those areas were located inside the Betari catchment area, where most of the settlements and abandoned lead mines are located. The fourth area was situated in the headwaters of the Pilões River, where agricultural activities are intense. Agriculture and human settlements were the activities most likely to cause impacts on aquatic ecosystems. Uses of risk assessment results include management of the PETAR and communication to stakeholders by the Park Administration.     

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.     

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.     

Morphology and reproduction of the cavefish Trichomycterus chaberti and the related epigean Trichomycterus cf. barbouri

Hypogean and epigean populations of Trichomycterus catfishes inhabit streams from different environments (cave, headwater, canyon and valley) in the Torotoro National Park in the Andes, Bolivia. A significant reduction in the diameter of the eyes and in the surface area of the mesencephalon was observed in subterranean populations, along with an increase in the surface area of the telencephalon. Contrary to expectations, the barbel did not appear to be longer in hypogean populations. The observed pattern of modification of the other variables (pigmentation, eye asymmetry, surface area of the cerebellum and rhombencephalon, fecundity and egg diameter) corresponded to a gradient of values from valley to canyon, headwater and subterranean populations. This result argues not for a simple distinction between epigean and hypogean populations but for an adaptation to an environmental gradient of constraints in which caves correspond to an extreme situation.     

Metabolic rates of a hypogean and an epigean species of copepod in an alluvial aquifer

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Electron transport system activity and oxygen consumption of two amphibious isopods,epigean Ligia italica Fabricius and hypogean Titanethes albus (Koch), in air and water

Electron transport system (ETS) activity and oxygen consumption (i.e. respiration, R) were measured in two amphibious isopods, epigean Ligia italica and hypogean Titanethes albus. The measurements were made in air and in water to estimate the exploitation of metabolic potential for actual metabolism in the two media. Oxygen consumption was measured in animals in air before their transfer to water, in water and again after their transfer back to air. Both species showed greater oxygen consumption during submergence in water than in air. Although epigean L. italica had higher oxygen consumption and ETS activity than hypogean T. albus, both species exhibited high and variable ETS/R ratios. A high and variable ETS/R ratio is one of the characteristics of amphibious isopods that enables them to cope with specific environmental conditions in their habitats.     

Temporal Organization in Locomotor Activity of the Hypogean Loach, Nemacheilus Evezardi, and its Epigean Ancestor

Locomotor activity rhythm in the hypogean population of Nemacheilus evezardi was recorded first under light-to-dark (LD) 12 : 12 h cycle and then DD. The results were compared with that of its epigean counterpart held under comparable regimes. In LD 12 : 12, while hypogean loach exhibited a distinct bimodality in its locomotor activity rhythm, it was altogether absent in the case of epigean population. In hypogean loach, dark-to-light transition peak in LD was observed to free-run under DD. The same was not discernible in case of epigean loach. The locomotor activity rhythm in epigean fish was noticed to free-run in DD either from the dawn peak or dusk peak in LD. It is hypothesized that the hypogean fish still possesses a functional oscillator underlying its overt circadian rhythm in locomotor activity. The ecophysiological significance of these findings is yet to be fully understood.     

Pattern and process in the biogeography of subterranean amphipods

The comparative data from studies of two ‘superfamily’ groups with large numbers of subterranean taxa, the exclusively freshwater Crangonyctoidea and the predominately marine Hadzioidea, support the hypothesis that distributional patterns and evolutionary processes of stygobiont amphipods are closely linked and that the former can be a useful indicator of the latter. Three major biogeographic patterns are indicated by the distribution of subterranean species in these groups, each apparently reflecting a particular mode of origin: (1) freshwater stygobionts (limnostygobionts) derived from epigean freshwater ancestors through colonizations probably influenced by adaptive shifts, or assisted by stream capture and spring failure; (2) freshwater stygobionts derived from marine/brackish water ancestors by stranding during regression of marine embayments; and (3) marine/brackish water stygobionts (thalassostygobionts) derived from epigean marine/brackish water ancestors through adaptive shifts possibly in concert with fluctuating sea levels.     

Is the reduced metabolism of hypogean amphipods solely a result of food limitation?

The epigean amphipod Gammarus lacustris possessed a rate of oxygen uptake (MO2) three times greater that of the hypogean amphipod Stygobromus sp. While much of the difference between these two species could be attributed to different feeding regimes, the hypogean amphipod still exhibited a lower rate of metabolism than the epigean species. This suggests that there can be both a genetic and an environmental (reduced food availability and/or hypoxia) component to the reduced metabolism characteristic of many hypogean animals. The results of this study have re-emphasised the pitfall of making species comparisons without knowledge of the extent of physiological variation within a species. This revised version was published online in July 2006 with corrections to the Cover Date.     

Behavioural, ventilatory and respiratory responses of epigean and hypogean crustaceans to different temperatures

Impact of temperature (from -2 to 28 degrees C) on survival, oxygen consumption, locomotory and ventilatory activities was measured in two aquatic subterranean crustaceans (Niphargus rhenorhodanensis and Niphargus virei) and in a morphologically close surface-dwelling crustacean (Gammarus fossarum). The hypogean N. virei presented all characteristics of a stenothermal organism: it showed small thermal plasticity and optimised its performance on a narrow range of temperature. In contrast, the epigean G. fossarum and more surprisingly the hypogean N. rhenorodanensis can be both characterized as eurythermal organisms: they exhibited important survival times and conserved their performance optimum throughout a large range of temperature. Such differences of survival and performance patterns in two hypogean organisms were unexpected since they both live in very thermally buffered biotopes. Our data suggest fresh hypotheses about the role of glaciations in the history and adaptation of hypogean crustaceans.     

Delimiting species by reproductive isolation: the genetic structure of epigean and hypogean <Emphasis Type="Italic">Trichomycterus </Emphasis>spp. (Teleostei,Siluriformes) in the restricted area of Torotoro (Upper Amazon,Bolivia)

Genetic variability of Trichomycterus from the region of Torotoro (Bolivia, Upper Amazon), distributed in the same watershed where the habitat is structured by waterfalls, canyons and a cave, was studied by allozyme (twelve putative loci) and RFLP-mtDNA (DLoop and cytochrome b) analyses. Alloenzymatic variation studied by Correspondence Analysis and Maximum Likelihood Analysis revealed a four-group structure, which was largely congruent with the distribution of the 14 mtDNA haplotypes. Two of these four clusters (I and II) were differentiated by two diagnostic loci (IDH and G3PDH), two semi-diagnostic loci (PGM and 6PGDH) and consequently a very high F_st value (estimator θ = 0.77). Therefore, clusters I and II are reproductively isolated. The distribution limit of these two (sibling) species does not correspond to those of the morphological species of Trichomycterus identified in this region: the epigean T. cf. barbouri and the hypogean T. chaberti. However, hypogean fish exhibited two mtDNA haplotypes, a private one and another shared with the epigean Trichomycterus from upstream reaches.     

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.     

Genome‐wide adaptive evolution to underground stresses in subterranean mammals: Hypoxia adaption,immunity promotion,and sensory specialization

Life underground has provided remarkable examples of adaptive evolution in subterranean mammals; however, genome‐wide adaptive evolution to underground stresses still needs further research. There are approximately 250 species of subterranean mammals across three suborders and six families. These species not only inhabit hypoxic and dark burrows but also exhibit evolved adaptation to hypoxia, cancer resistance, and specialized sensory systems, making them an excellent model of evolution. The adaptive evolution of subterranean mammals has attracted great attention and needs further study. In the present study, phylogenetic analysis of 5,853 single‐copy orthologous gene families of five subterranean mammals (Nannospalax galili, Heterocephalus glaber, Fukomys damarensis, Condylura cristata, and Chrysochloris asiatica) showed that they formed fou distinct clusters. This result is consistent with the traditional systematics of these species. Furthermore, comparison of the high‐quality genomes of these five subterranean mammalian species led to the identification of the genomic signatures of adaptive evolution. Our results show that the five subterranean mammalian did not share positively selected genes but had similar functional enrichment categories, including hypoxia tolerance, immunity promotion, and sensory specialization, which adapted to the environment of underground stresses. Moreover, variations in soil hardness, climate, and lifestyles have resulted in different molecular mechanisms of adaptation to the hypoxic environment and different degrees of visual degradation. These results provide insights into the genome‐wide adaptive evolution to underground stresses in subterranean mammals, with special focus on the characteristics of hypoxia adaption, immunity promotion, and sensory specialization response to the life underground.     

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.     

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.     

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.