Ontogeny of numerical abilities in fish

Background

It has been hypothesised that human adults, infants, and non-human primates share two non-verbal systems for enumerating objects, one for representing precisely small quantities (up to 3–4 items) and one for representing approximately larger quantities. Recent studies exploiting fish''s spontaneous tendency to join the larger group showed that their ability in numerical discrimination closely resembles that of primates but little is known as to whether these capacities are innate or acquired.

Methodology/Principal Findings

We used the spontaneous tendency to join the larger shoal to study the limits of the quantity discrimination of newborn and juvenile guppies. One-day old fish chose the larger shoal when the choice was between numbers in the small quantity range, 2 vs. 3 fish, but not when they had to choose between large numbers, 4 vs. 8 or 4 vs. 12, although the numerical ratio was larger in the latter case. To investigate the relative role of maturation and experience in large number discrimination, fish were raised in pairs (with no numerical experience) or in large social groups and tested at three ages. Forty-day old guppies from both treatments were able to discriminate 4 vs. 8 fish while at 20 days this was only observed in fish grown in groups. Control experiments showed that these capacities were maintained after guppies were prevented from using non numerical perceptual variables that co-vary with numerosity.

Conclusions/Significance

Overall, our results suggest the ability of guppies to discriminate small numbers is innate and is displayed immediately at birth while discrimination of large numbers emerges later as a result of both maturation and social experience. This developmental dissociation suggests that fish like primates might have separate systems for small and large number representation.     

The effect of risk-taking behaviour in epidemic models

We study an epidemic model that incorporates risk-taking behaviour as a response to a perceived low prevalence of infection that follows from the administration of an effective treatment or vaccine. We assume that knowledge about the number of infected, recovered and vaccinated individuals has an effect in the contact rate between susceptible and infectious individuals. We show that, whenever optimism prevails in the risk behaviour response, the fate of an epidemic may change from disease clearance to disease persistence. Moreover, under certain conditions on the parameters, increasing the efficiency of vaccine and/or treatment has the unwanted effect of increasing the epidemic reproductive number, suggesting a wider range of diseases may become endemic due to risk-taking alone. These results indicate that the manner in which treatment/vaccine effectiveness is advertised can have an important influence on how the epidemic unfolds.     

Influence of depth on sex-specific energy allocation patterns in a tropical reef fish

The effect of depth on the distribution and sex-specific energy allocation patterns of a common coral reef fish, Chrysiptera rollandi (Pomacentridae), was investigated using depth-stratified collections over a broad depth range (5–39 m) and a translocation experiment. C. rollandi consistently selected rubble habitats at each depth, however abundance patterns did not reflect the availability of the preferred microhabitat suggesting a preference for depth as well as microhabitat. Reproductive investment (gonado-somatic index), energy stores (liver cell density and hepatocyte vacuolation), and overall body condition (hepato-somatic index and Fulton’s K) of female fish varied significantly among depths and among the three reefs sampled. Male conspecifics displayed no variation between depth or reef. Depth influenced growth dynamics, with faster initial growth rates and smaller mean asymptotic lengths with decreasing depth. In female fish, relative gonad weight and overall body condition (Fulton’s K and hepato-somatic index) were generally higher in shallower depths (≤10 m). Hepatic lipid storage was highest at the deepest sites sampled on each reef, whereas hepatic glycogen stores tended to decrease with depth. Depth was found to influence energy allocation dynamics in C. rollandi. While it is unclear what processes directly influenced the depth-related patterns in energy allocation, this study shows that individuals across a broad depth gradient are not all in the same physiological state and may contribute differentially to the population reproductive output. Electronic supplementary material The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

Ontogeny and evolution of electric organs in gymnotiform fish

In order to further our understanding of the evolution of electric organs in the Neotropical gymnotiform fish, we studied the ontogeny of the electric organs in eight species. In Eigenmannia virescens, Sternopygus macrurus, and Apteronotus leptorhynchus the earliest electrocytes are located between muscle fibres of the hypaxial muscle (Type A electrocytes). We present arguments that these Type A electrocytes represent the plesiomorphic condition. In S. macrurus, in addition to the electrocytes in the hypaxial muscle, additional electrocytes were found in the epaxial muscle. In A. leptorhynchus a neurogenic organ develops later during ontogeny in the medial part of the hypaxial muscle in addition to the early myogenic organ. In E. virescens the early electrocytes in hypaxial muscle will degenerate later during ontogeny, and this organ will be replaced functionally by electrocytes located in the caudal appendage and below the hypaxial muscle. In Electrophorus electricus, two Gymnotus species, Rhamphichthys sp., and Brachyhypopomus pinnicaudatus the first electrocytes were found below the hypaxial muscle (Type B electrocytes); they are assumed to be the more derived stage. In R. sp., and B. pinnicaudatus the electrocytes of Type B developed directly into the adult organ. In the two Gymnotus ssp. electrocytes were also found in the medial part of the organ in-between muscle fibres of the hypaxial muscle. In E. electricus a germinative zone was observed to separate from the ventral myotome. This zone is generating electrocytes continuously so that, as a consequence, the relative proportion of electric organ to muscle increases greatly. In 45 mm long E. electricus a separation of low voltage orientation pulses and high voltage trains of pulses (shocks) was observed. A first appearance of Hunter’s organ was found in 140 mm specimens of E. electricus. The first discharges of all species studied were head- positive, with the exception of R. sp., which produced a triphasic discharge, its main component, however, being head-positive. The arguments presented indicate that the Type A electrocytes found in E. virescens, S. macrurus, and A. leptorhynchus would represent the plesiomorphic condition. On the basis of the evidence regarding the formation, cytological appearance, and anatomical location, as well as the early electrical recordings, we would hypothesise that during the evolution of gymnotiforms wave type species evolved first, and in a second step pulse type species followed. This view, however, is corroborated by only some phylogenetic hypotheses.     

Ontogeny of osmoregulation in postembryonic fish: a review

Salinity and its variations are among the key factors that affect survival, metabolism and distribution during the fish development. The successful establishment of a fish species in a given habitat depends on the ability of each developmental stage to cope with salinity through osmoregulation. It is well established that adult teleosts maintain their blood osmolality close to 300 mosM kg(-1) due to ion and water regulation effected at several sites: tegument, gut, branchial chambers, urinary organs. But fewer data are available in developing fish. We propose a review on the ontogeny of osmoregulation based on studies conducted in different species. Most teleost prelarvae are able to osmoregulate at hatch, and their ability increases in later stages. Before the occurrence of gills, the prelarval tegument where a high density of ionocytes (displaying high contents of Na+/K+-ATPase) is located appears temporarily as the main osmoregulatory site. Gills develop gradually during the prelarval stage along with the numerous ionocytes they support. The tegument and gill Na+/K+-ATPase activity varies ontogenetically. During the larval phase, the osmoregulatory function shifts from the skin to the gills, which become the main osmoregulatory site. The drinking rate normalized to body weight tends to decrease throughout development. The kidney and urinary bladder develop progressively during ontogeny and the capacity to produce hypotonic urine at low salinity increases accordingly. The development of the osmoregulatory functions is hormonally controlled. These events are inter-related and are correlated with changes in salinity tolerance, which often increases markedly at the metamorphic transition from larva to juvenile. In summary, the ability of ontogenetical stages of fish to tolerate salinity through osmoregulation relies on integumental ionocytes, then digestive tract development and drinking rate, developing branchial chambers and urinary organs. The physiological changes leading to variations in salinity tolerance are one of the main basis of the ontogenetical migrations or movements between habitats of different salinity regimes.     

Ontogeny of behaviour in larvae of marine demersal fishes

The development of behaviours that are relevant to larval dispersal of marine, demersal fishes is poorly understood. This review focuses on recent work that attempts to quantify the development of swimming, orientation, vertical distribution and sensory abilities. These behaviours are developed enough to influence dispersal outcomes during most of the pelagic larval stage. Larvae swim in the ocean at speeds similar to the currents found in many locations and at 3–15 body lengths per second (BL s⁻¹), although, based on laboratory measurements, species from cold environments swim slower than those from warm environments. At least in warm-water species, larvae swim in an inertial hydrodynamic environment for most of their pelagic period. Unfed swimming endurance is >10 km from about 8–10 mm, and reaches more than 50 km before settlement in several species. Larval fishes are efficient swimmers. In most species, a large majority of larvae have orientated swimming in the ocean, but the precision of orientation does not improve with growth. Swimming direction of the larvae frequently changes ontogenetically. Vertical distribution changes ontogenetically in most species, and both ontogenetic ascents and descents are found. Development of schooling is poorly understood, but it may influence speed, orientation and vertical distribution. Sensory abilities (hearing, olfaction, vision) form early, are well developed and are able to detect cues relevant to orientation for most of the pelagic larval stage. All this indicates that the passive portion of the pelagic larval duration will be short, at least in most warm-water species, and that behaviour must be taken into account when considering dispersal, and in particular in dispersal models. Although quantitative information on the ontogeny of some behaviours is available for a relatively small number of species, more research in this field is required, especially on species from colder waters.     

Realized heritability and repeatability of risk-taking behaviour in relation to avian personalities

Personalities are general properties of humans and other animals. Different personality traits are phenotypically correlated, and heritabilities of personality traits have been reported in humans and various animals. In great tits, consistent heritable differences have been found in relation to exploration, which is correlated with various other personality traits. In this paper, we investigate whether or not risk-taking behaviour is part of these avian personalities. We found that (i) risk-taking behaviour is repeatable and correlated with exploratory behaviour in wild-caught hand-reared birds, (ii) in a bi-directional selection experiment on 'fast' and 'slow' early exploratory behaviour, bird lines tend to differ in risk-taking behaviour, and (iii) within-nest variation of risk-taking behaviour is smaller than between-nest variation. To show that risk-taking behaviour has a genetic component in a natural bird population, we bred great tits in the laboratory and artificially selected 'high' and 'low' risk-taking behaviour for two generations. Here, we report a realized heritability of 19.3 +/- 3.3% (s.e.m.) for risk-taking behaviour. With these results we show in several ways that risk-taking behaviour is linked to exploratory behaviour, and we therefore have evidence for the existence of avian personalities. Moreover, we prove that there is heritable variation in more than one correlated personality trait in a natural population, which demonstrates the potential for correlated evolution.     

Ontogeny and behaviour of early macrophages in the zebrafish embryo.

In the zebrafish embryo, the only known site of hemopoieisis is an intra-embryonic blood island at the junction between trunk and tail that gives rise to erythroid cells. Using video-enhanced differential interference contrast microscopy, as well as in-situ hybridization for the expression of two new hemopoietic marker genes, draculin and leucocyte-specific plastin, we show that macrophages appear in the embryo at least as early as erythroid cells, but originate from ventro-lateral mesoderm situated at the other end of the embryo, just anterior to the cardiac field. These macrophage precursors migrate to the yolksac, and differentiate. From the yolksac, many invade the mesenchyme of the head, while others join the blood circulation. Apart from phagocytosing apoptotic corpses, these macrophages were observed to engulf and destroy large amounts of bacteria injected intravenously; the macrophages also sensed the presence of bacteria injected into body cavities that are isolated from the blood, migrated into these cavities and eradicated the microorganisms. Moreover, we observed that although only a fraction of the macrophage population goes to the site of infection, the entire population acquires an activated behaviour, similar to that of activated macrophages in mammals. Our results support the notion that in vertebrate embryos, macrophages endowed with proliferative capacity arise early from the hemopoietic lineage through a non-classical, rapid differentiation pathway, which bypasses the monocytic series that is well-documented in adult hemopoietic organs.     

The role of learning in fish behaviour

Summary The behavioural patterns of fish are the result of innate (built-in) patterns of maturation (developmental changes) and of learning processes (imprinting and trial-and-error learning). Innate behavioural patterns are considered to be hard-wired and inflexible. However, through learning, fish can adapt to environmental change. For instance, the homing behaviour of fish may be partly the result of the development of specific parts of the brain and partly because of changes in behaviour with experience. Similarly, one can assume that the feeding mode of fish involving snap-responses is innate, but learning enables fish to modify their foraging behaviour in response to a fluctuating environment. By reviewing these and other examples, such as the role of recognition learning and socially transmitted behaviour, one can illustrate the importance of learning in the everyday life of fishes. Although learning plays a large role in the behaviour of fishes, the learning capacity of fishes may also be useful to fisheries research and hatchery operations.     

Energy allocation in juveniles of a warm-temperate reef fish

During the first year of life, organisms are faced with competing demands for energy between growth and storage. Most research on energy allocation in young fishes has focused on cold-temperate species which are subjected to strong seasonal fluctuations in productivity, while few studies have considered those at lower latitudes where seasonality is less pronounced. Gag (Mycteroperca microlepis) of the northeastern Gulf of Mexico settle in coastal seagrass beds in the spring as juveniles and emigrate to offshore reefs in the fall. Upon settlement, these young fish grow at remarkably fast rates, but their growth slows considerably before emigration. Slowed growth can be explained by one of three hypotheses: (1) size-specific emigration times; (2) reduced feeding efficiency associated with declines in primary and secondary productivity; or (3) energetic shifts in allocation from growth to storage. Gag emigrate essentially as a cohort, so slowed growth does not result from differential emigration patterns based on fish size. They also emigrate before seasonal declines in primary and secondary productivity; thus, food remains abundant and feeding efficiency constant. The more plausible hypothesis is that there is an energetic shift from growth to storage. The liver serves as the primary site of lipid storage and the hepatosomatic index of juvenile gag increases coincident with reduced growth. The overall effect of increased energy stores is presumably for use during offshore migration and/or for overwinter survival.     

Ontogeny of thermoregulation and energy metabolism in pygoscelid penguin chicks

The ontogeny of thermoregulation and energy metabolism of chinstrap (Pygoscelis antarctica) and gentoo (P. papua) penguins was studied on King George Island, South Shetland Island, Antarctica. The major findings of this study are: Chinstrap and gentoo penguin chicks hatched completely poikilothermic, due to their poor heat-production ability at low ambient temperatures. They were able to maintain high body temperatures and metabolic rates only by being brooded by adults. Newly hatched chinstrap penguin chicks had, at a specified ambient temperature, significantly higher metabolic rates than newly hatched gentoos. Moreover, chinstrap chicks maintained a significantly higher body temperature. It is suggested that this is a non-acclimatory metabolic adaptation of chinstrap penguin chicks to the lower mean temperatures of their breeding areas. On the 15th day after hatching, chinstrap chicks were completely, and gentoo chicks almost completely, homeothermic. In spite of their high thermogenic capacity from about day 10, chicks were not at that time capable of controlling heat dissipation, and were still dependent on their parents. In older downy chicks and fledglings, heat loss at low temperatures, expressed as heat conductance (CA), was similar to that found for the adults of other penguin species. Just before moulting the CA of chicks was lower than after moulting. Moulting alone did not cause a clear increase in CA. Towards the end of their stay on land the CA of pre-fledged gentoos decreased by 31%. This decrease was not connected with the development of feathers or growth in the chicks' weight. The combination of the low CA and high SMR of chicks gave very low lower critical temperatures, near -15 degrees C. The wide thermoneutral zones of the chicks covered the whole range of air temperature variations in the breeding colonies of both species studied on King George Island. The CA values of homeothermic chinstrap chicks were not lower than those of gentoos, despite the more southern breeding range of the former species. The older chicks of both species are well protected against cold. Any further increase in insulation in chinstrap chicks would be of no adaptative importance.     

Survival against the odds: ontogenetic changes in selective pressure mediate growth-mortality trade-offs in a marine fish

For organisms with complex life cycles, variation among individuals in traits associated with survival in one life-history stage can strongly affect the performance in subsequent stages with important repercussions on population dynamics. To identify which individual attributes are the most influential in determining patterns of survival in a cohort of reef fish, we compared the characteristics of Pomacentrus amboinensis surviving early juvenile stages on the reef with those of the cohort from which they originated. Individuals were collected at hatching, the end of the planktonic phase, and two, three, four, six and eight weeks post-settlement. Information stored in the otoliths of individual fish revealed strong carry-over effects of larval condition at hatching on juvenile survival, weeks after settlement (i.e. smaller-is-better). Among the traits examined, planktonic growth history was, by far, the most influential and long-lasting trait associated with juvenile persistence in reef habitats. However, otolith increments suggested that larval growth rate may not be maintained during early juvenile life, when selective mortality swiftly reverses its direction. These changes in selective pressure may mediate growth-mortality trade-offs between predation and starvation risks during early juvenile life. Ontogenetic changes in the shape of selectivity may be a mechanism maintaining phenotypic variation in growth rate and size within a population.     

Ontogeny of vision in the Antarctic fish Pagothenia borchgrevinki (Nototheniidae)

Summary Pagothenia borchgrevinki ranging in size from 63 to 245 mm were captured from beneath sea ice in McMurdo Sound by fishing and diver collection. Changes in ocular morphology with increasing body size were measured, and assessed in relation to ingested prey. Relative eye size was highest among smaller fish (<100mm total length), and declined with increasing fish size. This was accompanied by a decrease in cone density in the retina from a maximum of 14,200 mm^–2 in the smallest fish examined (63 mm), to 1000 mm^–2 in a 220 mm long fish. Theoretical acuity was lowest among fish at either end of the size range examined (minimum separable angle 40–50) but approximately constant over the remainder of the size range (25–40). Rod density also decreased with increasing body size but rod numbers per unit visual arc were relatively constant, except in the smallest fish, where angular rod density was low. The same prey taxa occurred in fish of all sizes; however, prey items smaller than about 1.5 mm were not taken by fish of any body size.     

Ontogeny and disease responses of Langerhans-like cells in lymphoid tissues of salmonid fish

The ontogeny and disease responses of Langerhans-like cells within lymphoid tissues of Atlantic salmon, Salmo salar, and rainbow trout, Oncorhynchus mykiss, were investigated. These cells were studied in situ with the use of two markers: the ultrastructural presence of Birbeck-like granules and immunohistochemistry with an antibody against human langerin/CD207 that cross-reacts with salmonid tissues. The appearance of Birbeck-like granules was observed in rainbow trout at 2 weeks post-hatch (PH) in the thymus and anterior kidney prior to the development of the spleen. Spleen first appeared at 3 weeks PH in both Atlantic salmon and rainbow trout, and Birbeck-like granules were observed within cells of the newly developed spleens. The cross-reactivity of langerin as seen by immunohistochemistry was not clearly observed in kidney and spleen until 9 weeks PH, when a strong cytoplasmic reaction was observed. To study langerin-positive cells in spleen and kidney during disease, microsporidial gill disease (MGD) in rainbow trout was used as a known disease model inducing a strong cell-mediated adaptive immune response. Langerin-positive cells in healthy fish were seen predominantly in the spleen, and only low numbers were present in the anterior kidney. During MGD, langerin-positive cell numbers were elevated in the anterior kidney and were significantly higher during 5, 6, and 10 weeks post-exposure (PE) compared with healthy control tissue. During MGD, the distribution of langerin-positive cells in the spleen and anterior kidney shifted from having significantly higher numbers of cells in the spleen than in the kidney in controls and at 1 and 4 weeks PE to having a similar distribution of the cells in the two organs at 2, 3, 5, and 6 weeks PE. By 10 weeks PE, significantly higher numbers of langerin-positive cells occurred in the anterior kidney compared with the spleen.     

Ontogeny of prey attack behaviour in larvae and juveniles of three European cyprinids

Synopsis The ontogenetic change in time costs of prey attacks as well as the change in capture efficiency for representative cladoceran and cyclopoid prey was investigated in roach, Rutilus rutilus, bleak, Alburnus alburnus, and blue bream, Abramis ballerus. Video recordings were used for measuring the timing of attacks, whereas capture efficiencies were determined by direct observation. Decreases in the time cost of attacks reflect the decreasing importance of prey fixation during growth of the fish. No differences in capture efficiencies were found among the three cyprinid species, indicating that attack behaviour is unlikely to function as a basic mechanism leading to differences in prey selectivity among the investigated species. Increasing capture efficiency during early development may lead to increasing selectivity for cyclopoid prey in the field.     

Fitness consequences of habitat variability,trophic position,and energy allocation across the depth distribution of a coral-reef fish

Environmental clines such as latitude and depth that limit species’ distributions may be associated with gradients in habitat suitability that can affect the fitness of an organism. With the global loss of shallow-water photosynthetic coral reefs, mesophotic coral ecosystems (~30–150 m) may be buffered from some environmental stressors, thereby serving as refuges for a range of organisms including mobile obligate reef dwellers. Yet habitat suitability may be diminished at the depth boundary of photosynthetic coral reefs. We assessed the suitability of coral-reef habitats across the majority of the depth distribution of a common demersal reef fish (Stegastes partitus) ranging from shallow shelf (SS, <10 m) and deep shelf (DS, 20–30 m) habitats in the Florida Keys to mesophotic depths (MP, 60–70 m) at Pulley Ridge on the west Florida Shelf. Diet, behavior, and potential energetic trade-offs differed across study sites, but did not always have a monotonic relationship with depth, suggesting that some drivers of habitat suitability are decoupled from depth and may be linked with geographic location or the local environment. Feeding and diet composition differed among depths with the highest consumption of annelids, lowest ingestion of appendicularians, and the lowest gut fullness in DS habitats where predator densities were highest and fish exhibited risk-averse behavior that may restrict foraging. Fish in MP environments had a broader diet niche, higher trophic position, and higher muscle C:N ratios compared to shallower environments. High C:N ratios suggest increased tissue lipid content in fish in MP habitats that coincided with higher investment in reproduction based on gonado-somatic index. These results suggest that peripheral MP reefs are suitable habitats for demersal reef fish and may be important refuges for organisms common on declining shallow coral reefs.