Persistence and fluctuation of lateral dimorphism in fishes

Two morphological types ("righty" and "lefty") have been discovered in several fish species and are referred to as a typical example of antisymmetry. It has been suggested, first, that this dimorphism (called laterality) is inheritable; second, that the frequencies of laterality in each species fluctuate around 0.5; and third, that predators mainly exploit prey of the opposite laterality; that is, lefty and righty predators prey on righties and lefties, respectively. The latter is defined as "cross predation"; the antonym "parallel predation" means predation within the same laterality. We hypothesized that cross predation drives alternation of the survival and reproductive advantages between two morphological types, leading to frequency-dependent selection that maintains the dimorphism. To investigate this, we constructed mathematical models of population dynamics of one prey/one predator systems and three-trophic-level systems with omnivory. Mathematical analysis and computer simulations explained the behavior of the laterality frequency in nature well, insofar as cross predation dominated over parallel predation. Furthermore, the simulations showed that when only one of the morphological types exists in a species, the other type can invade. This suggests that dimorphism is maintained in all interacting 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.     

A population genetic model for lateral dimorphism frequency in fishes

Two morphological types, righty and lefty, are found in several fish species. Righty predators mainly prey on lefty prey and vice versa (called cross predation). This dimorphism is heritable in a Mendelian one-locus–two-allele fashion. The frequency of righty individuals in a population oscillates periodically. To determine the effect of cross predation on this oscillation, we constructed mathematical models that describe a genetic basis of lateral dimorphism assuming genetic drift in a one-predator–two-prey system and three trophic levels with omnivory. Both models have an equilibrium of both righty and lefty types at a frequency of 0.5. Mathematical analyses and computer simulations showed that the dimorphism is maintained and that its frequency oscillated with or without genetic drift. Large degrees of drift and high intrinsic growth rates and predation efficiencies of prey species caused the frequency oscillations to be amplified and their period to be long. When cross predation decreased as a proportion of all predation, the righty frequency of a prey species fluctuated non-periodically. These differences in fluctuation patterns were observed in natural systems. Our model suggests that both cross predation and genetic drift dictate the maintenance of dimorphism and the patterns of its fluctuations.     

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.     

Inheritance pattern of lateral dimorphism in two cichlids (a scale eater, Perissodus microlepis, and an herbivore, Neolamprologus moorii) in Lake Tanganyika

Antisymmetry in the direction of the mouth opening, to either the right ("lefty") or left ("righty"), was documented in the scale-eating cichlid Perissodus microlepis. This study revealed the presence of lefty and righty mouth morphs in the herbivorous cichlid Neolamprologus moorii, although the degree of deviation was not large. Both species are biparental brooders and guard their young. We examined the inheritance pattern of the dimorphism (laterality) using parents and broods of P. microlepis and N. moorii collected in the wild. In P. microlepis, lefty-lefty pairs had a 2:1 frequency of lefty:righty young, lefty-righty pairs a similar number of each type of young, and righty-righty pairs only righty young. Similar inheritance patterns were observed in N. moorii. We propose two hypotheses to explain the inheritance pattern: Mendelian genetics with the lefty allele dominant over the righty and the dominant allele homozygous lethal, and cross-incompatibility that is predominant in lefty homozygotes.     

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.     

Measuring and evaluating morphological asymmetry in fish: distinct lateral dimorphism in the jaws of scale‐eating cichlids

The left–right asymmetry of scale‐eating Tanganyikan cichlids is described as a unilateral topographical shift of the quadratomandibular joints. This morphological laterality has a genetic basis and has therefore been used as a model for studying negative frequency‐dependent selection and the resulting oscillation in frequencies of two genotypes, lefty and righty, in a population. This study aims were to confirm this laterality in Perissodus microlepis Boulenger and P. straeleni (Poll) and evaluate an appropriate method for measuring and testing the asymmetry. Left–right differences in the height of the mandible posterior ends (HMPE) and the angle between the neurocranium and vertebrae of P. microlepis and P. straeleni were measured on skeletal specimens. Snout‐bending angle was also measured using a dorsal image of the same individuals following a previous method. To define which distribution model, fluctuating asymmetry (FA), directional asymmetry (DA), or antisymmetry (AS), best fit to the lateral asymmetry of the traits, we provided an R package, IASD. As a result, HMPE and neurocranium–vertebrae angle of both species were best fitted to AS, suggesting that P. microlepis and P. straeleni showed a distinct dimorphism in these traits, although snout‐bending angle of P. microlepis was best fitted to FA. Measurement error was low for HMPE comparing the snout‐bending angle in P. microlepis, indicating that measuring HMPE is a more accurate method. The scale‐eating tribe Perissodini showed distinct antisymmetry in the jaw skeleton and neurocranium–vertebrae angle, and this laterality remains a valid marker for further evolutionary studies.     

Evidence of disassortative mating in a Tanganyikan cichlid fish and its role in the maintenance of intrapopulation dimorphism

Morphological dimorphism in the mouth-opening direction ('lefty' versus 'righty') has been documented in several fish species. It has been suggested that this deflection is heritable in a Mendelian one-locus, two-allele fashion. Several population models have demonstrated that lateral dimorphism is maintained by negative frequency-dependent selection, resulting from interactions between predator and prey species. However, other mechanisms for the maintenance of lateral dimorphism have not yet been tested. Here, we found that the scale-eating cichlid fish Perissodus microlepis exhibited disassortative mating, in which reproductive pairings between lefties and righties occurred at higher than expected frequency (p<0.001). A previous study reported that a lefty-righty pairing produces a 1:1 ratio of lefty:righty young, suggesting that disassortative mating contributes to the maintenance of lateral dimorphism. A combination of disassortative mating and negative frequency-dependent selection may stabilize lateral dimorphism more than would a single mechanism.     

Preparing the Perfect Cuttlefish Meal: Complex Prey Handling by Dolphins

Dolphins are well known for their complex social and foraging behaviours. Direct underwater observations of wild dolphin feeding behaviour however are rare. At mass spawning aggregations of giant cuttlefish (Sepia apama) in the Upper Spencer Gulf in South Australia, a wild female Indo-Pacific bottlenose dolphin (Tursiops aduncus) was observed and recorded repeatedly catching, killing and preparing cuttlefish for consumption using a specific and ordered sequence of behaviours. Cuttlefish were herded to a sand substrate, pinned to the seafloor, killed by downward thrust, raised mid-water and beaten by the dolphin with its snout until the ink was released and drained. The deceased cuttlefish was then returned to the seafloor, inverted and forced along the sand substrate in order to strip the thin dorsal layer of skin off the mantle, thus releasing the buoyant calcareous cuttlebone. This stepped behavioural sequence significantly improves prey quality through 1) removal of the ink (with constituent melanin and tyrosine), and 2) the calcareous cuttlebone. Observations of foraging dolphin pods from above-water at this site (including the surfacing of intact clean cuttlebones) suggest that some or all of this prey handling sequence may be used widely by dolphins in the region. Aspects of the unique mass spawning aggregations of giant cuttlefish in this region of South Australia may have contributed to the evolution of this behaviour through both high abundances of spawning and weakened post-spawning cuttlefish in a small area (>10,000 animals on several kilometres of narrow rocky reef), as well as potential long-term and regular visitation by dolphin pods to this site.     

Morphological asymmetry and behavioral laterality in the crayfish, Procambarus clarkii

Lateral asymmetry is found widely among vertebrates, but is scarcely observed in invertebrates. Here, morphological asymmetry and behavioral laterality of a wild crayfish, Procambarus clarkii, was investigated. The carapace morphology of crayfish showed left–right differences; in some, the right side of the carapace was larger than the left side, while in others, the left side was larger. A bimodal distribution in the direction of escape behaviors induced by a tactile stimulus was also observed. Experimental crayfish were definitively divided into two groups: individuals that frequently jumped leftward (right type) and those that jumped rightward (left type). Moreover, carapace asymmetry and lateralized escape responses were significantly correlated. These results suggest that crayfish exhibit left–right dimorphism in natural populations. The ecological advantages and maintenance mechanisms underlying these behaviors are also discussed.     

Morphological asymmetry of the abdomen and behavioral laterality in atyid shrimps

Morphological asymmetry and behavioral laterality in vertebrate species have been intensively studied in recent years, while comparable invertebrate studies are rare. Here we demonstrate asymmetry in the curvature of the abdomen and laterality in evasive responses for two atyid shrimps, Limnocaridina latipes and Neocaridina denticulata. The frequency distributions of the angle of the abdominal curvature in both species were discretely bimodal, suggesting that the two populations are composed of both left- and right-type individuals. In N. denticulata, behavioral analysis using high-speed filming illustrated that the escape direction for each individual, evoked by a sudden non-lateralized stimulus, was correlated with its abdominal curvature: left- (right-) type shrimp jumped back-leftward (-rightward) significantly more than often. A crossing experiment with N. denticulata indicated that the trait frequency in the F1 generation from two left-type parents differed significantly from that of the F1 generation from two right-type parents, and that the trait frequency for the F1 generation from parents of different laterality types did not deviate from random. That is, offspring laterality type is affected by the lateralities of the parents, indicating that abdominal dimorphism in shrimp is genetically derived. These results suggest that shrimp have an innate laterality that controls their escape direction, which in turn may affect prey-predator interactions in the aquatic community.     

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.     

Link between Aggressiveness and Shyness in the Spider <Emphasis Type="Italic">Philodromus albidus</Emphasis> (Araneae,Philodromidae): State Dependency over Stability

Behavioral syndromes, seen as correlations among two or more functionally different behaviors, are well documented in many different animal taxa. They may not be present automatically, however, and their consistency within populations and individuals also varies among studies. Here, we studied a behavioral syndrome comprising foraging aggressiveness and boldness/shyness and its time consistency in the cursorial spider Philodromus albidus. We measured foraging aggressiveness as the number of prey killed per 2-hour period. Boldness/shyness was assessed as a latency of initiating exploration in a novel environment. We found the presence of the behavioral syndrome in P. albidus, as bold individuals were also more aggressive than were shy individuals. The syndrome was consistent through time within the population but not consistent for individuals. We further discuss the possible causes of the pattern.     

A Continuum of Behavioral Plasticity in Urban and Desert Black Widows

Behavioral plasticity marks an individual's ability to modulate behavior across functional contexts. Behavioral syndromes, on the other hand, appear as consistent individual variation in behavior that is both repeatable for individuals within a functional context (e.g., consistent voracity toward prey) and correlated across contexts (e.g., high voracity toward prey and high levels of boldness toward enemies). Thus, adaptive plasticity and syndromes represent two extremes of a behavioral plasticity continuum upon which most behavioral phenotypes fall. We tested for both adaptive plasticity and behavioral syndromes in the western black widow spider, Latrodectus hesperus. We measured behavior in three contexts: startle, startle + prey, and startle + mate, and found (1) classic behaviorally plastic responses to predation risk, (2) high repeatability of behavior within contexts, and (3) evidence of a correlation between startle + prey and startle + mate contexts, indicative of a behavioral syndrome. As relative behavioral plasticity may vary across populations, we also compared urban and desert populations to test whether spiders from these habitats exhibit different behaviors and/or behavioral syndromes. While we found that urban males used in mating trials courted urban females significantly more than desert females, we found no other differences in the behavior of urban and desert black widows. Thus, black widows, regardless of habitat, are characterized by both context‐specific behavioral plasticity and across‐context correlations, presenting a phenotypic complexity that is likely exhibited, to varying degrees, by most organisms.     

基于内壳的西非乌贼日龄与生长特性

乌贼主要分布在北大西洋东部及非洲沿岸海域,是拖网渔业的重要捕捞对象,也是大西洋乌贼科最重要的商业种。本研究根据2015年7—8月西非沿岸采集的乌贼样本,测量了283 尾乌贼内壳外部形态参数,结合内壳日龄信息,对不同性别乌贼生长特性进行了研究。结果表明: 不同性别乌贼胴长和体重存在显著差异。通过读取内壳日龄,发现雌雄性优势日龄组均为80～100 d。内壳外部形态与日龄的拟合函数中,Logistic函数的拟合效果最佳。雌性个体内壳外部形态参数的最大似然估计值均大于雄性。雄性和雌性乌贼内壳长和内壳宽的绝对和瞬时相对生长率分别在110～120 d 和100～110 d 达到峰值。雄性和雌性的初次性成熟日龄分别为111 d和104 d。不同性别乌贼的生长差异可能与栖息环境密切相关。     

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.     

Scrounging behavior regulates population dynamics

The integration of behavioral and population ecology is necessary when behavior both feeds into demographic parameters and depends on population parameters. We show that scrounging behavior, the exploitation of others' resources, can affect both demographic parameters and population dynamics, including the stability of interactions with prey. Scrounging is a common tactic and its pay-offs exhibit both density- and frequency-dependence. We demonstrate that scrounging can act as a population regulator through its effects on individuals' reproductive rate and mortality. We also explore its effects on predator-prey population dynamics and show that the presence of scrounging predators allows an increased predator population size and contributes to the regulation of both predator and prey populations. Behavioral ecologists will appreciate that although scrounging is often pictured as imposing a social foraging cost to group membership, at the population level it also allows higher numbers of both prey and predators to coexist at equilibrium.     

Cuttlebone: Characterisation, Application and Development of Biomimetic Materials

Cuttlebone signifies a special class of ultra-lightweight cellular natural material possessing unique chemical,mechanical and structural properties,which have drawn considerable attention in the literature.The aim of this paper is to better understand the mechanical and biological roles of cuttlebone.First,the existing literature concerning the characterisation and potential applications inspired by this remarkable biomaterial is critiqued.Second,the finite element-based homogenisation method is used to verify that morphological variations within individual cuttlebone samples have minimal impact on the effective mechanical properties.This finding agrees with existing literature,which suggests that cuttlebone strength is dictated by the cuttlefish habitation depth.Subsequently,this homogenisation approach is further developed to characterise the effective mechanical bulk modulus and biofluidic permeability that cuttlebone provides,thereby quantifying its mechanical and transporting functionalities to inspire bionic design of structures and materials for more extensive applications.Finally,a brief rationale for the need to design a biomimetic material inspired by the cuttlebone microstructure is provided,based on the preceding investigation.     

Laterality of hand use pays off in foraging success for wild chimpanzees

The aim of this study was to see if behavioral lateralization in hand use benefits a lateralized organism in nature. We recorded wild chimpanzees (Pan troglodytes schweinfurthii) at Gombe, Tanzania, fishing for termites (Macrotermes spp.), an extractive foraging task using elementary technology. We compared individual apes who were completely lateralized, using only one hand or the other for the task, versus those who were incompletely lateralized, using either hand. Exclusively lateralized individuals were more efficient, that is, gathered more prey per unit effort, but were no different in success or error rate from incompletely lateralized apes. This is the first demonstration of a payoff to laterality of behavioral function in primates in conditions of ecological validity.