Food intake by mouthbrooding females ofCyphotilapia frontosa (Cichlidae) to feed both themselves and their young

Synopsis Feeding behaviour of mouthbrooding females ofCyphotilapia frontosa was observed in their natural habitat, and specimens of mouthbrooding females and the young in their mouths were examined in the laboratory. Mouthbrooding females exhibited feeding actions and their guts contained about one quarter as much food as those of nonbrooding adults. A substantial amount of food was found in young 12.5 mm TL who retained a large quantity of yolk, and gut fullness of young increased as they grew. Weight changes of the young suggested that the buccal feeding augmented their growth.     

Biparental mouthbrooding and guarding in a Tanganyikan CichlidHaplotaxodon microlepis

Differences between parental roles of males and females inHaplotaxodon microlepis (Cichlidae) were investigated in Lake Tanganyika, and the early ontogeny and growth of the species were studied in the aquarium. Eggs were mouthbrooded by the female, and it is suggested that small larvae (<9 mm in total length) were also mouthbrooded by females though such samples were not collected. Above this size the larvae began to feed, and parents jointly performed mouthbrooding and guarding until the young grew to 25–30 mm, nearly 2 months after spawning. Males and females mouthbrooded to the same extent, but when a part of the brood was released, females mainly guarded the released brood and males took the mouthbrooding role. Differences in parentalcare patterns betweenH. microlepis and other monogamous mouthbrooding cichlids are discussed.     

Female-to-male shift of mouthbrooding in a cichlid fish,Tanganicodus irsacae,with notes on breeding habits of two related species in Lake Tanganyika

Synopsis Parental-care patterns and mating systems of three goby-like cichlids in Lake Tanganyika were investigated. In Tanganicodus irsacae females mouthbrooded eggs and small young for about two weeks and then males took over the role for about one week. Field observations of tagged fish suggest that this species is monogamous: a male's home range largely overlapped with that of its mate, while their home ranges were segregated from those of similar-sized consexual adults. Eretmodus cyanostictus also performed female-to-male shift of mouthbrooding and appeared to be monogamous. The third species, Spathodus marlieri, however, exhibited exclusively maternal mouthbrooding. The differences in parental care and mating system among the three species are discussed in relation to their feeding habits, and the pattern of monogamy in the goby-like cichlids is compared with those of other fishes.     

The cost of parental care inHaplochromis ‘argens’ (Cichlidae)

Synopsis The cost of parental care in the maternal, mouthbrooding cichlid,Haplochromis ‘argens’ was measured in terms of parental survival, fecundity and breeding frequency. In comparison with non-parental females, those that mouthbrooded eggs for a period of 16 days took 33 % longer to respawn. Parental females also grew more slowly between spawnings, and this may affect their future fecundity. These costs were attributed to the cessation of feeding by parental females while mouthbrooding and/or the hormonal inhibition of oogenesis.     

Food deprivation explains effects of mouthbrooding on ovaries and steroid hormones, but not brain neuropeptide and receptor mRNAs, in an African cichlid fish

Feeding behavior and reproduction are coordinately regulated by the brain via neurotransmitters, circulating hormones, and neuropeptides. Reduced feeding allows animals to engage in other behaviors important for fitness, including mating and parental care. Some fishes cease feeding for weeks at a time in order to provide care to their young by brooding them inside the male or female parent's mouth. Maternal mouthbrooding is known to impact circulating hormones and subsequent reproductive cycles, but neither the full effects of food deprivation nor the neural mechanisms are known. Here we ask what effects mouthbrooding has on several physiological processes including gonad and body mass, brain neuropeptide and receptor gene expression, and circulating steroid hormones in a mouthbrooding cichlid species, Astatotilapia burtoni. We ask whether any observed changes can be explained by food deprivation, and show that during mouthbrooding, ovary size and circulating levels of androgens and estrogens match those seen during food deprivation. Levels of gonadotropin-releasing hormone 1 (GnRH1) mRNA in the brain were low in food-deprived females compared to controls and in mouthbrooding females compared to gravid females. Levels of mRNA encoding two peptides involved in regulating feeding, hypocretin and cholecystokinin, were increased in the brains of food-deprived females. Brain mRNA levels of two receptors, GnRH receptor 2 and NPY receptor Y8c, were elevated in mouthbrooding females compared to the fed condition, but NPY receptor Y8b mRNA was differently regulated by mouthbrooding. These results suggest that many, but not all, of the characteristic physiological changes that occur during mouthbrooding are consequences of food deprivation.     

Parental care and mating systems of cichlid fishes in Lake Tanganyika: a preliminary field survey

Reproductive ecology and ethology of 52 cichlid fishes were studied along the shore of Myako, east-middle coast of Lake Tanganyika. Seventeen species were substrate-brooders (guarders), 31 were mouthbrooders, and the remaining 4 were intermediate, performing prolonged biparental guarding of fry after mouthbrooding. Among the substrate-brooders maternal care (and polygyny) was seen about as frequently as biparental care. In most of the mouthbrooders only females took care of the brood, but in 3 species eggs and small larvae were mouthbrooded by females and larger fry by males. In most of the maternal mouthbrooders males defended mating territories which females visited to spawn. The mating system differed from lekking in that there was no concentration of territories and males fed within them. In the remaining maternal mouthbrooders males and overlapping home ranges and only temporarily defended courtship sites in each bout of spawning. Brood size, egg size, breeding site, and sexual differences in body size and color are described. The relationship between parentalcare patterns and mating systems within the family Cichlidae are discussed.     

Reproductive behavior of the Lake Malawi cichlid fish, <Emphasis Type="Italic">Tramitichromis intermedius</Emphasis>

Synopsis We studied the reproductive behavior of wild caught and captive-born, first generation offspring of the Lake Malawi fish, Tramitichromis intermedius(Teleostei, Cichlidae), held in aquaria. Spawning behavior includes an exchange of actions with dominant males performing bower construction and courtship behaviors while females focus on oviposition and mouthbrooding. Egg counts per oviposition and brooding and interbrooding periods of wild caught T. intermedius follow records of other mouthbrooding cichlid fishes. Observation of circling behavior suggests this behavioral trait may be used in mate choice as longer circling, indicating a secure territory and thus male dominance, leads to more oviposition events and hence the potential for larger broods. Comparisons of clutch size and total length of young at release from full-sized females vs. first spawners reveal smaller clutches and young from the younger females, most likely stemming from differences in body size. Investigation of spawning photoperiodicity also noted distinctions between the two groups with wild caught T. intermedius spawning activity peaking in the middle of the light cycle and captive-born, first spawners exhibiting no significant peak in activity. The trend to spawn midday is most likely influenced by predation factors, while the lack of a spawning periodicity in the offspring may be explained by developmental processes, the absence of environmental cues or the tendency for smaller males to be opportunistic in spawning events. The details of spawning behavior recorded in this study provide a database to investigate species differences and to indicate changes due to chemical and physical disturbances.     

Invisible pair bonds detected by molecular analyses

A focus on pair bonds between males and females is fundamental to study the evolution of social organization. Because pair bonds are generally identified from direct observations of pairs that maintain physical proximity, pair bonds may have been overlooked in animals that do not exhibit such visible pairs. The Lake Tanganyika cichlid fish Xenotilapia rotundiventralis forms schools that consist of mouthbrooding and non-brooding adults in mid-water, and visible pairs are not recognized. A previous study suggested that mouthbrooding females transfer fractions of the young to males when the young become large. However, it remains a mystery whether the mating pairs maintain pair bonds so that the females can transfer the young to their mates. To answer this question, we conducted a parentage analysis using 10 microsatellite markers. The analysis showed that the mouthbrooding adults were most likely genetic fathers and mothers of the young in their mouths. This finding suggests that the female-to-male shift of young takes place between mating partners, and thus the mating pairs maintain pair bonds at least until the shift of young. The present study is the first to detect pair bonds in animals in which physical proximity has not been observed.     

Biparental mouthbrooding of the catfish Phyllonemus filinemus in Lake Tanganyika

This article reports biparental mouthbrooding of the bagrid catfish Phyllonemus filinemus in Lake Tanganyika, based on analysis of specimens collected during SCUBA diving. This catfish was nocturnally active, and in the daytime it was concealed singly or in pairs beneath rocks. Within a breeding pair, the male or female alone incubated all the brood in the mouth until the offspring attained 12 mm or so in total length, but thereafter joint mouthbrooding or guarding by both parents took place. Most females of nonbrooding pairs showed high values of gonadosomatic index (GSI), whereas all females of brooding pairs and most single females showed low GSI values. This fact indicated that a pair is formed at a time near the gonadal maturation of the female and separates after the brood is reared. No significant difference in body condition among parents of different reproductive states was observed, which suggested that their condition does not deteriorate markedly as the result of foraging by an off-duty parent. Received: September 16, 2000 / Revised: November 18, 2000 / Accepted: January 23, 2001     

Cichlid spawning structures – bowers or nests?

Males of mouthbrooding cichlids build sand-castle or sand-scrape structures. These are used as display sites to attract females, eggs are laid and inseminated there and then taken away by the female for brooding elsewhere. It has been suggested that the structure be called a bower because it has the same role as the bowerbird's bower. Thew word bower is restricted in ornithological literature to complex structures which reminded Gould (1840) of garden bowers. Simpler display sites of other bowerbirds and other bird families are called courts. Bowerbirds use separate nests for egg-laying, cichlids do not. Other birds, e.g. many weavers, use nests for display purposes. The cichlid structure is the same as nests used by other non mouthbrooding fishes, but mouthbrooding has freed females from the need to stay in the nest. It is unacceptable to use the word bower for the cichlid structure because it is not a bower as defined in ornithological literature, and it is used for egg laying as well as display. Weaver birds use nests for display in a similar way to cichlids, thus the word nest should be retained for the cichlid sand structure. This revised version was published online in July 2006 with corrections to the Cover Date.     

Parental care in a monogamous mouthbrooding cichlidXenotilapia flavipinnis in Lake Tanganyika

Breeding pairs ofXenotilapia flavipinnis held their territories on the sandy bottom and repeated several breeding cycles. Females mouthbrooded the eggs and early larvae but afterward males took over the mouthbrooding role. When the young became free swimming, they were guarded by both parents and remained in the spawning territory. Males played a leading role in the guarding, while females were more active in foraging during the guarding period. It was concluded that males’ active participation in the parental care could accelerate the gonadal recovery of females and consequently could maximize the fecundity of serially monogamous pairs.     

Adaptive sequence evolution in a color gene involved in the formation of the characteristic egg-dummies of male haplochromine cichlid fishes

Background  

The exceptionally diverse species flocks of cichlid fishes in East Africa are prime examples of parallel adaptive radiations. About 80% of East Africa's more than 1 800 endemic cichlid species, and all species of the flocks of Lakes Victoria and Malawi, belong to a particularly rapidly evolving lineage, the haplochromines. One characteristic feature of the haplochromines is their possession of egg-dummies on the males' anal fins. These egg-spots mimic real eggs and play an important role in the mating system of these maternal mouthbrooding fish.     

Effect of Mate Removal on Current and Subsequent Parental Care in the Convict Cichlid (Pisces: Cichlidae)

In most biparental, substrate-brooding species of cichlid fishes, female and male roles differ. Females are usually more involved in direct care of the young while males spend more time away patrolling the territory. This study tested the flexibility of these sex roles with removal experiments in the convict cichlid, Cichlasoma nigrofasciatum. When males were removed, female fanning activity increased. When females were removed, males spent more time fanning and less time away from the brood. Other behavioural variables (frequency of digging, mouthing, foraging and retrieving) were not affected. Being alone or paired during a first breeding episode did not affect parental behaviour during a subsequent episode in which all fish were paired. Observations were carried out during the day and at night, and nocturnal fanning of fry is reported here for the first time. Female role appears less flexible than male role, as befits the more direct care normally given by females.     

Do maternal food deprivation and offspring predator cues interactively affect maternal effort in fish?

The state of the environment parents are exposed to during reproduction can either facilitate or impair their ability to take care of their young. Thus, the environmental conditions experienced by parents can have a transgenerational impact on offspring phenotype and survival. Parental energetic needs and the variance in offspring predation risk have both been recognized as important factors influencing the quality and amount of parental care, but surprisingly, they are rarely manipulated simultaneously to investigate how parents adjust care to these potentially conflicting demands. In the maternally mouthbrooding cichlid Simochromis pleurospilus, we manipulated female body condition before spawning and exposure to offspring predator cues during brood care in a two‐by‐two factorial experiment. Subsequently, we measured the duration of brood care and the number and size of the released young. Furthermore, we stimulated females to take up their young by staged predator attacks and recorded the time before the young were released again. We found that food‐deprived females produced smaller young and engaged less in brood care behaviour than well‐nourished females. Final brood size and, related to this, female protective behaviour were interactively determined by nutritional state and predator exposure: well‐nourished females without a predator encounter had smaller broods than all other females and at the same time were least likely to take up their young after a simulated predator attack. We discuss several mechanisms by which predator exposure and maternal nutrition might have influenced brood and offspring size. Our results highlight the importance to investigate the selective forces on parents and offspring in combination, if we aim to understand reproductive strategies.     

The African cichlid fish Astatotilapia burtoni uses acoustic communication for reproduction: sound production, hearing, and behavioral significance

Sexual reproduction in all animals depends on effective communication between signalers and receivers. Many fish species, especially the African cichlids, are well known for their bright coloration and the importance of visual signaling during courtship and mate choice, but little is known about what role acoustic communication plays during mating and how it contributes to sexual selection in this phenotypically diverse group of vertebrates. Here we examined acoustic communication during reproduction in the social cichlid fish, Astatotilapia burtoni. We characterized the sounds and associated behaviors produced by dominant males during courtship, tested for differences in hearing ability associated with female reproductive state and male social status, and then tested the hypothesis that female mate preference is influenced by male sound production. We show that dominant males produce intentional courtship sounds in close proximity to females, and that sounds are spectrally similar to their hearing abilities. Females were 2-5-fold more sensitive to low frequency sounds in the spectral range of male courtship sounds when they were sexually-receptive compared to during the mouthbrooding parental phase. Hearing thresholds were also negatively correlated with circulating sex-steroid levels in females but positively correlated in males, suggesting a potential role for steroids in reproductive-state auditory plasticity. Behavioral experiments showed that receptive females preferred to affiliate with males that were associated with playback of courtship sounds compared to noise controls, indicating that acoustic information is likely important for female mate choice. These data show for the first time in a Tanganyikan cichlid that acoustic communication is important during reproduction as part of a multimodal signaling repertoire, and that perception of auditory information changes depending on the animal's internal physiological state. Our results highlight the importance of examining non-visual sensory modalities as potential substrates for sexual selection contributing to the incredible phenotypic diversity of African cichlid fishes.     

Filial cannibalism by mouthbrooding males of the cardinal fish,Apogon doederleini, in relation to their physical condition

Synopsis Paternal brood cannibalism was observed in a population ofApogon doederleini in Shikoku Island, Japan. Of 361 egg masses mouthbrooded by males, 47 disappeared within a day of spawning. A stomach check with a syringe ascertained that they had been consumed by the males. The frequency of this cannibalism increased as the breeding season advanced. As males completed 4–7 breeding cycles in a breeding season and spent 80% of the time mouthbrooding without taking ordinary food, their physical condition deteriorated greatly late in the breeding season. We concluded that parental physical condition is an important factor in the occurrence of brood cannibalism.     

Active browsing by mouthbrooding females of Tropheus duboisi and Tropheus moorii (Cichlidae) to feed the young and/or themselves

Synopsis Fishes usually do not eat while brooding offspring in their mouths. In two epilithic algal eaters Tropheus duboisi and T. moorii in Lake Tanganyika, however, mouthbrooding females exhibited feeding actions. In T. duboisi, the feeding rate of mouthbrooding females was 80 percent of that of males and non brooding females irrespective of the developmental state of their offspring. In T. moori, females brooding early embryos rarely fed but their feeding rate increased with development of offspring. An examination of specimens revealed that such females took food for nourishment of themselves and the young in the former species but for nourishment of only the young in the latter.     

Role of Fish in Structuring Invertebrates on Stromatolites in Cuatro Ciénegas, México

Stromatolites, the dominant Precambrian life form, declined in the Phanerozoic to occur today in only a few sites. This decline has been attributed to evolution of metazoan grazers, but stromatolites in our study site, Cuatro Ciénegas, Coahuila, México, harbor diverse macroinvertebrates. Drawing on food chain theory, we hypothesized that fish predation on invertebrates controls invertebrate populations, allowing stromatolites to flourish in Cuatro Ciénegas. Our experiment used small mesh (1 mm) cages to exclude all but larval fishes, and larger (6.5 mm) cages to exclude all larger fishes (including the molluscivorous and omnivorous endemic polymorphic cichlid, Herichthys minckleyi), but allow access to all sizes of the abundant endemic pupfish, Cyprinodon bifasciatus. No effects of treatments on invertebrate densities were noted at 6 week, but significant effects were observed on specific taxonomic groups after 3 month. In absence of fishes, hydrobiidae snails and ceratopogonids increased 3- and 5-fold, respectively, and invertebrate assemblage composition varied among treatments. Algal biomass was not affected by treatments, but algal species composition appeared to change. Overall results suggest that fish assemblages structure invertebrate assemblages, and that fishes may also be factors in determining algal communities.     

PLASTICITY OF JAW AND SKULL MORPHOLOGY IN THE NEOTROPICAL CICHLIDS GEOPHAGUS BRASILIENSIS AND G. STEINDACHNERI

I examined plasticity of jaw and skull morphology induced by feeding different diets in two species of the neotropical cichlid genus Geophagus. The two species possess different modes of development, which affect the size at which young begin feeding. I hypothesized that the difference in size at first feeding could lead to a difference in the amount of change inducible in the two species. The young of the substrate-spawning species, G. brasiliensis, which begin feeding at a smaller size, were predicted to be more plastic than those of the mouthbrooding species, G. steindachneri. The two diets used to induce differences were brine shrimp nauplii and chironomid larvae. Numerous measures of the jaw and skull differed significantly between groups fed the two diets but the amount of plasticity induced was small and would not present a problem for taxonomists. Contrary to my prediction, both the magnitude and pattern of plasticity induced in the two species was similar. Thus, mode of parental care and the size at which young begin feeding do not affect the degree of plasticity. Fish fed brine shrimp nauplii were longer in oral jaw region, but were shorter and shallower in the area behind the oral jaws. An additional group of G. brasiliensis was fed flake food to compare the results of this study to other studies. The differences in measures between fish fed brine shrimp diets and flake food diets were greater than those between fish fed brine shrimp and chironomid larvae. A possible role of plasticity for enhancing rather than retarding morphological evolution is discussed.     

Mate size and breeding success in a monogamous cichlid fish

Synopsis The patterns of mate size and parental care of a monogamous cichlid fish,Cichlasoma maculicauda, were studied in Gatun Lake, Panama. Males defend territories which serve as courtship and nest sites. Within a population most mates in pairs are of equal size rank. In each pair the male is larger than the female, probably because most mature males are larger than most mature females. Clutch size increases with female body size. Male size affects breeding success in two ways. First, larger males provide nest sites less susceptible to destructive wave action. Second, young of larger males grow faster than young of smaller males. Large males defeat small males in contests for position in feeding areas, and this may provide their young with better feeding conditions. In the laboratory young growth rates increase with food abundance, and at high levels of food surpass those observed in nature. Fast growth of young reduces their vulnerability to predators and should allow parents to breed more often. Young survival rates improve with the size of the parents, so that larger fish raise more offspring at each breeding attempt. These observations suggest why preference for large mates should occur.