Speciation of endemic Lake Tana barbs (Cyprinidae, Ethiopia) driven by trophic resource partitioning; a molecular and ecomorphological approach

A unique species flock of large barbs (Barbus spp.) from Lake Tana is presented, from the level of fish stocks to molecules. Evidence is given for the species status of 14 morphotypes of large barbs. They distinctly differ in: (1) head and body morphometrics, (2) food preferences, (3) distribution patterns, (4) maximal body size, (5) spawning area and period, and (6) molecular genetic characters. Most types show early morphological divergence at small size. Major Histocompatibility Complex (MHC) genes, encoding cell membrane proteins involved in defence against pathogens, were found to be diagnostic for the species' genetic identity. A strong selective pressure on particular amino acid positions in the MHC protein sequence most probably arose in response to different pathogen loads from the newly invaded ecological niches after formation of Lake Tana, ca. two million years ago.Arguments for a sympatric origin of this species flock are discussed. An evolutionary scenario suggests a riverine ancestral Barbus intermedius invading Lake Tana after its formation by volcanic blocking of the Blue Nile river and its isolation by waterfalls. Specialisation for particular food types and disruptive selection on many feeding structures are hypothesized as the evolutionary drive in speciation. The causal relationship between the diversity in feeding structures and food types is explained from experiments and models. As an example, the potential food niche of three barb species is predicted from parameter values measured from a large set of feeding structures and tested against the actual gut contents. The co-occurrence of eight piscivorous barb species is unique for cyprinid fish, which lack oral jaw teeth and a stomach. The significance of this aquatic ecosystem as a multidisciplinary evolutionary laboratory and the need for a wise balance between exploitation and conservation is stressed.     

Food and feeding ecology of piscivorous fishes at Lake St Lucia, Zululand

The food and feeding ecology of piscivorous fish in Lake St Lucia was monitored for two years. Piscivorous fishes feed predominantly on the planktivorous Gilchristella aestuarius and Thryssa vitrirostris but a wide range of prey species was recorded. Numbers of the predominant piscivores, Argyrosomus hololepidotus and Elops machnata , in an area appear to be related to the densities of their major prey, T. vitrirostris and G. aestuarius . Large piscivorous fishes are restricted to the deeper portions of the lake, whereas small piscivores such as Johnius belengerii and Terapon jarbua feed predominantly on small fishes in the littoral zone. The highly significant correlation between the composition of prey fish species in the lake and prey fish species in the diet of piscivorous fishes, indicates that piscivores are feeding in a density dependent manner. However, factors such as habitat, fish size and swimming speed of prey species are shown to be important in prey selection. Juvenile fish of species such as Sarotherodon mossambicus, Liza macrolepis and Acanthopagrus berda remain in shallow marginal areas, thus avoiding large piscivorous fishes. However by frequenting shallow areas these species become vulnerable to bird predators, especially egrets and herons.     

Piscivorous fishes diet dominated by the Asian cyprinid invader,topmouth gudgeon (<Emphasis Type="Italic">Pseudorasbora parva</Emphasis>)

Predation on the non-native cyprinid, Pseudorasbora parva, was reported during an annual study in a small connecting canal about 40 km south of Brno, Czech Republic. Two cyprinid fish species (Pseudorasbora parva, Rutilus rutilus) were identified in the diet of 23 piscivores belonging to three native fishes (Perca fluviatilis, Sander lucioperca, Esox lucius). The relative abundance of prey fishes changed seasonally and was dominated by the topmouth gudgeon in spring. Thereafter roach incidence continuously increased. In contrast, topmouth gudgeon was found to be a more sized-available prey and was the most dominant prey species in the diet of all piscivorous fishes during the whole season. Strong piscivory towards this alien might be beneficial for its eradication or control to support ecological integrity in natural and modified seminatural habitats.     

Phenetic relationships and probable ways of morphological diversification of the African large barbs (<Emphasis Type="Italic">Barbus intermedius</Emphasis> complex) in Lake Tana (Ethiopia)

29 quantitative and 18 qualitative skull characters were studied in the African large barbs (Barbus intermedius complex) from Lake Tana (Ethiopia). Based on results of principle components analysis phenetic relationships of 12 morphotypes were assessed. External features diagnostic of the morphotypes were found in individuals substantially different in the skull characters. The obtained data along with the data on morphological diversity of large barbs from Ethiopia beyond the Lake Tana basin suggest origination of the Lake Tana complex of forms from a complex of forms that existed in the upper reaches of the Blue Nile before the lake came into being, and the extant morphotypes of the Lake Tana barbs originated from three or four forms that composed the ancestral riverine local complex.     

Piscivory and prey selection of four predator species in a whitefish dominated subarctic lake

According to logistic regressions derived for pike Esox lucius and burbot Lota lota , the probability of ingesting fishes in Lake Muddusjärvi, northern Finland, was 50% at 19·3 and 22·1 cm L _T, whereas Arctic charr Salvelinus alpinus and brown trout Salmo trutta shifted to piscivory at the lengths of 25·7 and 26·4 cm L _T. The specialist piscivores, pike and burbot, consumed more prey species and took a wider range of prey sizes than Arctic charr and brown trout. The prey length for all predators increased in relationship to predator length. Whitefish Coregonus lavaretus was the dominant prey species in the lake and in the diet of all the piscivorous species. The whitefish population was divided into three forms, of which the slow-growing, and the most numerous densely rakered whitefish form (DR), was selected by all predator species. This form also had the smallest average size and widest habitat range, utilizing both pelagic and epibenthic habitats. Two sparsely rakered whitefish forms (LSR and SSR) occupied only epibenthic habitats and had lower relative densities than DR. These forms, LSR and SSR, had a minor importance in the diet of predator species.     

The role of the thyroid gland hormone in ontogenesis and morphological diversification of Barbus intermedius sensu of Lake Tana in Ethiopia

The role of thyroid gland hormone in the ontogenesis of the Large African Barb Barbus intermedius sensu Banister, 1973 (Teleostei; Cyprinidae)--the supposed ancestral species which produced the species flock of the large African Barbs of the Lake Tana (Ethiopia)--has been studied. It has been shown that the thyroid hormone influences the period of many morphological processes and a change in its level causes heterochrony, reflecting on the definitive morphology of fish. Thus, it can be assumed that even a slight change in activity of the thyroid axis in the process of ontogenesis can be the cause of wide variability of the morphological features of B. intermedius and is at the basis for the fast diversification of the species flock of Big African Barbs of Lake Tana.     

Major histocompatibility genes in the Lake Tana African large barb species flock: evidence for complete partitioning of class II B, but not class I, genes among different species

The 16 African large barb fish species of Lake Tana inhabit different ecological niches, exploit different food webs and have different temporal and spatial spawning patterns within the lake. This unique fish species flock is thought to be the result of adaptive radiation within the past 5 million years. Previous analyses of major histocompatibility class II B exon 2 sequences in four Lake Tana African large barb species revealed that these sequences are indeed under selection. No sharing of class II B alleles was observed among the four Lake Tana African large barb species. In this study we analysed the class II B exon 2 sequences of seven additional Lake Tana African large barb species and African large barbs from the Blue Nile and its tributaries. In addition, the presence and variability of major histocompatibility complex class I UA exon 3 sequences in six Lake Tana and Blue Nile African large barb species was analysed. Phylogenetic lineages are maintained by purifying or neutral selection on non-peptide binding regions. Class II B intron 1 and exon 2 sequences were not shared among the different Lake Tana African large barb species or with the riverine barb species. In contrast, identical class I UA exon 3 sequences were found both in the lacustrine and riverine barb species. Our analyses demonstrate complete partitioning of class II B alleles among Lake Tana African large barb species. In contrast, class I alleles remain for the large part shared among species. These different modes of evolution probably reflect the unlinked nature of major histocompatibility genes in teleost fishes.Electronic Supplementary Material Supplementary material is available for this article at .An erratum to this article can be found at     

Functional groups in piscivorous fishes

Piscivory is a key ecological function in aquatic ecosystems, mediating energy flow within trophic networks. However, our understanding of the nature of piscivory is limited; we currently lack an empirical assessment of the dynamics of prey capture and how this differs between piscivores. We therefore conducted aquarium‐based performance experiments, to test the feeding abilities of 19 piscivorous fish species. We quantified their feeding morphology, striking, capturing, and processing behavior. We identify two major functional groups: grabbers and engulfers. Grabbers are characterized by horizontal, long‐distance strikes, capturing their prey tailfirst and subsequently processing their prey using their oral jaw teeth. Engulfers strike from short distances, from high angles above or below their prey, engulfing their prey and swallowing their prey whole. Based on a meta‐analysis of 2,209 published in situ predator–prey relationships in marine and freshwater aquatic environments, we show resource partitioning between grabbers and engulfers. Our results provide a functional classification for piscivorous fishes delineating patterns, which transcend habitats, that may help explain size structures in fish communities.     

Role of thyroid hormone in the ontogeny and morphological diversification of <Emphasis Type="Italic">Barbus intermedius sensu</Emphasis> Banister, 1973 of Lake Tana in Ethiopia

The role of thyroid hormone in the ontogeny of the Large African barb Barbus intermedius sensu Banister, 1973 (Teleostei; Cyprinidae)—the presumed ancestral species for the species flock of the large African Barbs of Lake Tana (Ethiopia)—has been studied. It has been shown that the thyroid hormone influences the timing and rate of many morphogenetic processes and a change in its level causes heterochronies, affecting the definitive morphology of fish. Thus, it can be assumed that even a slight change in activity of the thyroid axis during ontogeny can be the cause of wide morphological variability in B. intermedius and may underlie explosive diversification of the species flock of Large African Barbs of Lake Tana.     

Genetic divergence among morphotypes of Lake Tana (Ethiopia) barbs

The genus Barbus is a paraphyletic assemblage that includes three different ploidy levels: diploid, tetraploid and hexaploid. 'B.' intermedins , which inhabits Lake Tana (Ethiopia), is a hexaploid taxon that forms a 'species flock' consisting of at least 14 morphotypes. Thirty-one presumptive allozymic loci were analysed in a large sample of 'B.' intermedius. No diagnostic loci were observed between the morphotypes, but substantial differences in allele frequencies were found. One morphotype, Acute, differs significantly from the others. The presence of this genetic differentiation within the lake strongly suggests that the morphotypes are diverging lineages. Because of some parallel characteristics with cichlid species flocks, we put forward the hypothesis that the morphotypes of barbs in Lake Tana represent a species flock that originated via sympatric speciation with more rapid morphological than molecular differentiation. If the differentiation and the reproductive isolation are real, it is probable that the morphotypes already are or will soon reach the status of species.     

Accelerating the onset of piscivory: intersection of predator and prey phenologies

Piscivorous fishes tend to be able to consume other fishes early in development and generally experience a dramatic increase in growth after the ontogenetic diet shift to piscine prey. Hence, an acceleration of the onset of piscivory may be favoured strongly by natural selection. Temperate freshwater piscivores, for example, becomes piscivorous at a relatively young age by spawning in advance of, and thereby achieving a size advantage over, the young of their piscine prey. Research in various North American estuaries suggests that young-of-the-year (YOY) bluefish Pomatomus saltatrix , an offshore-spawning estuarine-dependent marine fish, may accelerate the onset of piscivory by being advected to higher latitudes and timing their estuarine entry with the appearance of small coastal fishes. This hypothesis was tested by: (i) determining the annual recruitment date of YOY bluefish and their prey; and (ii) examining the diet and prey size preferences, and predator size-prey size relationships, of YOY bluefish in two different estuarine systems: Great South Bay, and the lower Hudson River. Results suggest that the relationships between bluefish and their prey are determined by a complex interplay between recruitment timing of both predator and prey, prey size availability, predator selectivities, and the timing of vernal warming. It is concluded that YOY bluefish migration into northern estuaries at an advanced size provides them with a predatory size advantage over their principal piscine prey thereby facilitating an early diet shift to piscivory white minimizing the time spent as planktivores.     

Lacustrine spawning: is this a new reproductive strategy among ‘large’ African cyprinid fishes?

Changes in the gonado‐somatic index and abundance of the different Labeobarbus species in the mouths of four major afferent rivers of Lake Tana, Ethiopia, were monitored monthly during 1999 and 2000. Riverine spawning was characteristic for seven of Lake Tana's 15 contemporary Labeobarbus species. These seven did not show spatial segregation among afferent rivers but significant temporal segregation occurred in aggregating in the river mouths and migrating towards the upstream spawning areas during the breeding season (June–October). Among the eight other species, peak gonad development occurred generally in the same period as in the riverine spawners. These species, however, did not aggregate in the river mouths during the breeding period and were absent from the upstream spawning areas. A derived, novel strategy, lacustrine spawning was hypothesized for these eight Labeobarbus species. This hypothesis was further supported by observations of running female fishes in the littoral zones distant from any of the afferent rivers. This derived strategy is only common among the littoral‐dwelling Labeobarbus species with restricted distribution patterns. At present it is thought that sequential waves of speciation and habitat divergence followed by trophic specialization, shaped the diversity of Lake Tana labeobarbs.     

Diet segregation between two sympatric 'small'Barbus spp: an experimental study of mechanisms

Gut contents of two co‐occurring species of 'small' diploid barbs (<10  L _F cm) in Lake Tana revealed that zooplankton is the major diet component for B. tanapelagius (75% based on volume), but less prominent in B. humilis (40%). Functional response experiments in the laboratory were conducted to elucidate the mechanisms causing this difference. The type of functional response by the two 'small' barbs under different microcrustacean zooplankton densities (10, 20, 40, 60 and 80 ind.l⁻¹) was examined. The functional response of B. tanapelagius to increasing prey densities corroborates with Holling Type II model, whereas B. humilis exhibits a Type III functional response. Predation rate is higher for B. tanapelagius at low zooplankton density (<40 ind.l⁻¹) and equals the level of B. humilis at higher densities (>40 ind.l⁻¹). This suggests that at lower zooplankton densities B. humilis is a less efficient forager on zooplankton prey items than B. tanapelagius . In Lake Tana average zooplankton density is relatively low (<35 ind.l⁻¹). Under these food conditions, B. humilis is forced to feed on other food items (e.g. benthic invertebrates), whereas B. tanapelagius primarily feeds on zooplankton. The feeding potentials of the two 'small' barbs, as deduced from their morphology explain their different performances and their segregation in space and food resources.     

Comparison of losses of planktivorous fish by predation and seine-fishing in a lake undergoing long-term biomanipulation

SUMMARY 1. Piscivore stocking at artificially high densities and fishing are the two common approaches to reduce the amount of planktivorous and benthivorous fish in lake biomanipulation programmes. Both measures have advantages and disadvantages, but their relative efficacy has not previously been directly compared.
2. We calculated the average annual catch of roach and bream in a lake undergoing long-term biomanipulation (Feldberger Haussee, Germany) by seining each year between 1992 and 1998. We compared this value with a bioenergetics estimate of annual consumption rates of the dominant cohorts of piscivores, pikeperch and pike, in 1997 and 1998. We also determined species composition and length distribution of prey fish in stomachs of the piscivores.
3. Roach was the dominant prey species of both pikeperch and pike, whereas bream was rarely taken by either piscivorous species. Seining removed on average larger specimens of roach than were found in the stomachs of the piscivores.
4. Based on stocking densities of the piscivores, published mortality rates, and individual consumption rates, feeding of pikeperch and pike on roach exceeded the manual removal of roach by seining by a factor of 4–15 (biomass) in 1997 and 1998.
5. Based on these results, a combination of fishing and piscivore enhancement is recommended. Whereas the stocks of adult roach and bream have to be reduced mainly by fishing, the predation of piscivores should be directed predominantly towards the juvenile zooplanktivorous fish. Therefore, small size-classes of piscivorous fish should be promoted by fisheries management, including stocking and harvest regulations.     

Timing of the diet shift from zooplankton to macroinvertebrates and size at maturity determine whether normally piscivorous fish can persist in otherwise fishless lakes

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Phenetic diversity of the large barbs (Barbus intermedius complex sensu Banister) from the coastal zone of the Bahar Dar Gulf (Lake Tana, Ethiopia)

Phenetic structure of a sample of large African barbs Barbus intermedius complex) taken in November 2010 from the inshore part of the Bahar Dar Gulf (Lake Tana) was studied. Principal components analysis was performed on 28 indices characterizing skull proportions and shape of bones. The individuals under study formed distinct clusters in the principal component space. Composition of these clusters was considered. Many morphotypes described in the 1990s were absent in the sample taken in 2010, and there were individuals which did not comply with the diagnoses of the previously described morphotypes. It was suggested that some of these fish represented phenetic groups which did not occur in the offshore part of the gulf, some were, most probably, hybrids of the known morphotypes or originated from homonomic crossings but did not had diagnostic characters of the parental morphotype.     

Lake Tana large barbs: phenetics, growth and diversification

Among the Lake Tana large barbs of about 10 cm SL only representatives of the' acute'morphotype can be distinguished, in the size range 10–20 cm SL' bigmouth big eye' can be identified also. As for the rest, very few individuals can be confidently affiliated with a particular morphotype most of them looking like' intermedius'. Even within the range of 20–30 cm SL some individuals are still difficult to identify. Principal component analysis of cranial characters revealed discrete groups of morphotypes. Differences in both external and cranial characters of the morphotypes result from divergence which is most pronounced when fish are 4–5 years old and 20–25 cm SL. This divergence cannot be related exclusively with differences in the growth rates of individuals representing different morphotypes. Differences in food composition between the morphotypes probably increase in parallel with their morphological divergence. Differences between the morphotypes in the lateral line (11) and the gill rakers (Sb) counts were revealed using ANOVA. Comparison of the Lake Tana Barbus complex of forms with that previously known from Lake Lanao (Philippines) suggests that in both lakes the different forms arose sympatrically but that sympatric speciation in Lake Lanao has advanced further than in Lake Tana.     

Diet niche relationships among predator and prey fish species in their early life stages in Lake Võrtsjärv (Estonia)

In Lake Võrtsjärv pikeperch was observed not to shift to piscivory in their first autumn of life, although juvenile stages of a variety of fish species were abundant in the lake. It was hypothesized that the diets of predator and prey fish fry overlap and that coarse fish species are important food competitors for juvenile piscivores and thus, pikeperch and perch fry do not shift to piscivory during their first growing season. To discover the possible linkages in this pattern, in 2009 the feeding relationships of pikeperch, perch, ruffe and roach fry were analysed. The stomach content analyses showed that in the summer period, Mesocyclops leuckarti was the most frequent prey for perch and ruffe, pikeperch consumed Leptodora kindti in large quantities, and roach ate mostly plant material. Towards autumn, M. leuckarti was the most abundant prey for all percids. However, average stomach content weight and the number of prey items eaten by ruffe were considerably higher than for other fish fry. Since the feeding opportunities of fish fry are considered poor in the examined lake, the prey has the potential to restrict the recruitment to piscivory of their predators, as prey fish seem to have better abilities to persist in this ecosystem. Furthermore, supposed competition in the juvenile stage may result in a reduced top‐down effect on coarse fish.     

Resilience of predators to fishing pressure on coral patch reefs

Numbers and biomass of piscivorous fish and their predation on other fish may often be high in undisturbed coral reef communities. The effects of such predation have sometimes been studied by removal of piscivores (either experimentally or by fishermen). Such perturbations have usually involved removal of large, highly vulnerable, mobile piscivores that are often actively sought in fisheries. The effects of fishing on smaller, demersal, semi-resident piscivores have been little studied. We studied such effects on the fish communities of patch reefs at Midway atoll by experimentally removing major resident, demersal, piscivorous fishes. First, four control reefs and four experimental reefs were selected, their dimensions and habitats mapped, and their visible fish communities censused repeatedly over 1 year. Census of all control and experimental reefs was continued for the following 39 months, during which known piscivores were collected repeatedly by hand spearing. Records were kept of catch and effort to calculate CPUE as an index of predator density. Spearfishing on the experimental reefs removed 2504 piscivorous fish from 12 families and 43 taxa (mostly species). The species richness of the catch did not show an overall change over the duration of the experiment. Spearman rank correlation analysis showed some unexpected positive correlations for density in numbers and biomass of major fished piscivorous groups (especially lizardfish) over the experiment. Only two relatively minor fished piscivorous taxa declined in abundance over the experiment, while the overall abundance of piscivores increased. Visual censuses of fish on the experimental reefs also failed to show reduction of total piscivores over the full experimental period. No significant trend in the abundance of lizardfish censused over the full period was apparent on any of the control reefs. The high resilience of piscivores on these experimental reefs to relatively intense fishing pressure could result from their protracted recruitment seasons, high immigration rates, cryptic habits, or naturally high abundances. A major factor was the high immigration rates of lizardfish, replacing lizardfish and other less mobile piscivores removed from the reefs by spearing. On the fished reefs, the removed lizardfish population replaced itself >20 times during the experiment; other piscivorous taxa replaced themselves only 5 times.