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Sockeye salmon, Oncorhynchus nerka, are anadromous, semelparous fish that breed in freshwater-typically in streams, and juveniles in most populations feed in lakes for 1 or 2 years, then migrate to sea to feed for 2 or 3 additional years, before returning to their natal sites to spawn and die. This species undergoes important changes in behavior, habitat, and morphology through these multiple life history stages. However, the sensory systems that mediate these migratory patterns are not fully understood, and few studies have explored changes in sensory function and specialization throughout ontogeny. This study investigates changes in the olfactory rosette of sockeye salmon across four different life stages (fry, parr, smolt, and adult). Development of the olfactory rosette was assessed by comparing total rosette size (RS), lamellae number, and lamellae complexity from scanning electron microscopy images across life stages, as a proxy for olfactory capacity. Olfactory RS increased linearly with lamellae number and body size (p .001). The complexity of the rosette, including the distribution of sensory and nonsensory epithelia and the appearance of secondary lamellar folding, varied between fry and adult life stages. These differences in epithelial structure may indicate variation in odor-processing capacity between juveniles imprinting on their natal stream and adults using those odor memories in the final stages of homing to natal breeding sites. These findings improve our understanding of the development of the olfactory system throughout life in this species, highlighting that ontogenetic shifts in behavior and habitat may coincide with shifts in nervous system development.

The cetacean vertebral canal houses the spinal cord and arterial supply to and venous drainage from the entire central nervous system (CNS). Thus, unlike terrestrial mammals, the cetacean spinal cord lies within a highly vascularized space. We compared spinal cord size and vascular volumes within the vertebral canal across a sample of shallow and deep diving odontocetes. We predicted that the (a) spinal cord, a metabolically expensive tissue, would be relatively small, while (b) volumes of vascular structures would be relatively large, in deep versus shallow divers. Our sample included the shallow diving Tursiops truncatus (n = 2) and Delphinus delphis (n = 3), and deep diving Kogia breviceps (n = 2), Mesoplodon europaeus (n = 2), and Ziphius cavirostris (n = 1). Whole, frozen vertebral columns were cross-sectioned at each intervertebral disc, scaled photographs of vertebral canal contents acquired, and cross-sectional areas of structures digitally measured. Areas were multiplied by vertebral body lengths and summed to calculated volumes of neural and vascular structures. Allometric analyses revealed that the spinal cord scaled with negative allometry (b = 0.51 ± 0.13) with total body mass (TBM), and at a rate significantly lower than that of terrestrial mammals. As predicted, the spinal cord represented a smaller percentage of the total vertebral canal volume in the deep divers relative to shallow divers studied, as low as 2.8% in Z. cavirostris. Vascular volume scaled with positive allometry (b = 1.2 ± 0.22) with TBM and represented up to 96.1% (Z. cavirostris) of the total vertebral canal volume. The extreme deep diving beaked whales possessed 22-35 times more vascular volume than spinal cord volume within the vertebral canal, compared with the 6-10 ratio in the shallow diving delphinids. These data offer new insights into morphological specializations of neural and vascular structures that may contribute to differential diving capabilities across odontocete cetaceans.

The size (volume or mass) of the olfactory bulbs in relation to the whole brain has been used as a neuroanatomical proxy for olfactory capability in a range of vertebrates, including fishes. Here, we use diffusible iodine-based contrast-enhanced computed tomography (diceCT) to test the value of this novel bioimaging technique for generating accurate measurements of the relative volume of the main olfactory brain areas (olfactory bulbs, peduncles, and telencephalon) and to describe the morphological organisation of the ascending olfactory pathway in model fish species from two taxa, the brownbanded bamboo shark Chiloscyllium punctatum and the common goldfish Carassius auratus. We also describe the arrangement of primary projections to the olfactory bulb and secondary projections to the telencephalon in both species. Our results identified substantially larger olfactory bulbs and telencephalon in C. punctatum compared to C. auratus (comprising approximately 5.2% vs. 1.8%, and 51.8% vs. 11.8% of the total brain volume, respectively), reflecting differences between taxa, but also possibly in the role of olfaction in the sensory ecology of these species. We identified segregated primary projections to the bulbs, associated with a compartmentalised olfactory bulb in C. punctatum, which supports previous findings in elasmobranch fishes. DiceCT imaging has been crucial for visualising differences in the morphological organisation of the olfactory system of both model species. We consider comparative neuroanatomical studies between representative species of both elasmobranch and teleost fish groups are fundamental to further our understanding of the evolution of the olfactory system in early vertebrates and the neural basis of olfactory abilities.

Across vertebrates increased maternal investment (via increased pre- and postnatal provisioning) is associated with larger relative brain size, yet it remains unclear how brain organization is shaped by life history and ecology. Here, we tested whether maternal investment and ecological lifestyle are related to variation in brain size and organization across 100 chondrichthyans. We hypothesized that brain size and organization would vary with the level of maternal investment and habitat depth and complexity. We found that chondrichthyan brain organization varies along four main axes according to (1) absolute brain size, (2) relative diencephalon and mesencephalon size, (3) relative telencephalon and medulla size, and (4) relative cerebellum size. Increased maternal investment is associated with larger relative brain size, while ecological lifestyle is informative for variation between relative telencephalon and medulla size and relative cerebellum size after accounting for the independent effects of reproductive mode. Deepwater chondrichthyans generally provide low levels of yolk-only (lecithotrophic) maternal investment and have relatively small brains, predominantly composed of medulla (a major portion of the hindbrain), whereas matrotrophic chondrichthyans-which provide maternal provisioning beyond the initial yolk sac-found in coastal, reef, or shallow oceanic habitats have relatively large brains, predominantly composed of telencephalon (a major portion of the forebrain). We have demonstrated, for the first time, that both ecological lifestyle and maternal investment are independently associated with brain organization in a lineage with diverse life-history strategies and reproductive modes.

Studies on the auditory system of fishes can provide fundamental information about the early evolution of vertebrate hearing. While there are limited data available on the auditory system of bony fishes, comparatively far less is known about auditory structures in elasmobranchs, despite their critical basal position within vertebrate evolution. Specifically, while there is a high degree of plasticity in the nervous system, little is known about how the different sensory epithelia within the inner ear vary throughout life in elasmobranchs. Using a combination of immunohistochemistry and fluorescence microscopy, we quantified macular area, number of sensory hair cells, hair cell density, and hair cell orientations in the saccule, lagena, utricle, and macula neglecta of school sharks (Galeorhinus galeus) of varying body size. In all maculae, macular area and the number of hair cells increased significantly throughout ontogeny, while hair cell density displayed a concurrent ontogenetic decrease (excluding the utricle). There were also significant differences in macular area, hair cell number, and hair cell density between the four maculae. However, hair cell orientation patterns did not vary between individuals and did not change with body growth. These findings represent one of the first comprehensive characterisations of the inner ear sensory epithelia in an elasmobranch, and reveal changes in morphology that may have implications for auditory capabilities through ontogeny.

Throughout an animal’s life, species may occupy different environments and exhibit distinct life stages, known as ontogenetic shifts. The life histories of most sharks (class: Chondrichthyes) are characterized by these ontogenetic shifts, which can be defined by changes in habitat and diet as well as behavioral changes at the onset of sexual maturity. In addition, fishes experience indeterminate growth, whereby the brain and body grow throughout the organism’s life. Despite a presupposed lifelong neurogenesis in sharks, very little work has been done on ontogenetic changes in the brain, which may be informative about functional shifts in sensory and behavioral specializations. This study quantified changes in brain-body scaling and the scaling of six major brain regions (olfactory bulbs, telencephalon, diencephalon, optic tectum, cerebellum, and medulla oblongata) throughout ontogeny in the Atlantic sharpnose shark, Rhizoprio­nodon terraenovae. As documented in other fishes, brain size increased significantly with body mass throughout ontogeny in this species, with the steepest period of growth in early life. The telencephalon, diencephalon, optic tectum, and medulla oblongata scaled with negative allometry against the rest of the brain throughout ontogeny. However, notably, the olfactory bulbs and cerebellum scaled hyperallometrically to the rest of the brain, whereby these structures enlarged disproportionately as this species matured. Changes in the relative size of the olfactory bulbs throughout ontogeny may reflect an increased reliance on olfaction at later life history stages in R. terraenovae, while changes in the relative size of the cerebellum throughout ontogeny may be indicative of the ability to capture faster prey or an increase in migratory nature as this species moves to offshore habitats, associated with the onset of sexual maturity.

In cartilaginous fishes, variability in the size of the brain and its major regions is often associated with primary habitat and/or specific behavior patterns, which may allow for predictions on the relative importance of different sensory modalities. The Greenland (Somniosus microcephalus) and Pacific sleeper (S. pacificus) sharks are the only non-lamnid shark species found in the Arctic and are among the longest living vertebrates ever described. Despite a presumed visual impairment caused by the regular presence of parasitic ocular lesions, coupled with the fact that locomotory muscle power is often depressed at cold temperatures, these sharks remain capable of capturing active prey, including pinnipeds. Using magnetic resonance imaging (MRI), brain organization of S. microcephalus and S. pacificus was assessed in the context of up to 117 other cartilaginous fish species, using phylogenetic comparative techniques. Notably, the region of the brain responsible for motor control (cerebellum) is small and lacking foliation, a characteristic not yet described for any other large-bodied (>3 m) shark. Further, the development of the optic tectum is relatively reduced, while olfactory brain regions are among the largest of any shark species described to date, suggestive of an olfactory-mediated rather than a visually-mediated lifestyle.

The effect of sound on the behaviour of sharks has not been investigated since the 1970s. Sound is, however, an important sensory stimulus underwater, as it can spread in all directions quickly and propagate further than any other sensory cue. We used a baited underwater camera rig to record the behavioural responses of eight species of sharks (seven reef and coastal shark species and the white shark, Carcharodon carcharias) to the playback of two distinct sound stimuli in the wild: an orca call sequence and an artificially generated sound. When sounds were playing, reef and coastal sharks were less numerous in the area, were responsible for fewer interactions with the baited test rigs, and displayed less ‘inquisitive’ behaviour, compared to during silent control trials. White sharks spent less time around the baited camera rig when the artificial sound was presented, but showed no significant difference in behaviour in response to orca calls. The use of the presented acoustic stimuli alone is not an effective deterrent for C. carcharias. The behavioural response of reef sharks to sound raises concern about the effects of anthropogenic noise on these taxa.

Brain size varies dramatically, both within and across species, and this variation is often believed to be the result of trade-offs between the cognitive benefits of having a large brain for a given body size and the energetic cost of sustaining neural tissue. One potential consequence of having a large brain is that organisms must also meet the associated high energetic demands. Thus, a key question is whether metabolic rate correlates with brain size. However, using metabolic rate to measure energetic demand yields a relatively instantaneous and dynamic measure of energy turnover, which is incompatible with the longer evolutionary timescale of changes in brain size within and across species. Morphological traits associated with oxygen consumption, specifically gill surface area, have been shown to be correlates of oxygen demand and energy use, and thus may serve as integrated correlates of these processes, allowing us to assess whether evolutionary changes in brain size correlate with changes in longer-term oxygen demand and energy use. We tested how brain size relates to gill surface area in the blacktip shark Carcharhinus limbatus. First, we examined whether the allometric slope of brain mass (i.e., the rate that brain mass changes with body mass) is lower than the allometric slope of gill surface area across ontogeny. Second, we tested whether gill surface area explains variation in brain mass, after accounting for the effects of body mass on brain mass. We found that brain mass and gill surface area both had positive allometric slopes, with larger individuals having both larger brains and larger gill surface areas compared to smaller individuals. However, the allometric slope of brain mass was lower than the allometric slope of gill surface area, consistent with our prediction that the allometric slope of gill surface area could pose an upper limit to the allometric slope of brain mass. Finally, after accounting for body mass, individuals with larger brains tended to have larger gill surface areas. Together, our results provide clues as to how fishes may evolve and maintain large brains despite their high energetic cost, suggesting that C. limbatus individuals with a large gill surface area for their body mass may be able to support a higher energetic turnover, and, in turn, a larger brain for their body mass.

Contrast-enhanced X-ray imaging provides a non-destructive and flexible approach to optimising contrast in soft tissues, especially when incorporated with Lugol’s solution (1% I2, 2% KI), a technique currently referred to as diffusible-iodine contrast-enhanced computed tomography (diceCT). This stain exhibits high rates of penetration and results in excellent contrast between and within soft tissues, including the central nervous system. Here, we present a staining method for optimising contrast in the brain of a cartilaginous fish, the brownbanded bamboo shark, Chiloscyllium punctatum, and a bony fish, the common goldfish, Carassius auratus, using diceCT. The aim of this optimisation procedure is to provide suitable contrast between neural tissue and background tissue(s) of the head, thereby facilitating digital segmentation and volumetric analysis of the central nervous system. Both species were scanned prior to staining and were rescanned at time (T) intervals, either every 48h (C. punctatum) or every 24h (C. auratus), to assess stain penetration and contrast enhancement. To compare stain intensities, raw X-ray computed tomography (CT) data were reconstructed using air and water calibration phantoms that were scanned under identical conditions to the samples. Optimal contrast across the brain was achieved at T = 240h for C. punctatum and T = 96h for C. auratus. Higher resolution scans of the whole brain were obtained at the two optimised staining times for all the corresponding specimens. The use of diceCT provides a new and valuable tool for visualising differences in the anatomical organisation of both the central and peripheral nervous systems of fishes. SIGNIFICANCE STATEMENT This study uses an emerging bioimaging technique based on X-ray CT, to advance our visualisation, and thus understanding, of brain organisation and structure in a cartilaginous and bony fish model species. diceCT is a relatively new approach to improving contrast between/within soft tissues, and is becoming increasingly popular across many fields of research, including evolutionary biology, biomechanics, palaeontology and comparative anatomy. Few studies have undertaken a rigorous assessment of stain penetration using Lugol’s iodine, especially in the brain. Here, we present the first staining optimisation using diceCT in any species of fish. There is therefore a vital need to standardise the methodology used, to collect comparable, replicable data, and thus further develop its usage and value across disciplines and taxa.

Throughout an animal's life, species may occupy different environments and exhibit distinct life stages, known as ontogenetic shifts. The life histories of most sharks (class: Chondrichthyes) are characterized by these ontogenetic shifts, which can be defined by changes in habitat and diet as well as behavioral changes at the onset of sexual maturity. In addition, fishes experience indeterminate growth, whereby the brain and body grow throughout the organism's life. Despite a presupposed lifelong neurogenesis in sharks, very little work has been done on ontogenetic changes in the brain, which may be informative about functional shifts in sensory and behavioral specializations. This study quantified changes in brain-body scaling and the scaling of six major brain regions (olfactory bulbs, telencephalon, diencephalon, optic tectum, cerebellum, and medulla oblongata) throughout ontogeny in the Atlantic sharpnose shark, Rhizoprio-nodon terraenovae. As documented in other fishes, brain size increased significantly with body mass throughout ontogeny in this species, with the steepest period of growth in early life. The telencephalon, diencephalon, optic tectum, and medulla oblongata scaled with negative allometry against the rest of the brain throughout ontogeny. However, notably, the olfactory bulbs and cerebellum scaled hyperallometrically to the rest of the brain, whereby these structures enlarged disproportionately as this species matured. Changes in the relative size of the olfactory bulbs throughout ontogeny may reflect an increased reliance on olfaction at later life history stages in R. terraenovae, while changes in the relative size of the cerebellum throughout ontogeny may be indicative of the ability to capture faster prey or an increase in migratory nature as this species moves to offshore habitats, associated with the onset of sexual maturity.

The volume of the olfactory bulbs (OBs) relative to the brain has been used previously as a proxy for olfactory capabilities in many vertebrate taxa, including fishes. Although this gross approach has predictive power, a more accurate assessment of the number of afferent olfactory inputs and the convergence of this information at the level of the telencephalon is critical to our understanding of the role of olfaction in the behaviour of fishes. In this study, we used transmission electron microscopy to assess the number of first-order axons within the olfactory nerve (ON) and the number of second-order axons in the olfactory peduncle (OP) in established model species within cartilaginous (brownbanded bamboo shark, Chiloscyllium punctatum [CP]) and bony (common goldfish, Carassius auratus [CA]) fishes. The total number of axons varied from a mean of 18.12 ± 7.50 million in the ON to a mean of 0.38 ± 0.21 million in the OP of CP, versus 0.48 ± 0.16 million in the ON and 0.09 ± 0.02 million in the OP of CA. This resulted in a convergence ratio of approximately 50:1 and 5:1, respectively, for these two species. Based on astroglial ensheathing, axon type (unmyelinated [UM] and myelinated [M]) and axon size, we found no differentiated tracts in the OP of CP, whereas a lateral and a medial tract (both of which could be subdivided into two bundles or areas) were identified for CA, as previously described. Linear regression analyses revealed significant differences not only in axon density between species and locations (nerves and peduncles), but also in axon type and axon diameter (p < 0.05). However, UM axon diameter was larger in the OPs than in the nerve in both species (p = 0.005), with no significant differences in UM axon diameter in the ON (p = 0.06) between species. This study provides an in-depth analysis of the neuroanatomical organisation of the ascending olfactory pathway in two fish taxa and a quantitative anatomical comparison of the summation of olfactory information. Our results support the assertion that relative OB volume is a good indicator of the level of olfactory input and thereby a proxy for olfactory capabilities.

Personal shark deterrents offer the potential of a non-lethal solution to protect individuals from negative interactions with sharks, but the claims of effectiveness of most deterrents are based on theory rather than robust testing of the devices themselves. Therefore, there is a clear need for thorough testing of commercially available shark deterrents to provide the public with information on their effectiveness. Using a modified stereo-camera system, we quantified behavioural interactions between Carcharodon carcharias (white sharks) and a baited target in the presence of a commercially available electric anklet shark deterrent, the Electronic Shark Defense System (ESDS). The stereo-camera system enabled accurate assessment of the behavioural responses of C. carcharias when approaching an ESDS. We found that the ESDS had limited meaningful effect on the behaviour of C. carcharias, with no significant reduction in the proportion of sharks interacting with the bait in the presence of the active device. At close proximity (< 15.5 cm), the active ESDS did show a significant reduction in the number of sharks biting the bait, but this was countered by an increase in other, less aggressive, interactions. The ESDS discharged at a frequency of 7.8 Hz every 5.1 s for 2.5 s, followed by an inactive interval of 2.6 s. As a result, many sharks may have encountered the device in its inactive state, resulting in a reduced behavioural response. Consequently, decreasing the inactive interval between pulses may improve the overall effectiveness of the device, but this would not improve the effective deterrent range of the device, which is primarily a factor of the voltage gradient rather than the stimulus frequency. In conclusion, given the very short effective range of the ESDS and its unreliable deterrent effect, combined with the fact that shark-bite incidents are very rare, it is unlikely that the current device would significantly reduce the risk of a negative interaction with C. carcharias.

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.

The allometric relationship between brain and body size among vertebrates is often considered a manifestation of evolutionary constraints. However, birds and mammals have undergone remarkable encephalization, in which brain size has increased without corresponding changes in body size. Here, we explore the hypothesis that a reduction of phenotypic integration between brain and body size has facilitated encephalization in birds and mammals. Using a large dataset comprising 20,213 specimens across 4,587 species of jawed vertebrates, we show that the among-species (evolutionary) brain-body allometries are remarkably constant, both across vertebrate classes and across taxonomic levels. Birds and mammals, however, are exceptional in that their within-species (static) allometries are shallower and more variable than in other vertebrates. These patterns are consistent with the idea that birds and mammals have reduced allometric constraints that are otherwise ubiquitous across jawed vertebrates. Further exploration of ontogenetic allometries in selected taxa of birds, fishes and mammals reveals that birds and mammals have extended the period of fetal brain growth compared to fishes. Based on these findings, we propose that avian and mammalian encephalization has been contingent on increased variability in brain growth patterns.

Sensory systems play a central role in guiding animal behaviour. They can be manipulated to alter behavioural outcomes to limit negative interactions between humans and animals. Sharks are often seen as a threat to humans and there has been increasing interest in developing shark mitigation devices. Previous research has concentrated on stimulating the electrosensory and olfactory systems of sharks, whereas the influence of light and sound on their behaviour has received little attention. In this study, the effects of an intense strobe light and a loud, artificial sound composed of mixed frequencies and intensities on shark behaviour were assessed. We tested these stimuli individually and in combination on wild-caught captive Port Jackson (Heterodontus portusjacksoni) and epaulette (Hemiscyllium ocellatum) sharks in aquaria and on wild great white sharks (Carcharodon carcharias) in the field. When presented alone and in combination with sound, the lights reduced the number of times that the bait was taken by both H. portusjacksoni and H. ocellatum in captivity. The strobe light alone, however, did not affect the behaviour of white sharks, but when presented in combination with sound, white sharks spent significantly less time in proximity to the bait. As the lights and sound presented in this study did not show a pronounced deterrent effect on C. carcharias, we do not advise their use as a strategy for mitigating shark–human interactions. However, due to the potential effectiveness of strobe lights in deterring other species of sharks, there may be applications for this approach in the reduction of fisheries bycatch.

In this chapter we provide a description of the cerebellum in nonmammalian vertebrates. This includes comparative aspects of gross morphology, connectivity in the cerebellar cortex, and the organization of sagittal zones. We also examine variation in the degree of foliation of the cerebellum among species in relation to behavior and neural processing. Finally, we outline differences in the distribution of the expression of the molecular marker zebrin II by Purkinje cells and its implications for cerebellar evolution.

This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited., Sharks play a vital role in the health of marine ecosystems, but the potential threat that sharks pose to humans is a reminder of our vulnerability when entering the ocean. Personal shark deterrents are being marketed as the solution to mitigate the threat that sharks pose. However, the effectiveness claims of many personal deterrents are based on our knowledge of shark sensory biology rather than robust testing of the devices themselves, as most have not been subjected to independent scientific studies. Therefore, there is a clear need for thorough testing of commercially available shark deterrents to provide the public with recommendations of their effectiveness. Using a modified stereo-camera system, we quantified behavioural interactions between white sharks (Carcharodon carcharias) and a baited target in the presence of a commercially available, personal electric shark deterrent (Shark Shield Freedom7™). The stereo-camera system enabled an accurate assessment of the behavioural responses of C. carcharias when encountering a non-lethal electric field many times stronger than what they would naturally experience. Upon their first observed encounter, all C. carcharias were repelled at a mean (± std. error) proximity of 131 (± 10.3) cm, which corresponded to a mean voltage gradient of 9.7 (± 0.9) V/m. With each subsequent encounter, their proximity decreased by an average of 11.6 cm, which corresponded to an increase in tolerance to the electric field by an average of 2.6 (± 0.5) V/m per encounter. Despite the increase in tolerance, sharks continued to be deterred from interacting for the duration of each trial when in the presence of an active Shark Shield™. Furthermore, the findings provide no support to the theory that electric deterrents attract sharks. The results of this study provide quantitative evidence of the effectiveness of a non-lethal electric shark deterrent, its influence on the behaviour of C. carcharias, and an accurate method for testing other shark deterrent technologies.

It is a widely accepted view that neural development can reflect morphological adaptations and sensory specializations. The aim of this review is to give a broad overview of the current status of brain data available for cartilaginous fishes and examine how perspectives on allometric scaling of brain size across this group of fishes has changed within the last 50 years with the addition of new data and more rigorous statistical analyses. The current knowledge of neuroanatomy in cartilaginous fishes is reviewed and data on brain size (encephalization, n = 151) and interspecific variation in brain organization (n = 84) has been explored to ascertain scaling relationships across this clade. It is determined whether similar patterns of brain organization, termed cerebrotypes, exist in species that share certain lifestyle characteristics. Clear patterns of brain organization exist across cartilaginous fishes, irrespective of phylogenetic grouping and, although this study was not a functional analysis, it provides further evidence that chondrichthyan brain structures might have developed in conjunction with specific behaviours or enhanced cognitive capabilities. Larger brains, with well-developed telencephala and large, highly foliated cerebella are reported in species that occupy complex reef or oceanic habitats, potentially identifying a reef-associated cerebrotype. In contrast, benthic and benthopelagic demersal species comprise the group with the smallest brains, with a relatively reduced telencephalon and a smooth cerebellar corpus. There is also evidence herein of a bathyal cerebrotype; deep-sea benthopelagic sharks possess relatively small brains and show a clear relative hypertrophy of the medulla oblongata. Despite the patterns observed and documented, significant gaps in the literature have been highlighted. Brain mass data are only currently available on c. 16% of all chondrichthyan species, and only 8% of species have data available on their brain organization, with far less on subsections of major brain areas that receive distinct sensory input. The interspecific variability in brain organization further stresses the importance of performing functional studies on a greater range of species. Only an expansive data set, comprised of species that span a variety of habitats and taxonomic groups, with widely disparate behavioural repertoires, combined with further functional analyses, will help shed light on the extent to which chondrichthyan brains have evolved as a consequence of behaviour, habitat and lifestyle in addition to phylogeny.

In cartilaginous fishes (Chondrichthyes; sharks, skates and rays (batoids), and holocephalans), the midbrain or mesencephalon can be divided into two parts, the dorsal tectum mesencephali or optic tectum (analogous to the superior colliculus of mammals) and the ventral tegmentum mesencephali. Very little is known about interspecific variation in the relative size and organization of the components of the mesencephalon in these fishes. This study examined the relative development of the optic tectum and the tegmentum in 75 chondrichthyan species representing 32 families. This study also provided a critical assessment of attempts to quantify the size of the optic tectum in these fishes volumetrically using an idealized half-ellipsoid approach (method E), by comparing this method to measurements of the tectum from coronal cross sections (method S). Using species as independent data points and phylogenetically independent contrasts, relationships between the two midbrain structures and both brain and mesencephalon volume were assessed and the relative volume of each brain area (expressed as phylogenetically corrected residuals) was compared among species with different ecological niches (as defined by primary habitat and lifestyle). The relatively largest tecta and tegmenta were found in pelagic coastal/oceanic and oceanic sharks, benthopelagic reef sharks, and benthopelagic coastal sharks. The smallest tecta were found in all benthic sharks and batoids and the majority of bathyal (deep-sea) species. These results were consistent regardless of which method of estimating tectum volume was used. We found a highly significant correlation between optic tectum volume estimates calculated using method E and method S. Taxon-specific variation in the difference between tectum volumes calculated using the two methods appears to reflect variation in both the shape of the optic tectum relative to an idealized half-ellipsoid and the volume of the ventricular cavity. Because the optic tectum is the principal termination site for retinofugal fibers arising from the retinal ganglion cells, the relative size of this brain region has been associated with an increased reliance on vision in other vertebrate groups, including bony fishes. The neuroecological relationships between the relative size of the optic tectum and primary habitat and lifestyle we present here for cartilaginous fishes mirror those established for bony fishes; we speculate that the relative size of the optic tectum and tegmentum similarly reflects the importance of vision and sensory processing in cartilaginous fishes.

Several patterns of brain allometry previously observed in mammals have been found to hold for sharks and related taxa (chondrichthyans) as well. In each clade, the relative size of brain parts, with the notable exception of the olfactory bulbs, is highly predictable from the total brain size. Compared with total brain mass, each part scales with a characteristic slope, which is highest for the telencephalon and cerebellum. In addition, cerebellar foliation reflects both absolute and relative cerebellar size, in a manner analogous to mammalian cortical gyrification. This conserved pattern of brain scaling suggests that the fundamental brain plan that evolved in early vertebrates permits appropriate scaling in response to a range of factors, including phylogeny and ecology, where neural mass may be added and subtracted without compromising basic function.

Very little is known about the brain organization of the suction filter feeder, Rhincodon typus, and how it compares to other orectolobiforms in light of its specialization as a plankton-feeder. Brain size and overall brain organization was assessed in two specimens of R. typus in relation to both phylogeny and ecology, using magnetic resonance imaging (MRI). In comparison to over 60 other chondrichthyan species, R. typus demonstrated a relatively small brain for its body size (expressed in terms of encephalization quotients and residuals), similar to the lamniforms Carcharodon carcharias, Cetorhinus maximus, and Carcharias taurus. R. typus possessed a relatively small telencephalon with some development of the dorsal pallium, which was suggestive of moderate social behavior, in addition to a relatively large diencephalon and a relatively reduced mesencephalon. The most notable characteristic of the brain of Rhincodon was a large and highly foliated cerebellum, one of the largest cerebellums within the chondrichthyan clade. Early development of the brain was qualitatively assessed using an in situ MRI scan of the brain and chondrocranium of a neonate specimen of R. typus. There was evidence that folding of the cerebellar corpus appeared in early development, although the depth and number of folds might vary ontogenetically in this species. Hierarchical cluster analysis and multidimensional scaling ordinations showed evidence of convergent evolution with the basking shark, Cetorhinus maximus, another large-bodied filter feeding elasmobranch, supporting the claim that organization of the brain is more similar in species with analogous but independently evolved lifestyles than those that share taxonomic classification.

Interspecific variation in relative brain size (encephalization), the relative size of the five major brain areas (the telencephalon, diencephalon, mesencephalon, cerebellum, and medulla) and the level of cerebellar foliation was assessed in over 20 representative species of batoid (skates and rays), from eight families. Using species as independent data points and phylogenetically independent contrasts, relationships among each of the neuroanatomical variables and two ecological variables, habitat and lifestyle, were assessed. Variation in relative brain size and brain organization appears to be strongly correlated with phylogeny. Members of the basal orders Rajiformes and Torpediniformes tend to have relatively small brains, with relatively small telencephalons, large medullas, and smooth, unfoliated cerebellums. More advanced Myliobatiformes possess relatively large brains, with relatively large telencephalons, small medullas, and complex, heavily foliated cerebellums. Increased brain size, telencephalon size, and cerebellar foliation also correlate with living in a complex habitat (such as in association with coral reefs) and an active, benthopelagic lifestyle, but as primary habitat and lifestyle also closely match phylogenetic relationships in batoids, it is difficult to separate the influence of phylogeny and ecological factors on brain organization in these animals. However, the results of two forms of multivariate analysis (principal component analysis and cluster analysis) reveal that certain species are clustered with others that share ecological traits, rather than with more closely related species from the same order. This suggests that ecological factors do play a role in defining patterns of brain organization and there is some evidence for ‘cerebrotypes’ in batoids.

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.

A true cerebellum appeared at the onset of the chondrichthyan (sharks, batoids, and chimaerids) radiation and is known to be essential for executing fast, accurate, and efficient movement. In addition to a high degree of variation in size, the corpus cerebellum in this group has a high degree of variation in convolution (or foliation) and symmetry, which ranges from a smooth cerebellar surface to deep, branched convexities and folds, although the functional significance of this trait is unclear. As variation in the degree of foliation similarly exists throughout vertebrate evolution, it becomes critical to understand this evolutionary process in a wide variety of species. However, current methods are either qualitative and lack numerical rigor or they are restricted to two dimensions. In this paper, a recently developed method for the characterization of shapes embedded within noisy, three-dimensional data called spherical wave decomposition (SWD) is applied to the problem of characterizing cerebellar foliation in cartilaginous fishes. The SWD method provides a quantitative characterization of shapes in terms of well-defined mathematical functions. An additional feature of the SWD method is the construction of a statistical criterion for the optimal fit, which represents the most parsimonious choice of parameters that fits to the data without overfitting to background noise. We propose that this optimal fit can replace a previously described qualitative visual foliation index (VFI) in cartilaginous fishes with a quantitative analog, i.e. the cerebellar foliation index (CFI). The capability of the SWD method is demonstrated in a series of volumetric images of brains from different chondrichthyan species that span the range of foliation gradings currently described for this group. The CFI is consistent with the qualitative grading provided by the VFI, delivers a robust measure of cerebellar foliation, and can provide a quantitative basis for brain shape characterization across taxa.

1. Introduction 2. The Visual System 2.1. The Eye and Image Formation 2.2. Photoreception and Spectral Sensitivity 2.3. The Retina and the Choroidal Tapetum 2.4. Visual Sampling 2.5. Visual Abilities 3. The Non-visual System 4. The Auditory and Vestibular Systems 4.1. The Inner Ear 4.2. Vestibular Control 4.3. Auditory Abilities 5. The Electrosensory System 5.1. Structure and Spatial Sampling of the Ampullary Organs 5.2. Role in Passive Electroreception 5.3. Role in Magnetoreception 6. The Lateral Line System 6.1. Canal and Superficial Neuromasts 6.2. Sensitivity to Hydrodynamic Stimuli 7. Cutaneous Mechanoreception 8. The Chemosensory Systems 8.1. The Olfactory Apparatus and the Sampling of Water-Borne Substances 8.2. Olfactory Sensitivity 8.3. The Gustatory Apparatus 8.4. Gustatory Sampling and Sensitivity 8.5. The Common Chemical Sense 9. Sensory Input to the Central Nervous System in Elasmobranchs 9.1. Neuroanatomy 9.2. Assessing the Relative Importance of Each Sensory Modality 9.3. Encephalization 9.4. Neuroecology 10. Perspectives on Future Directions Elasmobranchs occupy a diversity of ecological niches with each species adapted to a complex set of environmental conditions. These conditions can be defined as a web of environmental signals, which are detected by a battery of senses, that have enabled these apex predators to survive relatively unchanged for over 400 million years. Signals such as light, odors, electric and magnetic fields, sound, and hydrodynamic disturbances all form a sensoryscape that each species can detect and process. However, the biophysical signals and their propagation within each ecological niche differ and place selection pressures on the ability of a specific sensory modality to detect and respond to prey, predator, and mate. This review investigates how elasmobranchs sense their environment by examining a diversity of species from different habitats, the ways in which they sample their sensoryscape, the sensitivity of each of their senses, and the effect this has on their behavior. The relative importance of each sensory modality is also investigated and how sensory input to the central nervous system can be assessed and used as a predictor of behavior. Although there is still a great deal we do not understand about elasmobranch sensory systems, the anatomical, physiological, molecular, and bioimaging approaches currently being used are enabling us to ask complex behavioral questions of these impressive predators.

Olfaction is a universal modality by which all animals sample chemical stimuli from their environment. In cartilaginous fishes, olfaction is critical for various survival tasks including localizing prey, avoiding predators, and chemosensory communication with conspecifics. Little is known, however, about interspecific variation in olfactory capability in these fishes, or whether the relative importance of olfaction in relation to other sensory systems varies with regard to ecological factors, such as habitat and lifestyle. In this study, we have addressed these questions by directly examining interspecific variation in the size of the olfactory bulbs (OB), the region of the brain that receives the primary sensory projections from the olfactory nerve, in 58 species of cartilaginous fishes. Relative OB size was compared among species occupying different ecological niches. Our results show that the OBs maintain a substantial level of allometric independence from the rest of the brain across cartilaginous fishes and that OB size is highly variable among species. These findings are supported by phylogenetic generalized least-squares models, which show that this variability is correlated with ecological niche, particularly habitat. The relatively largest OBs were found in pelagic-coastal/oceanic sharks, especially migratory species such as Carcharodon carcharias and Galeocerdo cuvier. Deep-sea species also possess large OBs, suggesting a greater reliance on olfaction in habitats where vision may be compromised. In contrast, the smallest OBs were found in the majority of reef-associated species, including sharks from the families Carcharhinidae and Hemiscyllidae and dasyatid batoids. These results suggest that there is great variability in the degree to which these fishes rely on olfactory cues. The OBs have been widely used as a neuroanatomical proxy for olfactory capability in vertebrates, and we speculate that differences in olfactory capabilities may be the result of functional rather than phylogenetic adaptations.

The cerebellum is well developed in cartilaginous fishes, with the same cell types (barring basket cells) and organizational features found in other vertebrate groups, including mammals. In particular, the lattice-like organization of cerebellar cortex (with a molecular layer of parallel fibers, interneurons, spiny Purkinje cell dendrites, and climbing fibers) is a defining characteristic. In addition to the cerebellum, cartilaginous fishes have cerebellum-like structures in the dorsolateral wall of the hindbrain. These structures are adjacent to and, in part, contiguous with the cerebellum. They are cerebellum-like in that they have a molecular layer of parallel fibers and inhibitory interneurons that has striking organizational similarities to the molecular layer of the cerebellar cortex. However, these structures also have characteristics that differ from the cerebellum. For example, cerebellum-like structures do not have climbing fibers and are clearly sensory. They receive direct afferent input from peripheral sensory receptors and relay their outputs to midbrain sensory areas. As a consequence of this close sensory association and the ability of researchers to characterize signal processing in these structures in a behaviorally relevant context, good progress has been made in determining the fundamental processing algorithm of the cerebellum-like structures. This algorithm enables the molecular layer to act as an adaptive filter that cancels self-generated noise in electrosensory and lateral line systems. Given the fundamental similarities of the molecular layer across these structures and the phylogeny of these structures across basal vertebrates, it is clear that these structures share a common genetic-developmental program. Syngeny is a term that has been used to describe similarity of structure due to a shared genetic-developmental program, whether the structures are phylogenetically homologous or not. Given that the cerebellum and cerebellum-like structures are physically adjacent, we propose that cerebellum-like structures were the evolutionary antecedent of the cerebellum and that the cerebellum arose through a change in the genetic-developmental program, amounting to a duplication of existing structure. Such duplication to form adjacent structures can be considered a special case of syngeny. On this view, the cerebellum is an evolutionary innovation in gnathostomes that is literally superimposed on pre-existing underlying brain structures and pathways. From this perspective, the cerebellum can be considered an example of ‘subsumption architecture’, a term that describes the addition of modules that add computational power while maintaining existing fundamental functionality. This addition is reflected in the finding that in elasmobranchs with relatively large brains, the size of the telencephalon and cerebellum enlarge disproportionately, while those parts of the brain that contain more direct sensory and motor connections do not. Added ‘computational’ power in the chondrichthyan brain and the comparative function and evolution of the cerebellum and cerebellum-like structures across the cartilaginous fishes supports the idea of the cerebellum as an example of subsumption architecture.

of the world after each molt. That is, ommatidia viewing the most anterior region of the animal's visual space now sample a more lateral region of visual space. As a consequence, the retinotopic map in the brain must undergo comparable rearrangements to accommodate inputs from new ommatidia sampling visual space in front of the animal. The retinotopic map has been determined for adult animals at the first two synaptic layers in the brain (6), but that of the juvenile remains to be studied. The retinotopic map must be plastic to accommodate the changing retinal mosaic as the eye grows. Supported by grants from the National Science Foundation, National Eye Institute, and the National Institutes of Mental Health. C. McGuiness and S. Meadors received REU Fellowships from the National Science Foundation. We thank the f the world after each molt. That is, ommatidia viewing the most terior egion f the animal's visual space now sample a more ateral region f visual space. As a consequence, the retinotopic ap in the brain must undergo comparable rear ng ments to ccommodate inputs from new ommatidia sampling visual space front of the animal. The retinotopic map has been determined for dult animals at the first two synaptic layers n the b ain (6), but at of the juvenil remains to be studied. The retinotopic map ust be plastic o accommodate the changing retinal mosaic as the Monomoy National Wildlife Refuge, Morris Island, Chatham, Massachusetts.

Very little is known about the brain organization of the suction filter feeder, Rhincodon typus, and how it compares to other orectolobiforms in light of its specialization as a plankton-feeder. Brain size and overall brain organization was assessed in two specimens of R. typus in relation to both phylogeny and ecology, using magnetic resonance imaging (MRI). In comparison to over 60 other chondrichthyan species, R. typus demonstrated a relatively small brain for its body size (expressed in terms of encephalization quotients and residuals), similar to the lamniforms Carcharodon carcharias, Cetorhinus maximus, and Carcharias taurus. R. typus possessed a relatively small telencephalon with some development of the dorsal pallium, which was suggestive of moderate social behavior, in addition to a relatively large diencephalon and a relatively reduced mesencephalon. The most notable characteristic of the brain of Rhincodon was a large and highly foliated cerebellum, one of the largest cerebellums within the chondrichthyan clade. Early development of the brain was qualitatively assessed using an in situ MRI scan of the brain and chondrocranium of a neonate specimen of R. typus. There was evidence that folding of the cerebellar corpus appeared in early development, although the depth and number of folds might vary ontogenetically in this species. Hierarchical cluster analysis and multidimensional scaling ordinations showed evidence of convergent evolution with the basking shark, Cetorhinus maximus, another large-bodied filter feeding elasmobranch, supporting the claim that organization of the brain is more similar in species with analogous but independently evolved lifestyles than those that share taxonomic classification.