Enhanced visual fields in hammerhead sharks.

Several factors that influence the evolution of the unusual head morphology of hammerhead sharks (family Sphyrnidae) are proposed but few are empirically tested. In this study we tested the 'enhanced binocular field' hypothesis (that proposes enhanced frontal binocularity) by comparison of the visual fields of three hammerhead species: the bonnethead shark, Sphyrna tiburo, the scalloped hammerhead shark, Sphyrna lewini, and the winghead shark, Eusphyra blochii, with that of two carcharhinid species: the lemon shark, Negaprion brevirostris, and the blacknose shark, Carcharhinus acronotus. Additionally, eye rotation and head yaw were quantified to determine if species compensate for large blind areas anterior to the head. The winghead shark possessed the largest anterior binocular overlap (48 deg.) and was nearly four times larger than that of the lemon (10 deg.) and blacknose (11 deg.) sharks. The binocular overlap in the scalloped hammerhead sharks (34 deg.) was greater than the bonnethead sharks (13 deg.) and carcharhinid species; however, the bonnethead shark did not differ from the carcharhinids. These results indicate that binocular overlap has increased with lateral head expansion in hammerhead sharks. The hammerhead species did not demonstrate greater eye rotation in the anterior or posterior direction. However, both the scalloped hammerhead and bonnethead sharks exhibited greater head yaw during swimming (16.9 deg. and 15.6 deg., respectively) than the lemon (15.1 deg.) and blacknose (15.0 deg.) sharks, indicating a behavioral compensation for the anterior blind area. This study illustrates the larger binocular overlap in hammerhead species relative to their carcharhinid sister taxa and is consistent with the 'enhanced binocular field' hypothesis.

Arginine vasotocin neuronal phenotypes among congeneric territorial and shoaling reef butterflyfishes: species, sex and reproductive season comparisons.

Arginine vasotocin (AVT) and the homologous arginine vasopressin (AVP) neuropeptides are involved in the control of aggression, spacing behaviour and mating systems in vertebrates, but the function of AVT in the regulation of social behaviour among closely-related fish species needs further clarification. We used immunocytochemical techniques to test whether AVT neurones show species, sex or seasonal differences in two sympatric butterflyfish sister species: the territorial monogamous multiband butterflyfish, Chaetodon multicinctus, and the shoaling polygamous milletseed butterflyfish, Chaetodon miliaris. The territorial species had larger AVT-immunoreactive (-ir) somata within the preoptic area, and higher AVT fibre densities within but not limited to the ventral telencephalon, medial and dorsal nucleus of the dorsal telencephalon, torus semicircularis, and tectum compared to the shoaling nonterritorial species. Furthermore, AVT-ir somata size and number did not differ among sexes or spawning periods in the territorial species, and showed only limited variation within the shoaling species. The distinct difference in AVT neuronal characteristics among species is likely to be independent of body size differences, and the lack of sex and seasonal variability is consistent with their divergent but stable social and mating systems. These phenotypic differences among species may be related to the influence of AVT on social spacing, aggression or monogamy, as reported for other fish, avian and mammalian models. The present study provides the first evidence for variation in vasotocin neural organisation in two congeneric and sympatric fish species with different social systems.

Neural readaptation to Earth's gravity following return from space.

The consequence of exposure to microgravity on the otolith organs was studied by recording the responses of vestibular nerve afferents supplying the utricular otolith organ to inertial accelerations in four toadfish, Opsanus tau, sequentially for 5 days following two National Aeronautics and Space Administration shuttle orbital flights. Within the first day postflight, the magnitude of response to an applied translation was on average three times greater than for controls. The reduced gravitational acceleration in orbit apparently resulted in an upregulation of the sensitivity of utricular afferents. By 30 h postflight, responses were statistically similar to control. The time course of return to normal afferent sensitivity parallels the reported decrease in vestibular disorientation in astronauts following return from space.

Androgen-induced changes in the response dynamics of ampullary electrosensory primary afferent neurons.

Male stingrays use their ampullary electroreceptors to locate mates, but the effect of gonadal androgens on electrosensory encoding during the reproductive season is unknown. We tested the hypothesis that gonadal androgens induce neurophysiological changes in the electrosense of male Atlantic stingrays. During the primary androgen increase in wild males, the electrosensory primary afferent neurons show an increase in discharge regularity, a downshift in best frequency (BF) and bandpass, and a greater sensitivity to low-frequency stimuli from 0.01 to 4 Hz. Experimental implants of dihydrotestosterone in male stingrays induced a similar lowered BF and bandpass and increased average neural sensitivity to low-frequency stimuli (0.5-2 Hz) by a factor of 1.5. Primary afferents from long ampullary canals (>3 cm) were more sensitive and had a lower bandpass and BF than did afferents from short canals (<2 cm). We propose that these androgen-induced changes in the frequency response properties of electrosensory afferents enhance mate detection by male stingrays and may ultimately increase the number of male reproductive encounters with females. Furthermore, differences in primary afferent sensitivity among short and long canals may facilitate detection, orientation, and localization of conspecifics during social interactions.

Annual cycles of steroid hormone production, gonad development, and reproductive behavior in the Atlantic stingray.

The mating season of the Atlantic stingray (Dasyatis sabina), which begins in August and continues through April, is the longest documented for any elasmobranch fish. Despite this protracted mating period, female stingrays ovulate synchronously at the end of the mating season and there is no evidence for sperm storage by females. Thus, the proximate causal factors and ultimate function of this extended preovulatory mating are unknown. Annual cycles of the gonadal steroids testosterone (T), dihydrotestosterone (DHT), 17beta-estradiol (E2), and progesterone (P4) were measured for 26 months in a wild estuarine population of Atlantic stingrays to test for associations with their reproductive biology, gametogenesis, and sexual behavior. Serum androgen levels in males showed four phases within an annual cycle: (1) androgen suppression between reproductive seasons (April-July), (2) primary androgen increase during the onset of spermatocyte development (August-October), (3) androgen decrease following maximum testis growth and spermatocyte development (November-December), and (4) secondary androgen increase during the peak of sperm maturation (January-March). Increases in male E2 and P4 were correlated with spermatocyte/spermatocyst formation, maximum testis weight, and the primary (but not secondary) androgen surge. We propose that the production of male androgens across the full seven-month preovulatory mating period promotes their aggressive reproductive behavior and drives the protracted mating season of this species. In females, serum T and DHT showed relatively brief increases near ovulation, whereas E2 and P4 showed brief increases near both ovulation and parturition. The increase in female androgens near ovulation may increase female aggression when they are impregnable by courting males and enhance their choice of mates. This estuary sample population shows higher absolute steroid levels and distinct differences in temporal cycles compared to another Florida fresh water lake population, but the cause and significance of these differences are unknown. Experiments are needed to confirm that the aggressive and protracted mating behavior is the result of prolonged male androgen production and to determine whether the sustained preovulatory mating serves some function related to female reproduction.

Differential distribution of gonadotropin-releasing hormone-immunoreactive neurons in the stingray brain: functional and evolutionary considerations.

Gonadotropin-releasing hormone (GnRH) is a neuropeptide that occurs in multiple structural forms among vertebrate species. Bony fishes, amphibians, reptiles, birds, and mammals express different forms of GnRH in the forebrain and endocrine regions of the hypothalamus which regulate the release of reproductive gonadotropins from the pituitary. In contrast, previous studies on bony fishes and tetrapods have localized the chicken GnRH-II (cGnRH-II) nucleus in the midbrain tegmentum and, combined with cladistic analyses, indicate that cGnRH-II is the most conserved form throughout vertebrate evolution. However, in elasmobranch fishes, the neuroanatomical distribution of cGnRH-II and dogfish GnRH (dfGnRH) cells and their relative projections in the brain are unknown. We used high-performance liquid chromatography and radioimmunoassay to test for differential distributions of various GnRH forms in tissues from the terminal nerve (TN) ganglia, preoptic area, and midbrain of the Atlantic stingray, Dasyatis sabina. These experiments identified major peaks that coelute with cGnRH-II and dfGnRH, minor peaks that coelute with lamprey GnRH-III (lGnRH-III), and unknown forms. Immunocytochemistry experiments on brain sections show that dfGnRH-immunoreactive (-ir) cell bodies are localized in the TN ganglia, the caudal ventral telencephalon, and the preoptic area. Axons of these cells project to regions of the hypothalamus and pituitary, diencephalic centers of sensory and behavioral integration, and the midbrain. A large, discrete, bilateral column of cGnRH-II-ir neurons in the midbrain tegmentum has sparse axonal projections to the hypothalamus and regions of the pituitary but numerous projections to sensory processing centers in the, midbrain and hindbrain. Immunocytochemical and chromatographic data are consistent with the presence of lGnRH-III and other GnRH forms in the TN that differ from dfGnRH and cGnRH-II. This is the first study that shows differential distribution of cGnRH-II and dfGnRH in the elasmobranch brain and supports the hypothesis of divergent function of GnRH variants related to gonadotropin control and neuromodulation of sensory function.

Response properties and biological function of the skate electrosensory system during ontogeny.

This study examined the response properties of skate electrosensory primary afferent neurons of pre-hatch embryo (8-11 weeks), post-hatch juvenile (1-8 months), and adult (> 2 year) clearnose skates (Raja eglanteria) to determine whether encoding of electrosensory information changes with age, and if the electrosense is adapted to encode natural bioelectric stimuli across life history stages. During ontogeny, electrosensory primary afferents increase resting discharge rate, spike regularity, and sensitivity at best frequency. Best frequency was at 1-2 Hz for embryos, showed an upwards shift to 5 Hz in juveniles, and a downward shift to 2-3 HZ in adults. Encapsulated embryos exhibit ventilatory movements that are interrupted by a "freeze response" when presented with weak uniform fields at 0.5 and 1 Hz. This phasic electric stimulus contains spectral information found in potentials produced by natural fish predators, and therefore indicates that the embryo electrosense can efficiently mediate predator detection and avoidance. In contrast, reproductively active adult clearnose skates discharge their electric organs at rates near the peak frequency sensitivity of the adult electrosensory system, which; facilitates electric communication during social behavior. We suggest that life-history-dependent functions such as these may shape the evolution of the low-frequency response properties for the elasmobranch electrosensory system.

Sensitivity and response dynamics of elasmobranch electrosensory primary afferent neurons to near threshold fields.

Elasmobranch fishes localize weak electric sources at field intensities of < 5 eta V cm-1, but the response dynamics of electrosensory primary afferent neurons to near threshold stimuli in situ are not well characterized. Electrosensory primary afferents in the round stingray, Urolophus halleri, have a relatively high discharge rate, a regular discharge pattern and entrain to 1-Hz sinusoidal peak electric field gradients of < or = 20 eta V cm-1. Peak neural discharge for units increases as a non-linear function of stimulus intensity, and unit sensitivity (gain) decreases as stimulus intensity increases. Average peak rate-intensity encoding is commonly lost when peak spike rate approximately doubles that of resting, and for many units occurs at intensities < 1 microV cm-1. Best neural sensitivity for nearly all units is at 1-2 Hz with a low-frequency slope of 8 dB/decade and a high-frequency slope of -23 dB/decade. The response characteristics of stingray electrosensory primary afferents indicate sensory adaptations for detection of extremely weak phasic fields near 1-2 Hz. We argue that these properties reflect evolutionary adaptations in elasmobranch fishes to enhance detection of prey, communication and social interactions, and possibly electric-mediated geomagnetic orientation.

Feeding mechanism and functional morphology of the jaws of the lemon shark Negaprion brevirostris (Chondrichthyes, Carcharhinidae)

This study tests the hypothesis that preparatory, expansive, compressive and recovery phases of biting behavior known for aquatically feeding anamniotes are conserved among extant elasmobranch fishes. The feeding mechanism of the lemon shark Negaprionbrevirostris is examined by anatomical dissection, electromyography and high-speed video analysis. Three types of feeding events are differentiated during feeding: (1) food ingestion primarily by ram feeding; (2) food manipulation; and (3) hydraulic transport of the food by suction. All feeding events are composed of the expansive, compressive and recovery phases common to aquatically feeding teleost fishes, salamanders and turtles. A preparatory phase is occasionally observed during ingestion bites, and there is no fast opening phase characteristic of some aquatically feeding vertebrates. During the compressive phase, palatoquadrate protrusion accounts for 26% of the gape distance during jaw closure and is concurrent with muscle activity in the dorsal and ventral preorbitalis and the levator palatoquadrati. Hydraulic transport events are shorter in duration than ram ingestion bites. Prey ingestion, manipulation and hydraulic transport events are all found to have a common series of kinematic and motor components. Individual sharks are capable of varying the duration and to a lesser extent the onset of muscle activity and, consequently, can vary their biting behavior. We propose a model for the feeding mechanism in carcharhinid sharks, including upper jaw protrusion. This study represents the first electromyographic and kinematic analysis of the feeding mechanism and behavior of an elasmobranch.

Seasonal dynamics of dental sexual dimorphism in the Atlantic stingray Dasyatis sabina

Cartilaginous fishes continuously replace their teeth throughout their life (polyphyodonty) and often show a sexually dimorphic dentition that was previously thought to be an invariant sex character. Radial vector analysis of tooth shape in the polyphyodontic stingray Dasyatis sabina across a consecutive 24 month period shows a stable molariform morphology for females but a periodic shift in male dentition from a female-like molariform to a recurved cuspidate form during the reproductive season. The grip tenacity of the male dentition is greater for the cuspidate form that occurs during the mating season than for the molariform dentition that occurs during the non-mating season. Dental sexual dimorphism and its sex-dependent temporal plasticity probably evolved via polyphyodontic preadaptation under selective pressures on both sexes for increased feeding efficiency and sexual selection in males to maximize mating success. These phenomena are important considerations for the identification and classification of cartilaginous fishes and possibly other polyphyodontic vertebrates in the fossil record.

Electrosensory optimization to conspecific phasic signals for mating.

Ampullary electroreceptor systems in fishes and aquatic amphibians are known to function in prey localization by the movement of the animal through a weak dc field produced by their prey. The round stingray produces an electric field with a complex geometry that is modulated rhythmically by movements of the spiracles and gill slits during ventilation. This weak stimulus is used in the field by reproductively active male stingrays to locate mates, and also by female rays to locate buried consexuals. Electrosensory primary afferent neurons are most sensitive to stimuli that vary sinusoidally at the same frequency as the natural respiratory movements. The match between primary afferent frequency sensitivity and the ventilatory phasic signals produced by conspecifics indicates that the electrosensory system serves an important biological function in the social behavior of elasmobranchs.

Action of the octavolateralis efferent system upon the lateral line of free-swimming toadfish, Opsanus tau.

The activation and action of the octavolateralis efferent system was studied by chronic recordings of discharge patterns from putative efferent and single primary afferent neurons in alert, free-swimming toadfish. Efferent axons isolated in the anterior lateral line nerve showed phasic discharges following touch stimuli applied to the head or trunk and demonstrated sustained discharges to visual stimuli. Resting discharge patterns of primary afferents were categorized into irregular, burster, regular, and silent classes. Afferent discharges were often modulated by low frequency (less than 1 Hz) water movement around the head generated during respiratory movements. When fish with recording electrodes implanted in the lateral line nerve were visually stimulated, modulated peak discharges and average (DC) firing rates were inhibited in irregular-type units only. Inhibition of irregular-type afferent neurons also followed visual presentation of natural prey and persisted long after prey stimuli were removed from view. The inhibitory action upon lateralis afferents when activated by biologically significant visual stimuli leads to the hypothesis that the octavolateralis efferent system functions in the peripheral processing of information carried by the lateral line in natural settings.

Visually mediated inhibition of lateral line primary afferent activity by the octavolateralis efferent system during predation in the free-swimming toadfish, Opsanus tau.

The activity of single lateral line afferent neurons was chronically recorded in free-swimming toadfish. CNS efferent neurons, known to be inhibitory upon peripheral lateral line mechanoreceptors, were activated by stroboscopic and natural visual stimuli. Discharges from irregular-type afferents caused by water movement relative to lateral line neuromasts decreased following stroboscopic stimulation of unrestrained and behaving fish. Visual presentation of natural prey also decreased mechanically evoked afferent firing rates. We show that visual stimuli can activate the efferent system and function in the peripheral processing of mechanical stimuli to the lateral line in biologically relevant contexts.