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1.
J Morphol ; 285(1): e21662, 2024 Jan.
Article in English | MEDLINE | ID: mdl-38100743

ABSTRACT

The Australian lungfish, Neoceratodus forsteri (Krefft 1870), is the sole extant member of the Ceratodontidae within the Dipnoi, a small order of sarcopterygian (lobe-finned) fishes, that is thought to be the earliest branching species of extant lungfishes, having changed little over the last 100 million years. To extend studies on anatomical adaptations associated with the fish-tetrapod transition, the ultrastructure of the cornea and iris is investigated using light and electron (transmission and scanning) microscopy to investigate structure-function relationships and compare these to other vertebrate corneas (other fishes and tetrapods). In contrast to previous studies, the cornea is found to have only three main components, comprising an epithelium with its basement membrane, a stroma with a Bowman's layer and an endothelium, and is not split into a dermal (secondary) spectacle and a scleral cornea. The epithelial cells are large, relatively low in density and similar to many species of non-aquatic tetrapods and uniquely possess numerous surface canals that contain and release mucous granules onto the corneal surface to avoid desiccation. A Bowman's layer is present and, in association with extensive branching and anastomosing of the collagen fibrils, may be an adaptation for the inhibition of swelling and/or splitting of the stroma during its amphibious lifestyle. The dorsal region of the stroma possesses aggregations of pigment granules that act as a yellow, short wavelength-absorbing filter during bright light conditions. Desçemet's membrane is absent and replaced by an incomplete basement membrane overlying a monocellular endothelium. The iris is pigmented, well-developed, vascularised and contractile containing reflective crystals anteriorly. Based upon its ultrastructure and functional adaptations, the cornea of N. forsteri is more similar to amphibians than to other bony fishes and is well-adapted for an amphibious lifestyle.


Subject(s)
Biological Evolution , Cornea , Fishes , Iris , Animals , Australia , Cornea/anatomy & histology , Fishes/anatomy & histology , Iris/anatomy & histology
2.
J Morphol ; 284(2): e21552, 2023 02.
Article in English | MEDLINE | ID: mdl-36601696

ABSTRACT

The Shorthead lamprey Mordacia mordax (Mordaciidae, Agnatha) represents one of the earliest stages of vertebrate evolution. This study investigates the ultrastructural anatomy of the cornea, iris and anterior chamber in the eyes of this species in both the downstream and upstream migrant phases of its protracted lifecycle to assess the morphological and quantitative changes associated with growth, corneal function and vision. Using light and both scanning and transmission electron microscopy, the cornea is found to be divided into dermal and scleral components separated by a mucoid layer. A range of distinguishing corneal features are compared in the two adult phases of the lifecycle, including epithelial microprojections, mucus-secreting epithelial cells, the number, thickness, formation and level of branching and anastomosing of collagen lamellae, the type and distribution of vertical sutures, the structure of the mucoid layer and annular ligament and the number and distribution of a large number of basement membranes throughout the cornea. Significant differences are found between the two phases, which are thought to reflect adaptations to the variable environmental conditions encountered throughout this species' lifecycle. The study provides insights into the evolutionary pressures on extant representatives of the earliest stages in the evolution of the vertebrate eye.


Subject(s)
Lampreys , Transients and Migrants , Animals , Humans , Fishes , Cornea , Vertebrates
3.
Elife ; 112022 07 12.
Article in English | MEDLINE | ID: mdl-35818828

ABSTRACT

The lobe-finned fish, lungfish (Dipnoi, Sarcoptergii), have persisted for ~400 million years from the Devonian Period to present day. The evolution of their dermal skull and dentition is relatively well understood, but this is not the case for the central nervous system. While the brain has poor preservation potential and is not currently known in any fossil lungfish, substantial indirect information about it and associated structures (e.g. labyrinths) can be obtained from the cranial endocast. However, before the recent development of X-ray tomography as a palaeontological tool, these endocasts could not be studied non-destructively, and few detailed studies were undertaken. Here, we describe and illustrate the endocasts of six Palaeozoic lungfish from tomographic scans. We combine these with six previously described digital lungfish endocasts (4 fossil and 2 recent taxa) into a 12-taxon dataset for multivariate morphometric analysis using 17 variables. We find that the olfactory region is more highly plastic than the hindbrain, and undergoes significant elongation in several taxa. Further, while the semicircular canals covary as an integrated module, the utriculus and sacculus vary independently of each other. Functional interpretation suggests that olfaction has remained a dominant sense throughout lungfish evolution, and changes in the labyrinth may potentially reflect a change from nektonic to near-shore environmental niches. Phylogenetic implications show that endocranial form fails to support monophyly of the 'chirodipterids'. Those with elongated crania similarly fail to form a distinct clade, suggesting these two paraphyletic groups have converged towards either head elongation or truncation driven by non-phylogenetic constraints.


Subject(s)
Biological Evolution , Fossils , Animals , Brain/diagnostic imaging , Fishes , Paleontology , Skull/anatomy & histology , Skull/diagnostic imaging
4.
J Exp Biol ; 225(11)2022 06 01.
Article in English | MEDLINE | ID: mdl-35582824

ABSTRACT

Despite lizards using a wide range of colour signals, the limited variation in photoreceptor spectral sensitivities across lizards suggests only weak selection for species-specific, spectral tuning of photoreceptors. Some species, however, have enhanced short-wavelength sensitivity, which probably helps with the detection of signals rich in ultraviolet and short wavelengths. In this study, we examined the visual system of Tiliqua rugosa, which has an ultraviolet/blue tongue, to gain insight into this species' visual ecology. We used electroretinograms, opsin sequencing and immunohistochemical labelling to characterize whole-eye spectral sensitivity and the elements that shape it. Our findings reveal that T. rugosa expresses all five opsins typically found in lizards (SWS1, SWS2, RH1, RH2 and LWS) but possesses greatly enhanced short-wavelength sensitivity compared with other diurnal lizards. This enhanced short-wavelength sensitivity is characterized by a broadening of the spectral sensitivity curve of the eye towards shorter wavelengths while the peak sensitivity of the eye at longer wavelengths (560 nm) remains similar to that of other diurnal lizards. While an increased abundance of SWS1 photoreceptors is thought to mediate elevated ultraviolet sensitivity in a couple of other lizard species, SWS1 photoreceptor abundance remains low in this species. Instead, our findings suggest that short-wavelength sensitivity is driven by multiple factors which include a potentially red-shifted SWS1 photoreceptor and the absence of short-wavelength-absorbing oil droplets. Examining the coincidence of enhanced short-wavelength sensitivity with blue tongues among lizards of this genus will provide further insight into the co-evolution of conspecific signals and whole-eye spectral sensitivity.


Subject(s)
Lizards , Animals , Electroretinography , Eye , Opsins/genetics , Phylogeny
5.
Biol Lett ; 18(3): 20210259, 2022 03.
Article in English | MEDLINE | ID: mdl-35259943

ABSTRACT

Sharks represent the earliest group of jawed vertebrates and as such, they may provide original insight for understanding the evolution of sleep in more derived animals. Unfortunately, beyond a single behavioural investigation, very little is known about sleep in these ancient predators. As such, recordings of physiological indicators of sleep in sharks have never been reported. Reduced energy expenditure arising from sustained restfulness and lowered metabolic rate during sleep have given rise to the hypothesis that sleep plays an important role for energy conservation. To determine whether this idea applies also to sharks, we compared metabolic rates of draughtsboard sharks (Cephaloscyllium isabellum) during periods ostensibly thought to be sleep, along with restful and actively swimming sharks across a 24 h period. We also investigated behaviours that often characterize sleep in other animals, including eye closure and postural recumbency, to establish relationships between physiology and behaviour. Overall, lower metabolic rate and a flat body posture reflect sleep in draughtsboard sharks, whereas eye closure is a poorer indication of sleep. Our results support the idea for the conservation of energy as a function of sleep in these basal vertebrates.


Subject(s)
Sharks , Animals , Eye , Sharks/physiology , Sleep/physiology , Swimming
6.
J R Soc Interface ; 18(183): 20210533, 2021 10.
Article in English | MEDLINE | ID: mdl-34699727

ABSTRACT

Shark bites on humans are rare but are sufficiently frequent to generate substantial public concern, which typically leads to measures to reduce their frequency. Unfortunately, we understand little about why sharks bite humans. One theory for bites occurring at the surface, e.g. on surfers, is that of mistaken identity, whereby sharks mistake humans for their typical prey (pinnipeds in the case of white sharks). This study tests the mistaken identity theory by comparing video footage of pinnipeds, humans swimming and humans paddling surfboards, from the perspective of a white shark viewing these objects from below. Videos were processed to reflect how a shark's retina would detect the visual motion and shape cues. Motion cues of humans swimming, humans paddling surfboards and pinnipeds swimming did not differ significantly. The shape of paddled surfboards and human swimmers was also similar to that of pinnipeds with their flippers abducted. The difference in shape between pinnipeds with abducted versus adducted flippers was bigger than between pinnipeds with flippers abducted and surfboards or human swimmers. From the perspective of a white shark, therefore, neither visual motion nor shape cues allow an unequivocal visual distinction between pinnipeds and humans, supporting the mistaken identity theory behind some bites.


Subject(s)
Bites and Stings , Sharks , Animals , Humans , Swimming
7.
J Anat ; 239(3): 732-746, 2021 09.
Article in English | MEDLINE | ID: mdl-33792036

ABSTRACT

The cornea is a specialized component of the vertebrate eye that provides protection, refractive power, transparency for optical imaging and mechanical support. However, the corneas of birds have received little attention with no comprehensive study of their functional morphology. Using light microscopy and both scanning and transmission electron microscopy, the first description of the ultrastructure of all of the main components of the cornea in two different-sized individuals of the Little Penguin Eudyptula minor is presented. Two types of microprojections protrude from the surface of the cornea with a predominance of microridges and microvilli found in central (flattened) and peripheral regions, respectively. Epithelial cell density is higher in peripheral cornea, especially in the larger (older) individual, while there is a reduction of epithelial cell density with age. The cornea comprises a thick epithelium uniquely attached to the basement membrane with numerous incursions rather than anchoring fibres and anchoring plaques as is found in other vertebrate corneas. Posterior to Bowman's layer, the orthogonally-arranged collagen fibril lamellae in the stroma form extensive branches and anastomoses. Desçemet's membrane is well-developed with an anterior or foetal portion with long banding. However, the thickness of Desçemet's membrane is larger in the older individual with the inclusion of an additional irregular pale-staining posterior portion. Polygonal endothelial cells extend across the cornea as a monolayer with often tortuous cell junctions. Endothelial cell density increases towards the periphery, but decreases with age. Primary cilia are observed protruding through the central region of some endothelial cells into the anterior segment but subsurface structures resembling cilia suggest that these features may be more common. The ultrastructure of the corneal components reveals a range of functional adaptations that reflect the amphibious lifestyle of this seabird.


Subject(s)
Cornea/ultrastructure , Spheniscidae/anatomy & histology , Animals , Epithelial Cells/ultrastructure , Microscopy, Electron, Transmission
8.
Science ; 371(6529)2021 02 05.
Article in English | MEDLINE | ID: mdl-33542110

ABSTRACT

Oceans have become substantially noisier since the Industrial Revolution. Shipping, resource exploration, and infrastructure development have increased the anthrophony (sounds generated by human activities), whereas the biophony (sounds of biological origin) has been reduced by hunting, fishing, and habitat degradation. Climate change is affecting geophony (abiotic, natural sounds). Existing evidence shows that anthrophony affects marine animals at multiple levels, including their behavior, physiology, and, in extreme cases, survival. This should prompt management actions to deploy existing solutions to reduce noise levels in the ocean, thereby allowing marine animals to reestablish their use of ocean sound as a central ecological trait in a healthy ocean.


Subject(s)
Aquatic Organisms/physiology , Hearing , Noise , Animals , Oceans and Seas
9.
Front Neuroanat ; 15: 786729, 2021.
Article in English | MEDLINE | ID: mdl-35002638

ABSTRACT

Extant lampreys (Petromyzontiformes) are one of two lineages of surviving jawless fishes or agnathans, and are therefore of critical importance to our understanding of vertebrate evolution. Anadromous lampreys undergo a protracted lifecycle, which includes metamorphosis from a larval ammocoete stage to an adult that moves between freshwater and saltwater with exposure to a range of lighting conditions. Previous studies have revealed that photoreception differs radically across the three extant families with the Pouched lamprey Geotria australis possessing a complex retina with the potential for pentachromacy. This study investigates the functional morphology of the cornea and anterior chamber of G. australis, which is specialised compared to its northern hemisphere counterparts. Using light microscopy, scanning and transmission electron microscopy and microcomputed tomography, the cornea is found to be split into a primary spectacle (dermal cornea) and a scleral cornea (continuous with the scleral eyecup), separated by a mucoid layer bounded on each side by a basement membrane. A number of other specialisations are described including mucin-secreting epithelial cells and microholes, four types of stromal sutures for the inhibition of stromal swelling, abundant anastomosing and branching of collagen lamellae, and a scleral endothelium bounded by basement membranes. The structure and function of the cornea including an annular and possibly a pectinate ligament and iris are discussed in the context of the evolution of the eye in vertebrates.

10.
J Sleep Res ; 30(3): e13139, 2021 06.
Article in English | MEDLINE | ID: mdl-32672393

ABSTRACT

Sleep is known to occur in most, if not all, animals studied thus far. Recent studies demonstrate the presence of sleep in flatworms and jellyfish, suggesting that this behaviour evolved early in the evolution of animals. Sharks are the earliest known extant, jawed vertebrates and may play an important role in understanding the evolutionary history of sleep in vertebrates, and yet, it is unknown whether they sleep. The Port Jackson (Heterodontus portusjacksoni) and draughtsboard (Cephaloscyllium isabellum) sharks are both benthic, buccal pumping species and remain motionless for extended periods of time. Whether these periods of prolonged inactivity represent sleep or quiet wakefulness is unknown. A key criterion for separating sleep from other quiescent states is an increased arousal threshold. We show here that inactive sharks of both species require significantly higher levels of electric stimulation before they show a visible response. Sharks deprived of rest, however, show no significant compensatory increase in restfulness during their normal active period following enforced swimming. Nonetheless, increased arousal thresholds in inactive animals suggest that these two species of shark sleep - the first such demonstration for members of this group of vertebrates. Further research, including electrophysiological studies, on these and other sharks, is required for a comprehensive understanding of sleep in cartilaginous fishes.


Subject(s)
Sleep/physiology , Animals , Sharks
11.
J Comp Neurol ; 529(9): 2265-2282, 2021 06.
Article in English | MEDLINE | ID: mdl-33336375

ABSTRACT

Lampreys are extant members of the agnathan (jawless) vertebrates that diverged ~500 million years ago, during a critical stage of vertebrate evolution when image-forming eyes first emerged. Among lamprey species assessed thus far, the retina of the southern hemisphere pouched lamprey, Geotria australis, is unique, in that it possesses morphologically distinct photoreceptors and expresses five visual photopigments. This study focused on determining the number of different photoreceptors present in the retina of G. australis and whether each cell type expresses a single opsin class. Five photoreceptor subtypes were identified based on ultrastructure and differential expression of one of each of the five different visual opsin classes (lws, sws1, sws2, rh1, and rh2) known to be expressed in the retina. This suggests, therefore, that the retina of G. australis possesses five spectrally and morphologically distinct photoreceptors, with the potential for complex color vision. Each photoreceptor subtype was shown to have a specific spatial distribution in the retina, which is potentially associated with changes in spectral radiance across different lines of sight. These results suggest that there have been strong selection pressures for G. australis to maintain broad spectral sensitivity for the brightly lit surface waters that this species inhabits during its marine phase. These findings provide important insights into the functional anatomy of the early vertebrate retina and the selection pressures that may have led to the evolution of complex color vision.


Subject(s)
Cone Opsins/biosynthesis , Cone Opsins/ultrastructure , Photoreceptor Cells, Vertebrate/metabolism , Photoreceptor Cells, Vertebrate/ultrastructure , Rod Opsins/biosynthesis , Rod Opsins/ultrastructure , Animals , Cone Opsins/analysis , Fluorescent Dyes/analysis , Lampreys , Photoreceptor Cells, Vertebrate/chemistry , Rod Opsins/analysis
12.
Exp Eye Res ; 202: 108396, 2021 01.
Article in English | MEDLINE | ID: mdl-33310055

ABSTRACT

The corneal ultrastructure of the pre- and post-metamorphic stages of the neotenic axolotl Ambystoma mexicanum is examined using light microscopy and both scanning and transmission electron microscopy to reveal whether there are any morphological changes associated with a switch in lifestyle. Although the complement of corneal layers remains the same, there are significant quantitative changes in corneal, epithelial and stromal thickness, epithelial and endothelial cell size and density, and the thickness of Bowman's layer and Desçemet's membrane. Microholes in the epithelium and vertical sutures within the stroma are predominant features in the pre-metamorphic stage but are rarely seen in the post-metamorphic stage. There are also significant quantitative centro-peripheral differences in the thickness of the whole cornea, primarily due to differences in the thickness of the stroma in both metamorphic stages. These changes may reflect the physiological demands on the cornea as it switches from a purely aquatic to an amphibious lifestyle, which includes venturing onto land.


Subject(s)
Cornea/ultrastructure , Metamorphosis, Biological/physiology , Ambystoma mexicanum , Animals , Cornea/growth & development , Corneal Stroma/ultrastructure , Endothelium, Corneal/ultrastructure , Microscopy, Electron, Transmission , Models, Animal
13.
Front Neuroanat ; 14: 560534, 2020.
Article in English | MEDLINE | ID: mdl-33324175

ABSTRACT

There is currently a limited understanding of the morphological and functional organization of the olfactory system in cartilaginous fishes, particularly when compared to bony fishes and terrestrial vertebrates. In this fish group, there is a clear paucity of information on the characterization, density, and distribution of olfactory receptor neurons (ORNs) within the sensory olfactory epithelium lining the paired olfactory rosettes, and their functional implications with respect to the hydrodynamics of incurrent water flow into the nares. This imaging study examines the brownbanded bamboo shark Chiloscyllium punctatum (Elasmobranchii) and combines immunohistochemical labeling using antisera raised against five G-protein α-subunits (Gαs/olf, Gαq/ 11 / 14, Gαi- 1 / 2 / 3, Gαi- 3, Gα o ) with light and electron microscopy, to characterize the morphological ORN types present. Three main ORNs ("long", "microvillous" and "crypt-like") are confirmed and up to three additional microvilli-bearing types are also described; "Kappe-like" (potential or homologous "Kappe" as in teleosts), "pear-shaped" and "teardrop-shaped" cells. These morphotypes will need to be confirmed molecularly in the future. Using X-ray diffusible iodine-based contrast-enhanced computed tomography (diceCT), high-resolution scans of the olfactory rosettes, olfactory bulbs (OBs), peduncles, and telencephalon reveal a lateral segregation of primary olfactory inputs within the OBs, with distinct medial and lateral clusters of glomeruli, suggesting a potential somatotopic organization. However, most ORN morphotypes are found to be ubiquitously distributed within the medial and lateral regions of the olfactory rosette, with at least three microvilli-bearing ORNs labeled with anti-Gα o found in significantly higher densities in lateral lamellae [in lateral lamellae] and on the anterior portion of lamellae (facing the olfactory cavity). These microvilli-bearing ORN morphotypes (microvillous, "Kappe-like," "pear-shaped," and "teardrop-shaped") are the most abundant across the olfactory rosette of this species, while ciliated ORNs are less common and crypt cells are rare. Spatial simulations of the fluid dynamics of the incurrent water flow into the nares and within the olfactory cavities indicate that the high densities of microvilli-bearing ORNs located within the lateral region of the rosette are important for sampling incoming odorants during swimming and may determine subsequent tracking behavior.

14.
Brain Behav Evol ; 95(3-4): 139-161, 2020.
Article in English | MEDLINE | ID: mdl-33171468

ABSTRACT

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.


Subject(s)
Axons/ultrastructure , Goldfish/anatomy & histology , Olfactory Bulb/cytology , Olfactory Nerve/cytology , Olfactory Pathways/cytology , Sharks/anatomy & histology , Animals , Microscopy, Electron, Transmission , Olfactory Bulb/ultrastructure , Olfactory Cortex/cytology , Olfactory Nerve/ultrastructure , Olfactory Pathways/ultrastructure
15.
Brain Struct Funct ; 225(8): 2347-2375, 2020 Nov.
Article in English | MEDLINE | ID: mdl-32870419

ABSTRACT

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.


Subject(s)
Olfactory Bulb/diagnostic imaging , Olfactory Pathways/diagnostic imaging , Smell/physiology , Telencephalon/diagnostic imaging , Animals , Goldfish , Organ Size , Sharks , Species Specificity , Tomography, X-Ray Computed/methods
16.
J Biol Rhythms ; 35(5): 476-488, 2020 10.
Article in English | MEDLINE | ID: mdl-32525441

ABSTRACT

Sharks are an interesting group of vertebrates, as many species swim continuously to "ram" oxygen-rich seawater over their gills (ram ventilators), whereas other species "pump" seawater over their gills by manipulating buccal cavity volume while remaining motionless (buccal pumpers). This difference in respiratory physiology raises the question: What are the implications of these differences in lifestyle for circadian rhythms? We investigated the diel activity patterns of 5 species of sharks, including 3 ram ventilating species: the school shark (Galeorhinus galeus), the spotted estuary smooth-hound (Mustelus lenticulatus), and the spiny dogfish (Squalus acanthias); and 2 buccal pumping species: the Port Jackson (Heterodontus portusjacksoni) and draughtsboard (Cephaloscyllium isabellum) sharks. We measured the amount, duration, and distance traveled while swimming over multiple days under a 12:12 light:dark light regime for all species and used modified light regimes for species with a clear diel rhythm in activity. We identified a surprising diversity of activity rhythms. The school shark and smooth-hound swam continuously; however, whereas the school shark swam at the same speed and covered the same distance during the day and night, the smooth-hound swam slower at night and traversed a shorter distance. A similar pattern was observed in the spiny dogfish, although this shark swam less overall. Both the Port Jackson and draughtsboard sharks showed a marked nocturnal preference for swimming. This pattern was muted and disrupted during constant light and constant dark regimes, although circadian organization of this pattern was maintained under certain conditions. The consequences of these patterns for other biological processes, such as sleep, remain unclear. Nonetheless, these 5 species demonstrate remarkable diversity within the activity rhythms of sharks.


Subject(s)
Circadian Rhythm , Sharks/physiology , Animals , Darkness , Female , Gills/metabolism , Male , Sleep , Sunlight , Swimming
17.
eNeuro ; 7(4)2020.
Article in English | MEDLINE | ID: mdl-32471849

ABSTRACT

Contrast-enhanced X-ray imaging provides a non-destructive and flexible approach to optimizing contrast in soft tissues, especially when incorporated with Lugol's solution (aqueous I2KI), a technique currently referred to as diffusible iodine-based 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 optimizing 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 optimization 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 before staining and were rescanned at time (T) intervals, either every 48 h (C. punctatum) or every 24 h (C. auratus), to assess stain penetration and contrast enhancement. To compare stain intensities, raw X-ray 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 = 240 h for C. punctatum and T = 96 h for C. auratus Higher resolution scans of the whole brain were obtained at the two optimized staining times for all the corresponding specimens. The use of diceCT provides a new and valuable tool for visualizing differences in the anatomic organization of both the central and peripheral nervous systems of fish.


Subject(s)
Iodine , Animals , Brain/diagnostic imaging , Contrast Media , Head , Tomography, X-Ray Computed
18.
J Comp Neurol ; 528(17): 3123-3133, 2020 12 01.
Article in English | MEDLINE | ID: mdl-32361986

ABSTRACT

This review in memoriam of Jack Pettigrew provides an overview of past and current research into the phenomenon of multistable perception across multiple animal species. Multistable perception is characterized by two or more perceptual interpretations spontaneously alternating, or rivaling, when animals are exposed to stimuli with inherent sensory ambiguity. There is a wide array of ambiguous stimuli across sensory modalities, ranging from the configural changes observed in simple line drawings, such as the famous Necker cube, to the alternating perception of entire visual scenes that can be instigated by interocular conflict. The latter phenomenon, called binocular rivalry, in particular caught the attention of the late Jack Pettigrew, who combined his interest in the neuronal basis of perception with a unique comparative biological approach that considered ambiguous sensation as a fundamental problem of sensory systems that has shaped the brain throughout evolution. Here, we examine the research findings on visual perceptual alternation and suppression in a wide variety of species including insects, fish, reptiles, and primates. We highlight several interesting commonalities across species and behavioral indicators of perceptual alternation. In addition, we show how the comparative approach provides new avenues for understanding how the brain suppresses opposing sensory signals and generates alternations in perceptual dominance.


Subject(s)
Optical Illusions/physiology , Photic Stimulation/methods , Psychomotor Performance/physiology , Visual Perception/physiology , Animals , Attention/physiology , Humans , Species Specificity
19.
J Exp Biol ; 223(Pt 10)2020 05 26.
Article in English | MEDLINE | ID: mdl-32321751

ABSTRACT

Ecological factors such as spatial habitat complexity and diet can explain variation in visual morphology, but few studies have sought to determine whether visual specialisation can occur among populations of the same species. We used a small Australian freshwater fish (the western rainbowfish, Melanotaenia australis) to determine whether populations showed variation in eye size and eye position, and whether this variation could be explained by environmental (light availability, turbidity) and ecological (predation risk, habitat complexity, invertebrate abundance) variables. We investigated three aspects of eye morphology - (1) eye size relative to body size, (2) pupil size relative to eye size and (3) eye position in the head - for fish collected from 14 sites in a major river catchment in northwest Western Australia. We found significant variation among populations in all three measures of eye morphology, but no effect of sex on eye size or eye position. Variation in eye diameter and eye position was best explained by the level of habitat complexity. Specifically, fish occurring in habitats with low complexity (i.e. open water) tended to have smaller, more dorsally located eyes than those occurring in more complex habitats (i.e. vegetation present). The size of the pupil relative to the size of the eye was most influenced by the presence of surrounding rock formations; fish living in gorge habitats had significantly smaller pupils (relative to eye size) than those occupying semi-gorge sites or open habitats. Our findings reveal that different ecological and environmental factors contribute to habitat-specific visual specialisations within a species.


Subject(s)
Poecilia , Animals , Australia , Ecosystem , Predatory Behavior , Western Australia
20.
J Comp Neurol ; 528(17): 2831-2847, 2020 12 01.
Article in English | MEDLINE | ID: mdl-32227480

ABSTRACT

In this study, we investigated the visual system of the Port Jackson shark Heterodontus portusjacksoni, a shallow-dwelling benthic species and generalist predator endemic to the temperate coastal waters around southern Australia. Measurements of retinal spectral sensitivity in juvenile sharks, made using single flash and heterochromatic flicker photometry under conditions of dark- or light-adaptation, indicated a peak sensitivity at around 500 nm, with no evidence of a spectral shift with increasing levels of light adaptation. Histological sections of the retina revealed a heavily rod dominated retina containing only a few small cell profiles in the photoreceptor layer that might represent a sparse cone population or may be immature rods. Assessment of retinal topography in juvenile sharks indicated the presence of a distinct specialisation for increased visual spatial acuity in the form of a horizontal streak of higher rod photoreceptor (~80,000 rods mm-2 ) and ganglion cell (~1,800 cells mm-2 ) densities across the horizontal meridian of the eye. This specialization would be adaptive for panoramic sampling of the part of the visual field corresponding to the substrate-water interface and remove the need for H. portusjacksoni to move its eyes extensively when resting on the sea floor. The estimated upper limit of spatial resolving power in juvenile H. portusjacksoni was 3.14 cycles deg-1 , which is at the lower end of values measured in elasmobranchs. Taken together, these results suggest that the retina of H. portusjacksoni is well adapted for nocturnal vision.


Subject(s)
Adaptation, Ocular/physiology , Dark Adaptation/physiology , Photic Stimulation/methods , Retina/cytology , Retina/physiology , Sharks/physiology , Animals , Female , Male , Photometry/methods , Retina/anatomy & histology , Retinal Cone Photoreceptor Cells/physiology , Retinal Rod Photoreceptor Cells/physiology
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