Ontogenetic Shifts in the Number of Axons in the Olfactory Tract and Optic Nerve in Two Species of Deep-Sea Grenadier Fish (Gadiformes: Macrouridae: Coryphaenoides)

Neuroanatomical studies of the peripheral sense organs and brains of deep-sea fishes are particularly useful for predicting their sensory capabilities and ultimately their behavior. Over the abyssal plane (between 2,000 and 6,000 m), communities of grenadiers (Gadiformes: Macrouridae) play an important ecological role as predator-scavengers. Previous studies suggest that these fishes rely heavily on chemosensation, especially olfaction. Furthermore, at least one species, Coryphaenoides armatus, undergoes an ontogenetic shift in the relative size of the optic tectum and the olfactory bulbs, suggesting. a shift from a reliance on vision to olfaction during ontogeny, apparently in association with a shift to a more scavenging lifestyle. Here, we compared the olfactory and visual sensory inputs to the brain in C. armatus, and in a second, closely-related species, Coryphaenoides profundicolus, by assessing the total number of axons (myelinated and unmyelinated) in the olfactory tract and optic nerve in a range of individuals from both species. In C. armatus, the numbers of axons in both tract and nerve increased with body size, with the total number of axons in the olfactory tract being far greater than the number of axons in the optic nerve. These differences became more pronounced in larger animals. In the two smaller C. profundicolus individuals (≤ 315 mm SL), there were more axons in the optic nerve than in the olfactory tract, but the opposite situation was found in larger individuals. As in C. armatus, the number of olfactory tract axons also increased with body size in C. profundicolus, but in contrast, the number of optic nerve axons decreased in this species. These results suggest that both C. armatus and C. profundicolus undergo an ontogenetic shift in sensory orientation, with olfaction becoming relatively more important than vision in larger animals. The differences in the ratio of olfactory tract to optic nerve axons in C. armatus indicate that olfaction is of particular importance to larger individuals of this species. In both species, the percentage of myelinated axons in the olfactory tract was relatively low, but we found evidence for interspecific and ontogenetic variation in the percentages of myelinated axons in the optic nerve

Multiple Cone Visual Pigments and the Potential for Trichromatic Colour Vision in Two Species of Elasmobranch

Elasmobranchs (sharks, skates and rays) are the modern descendents of the first jawed vertebrates and, as apex predators, often occupy the highest trophic levels of aquatic (predominantly marine) ecosystems. However, despite their crucial role in the structure of marine communities, their importance both to commercial and to recreational fisheries, and the inherent interest in their role in vertebrate evolution, very little is known about their visual capabilities, especially with regard to whether or not they have the potential for colour vision. Using microspectrophotometry, we show that the retinae of the giant shovelnose ray (Rhinobatos typus) and the eastern shovelnose ray (Aptychotrema rostrata) contain three spectrally distinct cone visual pigments with wavelengths of maximum absorbance (lamda_max) at 477, 502 and 561 nm and at 459, 492 and 553 nm, respectively. The retinae of R. typus and A. rostrata also contain a single type of rod visual pigment with lamda_max at 504 and 498 nm, respectively. R. typus, living in the same estuarine waters as A. rostrata, were found to have identical visual pigments to R. typus inhabiting coral reef flats, despite a considerable difference in habitat spectral radiance. This is the first time that multiple cone visual pigments have been measured directly in an elasmobranch. The finding raises the possibility that some species are able to discriminate colour - a visual ability traditionally thought to be lacking in this vertebrate class - and it is evident that the visual ecology of elasmobranchs is far more complex than once thought

Cone photoreceptor oil droplet pigmentation is affected by ambient light intensity

The cone photoreceptors of many vertebrates contain spherical organelles called oil droplets. In birds, turtles, lizards and some lungfish the oil droplets are heavily pigmented and function to filter the spectrum of light incident upon the visual pigment within the outer segment. Pigmented oil droplets are beneficial for colour discrimination in bright light, but at lower light levels the reduction in sensitivity caused by the pigmentation increasingly outweighs the benefits generated by spectral tuning. Consequently, it is expected that species with pigmented oil droplets should modulate the density of pigment in response to ambient light intensity and thereby regulate the amount of light transmitted to the outer segment. In this study, microspectrophotometry was used to measure the absorption spectra of cone oil droplets in chickens (Gallus gallus domesticus) reared under bright (unfiltered) or dim (filtered) sunlight. Oil droplet pigmentation was found to be dependent on the intensity of the ambient light and the duration of exposure to the different lighting treatments. In adult chickens reared in bright light, the oil droplets of all cone types (except the violet-sensitive single cones, whose oil droplet is always non-pigmented) were more densely pigmented than those in chickens reared in dim light. Calculations show that the reduced levels of oil droplet pigmentation in chickens reared in dim light would increase the sensitivity and spectral bandwidth of the outer segment significantly. The density of pigmentation in the oil droplets presumably represents a trade-off between the need for good colour discrimination and absolute sensitivity. This might also explain why nocturnal animals, or those that underwent a nocturnal phase during their evolution, have evolved oil droplets with low pigment densities or no pigmentation or have lost their oil droplets altogether

A Novel Method for Comparative Analysis of Retinal Specialization Traits from Topographic Maps

Abstract Vertebrates possess different types of retinal specializations that vary in number, size, shape, and position in the retina. This diversity in retinal configuration has been revealed through topographic maps, which show variations in neuron density across the retina. Although topographic maps of about 300 vertebrates are available, there is no method for characterizing retinal traits quantitatively. Our goal is to present a novel method to standardize information on the position of the retinal specializations and changes in retinal ganglion cell (RGC) density across the retina from published topographic maps. We measured the position of the retinal specialization using two Cartesian coordinates and the gradient in cell density by sampling ganglion cell density values along four axes (nasal, temporal, ventral, and dorsal). Using this information, along with the peak and lowest RGC densities, we conducted discriminant function analyses (DFAs) to establish if this method is sensitive to distinguish three common types of retinal specializations (fovea, area, and visual streak). The discrimination ability of the model was higher when considering terrestrial (78%–80% correct classification) and aquatic (77%–86% correct classification) species separately than together. Our method can be used in the future to test specific hypotheses on the differences in retinal morphology between retinal specializations and the association between retinal morphology and behavioral and ecological traits using comparative methods controlling for phylogenetic effects

Behavioural responses of humpback whales to food-related chemical stimuli

Publisher's version (útgefin grein)Baleen whales face the challenge of finding patchily distributed food in the open ocean. Their relatively well-developed olfactory structures suggest that they could identify the specific odours given off by planktonic prey such as krill aggregations. Like other marine predators, they may also detect dimethyl sulfide (DMS), a chemical released in areas of high marine productivity. However, dedicated behavioural studies still have to be conducted in baleen whales in order to confirm the involvement of chemoreception in their feeding ecology. We implemented 56 behavioural response experiments in humpback whales using two food-related chemical stimuli, krill extract and DMS, as well as their respective controls (orange clay and vegetable oil) in their breeding (Madagascar) and feeding grounds (Iceland and Antarctic Peninsula). The whales approached the stimulus area and stayed longer in the trial zone during krill extract trials compared to control trials, suggesting that they were attracted to the chemical source and spent time exploring its surroundings, probably in search of prey. This response was observed in Iceland, and to a lesser extend in Madagascar, but not in Antarctica. Surface behaviours indicative of sensory exploration, such as diving under the stimulus area and stopping navigation, were also observed more often during krill extract trials than during control trials. Exposure to DMS did not elicit such exploration behaviours in any of the study areas. However, acoustic analyses suggest that DMS and krill extract both modified the whales’ acoustic activity in Madagascar. Altogether, these results provide the first behavioural evidence that baleen whales actually perceive prey-derived chemical cues over distances of several hundred metres. Chemoreception, especially olfaction, could thus be used for locating prey aggregations and for navigation at sea, as it has been shown in other marine predators including seabirds.This research was funded by the Fondation Total (www.fondation.total.com), grant #144903 to A.C., and the Ministère de l'Enseignement Supérieur et de la Recherche (www.enseignementsup-recherche.gouv.fr) to B.B., Bourse doctorale. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.Peer Reviewe

Understanding the retinal basis of vision across species

The vertebrate retina first evolved some 500 million years ago in ancestral marine chordates. Since then, the eyes of different species have been tuned to best support their unique visuoecological lifestyles. Visual specializations in eye designs, large-scale inhomogeneities across the retinal surface and local circuit motifs mean that all species' retinas are unique. Computational theories, such as the efficient coding hypothesis, have come a long way towards an explanation of the basic features of retinal organization and function; however, they cannot explain the full extent of retinal diversity within and across species. To build a truly general understanding of vertebrate vision and the retina's computational purpose, it is therefore important to more quantitatively relate different species' retinal functions to their specific natural environments and behavioural requirements. Ultimately, the goal of such efforts should be to build up to a more general theory of vision

Head-bobbing in the Ring-billed Gull (Larus delawarensis)

Many birds bob their head as they walk or run on the ground. The functional significance of this behaviour is unclear, but there is strong evidence that it plays a significant role in enhancing visual perception. If head-bobbing is advantageous, however, then it is a puzzle that some birds do not head-bob. As a group, gulls (Laridae) are among the birds that reportedly do not head-bob,yet here we report head-bobbing among Ring-billed Gulls (Larus delawarensis), observed and filmed in Ontario, when walking relatively slowly while foraging on the ground. This suggests that head-bobbing plays a key role in the visual detection of food items in this species. We suggest that head-bobbing may be a relatively common behaviour in foraging Ring-billed Gulls and speculate that other gulls (and indeed other birds) previously thought not to head-bob may in fact do so under certain circumstances

Volumetric analysis of sensory brain areas indicates ontogenetic shifts in the relative importance of sensory systems in elasmobranchs

Studies on the brains of teleost fishes have shown that the relative size of sensory brain areas reflects sensory specialisations and the relative importance of a given sensory system. Moreover, the relative size of these brain areas can change in relation to ontogenetic shifts in habitat and feeding ecology. However, although elasmobranchs (sharks, skates and rays) also exhibit ontogenetic shifts in habitat and diet, little is known about how their sensory systems and brains may adapt to these changes. In this paper, we compare the relative volumes of four sensory brain areas; the olfactory bulbs, optic tectum, anterior lateral line lobes and posterior lateral line lobes (that receive input from the olfactory epithelium, eye, electroreceptors and lateral line, respectively) in juveniles and adults of seven species of elasmobranch (six species of shark and one species of ray). The relative volume of each brain area was expressed as proportion of the total sensory brain, the combined volume of the four brain areas. Significant differences were found in the relative proportions of the sensory brain areas between juveniles and adults. In all species, the optic tectum was relatively larger in juveniles, whereas the size of the olfactory bulbs was relatively greater in adults. This paper provides the first evidence for shifts in the size of sensory brain areas in elasmobranchs and suggests that vision is relatively more important than olfaction in juvenile elasmobranchs and vice versa in adults

Ontogenetic Shifts in Brain Organization in the Bluespotted Stingray Neotrygon kuhlii (Chondrichthyes: Dasyatidae)

Fishes exhibit lifelong neurogenesis and continual brain growth. One consequence of this continual growth is that the nervous system has the potential to respond with enhanced plasticity to changes in ecological conditions that occur during ontogeny. The life histories of many teleost fishes are composed of a series of distinct stages that are characterized by shifts in diet, habitat, and behavior. In many cases, these shifts correlate with changes in overall brain growth and brain organization, possibly reflecting the relative importance of different senses and locomotor performance imposed by the new ecological niches they encounter throughout life. Chondrichthyan (cartilaginous) fishes also undergo ontogenetic shifts in habitat, movement patterns, diet, and behavior, but very little is known about any corresponding shifts in the size and organization of their brains. Here, we investigated postparturition ontogenetic changes in brain-body size scaling, the allometric scaling of seven major brain areas (olfactory bulbs, telencephalon, diencephalon, optic tectum, tegmentum, cerebellum, and medulla oblongata) relative to the rest of the brain, and cerebellar foliation in a chondrichthyan, i.e., the bluespotted stingray Neotrygon kuhlii. We also investigated the unusual morphological asymmetry of the cerebellum in this and other batoids. As in teleosts, the brain continues to grow throughout life, with a period of rapid initial growth relative to body size, before slowing considerably at the onset of sexual maturity. The olfactory bulbs and the cerebellum scale with positive allometry relative to the rest of the brain, whereas the other five brain areas scale with varying degrees of negative allometry. None of the major brain areas showed the stage-specific differences in rates of growth often found in teleosts. Cerebellar foliation also increases at a faster rate than overall brain growth. We speculate that changes in the olfactory bulbs and cerebellum could reflect increased olfactory and locomotor capabilities, which may be associated with ontogenetic shifts in diet, habitat use, and activity patterns, as well as shifts in behavior that occur with the onset of sexual maturity. The frequency distributions of the three cerebellar morphologies exhibited in this species best fit a 2:1:1 (right-sided:left-sided:intermediate) distribution, mirroring previous findings for another stingray species.</p