Systematics, biogeography, and evolution of the Neotropical peacock basses Cichla (Perciformes: Cichlidae)

To investigate forces influencing diversification in Neotropical fishes, the phylogenetic relationships among species and populations of the cichlid genus Cichla were examined. Mitochondrial DNA was sequenced for 454 individuals of the 5 nominal Cichla species and several putative undescribed species. Phylogenetic analyses support the distinction of two major clades of Cichla. Clade A includes C. temensis and two undescribed species from the lower Amazonas and Xingu Rivers. Clade B includes C. orinocensis, C. monoculus, C. ocellaris. C, intermedia, and an undescribed species from the upper Madeira River. Species boundaries were relatively well-circumscribed for clade B, while incomplete lineage sorting was inferred for clade A. Three probable instances of introgression were observed, including a regional population of C. orinocensis from the Negro River that shows a history of introgression. Biogeographic patterns from Cichla are partially congruent with those seen in several other Neotropical fish clades, and the diversification of Cichla species is inferred to result from both vicariance and sympatric divergence.     

Genetic characterization of native and introduced populations of the neotropical cichlid genus Cichla in Brazil

A molecular phylogenetic analysis based on mitochondrial 16S ribosomal DNA and Control Region sequences from native and introduced populations was undertaken, in order to characterize the introduction of Cichla (peacock bass or tucunaré) species in Brazil. Mitochondrial DNA haplotypes found in introduced fish from Minas Gerais state (southeastern Brazil) clustered only with those from native species of the Tocantins River (Cichla piquiti and C. kelberi), thereby suggesting a single or, at most, few translocation acts in this area, even though with fish from the same source-population. Our study contributes to an understanding of the introduction of Cichla in regions of Brazil outside the Amazon basin, and adds phylogenetic data to the recently describe Cichla species, endemic from the Tocantins-Araguaia basin.     

Evidence for a natural hybrid of peacock bass (Cichla monoculus vs Cichla temensis) based on esterase electrophoretic patterns

Esterase (Est) and esterase-D (Est-D) electrophoretic patterns identified by starch gel electrophoresis of skeletal muscle protein extracts of 184 specimens of three species of peacock bass, locally known as tucunares (Cichla monoculus, C. temensis and Cichla sp), plus four specimens of a supposed hybrid (C. monoculus vs C. temensis), collected from the Central Amazon, were examined to determine if they could aid in identifying a supposed hybrid between C. monoculus and C. temensis. Six zones of electrophoretic activity were found with these enzyme systems. The Est enzyme showed one zone of activity, formed by bands 1, 2 and 3, plus three zones of activity, presumably controlled by Est-1, 2 and 3 loci. The Est-D enzyme had two zones of activity, presumably controlled by Est-D1 and Est-D2 loci. Cichla monoculus and C. temensis shared band 2 and alleles Est-1(1), Est-2(1), Est-3(2), and Est-D1(1), and therefore these were useless for identifying hybrids between the two species. However, a probable hybrid pattern of bands 1, 2, and 3, presumably generated by a combination of pattern 12 from C. monoculus with pattern 23 from C. temensis, resulting from a possible cross between these two species, was detected. Although the Est-D2 locus cannot be considered an ideal diagnostic marker for identifying the supposed hybrid (C. monoculus vs C. temensis), as it is polymorphic, it proved to be useful for determining the origin of the hybrid, i.e., which parental species were involved in the hybridization process.     

Feeding of introduced species of Cichla (Perciformes, Cichlidae) in Volta Grande reservoir, River Grande (MG/SP).

Both species studied, Cichla cf. ocellaris and Cichla monoculus, fed mainly on fish, the first on Cichla spp., Plagioscion squamosissimus, and Tilapia rendalli, and the second, Cichla monoculus, on Cichla spp. Both diets indicated a strong correlation among the food items. Remarkable ontogenetic change was noted in both species diet: the young fed on crustaceans and insects while the adults fed mainly on fishes. The species studied, which are highly adapted to a brief life span, cause serious damage to the fish communities by predation, competition, and cascade effects throughout the whole trophic chain.     

Genetic diversity of invasive and native Cichla (Pisces: Perciformes) populations in Brazil with evidence of interspecific hybridization

Invasive and native populations of the Amazonian fishes 'peacock bass' Cichla monoculus and of a not yet described species 'blue tucunaré' here referred as Cichla sp. 'Azul' were analysed for genetic diversity using the hypervariable domain of the mitochondrial DNA (mtDNA) control region plus steady diagnostic random amplified polymorphic DNA loci. There is no detailed historical record of the introduction of Cichla species into the Upper Paraná River basin, where they became invasive and a potential threat to local ichthyofauna. Genetic diversity among invasive populations confirmed the hypothesis of multiple introductions in this hydrographic basin. Moreover, a large and previously unknown population of natural fertile hybrids between C. cf. monoculus and Cichla sp. 'Azul' was identified in the Itaipu hydroelectric reservoir and in the floodplain of the Upper Paraná River. Crossbred morphotypes were similar to C. cf. monoculus , but their morphological identification was not unequivocal. This hybrid population was characterized by high genetic diversity and it was composed of hybrids possessing concurrently nuclear DNA fragments specific for C. cf. monoculus as well as fragments specific for Cichla sp. 'Azul'. The nuclear DNA markers indicated that reproductive isolation between C. cf. monoculus and Cichla sp. 'Azul' has broken down in the new environment, and mtDNA sequences revealed that both species can be the female donor in the interspecific crosses. The data presented herein are potentially useful for future taxonomic, genetic and evolutionary studies in the complex Cichla group, for monitoring of invasive populations, and for further development of ecological guidelines.     

Microsatellite markers for the Amazon peacock bass (Cichla piquiti)

A set of primers to amplify 10 microsatellite DNA loci was developed for the Neotropical fish Cichla piquiti, one of the largest sized cichlids in the Amazon Basin. These loci were used to genotype individuals from two populations, one native population from the Tocantins River, the other an introduced population in southeast Brazil, Upper Paraná River. Cross-amplification was also successful for another species of peacock bass, C. kelberi. An average of 4.4 alleles per locus (2-9 alleles) was detected. These markers will be useful for the characterization of genetic structure of native populations, and also for invasive biology studies since Cichla species have been introduced in many river basins outside their native ranges.     

Temporal patterns of resource partitioning among Cichla species in a Venezuelan blackwater river

In channel and floodplain habitats of the Cinaruco River, Venezuela, Cichla temensis was more abundant and larger than C. intermedia and C. orinocensis . Seasonal variation in hydrology influenced habitat use, spawning, and predator-prey interactions. The three piscivores partitioned habitat, with C. intermedia showing a strong affinity for structured habitats in the main channel during all water level fluctuations. C. orinocensis was most abundant in shallow areas with submerged structure in lagoons and, to a lesser extent, in low velocity regions of the channel, and C. temensis occupied a wide range of lotic and lentic habitats. During the low-water period, the feeding frequency and body condition of all three species declined, and this was related, in part, to preparation for spawning near the end of the low-water season. The diet of C. intermedia was least similar to its two congeners during falling and rising water. C. orinocensis and C. temensis had lowest diet overlap during the low-water conditions, the period when many individuals of these two species move into lagoons for nesting. Prey in stomachs were significantly larger during the falling-water than the rising-water period, and predation by Cichla and other large piscivores during the falling-water period may have reduced the abundance of large prey, particularly Semaprochilodus kneri . These migratory detritivorous fish were important prey for C. temensis during the falling-water period and probably contributed a substantial fraction of the annual energy intake for this species. Together, the three Cichla species consume a wide spectrum of prey from a diverse fish assemblage, but prey are subdivided based on habitat, prey type, and season.     

Comparative functional responses predict the predatory impact of the highly invasive fish Cichla kelberi

Hydrobiologia - Peacock basses (genus Cichla) are a group of Amazonian predatory fishes that invaded many systems worldwide. Severe ecological impacts have been reported, but no study investigated...     

Karyological evidence for interspecific hybridization between Cichla monoculus and C. temensis (Perciformes, Cichlidae) in the Amazon

Cichla monoculus, Cichla temensis (peacock bass or tucunare), and its presumed hybrids, were cytogenetically analyzed. The fish were collected at three distinct sites in the central Amazon basin, namely in the Uatuma (C. monoculus, C. temensis and their natural hybrid), Jau (C. temensis), and Solimoes rivers (C. monoculus). The two species and the natural hybrid showed the same diploid number, 2n=48 acrocentric chromosomes. Single NORs were detected in the distal region of the long arm in all three species. However, in C. monoculus, the NOR was found on the second pair of the complement, in C. temensis, on the third pair and in the hybrid two NOR patterns were found, one on the second pair and the other on the third pair of chromosomes. The two species and the hybrid have their constitutive heterochromatin located in the pericentromeric region of all chromosomes and an interstitial C-band located on the largest chromosome pair. The great similarity in the chromosome number and morphology, chromosome size class differences, the NOR patterns and C-banding suggested chromosomal stasis during speciation and hybridization of Cichla.     

Molecular analysis of invasive Cichla (Perciformes: Cichlidae) populations from neotropical ecosystems

Invasive Cichla populations in the São João River basin were genetically analysed and compared with Cichla populations from other neotropical hydrographic basins. Polymorphic sequences within the mitochondrial DNA D-loop region confirmed the introduction of different populations to the regions under analysis. Cichla kelberi was introduced to the Juturnaíba reservoir and a downstream area of the São João River, with Cichla monoculus restricted to downstream river areas. Results from this study will be useful for monitoring invasive Cichla populations in the coastal basin since it elucidated the taxonomic units in the reservoir and an areas downstream.     

Simultaneous delimitation of species and quantification of interspecific hybridization in Amazonian peacock cichlids (genus Cichla) using multi-locus data

ABSTRACT: BACKGROUND: Introgression likely plays a significant role in evolution, but understanding the extent and consequences of this process requires a clear identification of species boundaries in each focal group. The delimitation of species, however, is a contentious endeavor. This is true not only because of the inadequacy of current tools to identify species lineages, but also because of the inherent ambiguity between natural populations and species paradigms. The result has been a debate about the supremacy of various species concepts and criteria. Here, we utilized multiple separate sources of molecular data, mtDNA, nuclear sequences, and microsatellites, to delimit species under a polytypic species concept (PTSC) and estimate the frequency and genomic extent of introgression in a Neotropical genus of cichlid fishes (Cichla). We compared our inferences of species boundaries and introgression under this paradigm to those when species are identified under a diagnostic species concept (DSC). RESULTS: We find that, based on extensive molecular data and an inclusive species concept, 8 separate biological entities should be recognized rather than the 15 described species of Cichla. Under the PTSC, fewer individuals are expected to exhibit hybrid ancestry than under the DSC (~2% vs. ~12%), but more of the species exhibit introgression from at least one other species (75% vs. 60%). Under either species concept, the phylogenetic breadth of introgression in this group is notable, with both sister species and species from different major mtDNA clades exhibiting introgression. CONCLUSIONS: Introgression was observed to be a widespread phenomenon for delimited species in this group. While several instances of introgressive hybridization were observed in anthropogenically altered habitats, most were found in undisturbed natural habitats, suggesting that introgression is a natural but ephemeral part of the evolution of many tropical species. Nevertheless, even transient introgression may facilitate an increase in genetic diversity or transfer of adaptive mutations that have important consequences in the evolution of tropical biodiversity.     

Calyptospora tucunarensis n. sp. (Apicomplexa: Sporozoea) from the liver of tucunare Cichla ocellaris in Brazil

A coccidian infection of high prevalence and intensity was demonstrated in the liver of tucunare Cichla ocellaris from both natural waters of northeast Brazil and those cultured in fish farms. The immature oöcysts of this parasite were seen uniformly dispersed in the liver,and its mature oöcysts formed large aggregations. The sporocysts were characterised by a single sporopodium and a membranous veil surrounding them. The parasite is described as a new species, Calyptospora tucunarensis. This is the second report on a calyptosporid in a South American fish.     

First record of pughead deformity in Cichla kelberi (Teleostei: Cichlidae), an invasive species in an estuarine system in south‐eastern Brazil

The first record of pughead deformity in a Neotropical freshwater fish not raised in captivity is provided, based on an adult male of Cichla kelberi introduced into an estuary of Rio de Janeiro State, south‐eastern Brazil. A general biological characterization of the specimen is provided and aspects of its aberrant anatomy are described. Environmental and biological factors that may cause pughead deformity in fishes are discussed.     

Breeding behaviour and distribution of the tucunaréCichla aff. monoculus in a clear water river of the Bolivian Amazon

The breeding behaviour and distribution of tucunaré Cichla aff. monoculus were studied for 2 months during the breeding season in the Paraguá River, Bolivia. Tucunaré were more abundant in the old remnant channels and isolated lakes than in the main river channel. The breeding period was delayed for c . 1 month in the river compared to the old remnant channels and lakes. The batch fecundity ranged between 3712 and 10 355 for females weighing 460 and 1380 g, respectively. Gonad analysis of egg-guarding or juvenile-guarding females showed that a female was able to spawn more than once during the breeding season. Nests were significantly larger and deeper in the isolated lakes than in the old remnant channels and in the main river. The maximum depth of the nests also differed significantly, being deeper in the isolated lakes than in the river channel and in the old remnant channels.     

Spermiogenesis and sperm ultrastructure in Cichla intermedia with some considerations about Labroidei spermatozoa (Teleostei, Perciformes, Cichlidae)

Spermiogenesis and spermatozoal structure were studied in Cichla intermedia, a primitive species of Neotropical Cichlids. The analysis shows that spermiogenesis is characterized by chromatin compaction, flagellum development, nuclear rotation, nuclear fossa formation and residual cytoplasm elimination. In the spermatozoa, the head is round, the nucleus contains highly condensed filamentous clusters of chromatin and an acrosome is absent. The nuclear fossa is slightly eccentric and shows a projection that penetrates into the nuclear outline. The proximal centriole is located in the initial segment of the nuclear fossa. The midpiece and the cytoplasmic channel are long. The mitochondria, about 10 in number, are round or slightly elongated, disposed in two layers around the initial segment of the flagellum. The flagellum has a classical 9+2 axoneme and two lateral fins. The data available show that no characteristics of spermiogenesis or spermatozoa are exclusively found in members of the suborder Labroidei. However, three characteristics seem to be exclusively observed in Cichlidae: (1) compact filamentous clusters of chromatin; (2) slightly eccentric nuclear fossa; and, (3) number of mitochondria.     

Permanent Genetic Resources added to Molecular Ecology Resources Database 1 April 2012 - 31 May 2012

This article documents the addition of 123 microsatellite marker loci to the Molecular Ecology Resources Database. Loci were developed for the following species: Brenthis ino, Cichla orinocensis, Cichla temensis, Epinephelus striatus, Gobio gobio, Liocarcinus depurator, Macrolophus pygmaeus, Monilinia vaccinii-corymbosi, Pelochelys cantorii, Philotrypesis josephi, Romanogobio vladykovi, Takydromus luyeanus and Takydromus viridipunctatus. These loci were cross-tested on the following species: Cichla intermedia, Cichla ocellaris, Cichla pinima, Epinephelus acanthistius, Gobio carpathicus, Gobio obtusirostris, Gobio sp. 1, Gobio volgensis, Macrolophus costalis, Macrolophus melanotoma, Macrolophus pygmaeus, Romanogobio albipinnatus, Romanogobio banaticus, Romanogobio belingi, Romanogobio kesslerii, Romanogobio parvus, Romanogobio pentatrichus, Romanogobio uranoscopus, Takydromus formosanus, Takydromus hsuehshanesis and Takydromus stejnegeri.     

Digestive tract morphology of the Neotropical piscivorous fish Cichla kelberi (Perciformes: Cichlidae) introduced into an oligotrophic Brazilian reservoir

Despite being one of the most well-known cichlid fish of importance to artisanal and sport fishing, and among the largest fishes in the Neotropics, data on digestive tract anatomy of peacock basses (Cichla spp.) are largely lacking, especially for non-native populations. In this paper, we describe for the first time the digestive tract morphology of Cichla kelberi, a voracious piscivore that was introduced in the 1950s into an oligotrophic and physically low-complex impoundment in Brazil. Peacock basses were collected between 1994 and 2002 in Lajes Reservoir, through gillnets (25 to 55mm mesh; 20-50 x 2m), seines (10 x 2.5m; 8.0mm mesh), cast nets and angling. All the fishes were kept on ice in the field and then transferred to the laboratory, where they were identified, measured, weighed and dissected for digestive tract analyses. The Index of Relative Importance-IRI was calculated for diet characterization while linear and non-linear regressions were performed to assess growth patterns of four morphological characters related to feeding (e.g. mouth width, mouth height, stomach length and intestine length) and the number of gill rakers during the C. kelberi ontogeny. Most digestive tract structures were directly related to the piscivorous diet of C. kelberi, indicating that peacock bass is a diurnal, bathypelagic and gape-size limited predator that feeds largely on shallow-water prey species within the littoral zone. Mouth width and height grew allometrically (b > 1) with the size of peacock bass, broadening the size range in which prey can be eaten, but especially for predators smaller than -400mm of total length. Differently, stomach and intestine lengths increased isometrically (b = 1), which could constrain prey consumption for adult C. kelberi, especially those at advanced stages of gonadal maturation. The presence of longer-drawn, sharp and furcated gill rakers in C. kelberi may be related to increased prey retention in the resource-limited Lajes Reservoir, but further studies are necessary whether such features are randomly triggered by genetic or phenotypic anomalies, or effectively bring ecological advantages to the predator. In addition to contribute to improve the current biological knowledge on peacock basses, our results can be also useful to further comparisons on whether those morphological features related to feeding will change with transitions on prey consumption by C. kelberi and/or with the particular conditions of the invaded ecosystem.     

Reproductive ecology of a neotropical cichlid fish,Cichla monoculus (Osteichthyes: Cichlidae)

The reproductive ecology of the freshwater fish Cichla monoculus Spix, 1831 (Osteichthyes: Cichlidae) was investigated in the Campo Grande Reservoir, Northeast Brazil. Rainfall, temperature, pH, dissolved oxygen and electrical conductivity of the water were recorded monthly. Fish collected on a monthly basis were measured, weighted, dissected, sexed and the stage of maturation of the gonads were assessed by macro and microscopic means. The semi-arid study region has short spells of rain of 2-3 months duration interspersed with dry seasons. A positive correlation was observed between rainfall and air and water temperatures and conductivity of the water. The study population had an extended spawning season, with peak reproductive activity coinciding with low water temperatures. Males were longer and heavier than females on average and were larger at onset of sexual maturity. The size frequency distributions of the oocytes indicate that C. monoculus is a multiple spawner with an estimated batch fecundity of 3100. Condition factor showed an inverse relationship in relation to gonad size during maturation in both sexes and spent fish were in poor condition. In mature males, lipid stores in the post-occipital cephalic protuberance, a secondary sexual characteristic developed during the reproductive phase, which depleted in spent individuals. The success of this fish is attributed to its reproductive capacity and to the phenotypic plasticity that allows it to adapt to the harsh ecological conditions that prevail in the semi-arid region of Northeast Brazil.     

Ecology of Cichla monoculus (Osteichthyes: Cichlidae) from a reservoir in the semi-arid region of Brazil

The ecology of the freshwater fish Cichla monoculus Spix et Agassiz, 1831 (Osteichthyes: Cichlidae) was investigated in the Campo Grande Reservoir, Northeast Brazil. Rainfall, temperature, pH, dissolved oxygen and electrical conductivity of the water were recorded monthly. Fish collected on a monthly basis were measured, weighed, dissected, sexed and the stages of maturation of the gonads were assessed by macro and microscopic means. The semi-arid study region had short spells of rain interspaced with dry seasons. A positive correlation was observed between rainfall and air and water temperatures and electrical conductivity of the water. The study population had an extended spawning season, with peak of reproductive activity coinciding with low water temperatures. Males were longer and heavier than females on an average and were larger at onset of sexual maturity. The size frequency distributions of the oocytes indicate that C. monoculus is a multiple spawner with an estimated batch fecundity of 3100. Condition factor showed an inverse relationship with gonad size during maturation in both sexes and spent fish were in poor condition. In mature males, lipid stores in the post-occipital cephalic protuberance, a secondary sexual characteristic developed during the reproductive phase, were depleted in spent individuals. The success of this fish is attributed to its reproductive capacity and to the phenotypic plasticity that allows it to adapt to the harsh ecological conditions that prevail in the semi-arid region of Northeast Brazil.     

Fish fauna destruction after the introduction of a non-native predator (Cichla kelberi) in a Neotropical reservoir

In South America, the introduction of peacock-bass (Cichla), a voracious predator fish, has been an underestimated threat for native fish communities. Although this predator is widespread in many reservoirs, few studies have explored its impact on biodiversity. To investigate the relationship between invasion and fish diversity, the present study followed a natural experiment in the Rosana Reservoir (Paraná River basin), where Cichla kelberi were introduced in 2004. We monitored fish assemblages associated with submerged macrophytes between 2003 and 2007, using a 1 m² throw trap. In the years following the introduction, fish diversity dramatically changed. For example, in March 2007, mean fish density and richness were reduced by ca. 95 and 80%, respectively, and many small-sized species had vanished. One aspect was the gradual change of biodiversity, which unfolded at two times during each year: (1) impacts during summer/autumn periods, which coincided with large shoals of young C. kelberi in the patches; and (2) assemblage recovery during the spring. The sequence of extinction-colonization events, however, might not be able to maintain fish assemblages due to the decrease in recovery intensity each spring; assuming a constant decline rate in the coming years, we predict complete assemblage extinction by the summer of 2010. Results from this natural experiment provided evidence supporting the collapse of fish assemblages soon after the introduction of C. kelberi. Such rapid destruction (2 years) reveals an important homogenizing force behind this predator and stresses the need for control measures that prevent new transferences among South American basins.