Molecular phylogeny and speciation patterns in host-specific monogeneans (Cichlidogyrus,Dactylogyridae) parasitizing cichlid fishes (Cichliformes,Cichlidae) in Lake Tanganyika

Cichlidogyrus (including Scutogyrus) is the most speciose dactylogyridean monogenean genus known from African and Levantine cichlid fishes (Cichlidae). While its taxonomy is well established, little is known about the phylogenetic relationships and evolutionary history of this ectoparasite, especially from hosts belonging to one of the most impressive vertebrate radiations, the cichlid fishes from the East African Great Lakes and surrounding hydrological systems. Phylogenetic inference based on DNA sequences of the nuclear 18S, internal transcribed spacer 1 and 28S rDNA genes revealed that Cichlidogyrus parasitizing mainly West African cichlid tribes is paraphyletic with respect to species parasitizing hosts belonging to the East African cichlid radiation, which constitute a well-supported monophylum. Members of Cichlidogyrus from tylochromine and oreochromine hosts that colonised Lake Tanganyika only recently, cluster with their non-Lake Tanganyika relatives, indicating that they colonised Lake Tanganyika with their current host species, and did not jump over from any of the many cichlid species already present in the lake. The diversification of Cichlidogyrus in Lake Tanganyika seems to be driven by failure to diverge in old lineages of cichlids, cospeciation in more recently evolved ones, and host switching followed by parasite duplication at the level of the various host tribes. Evaluation of host specificity and structural evolution of haptoral and reproductive organs in Lake Tanganyika Cichlidogyrus revealed that strict specialist species together with larval hook size represent the ancestral state of haptor configuration, suggesting that members of Cichlidogyrus in this system evolved from a very simple form to a more complex one similarly to their West African congeners. Generalist species among Cichlidogyrus with a sclerotized vagina parasitizing ancient Lake Tanganyika lineages seem to have developed a different hook configuration, most probably to ensure successful colonisation of new, phylogenetically unrelated hosts.     

The life cycle of Euclinostomum heterostomum (Rudolphi, 1809) (Trematoda: Clinostomatidae)

In small forest streams of West Nigeria the snail species Bulinus globosus was found to be the first intermediate host of a clinostomatid species which proved in successful infection experiments with the cichlid fish Tilapia zillii as second intermediate host to be Euclinostomum heterostomum (Rudolphi, 1809). Final hosts are herons. The morphology of the redia and the morphology and behaviour of the cercaria are described for the first time. The metacercaria which settles dorsal to the swim-bladder or in the kidney of the host fish requires more than two months (at tropical temperatures) for full development. Histological sections of the metacercaria revealed that its pharynx is provided with only few muscle fibres but surrounded by many myoblast-like cells, and the fact that the interior surface of this organ has a dense brush-like lining consisting of long microtriches. The pathology of infected fish is briefly described, and remarks about the geographical distribution of the parasite are given.     

Ontogenetic and gender-related variation in the isotopic niche within and between three species of fur seals (genus <Emphasis Type="Italic">Arctocephalus</Emphasis>)

Differences in aggressiveness when competing for environmental resources are the main factor leading to social hierarchy in group living fish. Social status acquired is related to changes in physiological parameters, as metabolic rate. Habitat variation can interfere with aggressive behaviour and promote changes in physiological parameters associated with social status. The primary goal of our study was to investigate how differences in habitat complexity affect the relationship between resting metabolic rate (RMR) and social status in the Amazonian dwarf cichlid Apistogramma agassizii. We compared agonistic interactions between pairs of males in aquaria with different habitat enrichment levels, manipulated by adding shelters. RMR was measured before and after hierarchy establishment. Habitat enrichment promotes changes in aggressive behaviour and influences differences in metabolic rate between dominant and subordinate fish. We observed an increase in biting by dominant fish at high enrichment habitat, which could be related to the increase in territory value. We observed an increase in metabolic rate in dominant fish after hierarchy establishment. However, it occurs only in enriched habitats. We concluded that habitat structure interfere with behavioural characteristics in social hierarchies, as aggressiveness, and changes in aggressive interactions affect metabolic rate in different social ranks in the dwarf cichlid Apistogramma agassizii.     

Gill monogeneans of neotropical cichlid fish: diversity,phylogenetic relationships,and host-parasite cophylogenetic associations

Host-parasite coevolution is one of the main topics of the evolutionary biology of host-parasite associations. The majority of monogeneans parasitizing fish exhibit a high degree of host specificity. As a result, their evolutionary history might be intertwined with that of their fish hosts. The Cichlidae represent a diverse group of secondary freshwater fish with disjunctive distribution. Host-specific dactylogyrid monogeneans commonly parasitize cichlid fish. Their high diversity is associated with the main areas of cichlid distribution, i.e., Neotropical America and Africa. Nevertheless, the parasite fauna of cichlids from Neotropical America is still underexplored. A total of 31 cichlid species were examined for the presence of monogeneans, with 20 of them being parasitized. On these cichlids, 30 monogeneans belonging to the genera Gussevia, Trinidactylus, and Scadicleithrum were identified, 17 of them potentially representing new species for science. Phylogenetic analyses revealed three monophyletic groups of Neotropic cichlid monogeneans. Genus Gussevia was monophyletic, while Sciadicleithrum resulted polyphyletic. Sciedicleithrum from South America and Sciadicleithrum from Mexico represented two divergent lineages. The plesiomorphic Neotropical cichlid host group for dactylogyrid monogeneans was Cichlini, from which the representatives of other Neotropical cichlid tribes were colonised. Cophylogenetic analyses revealed a statistically significant cophylogenetic signal in the investigated host-parasite system, with host switch and duplication representing the main coevolutionary events for monogeneans parasitizing Neotropical cichlids. This scenario is in accordance with previous studies focussed on dactylogyridean monogeneans parasitizing freshwater fish in Europe and Africa.     

Behaviours Associated with Acoustic Communication in Nile Tilapia (Oreochromis niloticus)

Background

Sound production is widespread among fishes and accompanies many social interactions. The literature reports twenty-nine cichlid species known to produce sounds during aggressive and courtship displays, but the precise range in behavioural contexts is unclear. This study aims to describe the various Oreochromis niloticus behaviours that are associated with sound production in order to delimit the role of sound during different activities, including agonistic behaviours, pit activities, and reproduction and parental care by males and females of the species.

Methodology/Principal Findings

Sounds mostly occur during the day. The sounds recorded during this study accompany previously known behaviours, and no particular behaviour is systematically associated with sound production. Males and females make sounds during territorial defence but not during courtship and mating. Sounds support visual behaviours but are not used alone. During agonistic interactions, a calling Oreochromis niloticus does not bite after producing sounds, and more sounds are produced in defence of territory than for dominating individuals. Females produce sounds to defend eggs but not larvae.

Conclusion/Significance

Sounds are produced to reinforce visual behaviours. Moreover, comparisons with O. mossambicus indicate two sister species can differ in their use of sound, their acoustic characteristics, and the function of sound production. These findings support the role of sounds in differentiating species and promoting speciation. They also make clear that the association of sounds with specific life-cycle roles cannot be generalized to the entire taxa.     

A microsatellite-based genetic linkage map of the cichlid fish, Astatotilapia burtoni (Teleostei): a comparison of genomic architectures among rapidly speciating cichlids

Cichlid fishes compose an astonishingly large number of species and formed species flocks in record-breaking time. To facilitate efficient genome scans and comparisons of cichlid genomes, we constructed a medium-density genetic linkage map of microsatellite markers of Astatotilapia burtoni. The mapping cross was derived from two inbred laboratory lines to obtain F₂ progeny by intercrossing. The map revealed 25 linkage groups spanning 1249.3 cM of the genome (size ~950 Mb) with an average marker spacing of 6.12 cM. The seven Hox clusters, ParaHox C1, and two paralogs of Pdgfrβ were mapped to different linkage groups, thus supporting the hypothesis of a teleost-specific genome duplication. The A. burtoni linkage map was compared to the other two available maps for cichlids using shared markers that showed conservation and synteny among East African cichlid genomes. Interesting candidate genes for cichlid speciation were mapped using SNP markers.     

Complete Mitochondrial DNA Sequences of the Threadfin Cichlid (Petrochromis trewavasae) and the Blunthead Cichlid (Tropheus moorii) and Patterns of Mitochondrial Genome Evolution in Cichlid Fishes

The cichlid fishes of the East African Great Lakes represent a model especially suited to study adaptive radiation and speciation. With several African cichlid genome projects being in progress, a promising set of closely related genomes is emerging, which is expected to serve as a valuable data base to solve questions on genotype-phenotype relations. The mitochondrial (mt) genomes presented here are the first results of the assembly and annotation process for two closely related but eco-morphologically highly distinct Lake Tanganyika cichlids, Petrochromis trewavasae and Tropheus moorii. The genomic sequences comprise 16,588 bp (P. trewavasae) and 16,590 bp (T. moorii), and exhibit the typical mitochondrial structure, with 13 protein-coding genes, 2 rRNA genes, 22 tRNA genes, and a non-coding control region. Analyses confirmed that the two species are very closely related with an overall sequence similarity of 96%. We analyzed the newly generated sequences in the phylogenetic context of 21 published labroid fish mitochondrial genomes. Consistent with other vertebrates, the D-loop region was found to evolve faster than protein-coding genes, which in turn are followed by the rRNAs; the tRNAs vary greatly in the rate of sequence evolution, but on average evolve the slowest. Within the group of coding genes, ND6 evolves most rapidly. Codon usage is similar among examined cichlid tribes and labroid families; although a slight shift in usage patterns down the gene tree could be observed. Despite having a clearly different nucleotide composition, ND6 showed a similar codon usage. C-terminal ends of Cox1 exhibit variations, where the varying number of amino acids is related to the structure of the obtained phylogenetic tree. This variation may be of functional relevance for Cox1 synthesis.     

The effect of social isolation on androgen and corticosteroid levels in a cichlid fish (Haplochromis burtoni) and in swordtails (Xiphophorus helleri)

The blood androgen and glucocorticoid levels of male Haplochromis burtoni and Xiphophorus helleri were measured in socially isolated individuals (8 and 4 weeks, respectively) and nonisolated controls. In both species social isolation leads to significant reductions of mean concentrations and variances, both for androgens and corticosteroids. It is known for H. burtoni—and new evidence for X. helleri is presented—that social isolation reduces aggressivity in nonescalating situations. It is proposed that social stimuli in both species stimulate the testes to produce more androgenic hormones, and that this can lead to higher levels of aggression. At least in tropical fish species the androgenic optimum for defending a territory or a social status may be much more controlled by social stimuli than previously realized.     

Social organization and endocrine profiles of <Emphasis Type="Italic">Australoheros facetus</Emphasis>, an exotic freshwater fish in southern Portugal

Australoheros facetus is a neotropical cichlid and an exotic species in the Guadiana and Odelouca basins (Southern Portugal). In this research, we aimed to characterize the main behavioural patterns and circulating hormones, 17β-estradiol (E₂) for females, and testosterone, 11-ketotestosterone (11KT) and cortisol for both sexes, during the formation of social groups, a crucial step in the life-history of A. facetus. A pair-breeding strategy with territorial behaviour and aggressive interactions was found, with a positive correlation between dominance and size for both sexes. There were no significant differences between non-territorial and territorial individuals in the baseline levels of hormones, but 11KT was higher in males when they became territorial, as E₂ for territorial females, while there was no clear pattern for testosterone. In contrast, cortisol was higher in non-territorial males and correlated negatively with social dominance. These results suggest that size is the main driver for social dominance and that formation of stable hierarchies result in higher circulating 11KT and lowers stress in territorial males. Related to A. facetus’ behaviour, aggressiveness and biparental care may be an advantage during the invasion process of A. facetus, facilitating colonization of new habitats.     

Nocturnal Mate Recognition and Nest guarding by Female Convict Cichlids (Pisces,Cichlidae: Cichlasoma mgrofasciatum)

This study investigated the ability of nest-guarding convict cichlid (Cichlasoma mgrofasciatum) females to recognize their own mate and to defend their brood effectively against strangers at night. Cichlids in the laboratory bred in nesting boxes made of plexiglas. At the fry stage, various conspecific males were introduced, at night, into the nest box of brood-guarding females. Female reaction was observed with infrared equipment. If the introduced male was their own mate, females showed little reaction. If the introduced male was a stranger, females reacted by directing head shakes, tail beats, and pushes or bites at the intruder. The frequency of these acts was significantly higher in the presence of strangers than in the presence of mates; the frequency also rose significantly as the size of strangers increased. The two largest classes of strangers fought with the females. These fights included circling behaviour, but not mouth-locking. Some aspects of female behaviour suggested that mate recognition is based on short-range chemical cues and not on sound, size, or rapidly diffusing odours. Mate recognition in the nest, at night, is an example of non-visual communication in fish, and active nest defense at night shows that the convict cichlid, normally considered to be diurnal, can engage in coordinated and effective behaviour in the absence of light.     

Functional groups in the social behavior of a cichlid fish,the Oscar,Astronotus ocellatus

Dummy conspecifics were presented to isolated adults of the cichlid fish Astronotus ocellatus to investigate the functional organization of cichlid social behavior. Body size and 15 dummy-elicited activities were recorded during 15 min sessions and analyzed by principal components analysis (PCA) to reveal their temporal organization. Five principal components explained almost 80% of the variation in dummy-elicited behavior, and these five factors define functional groups for

• 1.(a) investigation,
• 2.(b) attack,
• 3.(c) nesting,
• 4.(d) boldness,
• 5.(e)distress.

Nest-oriented and attack modal action patterns are not mutually inhibitory during this time frame, and biting does not appear to function exclusively during an attack on a conspecific. Comparison with previous studies of New and Old World cichlids suggests evolutionary conservation of the functional organization of social behavior.     

From molecule to behavior: Brain aromatase (cyp19a1b) characterization,expression analysis and its relation with social status and male agonistic behavior in a Neotropical cichlid fish

The enzyme aromatase, responsible for the conversion of C19 androgens to C18 estrogens, exists as two paralogue copies in teleost fish: Cyp19a1a mostly expressed in the gonads, referred as gonadal aromatase, and Cyp19a1b, mostly expressed in the brain, accordingly known as brain aromatase. The neural localization of Cyp19a1b is greatly contained within the social behavior network and mesolimbic reward system in fish, suggesting a strong role of estrogen synthesis in the regulation of social behavior. In this work we aimed to analyze the variation in cyp19a1b expression in brain and pituitary of males of a highly social cichlid, Cichlasoma dimerus (locally known as chanchita), and its relation with inter-individual variability in agonistic behavior in a communal social environment. We first characterized chanchita's cyp19a1b mRNA and deduced amino acid sequence, which showed a high degree of conservation when compared to other teleost brain aromatase sequences, and its tissue expression patterns. Within the brain, Cyp19a1b was solely detected at putative radial glial cells of the forebrain, close to the brain ventricles. We then studied the relative expression levels of cyp19a1b by Real Time PCR in the brain and pituitary of males of different social status, territorial vs. non-territorial, and its relationship with an index of agonistic behavior. We found that even though, brain aromatase expression did not differ between types of males, pituitary cyp19a1b expression levels positively correlated with the index of agonistic behavior. This suggests a novel role of the pituitary in the regulation of social behavior by local estrogen synthesis.     

Introgression in Lake Malaŵi: Increasing the Threat of Human Urogenital Schistosomiasis?

For the last 15 years, we have studied the relationships among cichlid snail-eating fishes, intermediate snail-host density, and the prevalence of human infection of Schistosoma haematobium in Lake Mala?i and concluded that the increase of human infection is correlated with the decrease in snail-eating fishes in the shallow waters of the lake. We postulated that a strain of S. haematobium from other parts of Africa, which was introduced into the Cape Maclear region of Lake Mala?i by tourists, was compatible with Bulinus nyassanus—which is a close relative of B. truncatus, and interbred with the indigenous strain of S. haematobium, which ultimately produced via introgression a strain that can use both B. globosus and B. nyassanus as intermediate hosts. This actively evolving situation involving intermediate snail–host switching and decline of Trematocranus placodon, a natural cichlid snail predator, will impact on transmission of urogenital schistosomiasis within the local communities and on tourists who visit Lake Mala?i.     

Preliminary field observations on the marmoset,Callithrix humeralifer intermedius (Hershkovitz, 1977) at Dardanelos,Rio Aripuanã, Mato Grosso

The recently discoveredCallithrix humeralifer intermedius occurs between the Rios Roosevelt and Aripuanã in Brazil. This paper presents some preliminary observations ofC. h. intermedius in the wild from May to November 1978. They occupy dense primary forest, second growth and low white sand forest. Group size is between 4 and 13, the larger groups comprised of more than one adult pair. One group, watched for 160.5 hr, occupied a home range of 13.75 ha, during this period, travelling between 740 and 1,500 m during the day. Principal foods include small fruits, flowers, tree exudates and insects. Groups were observed with one pair of newborn infants during September and October, at the end of the dry season. Observations of social behaviour (including agonistic behaviour, grooming, tail coiling behaviour and scent marking), development of young, vocalizations and potential predators are described.     

Cyclic proceptivity in a captive female orang-utan (Pongo Pygmaeus Abelii)

An adult male—female pair of orang-utans was observed for a 3-month period, commencing with the introduction of the animals to each other. After approximately 2 weeks, the female began to show proceptive behaviors towards the male. Two other proceptive periods were observed, occuring from 26 to 30 days apart, and lasting for 4–6 days. These female-initiated periods of sexual activity began with increased locomotor activity, solitary play, proximity to the male, following the male, and social grooming. The peak periods of proceptive behaviour included hand—genital contact, mouth—genital contact, rolling the male onto his back, both dorso-ventral and ventro-ventral mounting, and pelvic thrusting. Although hormonal levels could not be assessed in this study, it is believed that these peaks coincided with ovulation. In previous reports, the presence of proceptive behaviors was perhaps over-shadowed by highly aggressive sexual behavior on the part of male orang-utans. The visibility of proceptivity in this study is attributed to the large cage which allowed the female to escape the male's advances, enabled distance between the animals when they preferred it, and continuous exposure of the orangs to each other. This female orang-utan behavior was compared to the female sexual behaviours of the other great ape species — the chimpanzee and the gorilla.     

Phillips Dikdiks (Madoqua saltiana phillipsi) in der Al Wabra Preservation (AWWP)/Katar

Since the 1990s Phillips dikdiks (Madoqua saltiana phillipsi) are kept and successfully bred at the Al Wabra Wildlife Preservation (AWWP) in Qatar. This paper presents the observations on the social behaviour and the biology of this subspecies of the Salt's dikdik, originated at the Somali gulf coast. Husbandry, nutrition and handling of this species are explained as well as the demography of the AWWP population, diseases and death causes. AWWP is so far the only known institution which keeps Phillips dikdiks.     

Etude de l'influence des facteurs visuels sur les comportements sexuels et agressifs de Mollienesia (Poecilia) velifera (Pisces,Poeciliidae)

One of the most striking features of cave fishes is their pronounced ocular regression. They are, however, perfectly adapted since they multiply and display the behaviour patterns which are biologically important in their surroundings. It is therefore of interest to study the relative role of visual factors in the corresponding behaviour patterns in related epigean species.Other authors have previously demonstrated the dominant role of chemical stimuli in the releasing of sexual behaviour patterns in M. sphenops, of which some forms are cavernicolous. In M. velifera and M. latipinna, on the contrary, visual factors seem more important. The releasers of the aggressive behaviour patterns of these three species seem to be predominantly visual. In the present study, the importance of visual factors has been verified experimentally in M. velifera by comparing the observed behavioural differences in experimentally blinded individuals and normal controls.The results of the pre-experimental phase show that there is no difference between these two groups before blinding, neither in the frequency of the patterns, nor in their numerical values.The results of the first experimental phase confirm the importance of visual releasers in the sexual behaviour patterns of M. velifera. Thus, sexual approaches, mouth—abdomen contacts and copulation attempts are totally absent in blinded pairs. Sexual motivation however is still present since the gonopodal flexions are equally frequent in both groups. On the other hand, it seems that aggressive behaviour patterns are maintained in blinded individuals but only when the partners are very close to each other or when an actual contact has taken place.The comparison of pairs in which only one of the partners is blinded (second experimental phase), as well as results of the first phase, suggest that experimental blinding does not cause hormonal changes liable to influence the observed patterns. In addition to this, the role of the ♀ in courtship has been specified. When a ♀ individual is intact and receptive, it will initiate courtship when it is placed in the company of an inactive blinded partner.     

CLEANING BEHAVIOUR BETWEEN THE CICHLID FISH TILAPIA RENDALLI FENDALLI BOULENGER 1896 AND THE CYPRINID,LABEO CYLINDRICUS PETERS, 1852

SUMMARY

A case of interspecific cleaning behaviour is described between a cichlid host Tilapia rendalli rendalli and a Juvenile cyprinid Labeo cylindricus, in captivity. The host fish initiated the cleaning behaviour with a ‘head down’ display.