Effects of extreme habitat conditions on otolith morphology: a case study on extremophile live bearing fishes (Poecilia mexicana, P. sulphuraria)

Our study was designed to evaluate if, and to what extent, restrictive environmental conditions affect otolith morphology. As a model, we chose two extremophile livebearing fishes: (i) Poecilia mexicana, a widespread species in various Mexican freshwater habitats, with locally adapted populations thriving in habitats characterized by the presence of one (or both) of the natural stressors hydrogen sulphide and darkness, and (ii) the closely related Poecilia sulphuraria living in a highly sulphidic habitat (Baños del Azufre). All three otolith types (lapilli, sagittae, and asterisci) of P. mexicana showed a decrease in size ranging from the non-sulphidic cave habitat (Cueva Luna Azufre), to non-sulphidic surface habitats, to the sulphidic cave (Cueva del Azufre), to sulphidic surface habitats (El Azufre), to P. sulphuraria. Although we found a distinct differentiation between ecotypes with respect to their otolith morphology, no clear-cut pattern of trait evolution along the two ecological gradients was discernible. Otoliths from extremophiles captured in the wild revealed only slight similarities to aberrant otoliths found in captive-bred fish. We therefore hypothesize that extremophile fishes have developed coping mechanisms enabling them to avoid aberrant otolith growth – an otherwise common phenomenon in fishes reared under stressful conditions.     

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.     

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 new and morphologically distinct population of cavernicolous Poecilia mexicana (Poeciliidae: Teleostei)

The cave molly, Poecilia mexicana, from the Cueva del Azufre, a sulfur cave in Tabasco, Mexico, ranks among the best-studied cave fishes worldwide, despite being known from a single population only. Here we describe a newly discovered second population of cave-dwelling P. mexicana from a nearby, but mostly non-sulfidic cave (Luna Azufre). Despite apparent similarities between the two populations (such as reduced eye diameter and reduced pigmentation), a geometric morphometric analysis revealed pronounced morphological differentiation between the two cave forms.     

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.     

Extreme habitats are not refuges: poeciliids suffer from increased aerial predation risk in sulphidic southern Mexican habitats

Extreme environments are often considered a predation refuge for organisms living in them. In southern Mexico several species of poeciliid fishes are undergoing incipient speciation in a variety of extreme (i.e. permanently dark and/or sulphidic) freshwater systems, and previous research has demonstrated reproductive isolation between populations from sulphidic and adjacent benign habitats. In the present study, we investigated bird predation rates (measured as successful captures per minute) in two sulphidic surface and several benign surface habitats, to test the hypothesis that extreme habitats are predation refuges. We found capture rates to be approximately 20 times higher in sulphidic environments: probably facilitated by extremophile poeciliids spending most of their time at the water surface, where they engage in aquatic surface respiration as a direct response to hypoxia. Even birds that are usually not considered major fish predators regularly engage in fish predation in the toxic habitats of southern Mexico. Our results demonstrate that extreme environments do not necessarily represent a refuge from predation, and we discuss the general importance of predation in driving incipient speciation in these systems. Finally, we hypothesize that natural selection via avian predation may play an important role in maintaining reproductive isolation between divergent poeciliid populations. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 101 , 417–426.     

Microgeographic diversity in the neotropical knife-fish Eigenmannia macrops (Gymnotiformes,Sternopygidae)

Synopsis Examination of 681 individuals of electric knife-fishes, Eigenmannia macrops, from the Orinoco River, Venezuela, revealed a pattern of morphological diversity which covaried with habitat. Fishes from the caños (small stream tributaries) are on average smaller than those from offshore habitats and lagoons. Even at the same body size the tails of caño fishes are relatively shorter, their bodies are deeper, and their heads are relatively wider than those from other habitats. Caño fishes are more different from fishes of the deep channels than from those of the shallow channels, beaches, or lagoons. Several factors are examined for their possible relationship to the origin of the observed diversity including electrophysiology, locomotory adaptation, growth rate and ecology. The problems of genetic versus physiological bases of morphological variation are addressed.     

Local adaptation and pronounced genetic differentiation in an extremophile fish, Poecilia mexicana, inhabiting a Mexican cave with toxic hydrogen sulphide

We investigated genetic differentiation and migration patterns in a small livebearing fish, Poecilia mexicana, inhabiting a sulfidic Mexican limestone cave (Cueva del Azufre). We examined fish from three different cave chambers, the sulfidic surface creek draining the cave (El Azufre) and a nearby surface creek without the toxic hydrogen sulphide (Arroyo Cristal). Using microsatellite analysis of 10 unlinked loci, we found pronounced genetic differentiation among the three major habitats: Arroyo Cristal, El Azufre and the cave. Genetic differentiation was also found within the cave between different pools. An estimation of first-generation migrants suggests that (i) migration is unidirectional, out of the cave, and (ii) migration among different cave chambers occurs to some extent. We investigated if the pattern of genetic differentiation is also reflected in a morphological trait, eye size. Relatively large eyes were found in surface habitats, small eyes in the anterior cave chambers, and the smallest eyes were detected in the innermost cave chamber (XIII). This pattern shows some congruence with a previously proposed morphocline in eye size. However, our data do not support the proposed mechanism for this morphocline, namely that it would be maintained by migration from both directions into the middle cave chambers. This would have led to an increased variance in eye size in the middle cave chambers, which we did not find. Restricted gene flow between the cave and the surface can be explained by local adaptations to extreme environmental conditions, namely H2S and absence of light. Within the cave system, habitat properties are patchy, and genetic differentiation between cave chambers despite migration could indicate local adaptation at an even smaller scale.     

Fish assemblages across a complex,tropical freshwater/marine ecotone

Synopsis Riverine fish assemblages in the temperate zone generally show strong longitudinal patterns of faunal turnover and increases in species richness with increasing stream order. We examined the composition and structure of tropical fish assemblages across a complex freshwater/marine ecotone in Tortuguero National Park on the Caribbean coast of Central America. Species turnover was high between four characteristic habitats that largely corresponded with a longitudinal gradient of stream order over distances of less than 30 km. Suites of common fish species characterized each habitat: creeks, rivers, lagoons, and the sea. In addition to the habitat endemics, several species spanned two habitat types, but only three species were collected in more than two habitats. Multivariate gradient analysis of fish assemblages reflected a gradient of habitats that to some extent corresponded to fluvial distances. Due to the unusual configuration of coastal lagoons lying parallel to the coast, the ordination gradient showed little correlation with linear distance to the coast. Environmental variables related to habitat size and salinity showed greatest correspondence with the fish assemblage ordination gradient. Invertebrate-feeding fishes were the predominant trophic group in 15 of 16 fish assemblages, and inland creek sites contained a greater proportion of herbivores and omnivores than other sites. The relative fraction of herbivorous and detritivorous fishes showed a monotonic decline along the longitudinal habitat gradient from inland to coast. Patterns of species composition and richness at Tortuguero Park appeared to agree well with earlier models of factors influencing temperate zone stream fishes. Headwaters have low aquatic primary productivity and contain small colonizing fish species subject to large fluctuations in local densities and intermittent competition. Lagoons contain both large and small species, the latter being restricted largely to shallow edge habitats by predation. Lagoons exhibit more lentic environmental conditions, experience relatively fewer periodic disturbances than headwaters, and their assemblages are inferred to be under relatively greater influence of biotic factors. Fish assemblages of rivers and caños (swampy side channels and braids) appear to be under less abiotic control than headwaters and influenced less by biotic factors than lagoons.     

Natural and sexual selection against immigrants maintains differentiation among micro‐allopatric populations

Local adaptation to divergent environmental conditions can promote population genetic differentiation even in the absence of geographic barriers and hence lead to speciation. But what mechanisms contribute to reproductive isolation among diverging populations? We tested for natural and sexual selection against immigrants in a fish species inhabiting (and adapting to) nonsulphidic surface habitats, sulphidic surface habitats and a sulphidic cave. Gene flow is strong among sample sites situated within the same habitat type, but low among divergent habitat types. Our results indicate that females of both sulphidic populations discriminate against immigrant males during mate choice. Furthermore, using reciprocal translocation experiments, we document natural selection against migrants between nonsulphidic and sulphidic habitats, whereas migrants between sulphidic cave and surface habitats did not exhibit increased mortality within the same time period. Consequently, both natural and sexual selection may contribute to isolation among parapatric populations, and selection against immigrants may be a powerful mechanism facilitating speciation among locally adapted populations even over very small spatial distances.     

Importance of Shallow Water Habitats for Demersal Fishes and Decapod Crustaceans in Penobscot Bay, Maine

We characterized demersal fish and decapod crustacean habitats in 14 shallow (< 12m) areas in Penobscot Bay, Maine, by mapping the distribution of subtidal substrata with an acoustic sea bottom profiler. We identified the aquatic vegetation and the fishes and decapods associated with these habitats. Samples of fishes and decapods in each habitat were collected with a small beam trawl. The seabed at most of the stations sampled was composed of a mosaic of substrata. More species of fishes tow^-1 and higher abundances of fishes and decapods were found in stations with vegetation present, particularly eelgrass, Zostera marina. Decapod species richness tow^-1 was similar between vegetated and unvegetated habitats. Shallow habitats in Penobscot Bay were dominated by juvenile fishes and function as nursery areas. The greater species diversity and higher abundances of epibenthic fishes and decapod crustaceans observed in vegetated habitats, particularly beds of Zostera marina, compared with unvegetated areas in Penobscot Bay conform to the hypothesis that increased habitat complexity results in increased species richness and abundance.The first author is also senior author     

The importance of mangroves, mud and sand flats, and seagrass beds as feeding areas for juvenile fishes in Chwaka Bay, Zanzibar: gut content and stable isotope analyses

The relative importance of bay habitats, consisting of mangrove creeks and channel, seagrass beds, and mud and sand flats, as feeding grounds for a number of fish species was studied in Chwaka Bay, Zanzibar, Tanzania, using gut content analysis and stable isotope analysis of carbon and nitrogen. Gut content analysis revealed that within fish species almost the same food items were consumed regardless of the different habitats in which they were caught. Crustaceans (mainly copepods, crabs and shrimps) were the preferred food for most zoobenthivores and omnivores, while fishes and algae were the preferred food for piscivores and herbivores, respectively. The mean δ¹³C values of fishes and food items from the mangrove habitats were significantly depleted to those from the seagrass habitats by 6·9 and 9·7‰ for fishes and food items, respectively, and to those from the mud and sand flats by 3·5 and 5·8‰, respectively. Fishes and food items from the mud and sand flats were significantly depleted as compared to those of the seagrass habitats by 3·4 and 3·9‰, for fishes and food, respectively. Similar to other studies done in different geographical locations, the importance of mangrove and seagrass themselves as a primary source of carbon to higher trophic levels is limited. The different bay habitats were all used as feeding grounds by different fish species. Individuals of the species Gerres filamentosus , Gerres oyena , Lethrinus lentjan , Lutjanus fulviflamma , Pelates quadrilineatus and Siganus sutor appeared to show a connectivity with respect to feeding between different habitats by having δ¹³C values which were in-between those of food items from two neighbouring habitats. This connectivity could be a result of either daily tidal migrations or recent ontogenetic migration.     

A new fish, Peristedion nesium (Scorpaeniformes: Peristediidae) from Isla del Coco, Costa Rica

Several expeditions in recent years to Isla del Coco have increased the total number of species of fishes known from the island. Several of these species have been described as new endemics (Bussing 1983, 1990, 1991a, 1991b, 1997). During the 1972 R/V Searcher Expedition to Costa Rica several trawl collections were made around Isla del Coco. At five localities in depths between 110 and 180m, 86 specimens of a new species of Peristedion were taken and are described herein. A key to the four species of Eastern Pacific Peristedion is included.     

Convergent changes in the trophic ecology of extremophile fish along replicated environmental gradients

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Size-dependent male mating behaviour and sexual harassment in a population of Atlantic mollies (Poecilia mexicana) from a sulphur creek

The Atlantic molly Poecilia mexicana inhabits a variety of habitats. In previous studies, small males from clear-water populations showed considerably more sexual behaviours than large males. Males from a sulphur creek, the El Azufre, or from a sulphur cave (cave molly) showed comparatively low sexual activity, and typical size-dependent mating behaviour was either absent or large males showed even more sexual behaviour than smaller ones. Sexually deprived cave molly males increased their sexual activity, but small males still did not show more sexual behaviour than large ones, suggesting that the genetic basis for typical size-dependent mating behaviour has been lost. Likely, the extreme abiotic conditions (hypoxia and toxic hydrogen sulphide) have selected against energetically costly behaviours. In this paper, we examined how El Azufre males would respond to sexual deprivation. We found these males to also increase their sexual activity after sexual deprivation but, unlike cave mollies, small males now showed more sexual behaviour than large ones, suggesting that the genetic basis for this behaviour is not lost in this population. Differences between populations may be due to the less harsh characteristics of El Azufre (e.g. less H₂S), resulting in weaker selection against energy-consuming behaviours. Furthermore, we tested for potential costs of male sexual harassment for females in terms of reduced feeding efficiency in the presence of a male, as was shown for P. mexicana from a clear-water population, but was not found in cave mollies or the El Azufre fish. Test females were either starved for 1 week to increase hunger levels or male sexual deprivation and female starvation were combined; however, we found no evidence for male sexual harassment even after these treatments. Our results parallel previous findings in the cave molly and suggest that El Azufre males have lost specific behavioural traits that cause sexual harassment.     

Habitat Use by Fishes in Coral Reefs,Seagrass Beds and Mangrove Habitats in the Philippines

Understanding the interconnectivity of organisms among different habitats is a key requirement for generating effective management plans in coastal ecosystems, particularly when determining component habitat structures in marine protected areas. To elucidate the patterns of habitat use by fishes among coral, seagrass, and mangrove habitats, and between natural and transplanted mangroves, visual censuses were conducted semiannually at two sites in the Philippines during September and March 2010–2012. In total, 265 species and 15,930 individuals were recorded. Species richness and abundance of fishes were significantly higher in coral reefs (234 species, 12,306 individuals) than in seagrass (38 species, 1,198 individuals) and mangrove (47 species, 2,426 individuals) habitats. Similarity tests revealed a highly significant difference among the three habitats. Fishes exhibited two different strategies for habitat use, inhabiting either a single (85.6% of recorded species) or several habitats (14.4%). Some fish that utilized multiple habitats, such as Lutjanus monostigma and Parupeneus barberinus, showed possible ontogenetic habitat shifts from mangroves and/or seagrass habitats to coral reefs. Moreover, over 20% of commercial fish species used multiple habitats, highlighting the importance of including different habitat types within marine protected areas to achieve efficient and effective resource management. Neither species richness nor abundance of fishes significantly differed between natural and transplanted mangroves. In addition, 14 fish species were recorded in a 20-year-old transplanted mangrove area, and over 90% of these species used multiple habitats, further demonstrating the key role of transplanted mangroves as a reef fish habitat in this region.     

Spatial ecology of monito del monte (Dromiciops gliroides) in a fragmented landscape of southern Chile

Habitat loss is one of the most important causes of biodiversity loss in South American temperate rainforests, where many endemic species exist. Among these is the monito del monte (Dromiciops gliroides), an arboreal marsupial with restricted distribution, and the only extant species of the order Microbiotheria. Current knowledge about monito del monte habitat use and its responses to human disturbances is scarce. To help fill this gap we investigated its habitat use and selection patterns in a fragmented landscape in southern Chile. Monito del monte individuals were abundant in a large and a small fragment, but rare or undetected in forest strips. Using telemetry data from 12 neighboring individuals in a large fragment and 2 individuals in a small fragment, we estimated their mean home range size of 1.6 ha±0.6 (1SD). Monitos del monte had a spatial overlap among individuals of 50±4%. Tracked individuals used old- and second-growth habitats as available, did not use the prairie habitats, and strongly avoided the scrublands. In the large fragment we estimated a relative population density of 21±5 individuals/ha (mean±1SD), whereas in the small fragment it was of 19±6 individuals/ha. This is, to our knowledge, the first study of the spatial ecology of the monito del monte based on telemetry data, and evidence presented here could have conservation and planning implications, not only for the target species but also its habitat.     

Variation of snail's abundance in two water bodies harboring strains of Pseudosuccinea columella resistant and susceptible to Fasciola hepatica miracidial infection, in Pinar del Río Province, Cuba

The abundance of freshwater snails in two rural sites of Pinar del Río, Cuba, which harbor Pseudosuccinea columella susceptible and resistant to miracidia of Fasciola hepatica was followed for one year. Susceptible snails were found in the most anthropic site (IPA) whereas the resistant population inhabited the most preserved one (El Azufre). Only two snail species coexisted with P. columella at IPA site (Physa cubensis and Tarebia granifera) while five species were found at El Azufre, including an endemic from that province (Hemisinus cubanianus). Populations of both resistant and susceptible snails showed stable densities throughout the year, although the susceptible strain attained higher abundance. The highest densities were observed in April-May 2004 for the susceptible population whereas the resistant strain attained its highest abundance in January 2004. No record of Fossaria cubensis was made and the thiarid T. granifera occurred only at low densities. One of the sampled sites (IPA) meets all the conditions for the first report of P. columella naturally infected with larvae of F. hepatica.     

Structure of the testis and spermatogenesis of the viviparous teleost Poecilia mexicana (Poeciliidae) from an active sulfur spring cave in Southern Mexico

We describe the histological characteristics of the testis and spermatogenesis of the cave molly Poecilia mexicana, a viviparous teleost inhabiting a sulfur spring cave, Cueva del Azufre, in Tabasco, Southern Mexico. P. mexicana has elongate spermatogonial restricted testes with spermatogonia arranged in the testicular periphery. Germ cell development occurs within spermatocysts. As spermatogenesis proceeds, the spermatocysts move longitudinally from the periphery of the testis to the efferent duct system, where mature spermatozoa are released. The efferent duct system consists of short efferent duct branches connected to a main efferent duct, opened into the genital pore. Spermatogenesis consisted of the following stages: spermatogonia (A and B), spermatocytes (primary and secondary), spermatids, and spermatozoa. The spermatozoa are situated within spermatocysts, with their heads oriented toward the periphery and flagella toward the center. Once in the efferent duct system, mature spermatozoa are packaged as unencapsulated sperm bundles, that is, spermatozeugmata. We suggest that the histological characteristics of the testis and spermatogenesis of P. mexicana from the Cueva del Azufre, and the viviparous condition where the spermatozoa enter in the female without been in the water, have allowed them to invade sulfurous and/or subterranean environments in Southern Mexico, without requiring complex morphofunctional changes in the testis or the spermatogenetic process.