Most of this diversity is located in lakes and river systems, particularly in the tropics [ 4 ]. However, other freshwater environments that often occur at small spatial scales can harbour a significant portion of biodiversity, not necessarily because of their species richness, but because of high levels of endemism.
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Many spatially restricted habitats can be considered extreme environments that are characterised by the presence of physicochemical stressors lying outside the range normally experienced by a taxon and requiring costly adaptations absent in closely related taxa for the maintenance of homeostasis [ 5 , 6 ]. Such adaptations allow some organisms to thrive in places that are lethal for most others, giving rise to unique ecological communities. Prime examples of extreme freshwater environments include subterranean streams and lakes [ 7 , 8 ], desert springs [ 9 , 10 ], Antarctic lakes [ 11 ], and environments with rampant hypoxia [ 12 ].
Extreme environments have provided excellent study systems in ecology and evolution research, as they allow elucidating the effects of physicochemical stressors at multiple levels of biological organization [ 13 , 14 ], yet patterns of biodiversity in extreme environments remain relatively understudied. Environments rich in naturally occurring hydrogen sulphide H 2 S are one form of extreme habitat found in aquatic systems throughout the world.
Because of its lipid solubility, H 2 S freely penetrates biological membranes and readily invades organisms [ 15 , 16 ]. Like cyanide, it is an inhibitor of cytochrome c oxidase and blocks electron transport in aerobic respiration, thereby hampering the function of mitochondria and the production of ATP [ 17 , 18 ]. H 2 S is also able to modify oxygen transport proteins [ 19 ] and inhibit about 20 other enzymes [ 15 ]. Consequently, H 2 S is highly toxic for aerobic organisms even in micromolar concentrations [ 16 , 20 , 21 ].
Naturally occurring H 2 S can be found in a variety of aquatic environments. It is produced in anoxic sediments of swamps, marshes, and cold seeps by bacterial metabolism of organic and inorganic carbon sources, and disturbance of sediments can result in high—but often temporally variable—H 2 S concentrations in the water column [ 22 , 23 , 24 , 25 ]. High and sustained concentrations of H 2 S can also be found in aquatic environments associated with oil deposits and geothermal activity [ 26 , 27 ].
The effects of H 2 S on biodiversity, as well as the ecology and evolution of organisms inhabiting sulphidic environments, have mostly been studied in cold seeps and deep-sea hydrothermal vents [ 28 , 29 , 30 , 31 , 32 , 33 ]. Here, we focus on patterns of macroinvertebrate and fish biodiversity in freshwater springs that discharge water rich in H 2 S.
We first qualitatively review the global occurrence of such springs and the organisms that have been able to colonize them, focusing in part on specific adaptations to sulphide-rich environments, and then provide a quantitative comparison of diversity patterns between sulphidic and adjacent non-sulphidic habitats in Southern Mexico. Freshwater springs discharging sulphide-rich waters can be found on all continents, with the exception of Antarctica see Figure 1 for an overview.
In general, the presence of sulphide is associated with either of two sources. First, sulphide springs can be associated with volcanic activity, where H 2 S from geological origins is enriched in groundwater through similar processes as those occurring in deep sea hydrothermal vents [ 34 , 35 ]. During the interaction of the water with hot basaltic rock, a diversity of chemicals leach into solution, including sulphate and other sulphur species that are readily transformed into sulphide under the highly reductive conditions [ 36 , 37 , 38 ].
Second, sulphide springs can be associated with underground oil deposits, where mineral-rich groundwater containing sulphate mixes with hydrocarbons derived from fossil organic matter in the absence of oxygen [ 39 , 40 , 41 ]. As in marine cold seeps, sulphur-reducing bacteria then reduce sulphate to H 2 S, while oxidizing organic compounds, during energy metabolism [ 22 , 42 ]. During this process, groundwater is being enriched in H 2 S and ultimately discharged through surface springs [ 40 , 43 ].
Figure 1. A Political map of the world indicating the locations of H 2 S-rich springs blue dots.
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Red dots represent sulphide springs with records of fish. Locality information was assembled by reviewing previously published literature see Table 1 and [ 35 , 40 , 41 , 44 , 45 , 46 , 47 , 48 , 49 , 50 , 51 , 52 , 53 , 54 , 55 , 56 , 57 , 58 , 59 ]. Table 1. Evolutionarily independent populations recorded from sulphide spring habitats, including specific localities and references. H 2 S concentrations found in freshwater sulphide springs can be highly variable across springs, although most springs tend to discharge relatively constant levels of H 2 S [ 78 ].
Currently available data suggest that H 2 S concentrations in most springs lie in between these extremes, with a large number of springs having concentrations towards the lower end of the spectrum i. Besides the presence of H 2 S, sulphide springs also differ from adjacent, non-sulphidic habitats in a series of other biologically relevant environmental parameters. Temperature variation appears to be related in part to the geographic location of springs as well as the ultimate sources of H 2 S production.
Sulphide springs are often also characterised by increased concentrations of bicarbonate, calcium sulphate, sodium chloride, and other ions leading to substantial increases of specific conductivity [ 39 ] , and by lower pH likely caused by the presence of sulphuric acid from chemical and bacterial H 2 S oxidation although pH reductions are dependent on the buffering capacity of the water in the region [ 57 , 76 , 82 ].
Finally, upon the discharge of sulphidic water at the surface, H 2 S spontaneously oxidizes in water, causing and aggravating hypoxic conditions in aquatic systems [ 83 , 84 ]. Consequently, environmental conditions in sulphide springs are not only toxic for most metazoans, but variation in correlated environmental parameters may also affect the acid-base balance, osmoregulation, and constrain oxygen acquisition of aquatic organisms [ 16 , 21 ].
H 2 S-rich freshwater environments Figure 2 have long captured the attention of microbiologists, because a wide variety of bacteria and archaea are associated with the natural sulphur cycle [ 85 , 86 , 87 ]. This not only includes sulphur reducing microbes, including the sulphate reducers involved in the production of H 2 S mentioned above [ 22 , 88 ], but the presence of H 2 S inevitably also supports a diversity of sulphur oxidizing bacteria [ 89 , 90 ]. The coexistence of sulphur reducers and oxidizers creates complex dynamics of sulphur cycling, where sulphate-reducing bacteria use sulphate as a terminal electron acceptor to metabolize a variety of carbon sources to produce sulphide as a by-product, which in turn is used by sulphide-oxidizing bacteria as an energy source to assimilate CO 2 and produce oxidised sulphur species as metabolic by-products [ 87 , 91 ].
Sulphur metabolizing microbes play a critical role in sulphidic ecosystems, because they contribute to primary production through chemoautotrophy [ 36 , 92 , 93 , 94 ] and can serve as a food source for consumers inhabiting sulphide springs.
Air‐Breathing Fishes: Evolution, Diversity and Adaptation
While biodiversity of microbes inhabiting sulphide-rich environments is relatively well understood at multiple levels of biological organization, few studies have addressed patterns of metazoan diversity. Figure 2. Examples of the diversity of sulphide springs inhabited by fishes. Macroinvertebrate diversity in environments with sulphurous waters has particularly been studied in hot mineral springs of Yellowstone National Park and other parts of the western United States, some of which contain elevated levels of H 2 S e.
Records from sulphide springs in other parts of the world are relatively scarce and often anecdotal. Larvae of dipterans appear to dominate sulphide-rich spring environments both in terms of diversity and abundance. Multiple families of dipterans are represented in sulphide springs, including a species of Ceratopogonidae Bezzia setulosa in Yellowstone [ 97 ], multiple species of Chironomidae [ 97 , 98 ], a species of Culicidae Culiseta incidens in springs of Western North America [ 99 ], two species of Ephydridae in California Thiomyia quatei and Yellowstone Ephydra thermophila [ 45 , 82 , 97 ], a species of Psychodidae Pericoma truncate in California [ 45 ], a species of Stratiomyidae Odontomyia cf.
Dipteran larvae are mostly found living in and feeding on bacterial mats within sulphide springs, and ephydrid and pyschodid adult flies have been observed feeding and reproducing on these mats as well [ 45 , 46 , 82 , ].
Besides dipterans, the only other insects reported from sulphide springs are trichopterans based on the presence of larval casings in Yellowstone [ ] and hemipterans of the genus Belostoma in Mexico [ ]. Finally, aquatic snails Gastropoda have also been recorded in sulphide springs. Melanoides tuberculata a livebearing snail of the family Thiaridae has been reported from a spring in Israel [ ], Physa gyrina Physidae and Helisoma trivolvis Planorbidae in Oklahoma [ 66 ], and Stagnicola palustris Lymnaeidae in Yellowstone [ 96 ].
While records for the macroinvertebrate fauna in surface sulphide springs remain fragmentary, it is important to note that such springs are also present in a variety of subterranean habitats, including the Movile Cave Romania [ 93 ], Frasassi Cave and Grotta de Fiume Coperto Italy [ , ], Villa Luz Cave Mexico [ , ], Lower Kane Cave Wyoming [ ], and the Edwards Aquifer Texas [ ].
The faunal communities of these subterranean aquatic habitats with elevated H 2 S concentrations have recently been reviewed by Summers Engel [ ]. The assembled data indicate that approximately 40 invertebrate species many of which remain to be identified or described from eight phyla inhabit H 2 S-rich waters, including members of the Oligohymenophorea, Rotifera, Platyhelminthes, Nematoda, Annelida, Mollusca, Crustacea, and Hexapoda. Most notably, some sulphidic caves — particularly Movile Cave—exhibit high levels of endemism [ 93 , ].
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It remains unclear whether differences in the reported biodiversity of surface and subterranean H 2 S-rich habitats are due to sampling bias or whether the combination of the presence of H 2 S or the absence of light causes differential persistence of populations in cave vs. How macroinvertebrates living in freshwater sulphide springs cope with the toxic levels of H 2 S has yet to be examined. Some taxa described above, such as hemipterans and the larvae of some dipteran groups, have the ability to breathe atmospheric air through respiratory siphons or tubes, which likely reduces their exposure to H 2 S dissolved in water [ , ].
Adaptations to sulphide-rich conditions have received more attention in invertebrates from marine environments, and depending on the taxonomic group, elevated tolerances have been associated with a wide variety of behavioural, physiological, and morphological modifications, including structural barriers that exclude H 2 S from the body, modification of molecular targets of H 2 S that reduce binding, reliance on anaerobic metabolism, active detoxification mechanisms, and symbioses with sulphide metabolizing microbes see [ 21 , ] for reviews.
The majority of records of fish inhabiting sulphide springs stem from North America and the Neotropics, with few additional reports from the Middle East. Overall, 24—putatively evolutionarily independent—invasions of sulphide springs have been documented Table 1 and references therein; Figure 1.
However, this number may be an underestimation even for documented populations, because the phylogenetic relationships of most species inhabiting multiple springs sometimes in different drainages remain to be studied. With one exception Ophisternon aenigmaticum , Synbranchidae , all sulphide spring fishes belong to the order Cyprinodontiformes. Pupfish Cyprinodontidae have been recorded from H 2 S-rich springs in Northern Mexico Cyprinodon bobmilleri and in Iran three species in the genus Aphanius.
One population of Poecilia mexicana also occurs in a H 2 S-rich cave in southern Mexico [ , , ]. Overall, six described species are highly endemic; they have been described from and exclusively inhabit sulphide springs Table 1. Even though not described as distinct species, several populations particularly in the family Poeciliidae also represent phenotypically divergent and genetically distinct ecotypes, indicating that they represent locally adapted populations restricted to H 2 S-rich environments [ 67 , 70 , 76 ].
However, additional research is required to test for the presence of local adaptation in the Cyprinodontidae and Synbranchidae, as at least some populations may be temporary or represent sinks that solely persist in H 2 S-rich environments because of continuous immigration from adjacent non-sulphidic habitats. For example, it is unlikely that Ophisternon aenigmaticum , which is occasionally collected in sulphide springs of Southern Mexico, maintains viable populations in toxic springs due to their extremely low abundance.
Although all sulphide springs inhabited by fish occur in geographic regions with considerable fish diversity, relatively few taxonomic groups have apparently managed to invade and persist in such extreme environments. This begs questions about what traits potentially characterize successful invaders.
All groups found in sulphide springs share the presence of alternative respiratory strategies that facilitate oxygen acquisition in the hypoxic waters [ , , ]. Synbranchids have aerial-respiratory surfaces in the mouth and branchial chambers, allowing them to extract oxygen directly from atmospheric air [ ]. Similarly, cyprinodontiforms are adapted to conducting aquatic surface respiration, where fish skim the uppermost water level that is disproportionally oxygenated because of direct contact to air, when exposed to hypoxic conditions [ , ].
The presence of alternative respiratory strategies could be critical for survival under sulphidic conditions, both because oxygen to fuel metabolism is scarce [ 16 ] and H 2 S detoxification is an oxygen consuming process [ ]. In addition, all members of the subfamily Poeciliinae are livebearing [ ].