Timothy C. Tricas

PERIODIC GONADAL ACTIVITY AND PROTRACTED MATING IN ELASMOBRANCH FISHES

Temporal patterns of gonad development are determined by environmental cues that regulate hormonal cycles and ultimately affect a populations mating system. Annual periodicity of gonad histology is essentially unknown for the more than 450 species of batoid elasmobranchs. Temporal periodicity in spermatogenic activity and ova production in the Atlantic stingray (Dasyatis sabina) were examined by histology over a consecutive 20 month period. Gonadosomatic index (GSI) shows three distinct phases associated with structural changes at the cellular level. Testes in the inactive phase occur from March through July, have a low GSI, and are represented only by germinal (SI) and early spermatocyst (SII) stages. The enlargement phase begins in mid-August, followed by rapid testicular growth that peaks in October. Testicular recrudescence is characterized by a decline in the proportion of early stage spermatocysts (SI, II) and a sequential maturation of cells to the spermatocyte (SIII), spermatid (SIV), immature sperm (SV), and mature spermatozoa (SVI) stages. The measure of absolute spermatogenic production (ASP) is maximum from about August through January. The diminution phase is characterized by a decrease in male GSI from October through April associated with a reduced tissue biomass and predominance of early spermatogenic stages. The annual succession of peaks in sperm formation indicates continuous spermatogenesis through the fall-winter and shows that peak sperm production lags maximum GSI by approximately 3–4 months. Further, seminal vesicle diameter peaks in February, which also lags maximum GSI by 4 months. Egg growth in females is a periodic process of 5–6 months duration that involves vitellogenesis of 2–4 oocytes. Maximum ova diameter increases after mid-September, peaks in March (x¯ = 10.62 mm), and covaries with the increase in female GSI. Despite the brief period of ovulation and fertilization in March-April, fresh mating scars and sperm in the lower reproductive tract of females confirm a protracted mating period from October through April-May. Thus, mating begins in the population at least 7 months prior to ovulation and fertilization. Current evidence indicates this protracted mating period is not explained by female sperm storage or arrested embryonic development. We suggest the protracted mating period serves some currently undetermined function such as induction of steroidogenesis, oocyte growth, or ovulation in females.

Determinants of feeding territory size in the corallivorous butterflyfish, Chaetodon multicinctus

Abstract Both sexes of the monogamous coral-feeding butterflyfish, Chaetodon multicinctus , forage as energy maximizers, are constrained by the time available for feeding, and vigorously defend their feeding territories from intrusions by conspecific competitors. Territory area was positively correlated with coral abundance when data were pooled from coral-poor and coral-rich habitats. In contrast, male lenght and total food were correlated with territory area within the coral-rich habitat. When food supply was increased, fish attempted to defend all food within original borders but were limited by aggressive interactions with conspecifics attracted to supplemental food. When coral abundance was reduced, residents expanded their territories. In comparison, territories were adjusted as an inverse function of competitor abundance and related costs of defence. Although these experiments support competitor-mediated models of territory size, food resources are also important in that they set a lower limit for minimum territory area and, when possible, are defended in surplus by this species.

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

Abstract 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 electro-sense 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.

Kinematic analysis of suction feeding in the nurse shark, Ginglymostoma cirratum (Orectolobiformes, Ginglymostomatidae)

Abstract Inertial suction feeding is known to occur in some sharks, but the sequence and temporal kinematics of head and jaw movements have not been defined. We investigated the feeding kinematics of a suction feeding shark, the nurse shark Ginglymostoma cirratum, to test for differences in the timing and magnitude of feeding components with other shark taxa when sharks were fed pieces of bony fish. Thirteen kinematic variables were measured from high-speed video recordings. Food capture in this species consists of expansive, compressive, and recovery phases, as in most other sharks, but there is little or no cranial elevation. Mean time to maximum gape (32 msec) is the fastest recorded for an elasmobranch fish. Other relatively rapid events include mandibular depression (26 msec), elevation (66 msec), and total bite time (100 msec). Buccal valves assist the unidirectional flow of water into the mouth and out of the gill chambers. Food capture under these experimental conditions appears to be a stereotyped modal action pattern but with significant interindividual variability in timing of kinematic events. Ginglymostoma cirratum exhibits a suite of specializations for inertial suction feeding that include (1) the formation of a small, anteriorly directed mouth that is approximately round and laterally enclosed by modified labial cartilages; (2) small teeth; (3) buccal valves to prevent the backflow of water; and (4) extremely rapid buccal expansion. Sharks that capture food by inertial suction have faster and more stereotyped capture behavior than sharks that primarily ram feed. Inertial suction feeding, which has evolved multiple times in sharks, represents an example of functional convergence with inertial suction feeding bony fishes.

Dermal bite wounds as indicators of reproductive seasonality and behaviour in the Atlantic stingray, Dasyatis sabina

Elasmobranch fishes exhibit a series of complex courtship and mating behaviours in which males inflict significant bite wounds to the body of female mates. However, the variety and frequency of mating wounds are not known across a full reproductive season for any species. We examined the distribution and abundance of dermal wounds in adult Atlantic stingrays, Dasyatis sabina, which have a protracted and defined mating season to determine (1) if dermal wounds can be used as indicators of mating activity, (2) whether different categories of bite wounds can be associated with specific mating behaviours, and (3) whether the skin thickness in females is sexually dimorphic. Adults of both sexes showed fresh wounds during the full duration of the mating season (October–June) and there was no relationship between ray size and wound density. Females had more total wounds than males in every month with a maximum average of 20.2 wounds per female in April. Mating wounds were categorized into five distinct forms: single track, double track, bite, margin abrasion and excision. Wounds were randomly distributed over the body of males but concentrated on the posterior half of the disc in females. Each wound type occurred in approximately equal proportions among sexes with the exception of the precopulatory and copulatory-induced margin abrasions which accounted for 13.7% of the total wounds in females but only 3.1% in males. We suggest that the pronounced and concurrent appearance of single track, double track and bite wounds among males results from random premating courtship attacks by males because females cannot be visually discriminated. However, the concentration of wounds on the posterior disc of females is consistent with the possible presence of olfactory cues (e.g. pheromones) that are released at the cloaca. The pectoral fin dermis of females was 50% thicker than that of males, which eliminated the excision of margins during male grasping and functions to reduce female injury. The temporal occurrence of wounds from October through June and peak in April is consistent with previous reproductive studies that show fresh sperm in the reproductive tract of females over the protracted mating period and also ovulation in late March or early April. The importance of social reproductive biting is discussed in relation to the reproductive induction hypothesis proposed to possibly explain the protracted mating of this species. Monitoring of dermal wounds provides a useful non-invasive technique to determine reproductive activity and a means for inference of social relationships in elasmobranch populations.

The neuroecology of the elasmobranch electrosensory world: why peripheral morphology shapes behavior

The adaptations of elasmobranch sensory systems can be studied by linking the morphological structure with the natural behavior and ecology of the organism. This paper presents the first step in a ‘neuroecological’ approach to interpret the spatial arrangement of the electrosensory ampullary organs in elasmobranch fishes. A brief review of the structure and function of the ampullae of Lorenzini is provided for interpretation of the organ system morphology in relation to the detection of dipole and uniform electric fields. The spatial projections of canals from discrete ampullary clusters were determined for the barndoor skate, Raja laevis, based upon a published figure in Raschi (1986), and measured directly from the head of the white shark, Carcharodon carcharias. The dorsoventrally flattened body of the skate restricts the projections of long canals to the horizontal plane. There is a distinct difference between dorsal and ventral projection patterns in all groups. Notable within-cluster features include a relatively long canal subgroup in the dorsal superficial ophthalmic (SOd) and dorsal hyoid (HYOd) clusters that are oriented parallel (bidirectionally) to the longitudinal axis of the body. It is postulated that this subgroup of canals may be important for detection and orientation to weak uniform fields. Ventral canal projections in the skate are primarily lateral, with the exception of the hyoid (HYOv) that also projects medially. This wide dispersion may function for the detection of prey located below the body and pectoral fins of the skate, and may also be used for orientation behavior. The mandibular canals located near the margin of the lower jaw (of both study species) are ideally positioned for use during prey manipulation or capture, and possibly for interspecific courtship or biting. The head of the white shark, which lacks the hyoid clusters, is ovoid in cross section and thus ampullary canals can project into three-dimensional space. The SOd and superficial ophthalmic ventral (SOv) clusters show strong rostral, dorsal and lateral projection components, whereas the SOv also detects rostral fields under the snout. In the sagittal plane, the SOv and SOd have robust dorsal projections as well as ventral in the SOv. Most notable are canal projections in the white shark buccal (BUC) ampullary cluster, which has a radial turnstile configuration on the ventrolateral side of the snout. The turnstile design and tilt between orthogonal planes indicates the white shark BUC may function in detection of uniform fields, including magnetically induced electric fields that may be used in orientation behaviors. These data can be used in future neuroecology behavioral performance experiments to (1) test for possible specializations of cluster groups to different natural electric stimuli, (2) the possibility of specialized canal subgroups within a cluster, and (3) test several models of navigation that argue for the use of geomagnetically induced electric cues.

Morphology of the mechanosensory lateral line system in the Atlantic Stingray, Dasyatissabina: The mechanotactile hypothesis

The biological function of anatomical specializations in the mechanosensory lateral line of elasmobranch fishes is essentially unknown. The gross and histological features of the lateral line in the Atlantic stingray, Dasyatis sabina, were examined with special reference to its role in the localization and capture of natural invertebrate prey. Superficial neuromasts are arranged in bilateral rows near the dorsal midline from the spiracle to the posterior body disk and in a lateral position along the entire length of the tail. All dorsal lateral line canals are pored, contain sensory neuromasts, and have accessory lateral tubules that most likely function to increase their receptive field. The pored ventral canal system consists of the lateral hyomandibular canal along the disk margin and the short, separate mandibular canal on the lower jaw. The extensive nonpored and relatively compliant ventral infraorbital, supraorbital, and medial hyomandibular canals form a continuous complex on the snout, around the mouth, and along the abdomen. Vesicles of Savi are small mechanosensory subdermal pouches that occur in bilateral rows only along the ventral midline of the rostrum. Superficial neuromasts are best positioned to detect water movements along the transverse body axis such as those produced by tidal currents, conspecifics, or predators. The pored dorsal canal system is positioned to detect water movements created by conspecifics, predators, or possibly distortions in the flow field during swimming. Based upon the stingray lateral line morphology and feeding behavior, we propose the Mechanotactile Hypothesis, which states that the ventral nonpored canals and vesicles of Savi function as specialized tactile mechanoreceptors that facilitate the detection and capture of small benthic invertebrate prey. J. Morphol. 238:1–22, 1998.

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.

Sound production and spectral hearing sensitivity in the Hawaiian sergeant damselfish, Abudefduf abdominalis.

SUMMARY Sounds provide important signals for inter- and intraspecific communication in fishes, but few studies examine fish acoustic behavior in the context of coevolution of sound production and hearing ability within a species. This study characterizes the acoustic behavior in a reproductive population of the Hawaiian sergeant fish, Abudefduf abdominalis, and compares acoustic features to hearing ability, measured by the auditory evoked potential (AEP) technique. Sergeant fish produce sounds at close distances to the intended receiver (⩽1–2 body lengths), with different pulse characteristics that are associated primarily with aggression, nest preparation and courtship–female-visit behaviors. Energy peaks of all sounds were between 90 and 380 Hz, whereas courtship–visit sounds had a pulse repetition rate of 125 Hz with harmonic intervals up to 1 kHz. AEP threshold, which is probably higher than the behavioral threshold, indicates best sensitivity at low frequencies (95–240 Hz), with the lowest threshold at 125 Hz (123–127 dBrms re: 1 μPa). Thus, sound production and hearing in A. abdominalis are closely matched in the frequency domain and are useful for courtship and mating at close distances. Measured hearing thresholds did not differ among males and females during spawning or non-spawning periods, which indicates a lack of sex differences and seasonal variation in hearing capabilities. These data provide the first evidence that Abudefduf uses true acoustic communication on a level similar to that of both more derived (e.g. Dascyllus, Chromis) and more basal (e.g. Stegastes) soniferous pomacentrids. This correlation between sound production and hearing ability is consistent with the sensory drive model of signal evolution in which the sender and receiver systems coevolve within the constraints of the environment to maximize information transfer of acoustic signals.

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

Abstract Elasmobranch fishes localize weak electric sources at field intensities of <5 ηV 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 ≤20 ηV 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 μV 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.