Endemic Species Flock Research Articles

Mastacembelid eels support Lake Tanganyika as an evolutionary hotspot of diversification

BackgroundLake Tanganyika (LT) is the oldest of the African Rift Lakes and is one of the richest freshwater ecosystems on Earth, with high levels of faunal diversity and endemism. The endemic species flocks that occur in this lake, such as cichlid fishes, gastropods, catfish and crabs, provide unique comparative systems for the study of patterns and processes of speciation. Mastacembelid eels (Teleostei: Mastacembelidae) are a predominately riverine family of freshwater fish, occurring across Africa and Asia, but which also form a small species flock in LT.MethodsIncluding 25 species across Africa, plus Asian representatives as outgroups, we present the first molecular phylogenetic analysis for the group, focusing particularly on the evolutionary history and biodiversity of LT mastacembelid eels. A combined matrix of nuclear and mitochondrial genes based on 3118 bp are analysed implementing different phylogenetic methods, including Bayesian inference and maximum likelihood.ResultsLT Mastacembelus are recovered as monophyletic, and analyses reveal the rapid diversification of five main LT lineages. Relaxed molecular clock dates provide age estimates for the LT flock at ~7-8 Myr, indicating intralacustrine diversification, with further speciation events coinciding with periods of lower lake level. Our analyses also reveal as yet undescribed diversity of lacustrine and riverine species. A Southern-Eastern African clade, that is younger than the LT flock, is also recovered, while West African taxa are basal members of the African mastacembelid clade.ConclusionsThat the LT species flock of mastacembelid eels appears to have colonised and immediately diversified soon after the formation of the lake, supports the view of LT as an evolutionary hotspot of diversification. We find evidence for biogeographic clades mirroring a similar pattern to other ichthyological faunas. In addition, our analyses also highlight a split of African and Asian mastacembelid eels at ~19 Myr that is considerably younger than the split between their associated continents, suggesting a dispersal scenario for their current distribution.

Phylogenetic relationships of species of Crenicichla (Teleostei: Cichlidae) from southern South America based on the mitochondrial cytochrome b gene

Phylogenetic analysis using Bayesian inference, likelihood and parsimony methods was conducted on 60 complete mitochondrial cytochrome b sequences from 21 species of Crenicichla, including all species known from Uruguay (Crenicichla celidochilus, Crenicichla lepidota Crenicichla minuano, Crenicichla missioneira, Crenicichla punctata, Crenicichla scottii, Crenicichla vittata), Crenicichla compressiceps, Crenicichla empheres, Crenicichla geayi, Crenicichla iguassuensis, Crenicichla macrophthalma, Crenicichla menezesi, Crenicichla notophthalmus, Crenicichla regani, Crenicichla cf. regani, Crenicichla semifasciata, Crenicichla sveni, Crenicichla tendybaguassu, two unidentified species, and also two species of Teleocichla. Bayesian analysis resulted in a trichotomy with three major groups: (1) The C. missioneira species group (C. celidochilus, C. empheres, C. minuano, C. missioneira, C. tendybaguassu, and an undescribed species analyzed); (2) a group of southern species (C. iguassuensis, C. punctata, C. scottii, C. vittata); and (3) a rather heterogeneous group comprising the type species C. macrophthalma, members of the Crenicichla reticulata species group (C. geayi, C. semifasciata), members of the Crenicichla wallacii species group (C. compressiceps, C. notophthalmus, C. regani, C. cf. regani), members of the Crenicichla saxatilis species group (C. lepidota, C. menezesi, C. sveni, C. sp.), and two species of Teleocichla. Parsimony jackknifing resulted in a quadritomy with: (1) C. macrophthalma, (2) Teleocichla, (3) the saxatilis + wallacii group species, and (4) the rest, which include C. geayi and C. semifasciata as sister group to a dichotomy with the C. missioneira group and the remaining southern species. The sequence variation within the C. missioneira group is remarkably minor despite considerable morphological differences, supporting the conclusion that it forms an endemic species flock in the Uruguay River basin. Previously proposed species groups within the speciose genus Crenicichla (more than 90 species known) are partly corroborated. However, C. celidochilus was not previously associated with the C. missioneira species group, and C. vittata has not previously been associated with C. scottii, C. iguassuensis, or C. punctata. Crenicichla lepidota, C. sveni, C. menezesi and C. sp. represent the C. saxatilis group. Species of small size, representing the C. wallacii species group and Teleocichla are characterized by very long branches, and the position of Teleocichla differed considerably between the Bayesian and parsimony trees. This finding does not invalidate Teleocichla but rather suggests that the several monophyletic major clades within Crenicichla may need nominal recognition. A putative hybrid specimen with a morphology combining components from C. vittata and C. scottii, but with a cytochrome b sequence from C. scottii was found in a sample from the Rio Quarai/Cuareim. Another putative hybrid specimen with a unique morphology but a cytochrome b sequence agreeing with C. scottii was found in a sample from Maldonado, but no other Crenicichla species than C. scottii is known from that locality.

Escape from the Ponto-Caspian: Evolution and biogeography of an endemic goby species flock (Benthophilinae: Gobiidae: Teleostei)

Endemic Ponto-Caspian gobies include a flock of ∼24 “neogobiin” species (containing the nominal genera and subgenera Apollonia, Babka, Neogobius, Mesogobius, Ponticola, and Proterorhinus; Teleostei: Gobiidae), of which a large proportion (5 species; ∼21%) recently escaped to invade other freshwater Eurasian systems and the North American Great Lakes. We provide its first comprehensive phylogenetic and biogeographic analysis based on 4709 bp sequences from two mitochondrial and two nuclear genes with maximum parsimony, likelihood, and Bayesian approaches. We additionally compare its relationships with the tadpole gobies ( Benthophilus and Caspiosoma), which comprise a related endemic Ponto-Caspian gobiid group; along with a variety of postulated relatives and outgroups. Results of all phylogenetic approaches are highly congruent and provide very strong support for recognizing the subfamily Benthophilinae; which encompasses both the “neogobiins” and tadpole gobies, and genetically diverges from other Gobiidae subfamilies—including (non-monophyletic) Gobiinae and Gobinellinae. Benthophilinae contains three tribes: Neogobiini ( Neogobius, which is synonymized here with Apollonia; containing the type species N. fluviatilis, along with N. melanostomus and N. caspius), Ponticolini (containing the genera Mesogobius, Proterorhinus, Babka, and Ponticola—elevating the latter two from subgenera and removing them from the formerly paraphyletic Neogobius), and Benthophilini (tadpole gobies). Within Ponticolini, Proterorhinus and Mesogobius comprise the sister clade of the Ponticola and Babka clade. Further work is needed to clarify the interrelationships of the tadpole gobies. Invasiveness is widespread in freshwater and euryhaline taxa of Neogobius, Proterorhinus, Babka, and Ponticola; but not in marine species, Mesogobius, or tadpole gobies.

Ancient lakes as hotspots of diversity: a morphological review of an endemic species flock of Tylomelania (Gastropoda: Cerithioidea: Pachychilidae) in the Malili lake system on Sulawesi, Indonesia

The viviparous freshwater gastropod Tylomelania (Caenogastropoda: Cerithioidea: Pachychilidae) endemic to the Indonesian island Sulawesi has radiated extensively in two ancient lake systems. We here present the first systematic species-level review of taxa in the five lakes of the Malili lake system, which contains the most diverse and best studied freshwater fauna on Sulawesi. Our results indicate a significantly higher diversity of Tylomelania in these lakes than previously perceived based on morphological evidence for delimiting the taxa. We describe nine new species, thus increasing the number of taxa known from the Malili lakes to 25. Tylomelania species are inhabiting all available substrates in the lakes, and the diversity of habitats is reflected in an unparalleled range of radula types in this closely related group. Several species show a high intraspecific variability in some characters, and their closer investigation will probably lead to the discovery of more cryptic species. As it is, this species flock on Sulawesi is among the largest freshwater mollusc radiations known. Since the Malili lake system also contains other large endemic species flocks of e.g. crustaceans and fishes, it is a major hotspot of freshwater biodiversity in Asia to become a conservation priority.

The impact of invasive fish on an endemic Cyprinodon species flock (Teleostei) from Laguna Chichancanab, Yucatan, Mexico

Abstract – Species that invade a new environment often may lead to population declines of endemic species. Here I document the invasions of an African cichlid (genus Oreochromis) in 1988 and the Mexican Astyanax fasciatus (Characidae) in 1996 into Laguna Chichancanab (Yucatan, Mexico), and the impact on an endemic Cyprinodon species flock and the poeciliid Gambusia sexradiata. After the invasion of Astyanax fasciatus, their relative abundances decreased enormously, most likely caused by predation on the fry. One species, Cyprinodon simus, might have even gone extinct or just occurs in extremely reduced numbers. Furthermore, it was observed that the percentage abundance of the detritivorous Cyprinodon beltrani increased significantly, in contrast to all other Cyprinodon species. This study also revealed that infestation by metacercaria (black spots) of an ectoparasitic trematode and of an endoparasitic nematode increased in the Cyprinodon spp. following the introduction of Oreochromis. Whereas the infestation by trematodes decreased after a period of 6 years, the prevalence and intensity of infestation by nematodes stayed at a high level. In contrast, in G. sexradiata the parasite load remained always very low.

Rapid evolution of sessility in an endemic species flock of the freshwater bivalve Corbicula from ancient lakes on Sulawesi, Indonesia

The fauna of ancient lakes frequently contains taxa with highly derived morphologies that resulted from in situ radiation of lacustrine lineages with high antiquity. We employed a molecular mtDNA phylogeny to investigate this claim for corbiculid freshwater bivalves in two ancient lake systems on the Indonesian island Sulawesi. Among the otherwise mobile corbiculid species flock, only one taxon, Posostrea anomioides, in the ancient Lake Poso exhibits a unique habit, i.e. cementing one valve to the substrate. Our data show that Corbicula on Sulawesi is polyphyletic, with the endemic riverine taxa in terminal position, and the lacustrine species flock being paraphyletic. Surprisingly, Posostrea is not confirmed as a genus distinct from Corbicula and genetic distances suggest a rather recent origin from the only other corbiculid species endemic to Lake Poso, the non-cementing Corbicula possoensis. While the cementing anomioides, despite its unique behavioural and morphological characteristics, clusters together with non-sessile Corbicula species, the latter exhibit strong genetic distances in the absence of morphological disparity and fall into several genetically rather distinct clades. These findings suggest that developmental plasticity of animals in ancient lakes rather than the antiquity of lineages might account for the unique morphology of some species.

Escalation and trophic specialization drive adaptive radiation of freshwater gastropods in ancient lakes on Sulawesi, Indonesia

Species flocks in ancient lakes have long been appreciated as ideal model systems for the study of speciation and adaptive processes. We here present data from a new invertebrate model system with intrinsic parameters distinct from those of other documented radiations. The ancient lakes on Sulawesi harbour an endemic species flock of at least 33 species of viviparous snails. Molecular data reveal multiple independent colonizations of the lakes by riverine ancestors. In each colonizing clade, parallel evolution of conspicuous shell morphologies, followed by a differentiation of trophic morphology and the development of habitat specificity can be observed. Extensive shell crushing experiments and strong dentition of the chelae observed in some lacustrine crab species suggest that coevolution with crabs, i.e. escalation, is the most likely cause of initial shell divergence. By contrast, repeated parallel evolution in radula morphology indicates that speciation within lineages is driven by divergent adaptation to different resources among sympatric taxa. The inclusion of coevolutionary processes is unique in this system compared with diversification models developed for vertebrate radiations.

Toothless predators: feeding performance and techniques among the piscivores within Lake Tana's endemic barbus species flock (Pisces:Cyprinidae)

With more than 2000 fish species the Cyprinidae is the largest family of vertebrates. Lake Tana, a large lake (3050 km2) situated in the NW‐ highlands of Ethiopia, harbours, as far as we know the only remaining intact species flock of large (max. 100 cm FL) cyprinid fishes (15 Barbus spp.). One of the most intriguing aspects of this endemic Barbus species flock is the large number of piscivores (8). Cyprinid fishes seem not well designed for piscivory, they lack teeth in the oral jaw, have a small slit‐shaped pharyngeal cavity and all lack a stomach with low pH for digesting large prey. Many barbs are benthivorous species, like the ancestral barb in Lake Tana's isolated system. Why then is piscivory, which is rare among cyprinids, so common in Lake Tana Barbus? The aim of present study was to compare the performance and techniques of these piscivorous Barbus with known piscivores from other fish families. We studied prey handling times over prey size, prey capture using high‐speed movies, and assessed the effect of prey size on performance and prey selection in the field. Performances were explained by functional morphology of their feeding system. Overall, Lake Tana's piscivorous Barbus perform relatively ‘poor’, compared to piscivores from other fish families. For example, Lake Tana's piscivores are only able to handle prey fish smaller than 16% of their own body length. However, Lake Tana lacks potential piscivorous competitors, rendering the piscivorous Barbus by far the ‘best’ and apparently highly successful. They have adapted to all available macro‐habitats (littoral, offshore pelagic and offshore benthic), using different techniques (ambush, pursuit and cruising), a unique scenario for barbs.

Ecological position of ‘small barbs’ and their potential for fisheries: An option to reduce fishing pressure on ‘large barbs’ of Lake Tana (Ethiopia)?

The two barbs, Barbus humilis and Barbus tanapelagius are important pelagic fish in Lake Tana. These ‘small barb’ species (<10 cm fork length) play a key role in the Lake's ecosystem as a link between zooplankton and the top predators, mostly ‘large barbs’. This paper presents an overview on the position of ‘small barbs’ in the food web of Lake Tana as indicated from gut content analysis. Barbus tanapelagius, the most abundant and specialized species, exploited zooplankton. Barbus humilis mostly fed on detritus and zooplankton. Barbus tanapelagius, and to some extent the benthopelagic Barbus humilis, transferred energy from zooplankton to the top level of the food web. Barbus humilis is a vector of energy and biomass from detritus to top predators. Pelagic fisheries are proposed as an option to reduce fishing pressure on the endemic species flock of ‘large barbs’. If, however, a fishery on the ‘small barbs’ is proposed to increase the sustainable yield, implications on the ecosystem balance should be critically assessed. Regulations should be recommended for these fisheries (gear, habitats and season) accounting for the biological constraints.

Declining stocks of Lake Tana’s endemic Barbus species flock (Pisces, Cyprinidae): natural variation or human impact?

The only remaining species flock of endemic, large cyprinid fishes is found in Lake Tana, Ethiopia. A monthly experimental trawl program was conducted in 1991–1993 and 1999–2001, sampling 12 stations distributed over three habitats differing in depth and distance to shore. The aim was to compare the total abundance, spatial distribution and proportion of juveniles of the most common Barbus species in the Bahar Dar Gulf between both periods. We found a sharp reduction (75%) in total abundance, both in number and biomass of the Barbus species and even more (90%) in the number of juveniles between the two periods. However, the spatial distribution of the different Barbus species over the three habitats had not changed. High natural variability in fish stocks might be expected in environmentally unstable lakes. Although strongly pulsed (seasonal), Lake Tana is a relatively stable system. No major differences were found in abiotic parameters in 1990s that could have caused the dramatic changes in abundance. The most likely explanation is the negative impact of the motorised, commercial gillnet fishery targeting the spawning aggregations of these barbs. The drastic decline in juveniles points especially towards serious recruitment over-fishing. The results stress the need for the immediate development of a sound management plan focussing on fishing effort restrictions during the Barbus breeding season.

Barbus tanapelagius, A New Species from Lake Tana (Ethiopia): its Morphology and Ecology

The endemic cyprinid species flock in Lake Tana consists of 15 species of large hexaploid barbs, eight of which are piscivorous. Previously, it was assumed that all piscivores preyed on the same small barb species, Barbus trispilopleura. In this paper we present a description of morphology and ecology of a new abundant small barb species, Barbus tanapelagius sp. nova (holotype RMNH 33731) from Lake Tana, Ethiopia, which appears to be the major prey species for the large pelagic piscivorous barbs. B. tanapelagius differs clearly in morphology from the other 3 small, diploid Barbus species known from Lake Tana, B. trispilopleura Boulenger, 1902, B. humilis Boulenger, 1902 and B. pleurogramma Boulenger, 1902. Conspicuous differences are its elongated body, large eye diameter, prominent and hooked lower jaw contour and colouration. Preliminary data suggest that B. tanapelagius also differs ecologically from the other small Barbus spp. by its pelagic, strictly zooplanktivorous feeding and its occurrence mainly in the deeper, offshore waters. The other small Barbus species are most probably largely benthic feeders and dominant in the shallow inshore waters. Previous views about the evolution of the present 8 endemic piscivorous large barb species therefore require reconsideration, as the present paper shows a more complex scenario including several prey species.

Resource partitioning by Lake Tana barbs predicted from fish morphometrics and prey characteristics

We develop a food-fish model (FFM), whichquantitatively relates properties of aquaticfood types (size, shape, escape velocity,habitat, mechanical properties and chemicalquality) to feeding structures of cyprinidfish. The model is based on functionalmorphology and experiments on search, capture,selection, and internal processing of food byfish. The FFM shows which food properties aremost critical in feeding and how fish canoptimise coping with them. Relative food sizeimposes the highest demands, followed by preyvelocity, food habitat and mechanicalproperties. These overrule taxonomic affinitiesof food types. Highly demanding food types(large, fast prey, suspensions of plankton,benthic prey and mechanically tough items)impose incompatible morphological requirementson fish. We apply the FFM to the endemic Barbus species flock of Lake Tana (Ethiopia),since the structural diversity of its 14species reflects recent adaptations to trophicniches. We predict their potentials inutilising different food types by quantitativecomparisons of 35 parameters, measured for eachspecies, with the values for each foodspecialist derived from the FFM. These dietpredictions are tested against gut contentsfrom 4,711 fish, sampled over seasons andhabitats. Gut contents and predictions show agood overall fit. The value of the model isshown by its resolution in predicting resourcepartitioning among the barbs. For the 14 barbsa trophic hierarchy with six major trophicgroups is reconstructed which closely matchesthe predictions. Trophic specialists (> 65%by volume of a single food type) are alsostructurally specialised, whereas less extremeanatomical structures characterise trophicgeneralists, allowing them to switch betweenfeeding modes. Trophic generalists are bestdefined by behavioral flexibility, sincefeeding modes integrate both fish and foodcharacters. The FFM is of practical use inevaluating the role of morphological diversityin an ecosystem and enables the analysis oftrophic interactions in fish communities and ofthe cascading effects by environmental change.Such an approach can be instrumental in thedevelopment of management strategies forfisheries and in conservation of biodiversity.

Persistence of neutral polymorphisms in Lake Victoria cichlid fish.

Phylogenetic trees for groups of closely related species often have different topologies, depending on the genes used. One explanation for the discordant topologies is the persistence of polymorphisms through the speciation phase, followed by differential fixation of alleles in the resulting species. The existence of transspecies polymorphisms has been documented for alleles maintained by balancing selection but not for neutral alleles. In the present study, transspecific persistence of neutral polymorphisms was tested in the endemic haplochromine species flock of Lake Victoria cichlid fish. Putative noncoding region polymorphisms were identified at four randomly selected nuclear loci and tested on a collection of 12 Lake Victoria species and their putative riverine ancestors. At all loci, the same polymorphism was found to be present in nearly all the tested species, both lacustrine and riverine. Different polymorphisms at these loci were found in cichlids of other East African lakes (Malawi and Tanganyika). The Lake Victoria polymorphisms must have therefore arisen after the flocks now inhabiting the three great lakes diverged from one another, but before the riverine ancestors of the Lake Victoria flock colonized the Lake. Calculations based on the mtDNA clock suggest that the polymorphisms have persisted for about 1.4 million years. To maintain neutral polymorphisms for such a long time, the population size must have remained large throughout the entire period.

The destruction of an endemic species flock: quantitative data on the decline of the haplochronic cichlids of Lake Victoria: F. Witte & 6 others, Environmental Biology of Fishes, 34(1), 1992, pp 1–28

The destruction of an endemic species flock: quantitative data on the decline of the haplochronic cichlids of Lake Victoria: F. Witte & 6 others, Environmental Biology of Fishes, 34(1), 1992, pp 1–28

The destruction of an endemic species flock: quantitative data on the decline of the haplochromine cichlids of Lake Victoria

The Lake Victoria fish fauna included an endemic cichlid flock of more than 300 species. To boost fisheries, Nile perch (Lates sp.) was introduced into the lake in the 1950s. In the early 1980s an explosive increase of this predator was observed. Simultaneously, catches of haplochromines decreased. This paper describes the species composition of haplochromines in a research area in the Mwanza Gulf of Lake Victoria prior to the Nile perch upsurge. The decline of the haplochromines as a group and the decline of the number of species in various habitats in the Mwanza Gulf was monitored between 1979 and 1990. Of the 123+ species originally caught at a series of sampling stations ca. 80 had disappeared from the catches after 1986. In deepwater regions and in sub-littoral regions haplochromine catches decreased to virtually zero after the Nile perch boom. Haplochromines were still caught in the littoral regions where Nile perch densities were lower. However, a considerable decrease of species occurred in these regions too. It is expected that a remnant of the original haplochromine fauna will survive in the littoral region of the lake. Extrapolation of the data of the Mwanza Gulf to the entire lake would imply that approximately 200 of the 300+ endemic haplochromine species have already disappeared, or are threatened with extinction. Although fishing had an impact on the haplochromine stocks, the main cause of their decline was predation by Nile perch. The speed of decline differed between species and appeared to depend on their abundance and size, and on the degree of habitat overlap with Nile perch. Since the Nile perch upsurge, the food web of Lake Victoria has changed considerably and the total yield of the fishery has increased three to four times. Dramatic declines of native species have also been observed in other lakes as a result of the introduction of alien predators. However, such data concern less speciose communities and, in most cases, the actual process of extinction has not been monitored.

The impact of the introduced sardine Limnothrissa miodon on the ecology of Lake Kariba

The sardine Limnothrissa miodon was introduced from Lake Tanganyika into the man-made Lake Kariba where it now supports a major fishery. The suggestion that this fish could be introduced into other African lakes has been strongly criticised and this paper outlines its effects on the ecology of Lake Kariba. It may have prevented an indigenous species from becoming a pelagic planktivore but the populations of the predatory tigerfish and some piscivorous birds increased following the sardine introduction. It has caused major changes, similar to those described elsewhere, to the zooplankton. The zooplankton biomass is now very low and it is not clear how it can maintain itself in the face of intense predation by the sardine. Cascade theory suggests that the sardines should have caused changes in the phytoplankton as well but there are too few data available to demonstrate this. The sardines may also have influenced the nutrient economy of the lake and contributed to the decline of the aquatic fern Salvinia molesta, which once covered large areas of the lake. It is concluded that while this species is a suitable candidate for stocking into man-made lakes its introduction into natural lakes is undesirable. This is especially so in Lake Malawi because the sardine's capacity to change the plankton population could threaten the lake's endemic species flocks.

SOME CONTROVERSIAL ASPECTS OF SPECIATION OF AFRICAN CICHLID FISHES

A clear distinction must be made between the intralacustrine speciation shown by some groups of African cichlid fishes and the simple specific proliferation shown by others. The former phenomenon is exhibited by several genera but hardly at all by the genus Tilapia.Inshore dwelling habits and an algal diet have not had restrictive effects on speciation. In fact it is among inshore species that speciation has been most active.While, partially by exploiting their small size, genera which have given rise to the endemic species flocks of the great lakes have become highly specialized for the exploitation of specific niches, the species of Tilapia have usually remained large and unspecialized and therefore capable of existing in a variety of environments.Further consideration of the effects of predation supports the idea that it has accelerated rather than retarded the process of speciation.If certain conditions are fulfilled, closely related species can co‐exist throughout life in one habitat, eat the same kind of food and breed in close proximity to each other.