Handed foraging behavior in scale-eating cichlid fish: its potential role in shaping morphological asymmetry

Scale-eating cichlid fish, Perissodus microlepis, from Lake Tanganyika display handed (lateralized) foraging behavior, where an asymmetric 'left' mouth morph preferentially feeds on the scales of the right side of its victim fish and a 'right' morph bites the scales of the left side. This species has therefore become a textbook example of the astonishing degree of ecological specialization and negative frequency-dependent selection. We investigated the strength of handedness of foraging behavior as well as its interaction with morphological mouth laterality in P. microlepis. In wild-caught adult fish we found that mouth laterality is, as expected, a strong predictor of their preferred attack orientation. Also laboratory-reared juvenile fish exhibited a strong laterality in behavioral preference to feed on scales, even at an early age, although the initial level of mouth asymmetry appeared to be small. This suggests that pronounced mouth asymmetry is not a prerequisite for handed foraging behavior in juvenile scale-eating cichlid fish and might suggest that behavioral preference to attack a particular side of the prey plays a role in facilitating morphological asymmetry of this species.     

Righty fish are hooked on the right side of their mouths - observations from an angling experiment with largemouth bass, Micropterus salmoides

The development of muscles and bones in fish is laterally asymmetric (laterality). A "lefty" individual has a "C"-shaped body, with its left-side muscles more developed and the left side of its head facing forward. The body of a "righty" is the mirror-image. This laterality causes asymmetric interactions between individuals of different fish species, in that a righty or lefty fish consumes more lefty or righty fish, respectively. To investigate the coupling mechanisms between body asymmetry and predatory behavior, we conducted angling experiments with largemouth bass (Micropterus salmoides). We used the position of the fishhook set in the mouth to indicate the movement direction of the fish when it took the bait. Righty fish had more hooks set on the right side, whereas lefty fish had more on the left side, indicating that righty fish moved more to the left, and lefty fish moved more to the right, in successful catches. The relationship between the hooked position and movement direction was confirmed by video-image analysis of the angling.     

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.     

Mouth asymmetry in the textbook example of scale-eating cichlid fish is not a discrete dimorphism after all

Individuals of the scale-eating cichlid fish, Perissodus microlepis, from Lake Tanganyika tend to have remarkably asymmetric heads that are either left-bending or right-bending. The ‘left’ morph opens its mouth markedly towards the left and preferentially feeds on the scales from the right-hand side of its victim fish, and the ‘right’ morph bites scales from the victims’ left-hand side. This striking dimorphism made these fish a textbook example of their astonishing degree of ecological specialization and as one of the few known incidences of negative frequency-dependent selection acting on an asymmetric morphological trait, where left and right forms are equally frequent within a species. We investigated the degree and the shape of the frequency distribution of head asymmetry in P. microlepis to test whether the variation conforms to a discrete dimorphism, as generally assumed. In both adult and juvenile fish, mouth asymmetry appeared to be continuously and unimodally distributed with no clear evidence for a discrete dimorphism. Mixture analyses did not reveal evidence of a discrete or even strong dimorphism. These results raise doubts about previous claims, as reported in textbooks, that head variation in P. microlepis represents a discrete dimorphism of left- and right-bending forms. Based on extensive field sampling that excluded ambiguous (i.e. symmetric or weakly asymmetric) individual adults, we found that left and right morphs occur in equal abundance in five populations. Moreover, mate pairing for 51 wild-caught pairs was random with regard to head laterality, calling into question reports that this laterality is maintained through disassortative mating.     

Acquisition of Lateralized Predation Behavior Associated with Development of Mouth Asymmetry in a Lake Tanganyika Scale-Eating Cichlid Fish

The scale-eating cichlid Perissodus microlepis with asymmetric mouth is an attractive model of behavioral laterality: each adult tears off scales from prey fishes’ left or right flanks according to the direction in which its mouth is skewed. To investigate the development of behavioral laterality and mouth asymmetry, we analyzed stomach contents and lower jaw-bone asymmetry of various-sized P. microlepis (22≤SL<115mm) sampled in Lake Tanganyika. The shapes of the pored scales found in each specimen’s stomach indicated its attack side preference. Early-juvenile specimens (SL<45mm) feeding mainly on zooplankton exhibited slight but significant mouth asymmetry. As the fish acquired scale-eating (45mm≤SL), attack side preference was gradually strengthened, as was mouth asymmetry. Among size-matched individuals, those with more skewed mouths ate more scales. These findings show that behavioral laterality in scale-eating P. microlepis is established in association with development of mouth asymmetry which precedes the behavioral acquisition, and that this synergistic interaction between physical and behavioral literalities may contribute to efficient scale-eating.     

True imitation in marmosets

Marmosets, Callithrix jacchus, observed a demonstrator removing the lids from a series of plastic canisters to obtain a mealworm. When subsequently allowed access to the canisters, marmosets that observed a demonstrator using its hands to remove the lids used only their hands. In contrast, marmosets that observed a demonstrator using its mouth also used their mouth to remove the lids. Since hand and mouth demonstrators brought about identical changes in the canisters, the differential test behaviour of the observer groups suggests that they learned about the demonstrator's behaviour. Furthermore, marmosets that had not been given the opportunity to observe a demonstrator prior to testing had a low probability of mouth opening, even if the canisters were previously opened by a mouth-opening demonstrator in an olfactory control experiment. Corroborating Bugnyar & Huber's (1997, Animal Behaviour, 54, 817-831) earlier findings, our results provide further evidence that marmosets can imitate. Copyright 2000 The Association for the Study of Animal Behaviour.     

Jaw laterality and related handedness in the hunting behavior of a scale-eating characin, Exodon paradoxus

Background

Asymmetry in animal bodies and behavior has evolved several times, but our knowledge of their linkage is limited. Tanganyikan scale-eating cichlids have well-known antisymmetry in their bodies and behavior; individuals open their mouths leftward (righty) or rightward (lefty), and righties always attack the right flank of the prey, whereas lefties attack the left. This study analyzed the morphological asymmetry in a scale-eating characiform, Exodon paradoxus, and its behavioral handedness.

Methodology/Principal Findings

Each eight E. paradoxus was observed for 1-h with a prey goldfish in an aquarium to detect the behavioral handedness. Following the experiment, the lateral differences in the mandibles and head-inclination of these eight and ten additional specimens were analyzed. Both measurements on the morphology showed a bimodal distribution, and the laterality identified by these two methods was always consistent within a given individual, indicating that the characin has morphological antisymmetry. Furthermore, this laterality significantly corresponded to behavioral handedness; that is, lefties more often rasped scales from the right flank of the prey and vice versa. However, the correlation between laterality and handedness is the opposite of that in the cichlids. This is due to differences in the feeding apparatus and technique. The characin has cuspids pointing forward on the external side of the premaxilla, and it thrusts its dominant body side outward from its body axis on the flank of the prey to tear off scales. By contrast, the cichlids draw their dominant body side inward toward the axis or rotate it to scrape or wrench off scales with the teeth lined in the opened mouth.

Conclusions/Significance

This study demonstrated that the antisymmetry in external morphology and the corresponding behavioral handedness have evolved in two lineages of scale-eating fishes independently, and these fishes adopt different utilization of their body asymmetry to tear off scales.     

Energetic stress and the degree of fluctuating asymmetry: Implications for a long-lasting,honest signal

Summary Duplicate, bilateral structures of individual animals are usually symmetrical. In cases where such structures are asymmetrical, the degree of asymmetry may indicate the propensity of an individual to stray from the genetically programmed outcome during the development of the structure. Asymmetries have recently been assumed to constitute an honest signal of male quality and, as such, a cue for female choice. I tested the assumption that different rates of energy intake would produce differences in the degree of asymmetry by measuring original and induced fourth rectrices of both sides of the body in European nuthatchesSitta europaea. I found no predominance for the right or left side, thus showing the fluctuating nature of the asymmetry at a population level. This was not the case within individuals which consistently had a longer fourth rectrix on one or the other side of the body. Induced rectrices, grown during winter when food availability was relatively low, exhibited a higher degree of asymmetry than did such rectrices grown during winter after hoardable food had been provided earlier during the winter. The original rectrices, grown during relatively benign conditions in late summer, showed the smallest degree of fluctuating asymmetry. This indicates that the degree of asymmetry is affected by the rate of energy intake. Thus, male quality, reflecting the rate with which energy can be secured and shown by differing degrees of asymmetry, can be used as an honest, long-lasting cue by females in their choice of a mate.     

How birds use their eyes: Opposite left-right specialization for the lateral and frontal visual hemifield in the domestic chick

Recent evidence has demonstrated that, in animals with laterally placed eyes, functional cerebral asymmetry is revealed by preferential use of either the left or right eye in a range of behaviors (birds: [1, 2, 3]; fish: [4, 5]; reptiles: [6, 7]). These findings pose a theoretical problem. It seems that there would be disadvantages in having a substantial degree of asymmetry in the use of the two eyes; a deficit on one side would leave the organism vulnerable to attack on that side or unable to exploit resources appearing on one side. We here report a possible solution to the problem. We have found that domestic chicks show selective use of the lateral visual field of the left eye and of the right hemifield in the binocular, frontal visual field when they peck at strangers but not at cagemates. Thus, during social recognition, there seems to be opposite and complementary left-right specialization for the lateral and frontal visual fields of the two eyes. These findings can reconcile the computational advantages associated with asymmetry of the left and right sides of the brain with the ecological demands for an animal to perceive and respond equally well to the left and right sides of its midline.     

Gene(s) and individual feeding behavior: Exploring eco‐evolutionary dynamics underlying left‐right asymmetry in the scale‐eating cichlid fish Perissodus microlepis

The scale‐eating cichlid fish Perissodus microlepis is a textbook example of bilateral asymmetry due to its left or right‐bending heads and of negative frequency‐dependent selection, which is proposed to maintain this stable polymorphism. The mechanisms that underlie this asymmetry remain elusive. Several studies had initially postulated a simple genetic basis for this trait, but this explanation has been questioned, particularly by reports observing a unimodal distribution of mouth shapes. We hypothesize that this unimodal distribution might be due to a combination of genetic and phenotypically plastic components. Here, we expanded on previous work by investigating a formerly identified candidate SNP associated to mouth laterality, documenting inter‐individual variation in feeding preference using stable isotope analyses, and testing their association with mouth asymmetry. Our results suggest that this polymorphism is influenced by both a polygenic basis and inter‐individual non‐genetic variation, possibly due to feeding experience, individual specialization, and intraspecific competition. We introduce a hypothesis potentially explaining the simultaneous maintenance of left, right, asymmetric and symmetric mouth phenotypes due to the interaction between diverse eco‐evolutionary dynamics including niche construction and balancing selection. Future studies will have to further tease apart the relative contribution of genetic and environmental factors and their interactions in an integrated fashion.     

Sagittal otolith morphogenesis asymmetry in marine fishes

This study investigated and compared asymmetry in sagittal otolith shape and length between left and right inner ears in four roundfish and four flatfish species of commercial interest. For each species, the effects of ontogenetic changes (individual age and total body length), sexual dimorphism (individual sex) and the otolith's location on the right or left side of the head, on the shape and length of paired otoliths (between 143 and 702 pairs according to species) were evaluated. Ontogenetic changes in otolith shape and length were observed for all species. Sexual dimorphism, either in otolith shape and length or in their ontogenetic changes, was detected for half of the species, be they round or flat. Significant directional asymmetry in otolith shape and length was detected in one roundfish species each, but its inconsistency across species and its small average amplitude (6·17% for shape and 1·99% for length) suggested that it has barely any biological relevance. Significant directional asymmetry in otolith shape and length was found for all flatfish species except otolith length for one species. Its average amplitude varied between 2·06 and 17·50% for shape and between 0·00 and 11·83% for length and increased significantly throughout ontogeny for two species, one dextral and one sinistral. The longer (length) and rounder otolith (shape) appeared to be always on the blind side whatever the species. These results suggest differential biomineralization between the blind and ocular inner ears in flatfish species that could result from perturbations of the proximal‐distal gradient of otolith precursors in the endolymph and the otolith position relative to the geometry of the saccular epithelium due to body morphology asymmetry and lateralized behaviour. The fact that asymmetry never exceeded 18% even at the individual level suggests an evolutionary canalization of otolith shape symmetry to avoid negative effects on fish hearing and balance. Technically, asymmetry should be accounted for in future studies based on otolith shape.     

Strategic exploitation of fluctuating asymmetry in male Endler's guppy courtship displays is modulated by social environment

Lateral asymmetry in signalling traits enables males to strategically exploit their best side. In many animals, both body colouration and fluctuating asymmetry are signals of male attractiveness. We demonstrated experimentally that even sexually naïve male Poecilia wingei were able to identify their most attractive side (i.e. that with a higher proportion of carotenoid pigmentation) and use it preferentially during courtship. Notably, males retained their strategic signalling in a male‐biased social environment, whereas they ceased to signal strategically in a female‐biased environment. The degree of asymmetry in colouration did not affect overall courtship activity. Strategic lateralization in courtship displays was strongest and most repeatable in the male‐biased social environment where males competed with rivals for matings. Individual asymmetry in colouration changed considerably over a period of 3 months. This suggests that colouration is a dynamic feature during adulthood and that males are capable of tracking and strategically exploiting their lateral asymmetry in accordance with their social environment.     

Genetic and environmental effects on the morphological asymmetry in the scale‐eating cichlid fish,Perissodus microlepis

The scale‐eating cichlid fish, Perissodus microlepis, from Lake Tanganyika are a well‐known example of an asymmetry dimorphism because the mouth/head is either left‐bending or right‐bending. However, how strongly its pronounced morphological laterality is affected by genetic and environmental factors remains unclear. Using quantitative assessments of mouth asymmetry, we investigated its origin by estimating narrow‐sense heritability (h²) using midparent–offspring regression. The heritability estimates [field estimate: h² = 0.22 ± 0.06, P = 0.013; laboratory estimate: h² = 0.18 ± 0.05, P = 0.004] suggest that although variation in laterality has some additive genetic component, it is strongly environmentally influenced. Family‐level association analyses of a putative microsatellite marker that was claimed to be linked to gene(s) for laterality revealed no association of this locus with laterality. Moreover, the observed phenotype frequencies in offspring from parents of different phenotype combinations were not consistent with a previously suggested single‐locus two‐allele model, but they neither were able to reject with confidence a random asymmetry model. These results reconcile the disputed mechanisms for this textbook case of mouth asymmetry where both genetic and environmental factors contribute to this remarkable case of morphological asymmetry.     

Lopsided Fish in the Snake River Basin — Fluctuating Asymmetry as a way of Assessing Impact of Hatchery Supplementation in Chinook Salmon, Oncorhynchus tshawytscha

The use of developmental instability (an individual's failure to produce a consistent phenotype in a given environment) was evaluated to detect the effects of outplanting hatchery fish on wild salmon. Juvenile chinook salmon were collected in 1989, 1990, and 1991 from five drainages in the Snake River Basin. In each drainage we attempted to collect fish from streams with no hatchery supplementation (wild), naturally spawning fish from streams with hatchery supplementation (natural), and fish collected at a hatchery. Forty fish were collected per site and the number of elements in bilateral characters were counted on each side of the fish. Indices of fluctuating asymmetry (FA), a measure of minor, random deviations in perfect symmetry of bilateral counts, were calculated as an estimator of developmental instability. Analysis of character counts from seven paired characters revealed normal distributions. Only one of the characters displayed counts that were statistically larger on one side than the other, indicating that directional asymmetry (DA) or antisymmetry was not a major bias of FA. However, the means of all individual characters revealed a non-statistically significant left side bias. We analyzed our data using two indices of FA (FA1 and FA5) with different levels of sensitivity to DA. Differences in both FA indices were found among years, with collection sites in 1989 having significantly larger FA values than in 1991 (FA p < 0.01). Levels of FA among wild, natural, and hatchery fish were comparatively small (FA1 p = 0.17). This suggests developmental conditions were different in the first year of the study than in the last. The cause of these differences may be linked to either genetic or environmental variation or to gene—environment interactions, but the general population declines of salmon that occurred during this time obscures more specific conclusions.     

Patterns of asymmetry in the twining vine Dalechampia scandens (Euphorbiaceae): ontogenetic and hierarchical perspectives

We studied patterns of fluctuating asymmetry (FA) in leaves of four populations of the neotropical vine Dalechampia scandens to obtain insight into the origin of leaf FA and the level at which it is controlled. We analysed correlations in signed and unsigned asymmetry at different organizational levels. We also analysed the ontogeny of FA during leaf expansion to test whether asymmetry is regulated during cell expansion, and whether fast-expanding leaves are more or less asymmetrical. Signed asymmetry was negatively correlated between successive leaves, that is, when the right side of a leaf was larger than the left side, the next leaf on the shoot tended to show the opposite pattern. The magnitude of FA, however, was very weakly correlated among successive leaves or among leaves measured on different shoots. The direction of asymmetry did not change during leaf expansion, but the relative asymmetry, that is, asymmetry corrected for difference in trait size, decreased during expansion. We found a weak negative relationship between leaf expansion rate and relative asymmetry on the fully expanded leaves. These results suggest that leaf asymmetry in Dalechampia originates from perturbations in cell proliferation in the stem, creating asymmetries in opposite directions in successive leaves. These asymmetries persist during leaf expansion, but tend to be reduced by unknown mechanisms.     

Further investigation on nuclear transplantation in different orders of teleost: the combination of the nucleus of Tilapia (Oreochromis nilotica) and the cytoplasm of Loach (Paramisgurnus dabryanus).

The nucleus of a blastula cell from Tilapia (Oreochromis nilotica, family Cichlidae, order Perciformes) was transplanted into an enucleated egg of Loach (Paramisgurnus dabryanus, family Cobitidae, order Cypriniformes). From among 3747 nucleo-cytoplasmic hybrid (NCH) eggs two NCH larval fish (0.05%) were obtained; one died on the 6th day and the other died on the 12th day after the operation. Morphological examinations showed that both NCH larval fish had developed normally with an opened mouth except they could not take food after complete utilization of their egg yolk on the 5th day of development. The possible mechanisms for obtaining such inter-order NCH larval fish are discussed. This is the first report indicating that inter-order NCH larval fish can be obtained in spite of their evolutionary divergence.     

Competition among growing organs and developmental control of morphological asymmetry

Fluctuating asymmetry is often used as a measure of developmental instability, although its developmental basis is poorly understood. Theoretical models and experimental studies have suggested that feedback interactions between structures on the left and right body sides play a pivotal role in the control of asymmetry. Here we provide experimental evidence that competition for a limiting resource can generate such interactions between growing organs. In our experiments in the butterfly Precis coenia (Lepidoptera: Nymphalidae), hindwing imaginal discs were removed from one or both body sides of caterpillars. Emerging butterflies were thus missing one or both hindwings, but had heavier forewings, mid- and hindlegs than untreated controls. When only one hindwing was removed, the forewing and hindleg on the treated side were heavier than on the untreated side. The asymmetry and overall weight increase in response to wing disc removal diminished with increasing physical distance of the responding tissue from the imaginal disc removed. Our findings are consistent with the hypothesis that growing imaginal discs compete for a haemolymph-borne resource, such as a nutrient or growth factor. Such competition is a possible mechanism for feedback interactions and may thus participate in the developmental control of asymmetry.     

Phenotypic modification of roach (Rutilus rutilus L.) infected with Ligula intestinalis L. (Cestoda: Pseudophyllidea).

In European freshwater, cyprinid fish may be heavily infected by plerocercoids of the pseudophyllidea cestode Ligula intestinalis (L.). During their development, these parasites grow rapidly to a large size in the fish's body cavity, characteristically distending the abdomen. In this study, the influence of this tapeworm on roach (Rutilus rutilus L.) morphology was analyzed. Forty-five infected and 45 uninfected roach were collected from the Lavernose-Lacasse gravel pit in Toulouse, south western France and examined for 40 morphological measurements to study phenotypic modification of the body and 14 bilateral characters for an analysis of asymmetry. Results indicate that the degree of bilateral asymmetry does not change between infected and uninfected roach, despite the strong host-morphological modifications such as deformation of the abdomen, fin displacements at the level of the tail, and sagging of the vertebral column. The intensity of abdominal distension and fish morphology changes depends on the total parasite biomass present. Differences were observed in morphology at different levels of infection, which relate to established effects of L. intestinalis on the physiology and behavior of intermediate hosts. These morphological changes induced by the parasite could increase trophic transmission to the definitive avian hosts.     

The SOOF lift: its role in correcting midfacial and lower facial asymmetry in patients with partial facial palsy

Subperiosteal face lifting has gained wide acceptance in aesthetic surgical practice. It may also have a role to play in patients with partial facial palsy. These patients demonstrate poor static position of the mouth but maintain some degree of facial movement. This study examined the role of subperiosteal facial suspension as an alternative treatment modality in this patient group. In this series, five patients with varying degrees of partial facial palsy underwent subperiosteal face lifting, including sub-orbicularis oculi fat elevation via a temporal, lower lid, and buccal approach, thereby mobilizing and elevating and suspending the zygomaticus major and levator labii superioris muscles on the facial skeleton. An attempt was made to categorize the patients according to overall House-Brackmann score. It was not possible to precisely classify the patients by this method, although the approximate scores were two patients scoring 3, two patients scoring 4, and one patient scoring 5. To overcome inconsistencies with this method, the degree of static and dynamic asymmetry of the mouth and also the excursion of the mouth were graded separately. Four patients with mild to moderate dynamic and static asymmetry (House-Brackmann score of approximately 3 and 4) who maintained excellent or good excursion of the mouth achieved excellent or good results. One patient with poor excursion and severe partial facial palsy (House-Brackmann score of 5) was improved but remained markedly asymmetric (follow-up, 4 months to 1 year). Subperiosteal face lifting is a useful therapeutic modality for management of selected patients with mild partial facial palsy. These patients demonstrate asymmetric static position but maintain some degree of muscle excursion. Patients with severe facial palsies with poor muscle excursion continue to require muscle transfer or sling procedures. The authors hope that long-term follow-up will confirm the sustained effect of midfacial suspension in this selected patient group.     

Asymmetrical Resource Ownership Increases Owners’ and Reduces Non‐Owners’ Motivation to Fight in the Mangrove Rivulus,Kryptolebias marmoratus

Resource ownership often increases an individual's aggressiveness and its probability of defeating a competitor. Individuals contesting resource owners could therefore incur higher costs, making individuals reluctant to compete with owners. We tested the hypothesis that animals use asymmetry in resource ownership as a cue for contest costs and adjust contest decisions accordingly. Using a mangrove rivulus fish (Kryptolebias marmoratus), we staged (1) contests with a randomly assigned asymmetry in resource ownership (one fish was provided with a shelter) and (2) contests in which neither fish had a shelter. Owners that were in their shelters at the contest start showed a greater tendency to fight and won more contests than their intruder opponents; those outside the shelter at the start did not. Compared with fish in contests with no shelters at stake, shelter owners had a higher tendency to fight whether or not they were in their shelters at the start; intruders, however, had a lower tendency to fight only against owners that were inside the shelter at the start. These results demonstrate (1) that ownership status influences both owners’ and intruders’ contest decisions (and in opposite directions), producing a detectable ownership advantage and (2) that intruders required confirmation of their opponents’ ownership status before retreating without challenging them. Ownership status per se is therefore important to the fish's contest decisions.