Asymmetry of Mouth-Opening of a Small Herbivorous Cichlid Fish Telmatochromis temporalis in Lake Tanganyika

Direction of mouth-opening of a small herbivorous Tanganyikan cichlid, Telmatochromis temporalis, was studied. Each sample fish opened its mouth either rightward or leftward in some degree. The directions of mouth-opening were independent of the body curve directions, and the asymmetry will be due to asymmetric mouth morph individually specific. The degree of the mouth asymmetry was not related to body size, suggesting the asymmetry being not acquired characters. No fish opened the mouth in lateral symmetry, indicating that the asymmetry is different from "fluctuating asymmetry". This fish took algae on rock surface usually using right or left side of its mouth. However, strong relations between directions of mouth-openings and frequencies of mouth side used in foraging were not found, and the biological role of the asymmetry, if any, is not clear now.     

Size-Dependent Male Alternative Reproductive Tactics in the Shell-Brooding Cichlid Fish Lamprologus callipterus in Lake Tanganyika

Reproductive parasitism among males is prevalent in fishes. Typically, small ripe males parasitize the reproductive effort of large bourgeois males by using various behavioural tactics. We examined the size‐dependent advantages of parasitic behavioural tactics in a shell‐brooding cichlid fish of Lake Tanganyika with three male types (large bourgeois males and medium–dwarf parasitic males). The extremely small ‘dwarf males’ weighing only 2.5% on average of large males, perform a specialized tactic in which they avoid attacks by the resident large males by entering the inner part of the whorl of the shell where a female is spawning. Field observations and a manipulation experiment revealed that the very small size of dwarf males is essential for utilizing this positional advantage. Larger dwarf males and medium males opportunistically adopt darting and sneaking which likely result in very low reproductive outcomes. The size associated advantage and disadvantage of parasitic tactics are the major factors shaping the size distribution of ripe males in this species. The success of parasitic spawning by dwarf males is determined not only by body size of the males, but also by the relative sizes of females and shells in which they spawn. These factors would affect the choice of different tactics among dwarf males. The analyses of body condition among ripe and unripe males across a wide range of body sizes suggested that onset of sexual activities at very small body sizes in dwarf males may be associated with higher condition factors that is a pre‐requisite for maintaining investment in testes and intense reproductive activities.     

Cooperative Breeding in the Lake Tanganyika Cichlid Julidochromis ornatus

Cooperative breeding has been described for several cichlids from the genus Julidochromis (Perciformes: Cichlidae) under laboratory conditions, but field evidence is scarce. Here we describe the breeding system of the cichlid Julidochromis ornatus (Boulenger) in Lake Tanganyika (Zambia). Groups defended a breeding shelter under a large flat stone. Smaller group members stayed and fed under or close to the stone, actively guarded by the larger group members. Six out of 28 groups were newly established by breeders, joined by subordinates from a large pool of independent fish (comprising 50–70% of the total population), and four groups were seen to dissolve during a total of 77 observation days. Breeding groups consisted of a large breeding male and female with zero to five smaller subordinates (average 2). Larger breeders and subordinates were found in larger groups. All group members participated in territory defence and -maintenance, but the breeders were only present at the shelter 48% of the time, in contrast to the subordinates which guarded the breeding shelter 94% of the time. Smaller group members showed submissive behaviours to larger group members. We conclude subordinates in J. ornatus are helpers, but we did not find evidence that helpers increased the group’s current reproductive success. Personal observations combined with a literature review revealed at least 19 species of Lake Tanganyika cichlids show evidence of cooperative breeding, entirely confined to the substrate breeding tribe of the Lamprologini (24% of 80 species in total): 2 Chalinochromis spp., 5 Julidochromis spp., 12 Neolamprologus spp. More effort should be put into detecting cooperative breeding in American and Asian substrate breeding cichlid species.     

Lateralized kinematics of predation behavior in a Lake Tanganyika scale-eating cichlid fish

Behavioral lateralization has been documented in many vertebrates. The scale-eating cichlid fish Perissodus microlepis is well known for exhibiting lateral dimorphism in its mouth morphology and lateralized behavior in robbing scales from prey fish. A previous field study indicated that this mouth asymmetry closely correlates with the side on which prey is attacked, but details of this species' predation behavior have not been previously analyzed because of the rapidity of the movements. Here, we studied scale-eating behavior in cichlids in a tank through high-speed video monitoring and quantitative assessment of behavioral laterality and kinematics. The fish observed showed a clear bias toward striking on one side, which closely correlated with their asymmetric mouth morphologies. Furthermore, the maximum angular velocity and amplitude of body flexion were significantly larger during attacks on the preferred side compared to those on the nonpreferred side, permitting increased predation success. In contrast, no such lateral difference in movement elements was observed in acoustically evoked flexion during the escape response, which is similar to flexion during scale eating and suggests that they share a common motor control pathway. Thus the neuronal circuits controlling body flexion during scale eating may be functionally lateralized upstream of this common motor pathway.     

Evolutionary Relationships of the Limnochromini, a Tribe of Benthic Deepwater Cichlid Fish Endemic to Lake Tanganyika, East Africa

Lake Tanganyika harbors an enormous diversity of cichlid fish that stem from eight distinct ancestral lineages, which colonized the lake after its formation 9 to 12 million years ago. Six of twelve currently described tribes are assigned to the H-lineage, an assemblage of exclusively mouthbrood-ing cichlids, all of which evolved during a short period of time during the course of the primary radiation of lacustrine species. Our study focuses on the deepwater tribe Limnochromini, comprising bi-parental mouthbrooders, and is based on phylogenetic analysis of two mitochondrial gene segments. We confirm the polyphyletic origin of the Limnochromini as they are defined to date, in that Gnathochromis pfefferi is placed among the Tropheini, whereas the genus Benthochromis is presented as an independent lineage. The remaining nine species were unambiguously resolved as monophyletic and should be redefined as the tribe Limnochromini. Concerning generic assignments, the genus Greenwoodochromis appeared as monophyletic, Limnochromis as paraphyletic, and the genera Reganochromis and Baileychromis as monophyletic sister genera. The linearized tree analysis and the comparison of average sequence divergences to that of the remaining tribes of the H-lineage revealed a relatively recent but simultaneous proliferation of the Limnochromini, suggesting that the same environmental changes triggered the radiation of particular deepwater, benthic, pelagic, and littoral lineages. By using a preliminary calibration of a molecular clock based on gamma-corrected amino acid distances of the NADH2 gene, the diversification of the Limnochromini could tentatively be dated to 2.9–3.5 MYA, coinciding with a period of aridification in East Africa between 2.5 and 3 MYA. The lack of geographic color morphs and the structural uniformity and resource scarcity of deepwater habitats suggest that competition and resource partitioning leading to differential trophic specialization promoted speciation within the Limnochromini, rather than an allopatric model.Reviewing Editor: Dr. Axel Meyer     

Sound Production and Associated Behaviour in a Cichlid Fish,Cichlasoma centrarchus

Das Verhalten zwischen je zwei C. centrarchus-♂♂ wurde daraufhin untersucht, ob Laute auftraten und ob solche Laute der Verständigung zwischen den Tieren dienen. Die Laute, die produziert wurden, waren gleichartiges tiefes Knurren; es gab individuelle Unterschiede in der Dauer und im zeitlichen Muster des Knurrens. Diese Laute sind nicht zufallsverteilt, sondern stark mit aggressivem Verhalten korreliert. Diese Korrelation besteht auch zum Verhalten, das auf den Laut folgt; Angriffe folgen viel öfter auf Verhalten mit als auf solches ohne Lautproduktion, auch ist die Reaktion anderer Tiere darauf unterschiedlich. Auf lautlose Verhaltensweisen reagieren sie meist “nachahmend”, auf Laute meist “vermeidend”, selten “drohend”. Informationstheoretische Analyse bewies, daß die übermittelte Informationsmenge anders war, wenn die Tiere einander hören und sehen konnten, als wenn sie einander nur sehen konnten. Es scheint, daß Laute aggressives Verhalten im Empfänger hemmen. Im natürlichen Lebensraum benützt C. centrarchus wahrscheinlich Laute, um Artgenossen vom Eindringen in ihr Revier, Rivalisieren um Nahrung oder Stören der Brut abzuschrecken. Vielleicht dient akustische Verständigung zwischen verschiedenen Arten denselben Zwecken.     

The Nesting Site of a Piscivorous Cichlid Lepidiolamprologus profundicola as a Safety Zone for Juveniles of a Zooplanktivorous Cichlid Cyprichromis leptosoma in Lake Tanganyika

Juvenile Cyprichromis leptosoma, an endemic cichlid fish in Lake Tanganyika, form large schools near the nesting sites of the piscivorous cichlid Lepidiolamprologus profundicola. The female L. profundicola guarding the nesting site drove away piscivorous fish that approached the nest. After the disappearance of the guarding L. profundicola, the frequency of predatory dashes toward the school of juvenile C. leptosoma near the nesting site increased markedly. This suggests that juvenile C. leptosoma use the breeding territory of L. profundicola as a safety zone from their potential predators. The relationship between C. leptosoma and L. profundicola should be regarded as a type of commensalism.     

Peripheral Isolate Speciation of a Lake Malawi Cichlid Fish from Shallow Muddy Habitats

Much of the exceptional diversity of cichlid fishes in the African Great Lakes can be explained by geographic variation among isolated populations of species specialised to live on patchily distributed rocky habitat. However, there are also many endemic species that are not specialised for rocky shores. These appear to experience weaker geographic isolation. Major decreases in lake volume may have segregated such populations in isolated refugia in the distant past, but subsequent range changes have likely eliminated most of the phylogeographic signal of these events. Divergence in currently isolated peripheral water bodies may be more amenable to the study of recent processes of allopatric divergence. We investigate a haplochromine cichlid fish, here referred to as Lethrinops sp. ‘chilingali’, isolated in a small satellite lake near Lake Malawi, and the candidate sister taxon, Lethrinops lethrinus, which inhabits shallow muddy habitats in the main lake and associated water bodies. The satellite lake form from Lake Chilingali showed significant morphological differentiation, with a less ventrally-placed mouth and shorter snout, associated with a shift in diet from a diverse range of benthic invertebrates towards specialisation on mid-water chaoborid larvae and pupae. The Lake Chilingali population showed substantially reduced mitochondrial DNA diversity and no haplotype sharing was observed with populations from the main lake system. In laboratory experiments, putative species showed a high degree of assortative mating and territorial males were significantly more aggressive towards intruders of their own population. This study adds to the evidence that rapid evolution of novel phenotypes in peripheral habitats can add to the diversity of lacustrine cichlids through the evolution of at least partial reproductive isolation in allopatry.     

Facial Recognition in a Group-Living Cichlid Fish

The theoretical underpinnings of the mechanisms of sociality, e.g. territoriality, hierarchy, and reciprocity, are based on assumptions of individual recognition. While behavioural evidence suggests individual recognition is widespread, the cues that animals use to recognise individuals are established in only a handful of systems. Here, we use digital models to demonstrate that facial features are the visual cue used for individual recognition in the social fish Neolamprologus pulcher. Focal fish were exposed to digital images showing four different combinations of familiar and unfamiliar face and body colorations. Focal fish attended to digital models with unfamiliar faces longer and from a further distance to the model than to models with familiar faces. These results strongly suggest that fish can distinguish individuals accurately using facial colour patterns. Our observations also suggest that fish are able to rapidly (≤ 0.5 sec) discriminate between familiar and unfamiliar individuals, a speed of recognition comparable to primates including humans.     

Oral Fertilization in a Mouthbrooding Cichlid Fish

It has been hypothesized that in maternal mouthbrooding cichlids the conspicuous markings on the male's anal fin function as “egg-dummies” by fooling the female into snapping at them, thereby inhaling sperm and assuring fertilization of the eggs in the mouth. I show experimentally in Pseudocrenilabrus multicolor, an East African maternal mouthbrooder, that indeed oral fertilization takes place. Nevertheless, external fertilization plays a significant role, too.     

Comparative Phylogenetic Analyses of the Adaptive Radiation of Lake Tanganyika Cichlid Fish: Nuclear Sequences Are Less Homoplasious But Also Less Informative Than Mitochondrial DNA

Over 200 described endemic species make up the adaptive radiation of cichlids in Lake Tanga-nyika. This species assemblage has been viewed as both an evolutionary reservoir of old cichlid lineages and an evolutionary hotspot from which the modern cichlid lineages arose, seeding the adaptive radiations in Lakes Victoria and Malawi. Here we report on a phylogenetic analysis of Lake Tanganyika cichlids combining the previously determined sequences of the mitochondrial ND2 gene (1047 bp) with newly derived sequences of the nuclear RAG1 gene (∼700 bp of intron 2 and ∼1100 bp of exon 3). The nuclear data—in agreement with mitochondrial DNA—suggest that Lake Tanganyika harbors several ancient lineages that did not undergo rampant speciation (e.g., Bathybatini, Trematocarini). We find strong support for the monophyly of the most species-rich Tanganyikan group, the Lamprologini, and we propose a new taxonomic group that we term the C-lineage. The Haplochromini and Tropheini both have an 11-bp deletion in the intron of RAG1, strongly supporting the monophyly of this clade and its derived position. Mapping the phylogenetically informative positions revealed that, for certain branches, there are six times fewer apomorphies in RAG1. However, the consistency index of these positions is higher compared to the mitochondrial ND2 gene. Nuclear data therefore provide, on a per–base pair basis, less but more reliable phylogenetic information. Even if in our case RAG1 has not provided as much phylogenetic information as we expected, we suggest that this marker might be useful in the resolution of the phylogeny of older groups. Reviewing Editor: Dr. Rafael Zardoya     

The Inhibition of Aggressive Behavior by Sound in the Cichlid Fish,Cichlasoma centrarchus

Frühere Arbeiten über die Lautproduktion von Cichlasoma centrarchus deuteten darauf hin, daß Laute aggressives Verhalten der Fische untereinander verringern (Schwarz 1974). Diese Hypothese wurde experimentell geprüft. Test-♂♂ bekamen gleichzeitig den Anblick eines Artgenossen und entweder Schweigen (S) oder vom Band gespielte Kontrollaute (CN) oder Fischlaute (FN) geboten; dann wurde die Zahl der darauf folgenden hoch aggressiven (HAE) und schwach aggressiven (LAE) Begegnungen bestimmt. Vorspielen der CN änderte die Anzahl der HAE nicht, Vorspielen der FN verringerte sie erheblich. FN hemmte HAE bei ♂♂ mehr als bei ♀♀. Da die ♀♀ Laute produzieren, die denen der ♂♂ in Art und Wirkung ähneln (Schwarz in prep.), kann man dieses Ergebnis durch gelegentliches nichtaggressives, optisch auffallendes Verhalten der ♀♀ zum Teil erklären.     

The Role of Urine in Parent-Offspring Communication in a Cichlid Fish

The fry of the Midas cichlid, Cichlasoma citrinellum, preferred over blank water, a urine solution from either parent or from a nonparental adult of either sex. They failed to show a preference for the urine of a predator, C. managuense, or for the mucus from the mother. It is possible that steroid titers in urine could provide information on sex, and that peptide chains in urine could indicate species. The chemosensory acuity of fry is high, as they were able to detect a “concentration” of pheromone as low as one sibling per 2 1 of water. This high acuity implies that olfaction rather than gustation mediated the chemosensory responses described above.     

The Ontogeny of Social Behavior and Body Coloration in the African Cichlid Fish Haplochromis burtoni

The ontogeny of behavioral patterns and body coloration are described for the African cichlid fish, Haplochromis burtoni. The development of particular color patterns correlates directly with appearance of behavioral patterns which “use” those color patterns. There is a flexible timetable associated with these events which depends on both social and environmental factors.     

Evolutionary Relationships in the Sand-Dwelling Cichlid Lineage of Lake Tanganyika Suggest Multiple Colonization of Rocky Habitats and Convergent Origin of Biparental Mouthbrooding

The cichlid species flock of Lake Tanganyika is comprised of seven seeding lineages that evolved in step with changes of the lake environment. One seeding lineage diversified into at least six lineages within a short period of time. Our study focuses on the diversification of one of these lineages, the Ectodini, comprising highly specialized, sand- and rock-dwelling species. They display two distinct breeding styles: maternal and biparental mouthbrooding. By analyzing three mtDNA gene segments in 30 species representing all 13 described genera, we show that the Ectodini rapidly diversified into four clades at the onset of their radiation. The monotypic genus Grammatotria is likely to represent the most ancestral split, followed by the almost contemporary origin of three additional clades, the first comprising the benthic genus Callochromis, the second comprising the benthic genera Asprotilapia, Xenotilapia, Enantiopus, and Microdontochromis, and the third comprising the semi-pelagic genera Ophthalmotilapia, Cardiopharynx, Cyathopharynx, Ectodus, Aulonocranus, Lestradea, and Cunningtonia. Our study confirms the benthic and sand-dwelling life-style as ancestral. Rocky habitats were colonized independently in the Xenotilapia- and Ophthalmotilapia-clade. The Xenotilapia-clade comprises both maternal and biparental mouthbrooders. Their mode of breeding appears to be highly plastic: biparental mouthbrooding either evolved once in the common ancestor of the clade, to be reverted at least three times, or evolved at least five times independently from a maternally mouthbrooding ancestor. Furthermore, the genera Xenotilapia, Microdontochromis, Lestradea, and Ophthalmotilapia appeared paraphyletic in our analyses, suggesting the need of taxonomic revision.     

Drivers of phytoplankton diversity in Lake Tanganyika

In keeping with the theme of this volume, the present article commemorates the 50 years of Hutchinson’s (Am Nat 93:145–159, 1959) famous publication on the ‘very general question of animal diversity’, which obviously leads to the more important question regarding the driving forces of biodiversity and their limitation in various habitats. The study of phytoplankton in large lakes is a challenging task which requires the use of a wide variety of techniques to capture the range of spatial and temporal variations. The analysis of marker pigments may provide an adequate tool for phytoplankton surveys in large water bodies, thanks to automated analysis for processing numerous individual samples, and by achieving sufficient taxonomic resolution for ecological studies. Chlorophylls and carotenoids were analysed by HPLC in water column samples of Lake Tanganyika from 2002 through 2006, at two study sites, off Kigoma (north basin) and off Mpulungu (south basin). Using the CHEMTAX software for calculating contributions of the main algal groups to chlorophyll a, variations of phytoplankton composition and biomass were determined. We also investigated selected samples according to standard taxonomic techniques for elucidating the dominant species composition. Most of the phytoplankton biomass was located in the 0–40 m layer, with maxima at 0 or 20 m, and more rarely at 40 m. Deep chlorophyll maxima (DCM) and surface ‘blooms’ were occasionally observed. The phytoplankton assemblage was essentially dominated by chlorophytes and cyanobacteria, with diatoms developing mainly in the dry season. The dominant cyanobacteria were very small unicells (mostly Synechococcus), which were much more abundant in the southern basin, whereas green algae dominated on average at the northern site. A canonical correspondence analysis (CCA) including the main limnological variables, dissolved nutrients and zooplankton abundance was run to explore environment–phytoplankton relations. The CCA points to physical factors, site and season as key determinants of the phytoplankton assemblage, but also indicates a significant role, depending on the studied site, of calanoid copepods and of nauplii stages. Our data suggest that the factors allowing coexistence of several phytoplankton taxa in the pelagic zone of Lake Tanganyika are likely differential vertical distribution in the water column, which allows spatial partitioning of light and nutrients, and temporal variability (occurring at time scales preventing long-term dominance by a single taxon), along with effects of predation by grazers.     

Social organization of a polygynous CichlidLamprologns furcifer in Lake Tanganyika

Lamprologus furcifer inhabited vertical or overhanging rock surfaces. Females persistently stayed at particular sites and singly guarded the offspring there. Males also stayed at particular sites but often left them to visit females. A dominant male controlled the territories of several breeding females at a time. Schools of young under maternal care spread horizontally on the rock surface as they developed and fed mainly on benthic organisms such as atyid shrimps. It is suggested that the emancipation of males from brood care is attributed to the benthic life of young.     

Complete mitochondrial DNA replacement in a Lake Tanganyika cichlid fish

We used nuclear and mitochondrial DNA (mtDNA) sequences from specimens collected throughout Lake Tanganyika to clarify the evolutionary relationship between Lamprologus callipterus and Neolamprologus fasciatus . The nuclear data support the reciprocal monophyly of these two shell-breeding lamprologine cichlids. However, mtDNA sequences show that (i) L. callipterus includes two divergent and geographically disjunct (North–South) mtDNA lineages; and that (ii) N. fasciatus individuals cluster in a lineage sister group to the northern lineage of L. callipterus . The two mtDNA lineages of L. callipterus diverged c . 684 kya to 1.2 Ma, coinciding with a major water level low stand in Lake Tanganyika, which divided the lake into isolated sub-lakes. This suggests that the two mtDNA lineages originated as the result of the separation of L. callipterus populations in different sub-basins. The incongruent phylogenetic position of N. fasciatus can best be explained by an ancient unidirectional introgression from L. callipterus into N. fasciatus. Remarkably, our data indicate that this event resulted in the complete mtDNA replacement in N. fasciatus . Our data suggest that hybridization occurred soon after the divergence of the two L. callipterus mtDNA lineages, probably still during the water level low stand, and that subsequently the invading mtDNA lineage spread throughout the lake.