Annual Fish Species Research Articles

River drainage rearrangements and the phylogeographic pattern of the annual fish Austrolebias arachan (Cyprinodontiformes, Rivulidae)

AbstractPalaeogeographical and climatic processes are among the main factors affecting biological diversity and distribution patterns. In freshwater systems, major dispersal processes are caused by river drainage rearrangements where the direction of flow of a stream changes, allowing range expansions and connection of previously isolated communities. In the Neotropical region, this process has been known to connect part of the southwestern Amazon basin with La Plata basin during the formation of the Bolivian Orocline, and La Plata basin with Atlantic coastal basins since the split from Africa. Several species of annual fishes of the genus Austrolebias are known to inhabit seasonal ponds both in the Rio Negro basin (southern tip of Brazilian shield, Lower Uruguay ecoregion), and the headwaters of rivers draining into the Merín lagoon (coastal drainages, Laguna dos Patos ecoregion). The aim of this article was to analyse the phylogeographic pattern of Austrolebias arachan in the context of putative river rearrangements. Two hypotheses were tested: (a) the spatial configuration of river basins determines the genetic structure and distribution of this species, and (b) coastal drainages captured sections of upland shield river drainages. We analysed a fragment of the mitochondrial cytochrome b gene and a fragment of a nuclear intron locus. Results support the prediction of the first hypothesis: geographic variation within A. arachan is structured according to geography. The second hypothesis was in part confirmed: the migration analyses showed that Rio Negro basin populations could have acted as a source for Laguna Merin basin. However, migration estimates also support gene flow in the opposite direction. The cytochrome b haplotype network configuration and its phylogenetic pattern suggests at least two independent events of capture, with divergence time estimated at the onset of Pleistocene glacial cycles.

Effects of temperature and heat waves on embryonic development of annual fishes from Neotropical wetlands: Implications for climate change scenarios

AbstractClimate change projections predict warmer temperatures and increased frequency of heat waves in many regions across the globe. These scenarios are expected to strongly impact temperature‐dependent life‐history traits of aquatic species, such as the embryonic stage of annual fishes inhabiting temporary freshwater wetlands. Here, we assessed the effects of different incubation temperatures (18, 24, 27 and 30°C) and exposure to heat waves (18–30°C for 6 h) on aspects of the embryonic development: mortality and trajectory (direct development or diapause entry) of two Neotropical species of annual fishes from high‐ (Austrolebias nubium) and low‐altitude (A. cyaneus) areas. Temperatures of 30°C resulted in 100% embryo mortality in both species, and development trajectory differed between species across temperatures. Embryo mortality in the high‐altitude species was higher at 27°C, while a higher number of embryos of the low‐altitude species entered diapause II at 18°C. Embryo mortality and development trajectory after exposure to heat waves were similar between species. In terms of implications for climate change scenarios, temperatures above 27°C seem critical for the embryo survival of both species studied, although they seem capable to endure short‐term events of heat waves. In summary, our results indicate that the persistence of populations of high‐altitude annual fish species may be subject to higher threat under warming scenarios, since embryos from this species were more sensitive to increasing temperatures than the low‐altitude species.

Desenvolvimento embrionário de Austrolebias wolterstorffi, uma espécie de peixe anual neotropical criticamente ameaçada de extinção

Annual fish live exclusively in temporary wetlands and are among the shortest-lived vertebrates in the world. These fish persist in these habitats due to drought-resistant eggs, that which, through diapauses are able to detect stimuli from the environment to start the development processes. They are also able to direct their embryonic development in different trajectories with different development times. Our objective in this paper was to describe the different stages of embryonic development of Austrolebias wolterstorffi, a critically endangered annual fish. A total of 27 stages of embryonic development were identified for the two observed developmental pathways (direct and diapause 2). Of these 27 developmental stages observed, 24 were identical between the two types of trajectories and three different. A total of 90% of the embryos that completed their development proceeded normally, without pauses. One embryo had a different development from the others, entering diapause 2, with a pause in development for 48 h. Although the embryonic development of A. wolterstorffi is similar to that of other Neotropical annual fish species, the diapause 2 occurs when the embryo has a large body size and a well-developed brain, indicating that the lack of embryonic information of the genus Austrolebias may hide characteristics still undescribed or even different survival strategies than what has been observed for other annual fish.

Recognizing the enemy: do predator cues influence hatching in Neotropical annual killifish?

Annual fish species have evolved complex adaptations to survive in temporary wetlands. The main adaptation of these fish is the ability to produce embryos that survive dry periods. Embryo development of this fish can show variation at multiple levels influenced by many environmental factors, such as photoperiod and temperature. Predator cues are another factor that can influence the embryonic stage. One way in which annual fish could adapt to predators is by using risk-spreading strategies (through bet-hedging). Nonetheless, this strategy depends on the coevolutionary history between predators and preys and on the degree of environmental unpredictability, resulting in different responses across different species. This study investigated the influence of predator cues on the embryonic development and hatching of two Austrolebias species that inhabit ponds that present differences in hydroperiod and the risk of predator presence. The results confirmed a differentiated response between the two annual fish species tested, corroborating the modulation of hatching against the risk of predation by native predatory fish. The authors further showed that development times varied between the two annual fish species, regardless of the presence of predators. They highlight that the variation in embryonic development is strongly affected by different levels of hydroperiod unpredictability faced by the two species. To unravel finer-scale local adaptations in the annual fish embryo development, future studies should focus on a region with greater spatial gradient.

Annual and non‐annual fish assemblages respond differently to environmental and spatiotemporal variations of temporary wetlands from southern Brazil

Abstract The fish community of temporary wetlands is highly dynamic due to the marked seasonal changes in hydrological and limnological conditions. In this study, we evaluated spatiotemporal variation in the fish community and the influence of environmental factors on this variation in temporary wetlands in southern Brazil. Two different life cycles—annual and non‐annual fishes—were recorded among species. Variation in the fish community appeared to be associated with differences in the life history strategy of species. While species of annual fish were present throughout the hydroperiod, gradually decreasing in density over time, non‐annual fish species had an opposite pattern, with higher densities in the final phase of the hydrological cycle. Variations in the composition and abundance of fish community in temporary wetlands were related to habitat and landscape attributes (area, number of microhabitats and isolation between temporary wetlands) and climate indicators of water availability (air temperature, average rainfall, and water level of the São Gonçalo channel), but not to water conditions (dissolved oxygen, pH, conductivity and water temperature). We concluded that the ichthyofauna of temporary wetlands are composed both of rare species, highly specialised for life within these ephemeral environments, and widespread generalist species that reach the wetlands opportunistically for short periods. Habitat and landscape attributes and changes in climate and hydrological variables over the hydroperiod are the factors that had the greatest influence on spatiotemporal variation of the fish community. Maintaining physical characteristics and the hydrological cycle of temporary wetlands is critical for the conservation of fish species inhabiting these vulnerable environments in southern Brazil. Habitat and landscape attributes and climate and hydrology fluctuations affect the annual and non‐annual fishes inhabiting temporary wetlands differently.

Austrolebias queguay (Cyprinodontiformes, Rivulidae), a new species of annual killifish endemic to the lower Uruguay river basin

In this article we describe a new species of the annual fish genusAustrolebiasfrom the lower Uruguay river basin. The fusion of the urogenital papilla to the first anal fin ray in males and the pigmentation pattern, indicates a close relationship with the clade formed byA.bellottii,A.melanoorus, andA.univentripinnis. The new species can be differentiated from those by the following combination of characters: presence of well-defined light bands contrasting with the sides of the body, the distal portion of the anal fin dark gray, pelvic fins dark bluish green and bases united at about 50–80% on their medial margins, pectoral fins with iridescent blue sub-marginal band, and general coloration of body bluish green. The new species can only be found in wetlands of the Queguay river, an area included in the Uruguayan protected areas system and represents so far the only annual fish species endemic to the lower Uruguay river basin.

Phenology of three coexisting annual fish species: seasonal patterns in hatching dates

Annual fish are specialized freshwater fishes that are adapted to live in seasonal freshwater pools. Their life cycle is tightly adapted to seasonally predictable aquatic and desiccated phases in their habitat. We used daily increments in otoliths to test the hypothesis of the direct association between seasonal rains and hatching dates of three coexisting Austrolebias species across 14 temporary pools in the Uruguayan pampa. Hatching was relatively synchronous within and between species across a small but topographically diverse region. Hatching occurred over 1 month in midautumn and peaked between 15 and 20 April 2015. The prediction of earlier hatching of a large predatory annual fish species was not confirmed. Unexpectedly, an unusual desiccation event in the middle of the winter growing season (May–July) affected many pools. Some pools re-filled after extensive precipitation in August, followed by the hatching of a new cohort in some (but not all) of those pools. The first cohort survived throughout the year (until late spring) in the pools that did not desiccate. Our study demonstrates how annual fish can cope with unexpected seasonal rainfall patterns that may be a consequence of current climate change.

Life stage dependent responses to desiccation risk in the annual killifish Nothobranchius wattersi.

To assess whether the annual killifish Nothobranchius wattersi responds plastically to a desiccation risk and whether this response is life stage dependent, life-history traits such as maturation time, fecundity and life span were experimentally measured in N. wattersi that were subjected to a drop in water level either as juveniles, as adults or both as juveniles and adults. Fish that were exposed to simulated pool drying as juveniles did not show changes in reproductive output or life span. Adults reacted by doubling short term egg deposition at the cost of a shorter lifespan. Overall, these results suggest that annual fish species can use phenotypic plasticity to maximize their reproductive output when faced with early pond drying, but this response appears to be life-stage specific. In addition to frogs and aquatic insects, phenotypic plasticity induced by forthcoming drought is now also confirmed in annual fishes and could well be a common feature of the limited number of fish taxa that manage to survive in this extreme environment.

Seasonal dynamics in community structure, abundance, body size and sex ratio in two species of Neotropical annual fishes.

Seven ephemeral pools on the coastal plain of southern Brazil were found to be inhabited by three annual and 22 non-annual fish species. Two common annual species (Austrolebias minuano and Cynopoecilus fulgens) exhibited clear seasonal dynamics, with the appearance of young fishes in the austral autumn (May to June) and a decline in abundance over the seasonal cycle. The third annual species, Austrolebias wolterstorffii, was rare. No seasonal dynamics were observed in non-annual fishes. The relative abundance of non-annual fishes compared with annual fishes increased over the seasonal cycle, but they coexisted widely. The size structure of annual fishes suggested the presence of a single age cohort in most pools though a second age cohort was registered in one pool in August, coinciding with a large flooding. Strong sexual dimorphism in body size was found in C. fulgens throughout the seasonal cycle, while no sexual dimorphism in body size was found in A. minuano. Female-biased sex ratios were recorded in both common annual fish species in the last three sampling dates (in spring), but not during the first two sampling dates (in winter). The natural lifespan of annual fishes was <8 months. Annual fishes disappeared before habitat desiccation in half of the pools, while non-annual fishes were still present.

Description of two new species of annual fishes of the Hypsolebias antenorispecies group (Cyprinodontiformes: Rivulidae), from Northeast Brazil.

The Hypsolebias antenori species group comprises a monophyletic clade of annual fishes occurring in the semi-arid region of Northeastern Brazil. Most species of this group are found in the Rio São Francisco basin, but there are three species that inhabit small coastal basins. Hypsolebias faouri new species, is described from a temporary pool located near Rio Preto, a tributary of the Rio São Francisco, and Hypsolebias martinsi new species, is described from an annual pool near Rio Icaraizinho, a coastal drainage. Molecular data corroborates the monophyly of Hypsolebias and both new species.

Assessing oocyte development and maturation in the threatened Delta Smelt, Hypomesus transpacificus

Delta Smelt is a pelagic annual fish species endemic to the San Francisco Estuary, which is protected under U.S. Federal and California State Endangered Acts. In this study we established criteria for scoring Delta Smelt maturity based on the histological features in ovary, as well as measurements of the female sex hormone 17β-estradiol (E2) from liver tissue using radioimmunoassay. We then analyzed the reproductive status of maturing females caught from November 2011 through April 2012 (2011 year-class) by histological examination, E2 quantification, and several common fish metrics including size of oocytes, gonadosomatic index, hepatosomatic index, and condition factor. Histological scoring revealed that Delta Smelt oocytes matured in February through April 2012. The presence of postovulatory follicles with immature oocytes (Stage 1 to 3) further suggests that Delta Smelt are iteroparous, capable of reproducing multiple times during the spawning season. Hepatic E2 concentration was significantly correlated with gonadosomatic index, hepatosomatic index, size of oocytes, and maturation stage. Histological examination of ovaries combined with measures of hepatic E2 and size of oocytes provide a powerful approach to evaluate reproductive performance and maturation timing for the imperiled Delta Smelt.

Delta Smelt Habitat in the San Francisco Estuary: A Reply to Manly, Fullerton, Hendrix, and Burnham’s “Comments on Feyrer et al. Modeling the Effects of Future Outflow on the Abiotic Habitat of an Imperiled Estuarine Fish”

Manly et al. (2015) commented on the approach we (Feyrer et al. 2011) used to calculate an index of the abiotic habitat of delta smelt Hypomesus transpacificus. The delta smelt is an annual fish species endemic to the San Francisco Estuary (SFE) in California, USA. Conserving the delta smelt population while providing reliability to California’s water supply with water diverted from the SFE ecosystem is a major management and policy issue. Feyrer et al. (2011) evaluated historic and projected future abiotic habitat conditions for delta smelt. Manly et al. (2015) specifically commented regarding the following: (1) use of an independent abundance estimate, (2) spatial bias in the habitat index, and (3) application of the habitat index to future climate change projections. Here, we provide our reply to these three topics. While we agree that some of the concepts raised by Manly et al. (2015) have the potential to improve habitat assessments and their application to climate change scenarios as knowledge is gained, we note that the Feyrer et al. (2011) delta smelt habitat index is essentially identical to one reconstructed usingManly et al.’s (2015) preferred approach (their model 8), as shown here in Fig. 1.

The morphology–diet relationship and its role in the coexistence of two species of annual fishes

AbstractAnnual fishes, which inhabit temporary pools with extremely limited habitat complexity and niche availability, display remarkable sexual dimorphism, rapid growth, and enormous investment into reproduction, all traits associated with high energy requirement. This study tests three hypotheses for two syntopic annual fishes (Austrolebias minuano and Cynopoecilus fulgens) found in six wetlands of southern Brazil: (i) considerable morphological differences result in low dietary overlap, (ii) sexual dimorphism in both species leads to intraspecific diet segregation, and (iii) dietary richness increases during ontogenetic development, and is narrower in C. fulgens than A. minuano due to morphological limitations imposed by reduced size. The diet of 82 A. minuano and 211 C. fulgens individuals was analyzed over two annual cycles. The morphology was characterized by 26 measurements covering the entire body of both species. There was no evidence of morphological specialization related to food competition and the diet of A. minuano and C. fulgens showed high overlap. High food availability, high predator abundance, and high connectivity of adjacent wetlands are likely the main mechanisms allowing coexistence of both species. Within species, sexual dimorphism did not result in a decrease in dietary overlap, which reinforces the idea that morphological differences between the sexes did not evolve as a mechanism to decrease food competition. Large A. minuano did not have a more diverse diet than the smaller C. fulgens; however, increase in body size allowed both species to ingest larger prey. Morphological variability in both species was mainly related to ontogenetic development and reproduction.

Abundance variations and life history traits of two sympatric species of Neotropical annual fish (Cyprinodontiformes: Rivulidae) in temporary ponds of southern Brazil

We investigated abundance variations and life history traits (body size, sex ratio, length–weight relationships and condition factor) of two species of annual fish (Austrolebias minuano Costa and Cheffe and Cynopoecilus fulgens Costa) in temporary ponds of southern Brazil. Six samples were taken from small temporary ponds during three annual seasons over 2 years (2008–2009). A total of 104 individuals of A. minuano and 433 individuals of C. fulgens were collected. The abundance of both species tended to decrease from autumn to spring in the 2 years. The overall sex ratio of A. minuano and C. fulgens were 1.0 male to 1.8 females and 1 male to 1.04 females, respectively. Juveniles of both species occurred only in autumn over the two years and no adult was observed during this season. While the length–weight relationship of A. minuano indicated hyperallometric growth, the relationship of C. fulgens indicated values close to isometric growth.

Reproduction of the threatened Annual Killifish Austrolebias nigrofasciatus (Cyprinodontiformes: Rivulidae), confined in a natural environment

This study concerns the reproduction of Austrolebias nigrofasciatus, an endangered annual fish species endemic to the waters of the Sao Goncalo channel and its tributaries in southern Brazil. Three breeding pairs confined in small cages for four weeks in their biotope were observed to produce an average of 21.5 plus or minus 12.0 eggs/week/female, with a range of 3-39 eggs/female/week. Average egg diameter was 1.51 plus or minus 0.12 mm, with abrupt changes observed throughout the period of study. The mean oviposition observed was within the range found for other killifishes and demonstrates the high fecundity rate of the species even under confinement conditions.

Distribution, habitat and conservation status of two threatened annual fishes (Rivulidae) from southern Brazil

This study presents information on the distribution of Austrolebias cyaneus and A. juan- langi, 2 annual fish species of southern Brazil considered threatened. Furthermore, data are provided on the conservation status of these species and their habitat characteristics to assist in the develop- ment of management plans and in the selection of priority areas for conservation of annual fishes in southern Brazil. A total of 6 populations of A. cyaneus and 3 populations of A. juanlangi were sam- pled from small ponds less than 1000 m 2 in surface area. We sampled 104 specimens of A. cyaneus, distributed in the municipality of Rio Pardo and Minas do Leao in the basins of the Francisquinho, Capivari, and Dom Marcos streams, Jacui River basin. A. juanlangi was recorded in the municipali- ties of Herval, Hulha Negra, and Pedras Altas, Jaguarao River basin, with 53 specimens being cap- tured. At the sampling sites, the main threat to both species was rice cultivation. All pools were altered, isolated, and in an advanced state of degradation as a result of this monoculture. The restricted distribution area of the annual fishes and the advanced state of degradation and habitat loss of the wetlands sampled in this study justify the creation of conservation units in the areas of occurrence of Rivulidae species.

Reproductive behavior in the annual fish Austrolebias reicherti Loureiro &amp; García 2004 (Cyprinodontiformes: Rivulidae)

Annual fishes inhabit temporary ponds that dry out seasonally and the adaptations to survive this extreme condition include high metabolic rates and an elaborate courtship behavior which ends in the deposition of drought-resistant eggs, capable of going through diapause stages in the substrate. The pronounced sexual dimorphism that these fishes show suggests that sexual selection could play a key role in the differentiation, speciation and evolution of this diverse group of fishes. However, there is scarce information about their reproductive isolation mechanisms, including detailed analysis of courtship signals. Herein, we analyzed, qualitatively and quantitatively, the reproductive behavior of Austrolebias reicherti. The behavioral units recognized in this study correspond with the previous analysis of other species of annual fishes. The most frequent unit in males was the lateral display where specific morphological and coloration patterns are displayed to the female. The female's high relative frequency and time of quietness suggest that this unit may have an evaluation role during courtship. In addition to visual displays during courtship, males perform vibrations of the dorsal and anal fins as well as body undulations; these indicate that mechanical signals may be important for attracting females. Our results support the hypothesis of multimodal signals. The conservation of behavioral patterns in courtship displays within Austrolebias suggests that species-level recognition and the barrier to hybridization may not occur at this stage, unless quantitative differences can be identified.

Austrolebias toba (Cyprinodontiformes: Rivulidae), una especie nueva de pez anual de la Argentina

Austrolebias toba (Cyprinodontiformes: Rivulidae), una especie nueva de pez anual de la Argentina

Austrolebias arachan (Cyprinodontiformes, Rivulidae), a new species of annual fish from northeastern Uruguay

The annual fish Austrolebias arachan is described from temporary ponds of Rio Tacuari (Los Patos-Merin system) and Rio Negro (Rio Uruguay drainage) basins. Austrolebias arachan is easily distinguished from otherAustrolebias species by the combination of the following characters: body of males dark brown to black, with light narrow yellow vertical bands, dorsal fin dark brown with vertically elongated light yellow dots in the proximal half, pectoral fin light grey with margin black; females with anterior anal fin rays elongated, forming a triangular-shaped fin. Both sexes with pelvic fins joined to each other in different degrees; two to four parietal neuromasts; three pectoral radials in most individuals. The new species is closely related to A. adloffi species group and to A. viarius.

Observations on the lifespans of several species of annual fishes and of the world's smallest fishes

Three species of South American annual fishes ( Cynolebias adloffi, C. bellottii and C. wolterstorffi) were maintained in the laboratory at 15–16°C and 20–22°C. They grew faster, reached a larger eventual size and lived up to twice as long at the lower temperature range. Two species of gobies, collected as adults and representing the smallest known species of vertebrates, lived one to two years in the laboratory. The potential lifespan of these minute fish is probably greater than that of the annuals, suggesting that a strict relationship between body size and longevity does not obtain in teleosts.