1985 AES Annual Meeting Abstracts

AGE AND GROWTH ESTIMATES OF THE TIGER SHARK, GALEOCERDO CUVIERI, AND THE SPINNER SHARK, CARCHARHINUS BREVIPINNA, FROM THE NORTHWESTERN GULF OF MEXICO

Age and growth estimates are presented for the tiger shark, Gaieocerdo cuvieri, and the spinner shark, Carcharhinus brevipinna. Young-of-the-year to large adults were examined for each species. Ages were estimated from rings or bands found in vertebral centra. Ring counts were made from the face of the centra, and compared to counts in rings in longitudinal sections. One summer opaque band and a more translucent winter band are formed each year. Verification and validation of ring periodicity are discussed. For both species, a von Bertalanaffy growth curve fit the observed data. For the tiger shark, a computer generated (Fabens, 1965) curve estimated the growth parameters as L_max=388 cm TL, K=. 1838, to=-I. 13; a Ford/Walford plot gave a more realistic estimate of L_max=478 cm TL. Von Bertalanffy parameters were estimated for the spinner shark using Beverton’s (1954) methods: L_max=230 cm TL, K=0.212, t_o= -1.94. The largest tiger shark examined (340 cm TL) was 8+ yr old, and the largest spinner shark (208 cm TL) was 10+ yr old.

ELASMOBRANCH AGE DETERMINATION AND VERIFICATION TECHNIQUES: APPLICATION TO CALIFORNIA ELASMOBRANCHS

Few studies have verified the temporal periodicity of deposition of the translucent and opaque bands used to estimate ages and generate growth curves for elasmosbranchs. We review the methods used to estimate ages in elasmobranchs, using California elasmosbranchs as examples. We then review and evaluate the approaches used to verify these ages, including size frequency analysis, growth model parameters, centrum edge characteristics, laboratory grow-out studies, field tag recapture results, and tetracycline marking. We also present electron microprobe analyses for calcium and phosphorus across vertebral centra from a tropical and a temperate species of shark, which support the annual periodicity of band formation for these two species. Finally, we present radiometric dating estimates on several elasmobranch species from California which illustrate some of the problems inherent in cartilage growth and calcification processes.

THE VISUAL SYSTEM OF THE SIXGILL SHARK, HEXANCHUS GRISEUS

The sixgill shark, Hexanchus griseus can be found in waters as deep as 1875 meters. Very little is known of its behavior and even less is known of the capabilities of its sensory systems. This study is an investigation of the anatomy and physiology of the retina of this animal. Only rod photoreceptors were seen in the retina of the sixgill shark. The rod outer segment averaged 26.4 um in length. The average total length of the rods was 38.4 um. The ratio of rod to ganglion cell was 24. I. Spectral sensitivity as determined by the electroretinogram revealed a curve with a peak at approximately 460 nm.

Thus, the sixgill shark has an extensively summated retina and very long rod outer segments to give it maximum sensitivity. It is most sensitive to that wavelength of light which predominates in the deep sea. It is therefore very well adapted for life in the deep ocean.

THE TERMINAL NERVE AND REPRODUCTION IN ELASMOBRANCHS

Elasmobranchs have the largest brains among anamniotes, overlapping some birds and mammals in brain-body ratios. They also have complex modes of reproduction which include internal fertilization, prolonged fetal development and elaborate social behaviors. It is likely that the neural and reproductive systems have depended on each other for their advanced development. Important substrates interrelating the two systems include sex-steroid sensitive brain areas and neural systems containing lutenizing-hormone-releasing-hormone (LHRH) -like peptide. One of these, the nervus terminalis, may influence widespread reproductive responses via central release of the peptide. Recent studies have bequn to characterize the anatomy and physiology of this cranial nerve. In rays (Urolophus halleri, Platyrhinoides triseriata) and sharks (Squalus acanthias) it contains cells and fibers with large, dense core grm 0.2 um) which may represent the LHRH-like peptides. Some of these fibers enter perivascular spaces near the nerve and may thus secrete peptides directly into the systemic circulation. Activity in the nerve is usually 3-8 spikes per second, but bursts to 14-18 spikes per second have been recorded.

INTERRELATIONSHIPS OF ORECTOLOBIFORM SHARKS

Based upon skeletal anatomy and external morphology, the Order Orectolobiformes as herein defined consists of eleven genera in five families. These are: 1) Hemiscyllidae withHemiscyllium and Chiloscyllium; 2) Rhincodontidae with Ginglymostoma, Nebrius,Stegostoma, and Rhincodon: 3) Parascyllidae with Parascyllium and Cirrhiscyllium; 4) Brachcaeluridae with Brachaelurus; 5) Orectoldbidae with Orectolobus andCrossorhinus.

Features of their skeletal anatomy including chondrocranium pectoral girdle and fins, pelvic girdle and fins, dorsal, anal, and caudal fins, and gill and hyoid arches, dental make:-up, dermal denticles, and external morphology will be described and discussed. Based upon these characteristics a phylogenetic scheme of interrelationships will be presented for the order.

IS THE COMMON THRESHER SHARK (ALOPIAS VULPINUS) WARM-BODIED? HEMATOLOGICAL AND MORPHOLOGICAL EVIDENCE

The common thresher shark exhibits hemoglobin and hematocrit levels similar to those found in other warm-bodied species of shark. Heart muscularity, shape, and ventricular volumes are also similar to those of warm-bodied species. Weight-specific gill surface area in the common thresher is well in excess of surface areas documented in any ectothermic elasmobranch. These mammalian-level hemoglobin and hematocrit levels, combined with a high-pressure style cardiac pump and large respiratory surface area provide strong indirect evidence of a potentially high metabolic rate in this species.

ORSERVATIONS ON THE BITlNG MECHANICS OF LEMONSHARKS (NEGAPRION BREVIROSTRIS) AND SOME OTHERS

Several species of carcharhinid sharks, Carcharhinus limbatus, Carcharhinus acronotusand (especially) Neqaprion brevirostris were studied by means of high speed underwater cinematoqraphy, analysis of fresh dissectible specimens, and bites recorded in wax forms. The movements of the jaws during the grasp of relatively small prey involves complex movements of the jaws and hyomandibula that can reorient the tooth tips. There is evidence that when a large “prey” is involved, the bite may involve asymmetrical force loadings, and that the incomplete rigidity of the teeth may aid in cutting the food object.

THE BACTERIAL FLORA OF SHARKS

Sharks of the genera Negaprion, Carcharhinus, Rhizoprionodon, Galeocerdo, Squalus, and Ginglymostoma contain a bacterial flora primarily of the genus Vibrio, althoughListonella, Photobacterium, Proteus, Clostridium, Fusobacterium and others have been isolated. Teeth, skin, alimentary canal, liver, spleen, kidney, fetuses and pancreas contain bacteria; blood samples are usually sterile. Potential portals of entry include ectoparasites, gill parasites, mating bite lacerations, and the milieu of sperm and seawater that male sharks introduce into females during copulation. Healthy, free-ranging sharks carry bacteria with little or no detectable consequence. In contrast, compromised sharks rapidly succumb to disease, typically of Vibrio etiology, and die. Most isolates (ca. 70%) have proven to be ureoiytic, suggesting a xlistic relationship with shark hosts. 5s RNA sequencing studies of Vibrio spp. associated with sharks suggest that these bacteria shared a common ancestor in excess of 10⁶ years ago.

ASSESSMENT OF TWO LEMON SHARK, NEGAPRION BREVIROSTRIS, POPULATIONS BY MULTIPLE MARK PROCEDURES

1923 juvenile lemon sharks were tagged and released in the Florida Keys between 1979 and 1984. A further 207 lemon sharks were tagged in Bimini, Bahamas between 1982 and 1984. As of January 1985, 120 were recaptured in the Keys and 52 in Bimini. Time at liberty for the Keys recaptures averaged I98 days and growth averaged 0.227 mm day-l. Time at liberty in Bimini averaged 269 days with growth of 0.226 mm day-l. Estimates of the Bimini population were 490 and 530 with a density of 5 sharks per Km-. Metal dart togs are retained for at least 2 years at a rate of 73%, while other external tags, such as nylon dart tags are retained at a rate of only 17%. Net movement of Bimini recaptures ranged from 0 Km to 6.5 Km, while net movement of Keys recaptures ranged from 0 Km to approximately 100 Km, averaging 8 Km. Monthly catches show that lemon sharks are born from April to July and grow 0.289 mm day-l PCL. Parameters are being estimated by recapture information. Supported by NSF Grant OCE 8309831 to SHG.

VISION IN SHARKS: RETlN0TECTAL MAPPING OF VISUAL FIELDS TO ASSESS PRIMARY VISUAL AXES AND FUNCTIONAL. VISUAL ACUITY

The extraordinary sensory systems of sharks in general are well known, but the proper assessment of their visual capabilities has been hampered by a lack of understanding of the spatial organization of visual information in these animals. For example, measures of visual discriminatory ability and refractive state in sharks have been conducted without knowledge of the primary visual axes in the shark species under study, perhaps resulting in underestimates of their potential acuity. Using electrophysiological and histological procedures, I have mapped the spatial topography of the retina and mesencephalon optic tectum in juvenile lemon sharks. Although this technique of retinotectal mapping has been employed previously in studies on a broad range of vertebrates, no chondrichthyan has been investigated before. By combining the results of these mapping studies with other research on the optics of the shark eye, the key features of spatial visual performance in sharks–visual fields, primary lines of sight, refractive errors, and functional visual acuity–can be properly evaluated.

ANALYTIC lNDlCATlON OF THE IMPRACTICABILITY OF INCAPACITATING AN ATTACKING SHARK BY EXPOSURE TO WATERBORNE DRUGS: A SECOND, CONFIRMING LOOK

Parametric studies of three dimensional diffusion in the ocean make it possible to estimate the release rate that would be required to maintain a desired concentration of a chemical at the outer boundary of a specified volume of water surrounding a point source under steady state conditions. For example, maintenance of a chemical (repellent) concentration of only one gram per cubic meter (i.e., approximately 1 PPM) along the outer boundary of one cubic meter of sea water would require that chemical to be released from an enclosed point source at the rate of about 800 grams per hour. Such calculations will be presented in terms of their clear implications regarding the inherent impracticability of chemical shark repellents when deployed in the “enveloping cloud” mode.

ON THE DIVERSITY OF CARBONIFEROUS CHONDRICHTHYES

Little has been known of the early history of the Chondrichthyes aside from a few poorly preserved sharks and multitudes of isolated ichthyodurulites. Chondrichthyes in the Carboniferous Bear Gulch Limestone fish fauna constitute 54% of the species, but only 20% of the individuals. Feeding and propulsive adaptations are virtually as diverse as in modern teleosts, and a review of adaptive morphology shows that all are feeding, locomotor and/or reproductive specialists. Secondary sexual dimorphism is prevalent through the class. Not all Bear Gulch chondrichthyan groups have been studied phyletically, but two have been examined in detail. The Chimaeriformes are demonstrated to be the sister group of the Cochliodontiformes. The Helodontiformes (Helodus, Psephodus) are the primitive sister group of the Cochliodontiformes. A new order is proposed for the coordinate sister taxon, a group of heterodontous holostylic fish including Janassa,Climaxodus, Tanaodus, and Lisgodus; body forms are as diverse as dentitions in this group. A cladistic scheme for the Chimaeriformes and related forms is presented.

TENNESSEE CLADOSELACHIAN PROVIDES IMPORTANT DATA ON EARLY CHONDRICHTHYAN JAW SUSPENSlON

A well preserved cladoselachian head and trunk region from the Chattanooga Shale of Tennessee is described. Elements of the jaws, hyoid arch and bronchial skeleton are preserved in a three-dimensional articular relationship. Impressions of major head muscles are evident. According to Zangerl and William’s criteria the arrangement would be aphetohyoidean, but the fossil clearly demonstrates closure of the hyoidean gill cleft. There are five bronchial arches. In the hyoid arch there is some evidence of an interhyal. This, plus tile presence of an “intermediate” element in Acanthodes and an additional element in the chimaeroid hyoid arch, has important implications for gnathostomes.

OBSERVATIONS AND TELEMETRlC STUDIES OF FREE-RANGING WHITE SHARKS

Fourteen white sharks (Carcharodon carcharias) were observed in South Australia during January 1985. Instantaneous velocity and visceral temperature of two free-ranging males were telemetrically recorded. Post-prandial stomach temperatures as much as 700 C above ambient seawater were observed. Refractory periods associated with stomach cooling during feeding appear brief enough to allow feeding periodicity studies. Feeding behavior of sharks upon humans was analyzed with a series of dummies. A curious relationship ofCarcharodon to penguins will be put forth.

MORPHOLOGICAL LIMITS AND PHYLOGENETIC INTERRELATlONSHlPS OF THE RAJA SUBGENERA OKAMEJEI ANDRAJA (CHONDRICHTHYES, RAJOIDEI)

Discovery of a new species of skate from the Gulf of California which resembles both Rajasubgenera Okamejei and Raja led to a thorough anatomical study of the morphological distinctions and systematic limits of these taxa. The two subgenera are very similar in neurocranial, hyobranchial, scapulocoracoid and pelvic girdle structure but are distinguished by the anatomy of the clasper. The two subgenera are considered sister groups which form the sister group of Raja (Dipturus). Zoogeographical patterns of all three taxa are discussed.

DISTRIBUTION AND ABUNDANCE OF SHARKS IN THE CHESAPEAKE BIGHT

The seasonal distribution and abundance of sharks between Cape Henlopen, Delaware and Cape Hatteras, North Carolina is described on the basis of long-line collections made between 1973 and 1984. Long-lining was concentrated from May through October when a diverse sub-tropical galeoid shark fauna occupies the region. This entire fauna migrates south of Cape Hatteras in winter and is replaced by the abundant boreal squaloid Squalus acanthias. Carcharhinus plumbeus was the most abundant species during the warmer months when the water temperature > 18- I9OC. Large females entered lower Chesapeake Bay and the lagoons of the Eastern Shore of Virginia to pup in June. Subsequently they migrated offshore to deeper water (20-30 m). Adult males were uncommon and occurred only offshore (> 35 m). The pups remained in their estuarine nurseries till fall. The second most abundant species was C. obscurus. Large females occurred along the coast (c IO m) in June and early July and $pped along the shoals which fringe the Eastern Shore. After pupping these females also migrated offshore to deeper water. Other species which were common included C. altimus, C. limbatus, Galeocerdo cuvieri, Isurus oxyrinchus, Mustelus canis, Neqaprion brevirostris, Odontaspis taurus, and Rhizopriondon terraenovae.

FIELD TESTING OF SURFACTANTS AS SHARK REPELLENTS

Tests were conducted in the ocean off southern California to assess the practicality of using inexpensive surfactant chemicals to repel sharks in certain situations. Thus far, trials have been on blue sharks, Prionace glauca, baited to the boat, and have involved two delivery techniques: (I) squirt application by diver, and (2) direct oral delivery – via a 250 ml rupturable latex packet tied to a bait. The surfactant used was commercial grade sodium lauryl sulfate. Squirt trials used a pump/hose system or an air-powered syringe gun, and consisted of aiming a stream (spreading plume) of solution directly into the shark’s face as it approached or mouthed bait. With decreasing repellent concentration, response latency increased and intensity decreased. For trials at 30-60 cm nozzle-to-shark distance and 250 ml/set flow, a IO% solution caused strong repellency in I set (rapid withdrawal, head shaking, wide mouth gape), at 2% it required about 3 set for a similar response, and at I% it took 5-6 set for a moderate repellency with intermittent gaping and incomplete departure. A concentration of 0.5% appeared near threshold for any obvious repellency in both squirt and packet tests.

MOVEMENTS, DISTRIBUTION, FEEDING, AND GROWTH OF THE PACIFIC ANGEL SHARK, SQUATINA CALIFORNICA, AT CATALINA ISLAND, CALIFORNIA

Daily and seasonal movement patterns, distribution, feeding, growth, and population size were examined for the Pacific angel shark, Squatina californica, at Catalina Island, California. Results of telemetry tracking and conventional tagging indicated the sharks were a single resident population. Movements were nocturnal, but did not occur every night. They were found near the rock-sand interface at the base of rocky reefs during the warmer months of the year and farther out on the sand during the colder months. The sharks fed on fishes when near the reef and on squid when farther away. Growth rates slowed with increasing length and ranged from lricm/yr to Ocm/yr. Of the 402 sharks tagged with conventional tags, 111 (27.6%) were resighted at least once. Population size statistics, based on the tag recapture and reobservation data, estimate a total of 3644 (SE = 285, N=41) angel sharks around Catalina Island.

VERTICAL MOVEMENTS AND TAILBEAT FREQUENCIES OF FREE-SWIMMING BLUE SHARKS

Acoustic telemetry was used to monitor depth and tailbeat frequency from two free-swimming blue sharks in slope waters near Hudson Canyon. Both sharks alternated periods of surface swimming with dives to depths of 100-450 m, the dives occurring at two-hour intervals and lasting about an hour. Mean tailbeat frequencies ranged from 0.2 beats/set during descent to 0.4 set during ascent, and rarely exceeded 0.5/sec. Gliding periods, during which no tailbeats were detected, were recorded 17 times in 36 dives and were associated with the most rapid descent rates. Weihs has shown that a swimming pattern involving passive downward gliding followed by upward swimming would reduce the theoretical energy cost of swimming for negatively buoyant fish. However, based on estimated rates of horizontal movement, the descent angles exhibited by these blue sharks are considerably steeper and ascent angles shallower than those calculated to provide maximum energy savings. This suggests that some consideration other than energy efficiency, such as feeding or temperature regulation, is involved in this swimming behavior.

GASTRIC EVACUATION OF THE LEMON SHARK NEGAPRION BREVIROSTRIS, (POEY) UNDER CONTROLLED CONDITIONS

Gastric evacuation of the juvenile lemon shark, Negaprion brevirostris, a tropical, inshore apex predator was studied in the laboratory under conditions of 25^oC and 32^o/oo salinity. Sharks were starved for 96 h, fed a 2.7% bw meal of fish fillet and gastric evacuation followed by stomach lavage in three hour intervals for 24 h. Results showed that gastric evacuation may be described by the equation Y=Y_oe-bt and is thus similar in kinetics to teleosts. However time to completion (24 h) is significantly longer. Caloric content of recovered food increased up to 12 h as carbohydrate (glycogen) was digested. After 12 h the caloric value fell as proteins were digested. No differences in evacuation rate between males and females were observed. Supported by NSF-OCE 8309831 to SHG.

LIGHT AT THE END OF THE TUNNEL: BIOLUMINESCENCE IN MEGAMOUTH (MEGACHASMA PELAGIOS)

Capture of a second specimen of megamouth shark (Megachasma pelaqios) has allowed a detailed study of the histology and fine structure of the oral tissue. It was speculated that the lining of the roof of the mouth might be bioluminescent, but due to the deteriorated state of tissue from the holotype, the hypothesis that megamouth might be bioluminescent remained untested. A review of bioluminescence in elasmobranchs (selachimorphs) revealed that as many as 27 species of (including Megachasma) may be bioluminescent. Twenty-six belong to. The squaliform Squaloidei (Squalinae and Dalatiinae) and are considered mostly mid-todeep water sharks. Megachasma has recently been assigned to the lamniform Cetorhinidae. Data will be presented that indicate the presence of an oral luminescent system in Megachasma (the first luminescent non-squaloid) that is unique among bioluminescent sharks.

SHARK REPELLENCY STUDIES IN. A LABORATORY SITUATION

Chemical repellency studies, using mostly the commercial surfactant sodium lauryl sulfate, were conducted in a specially designed roundabout tank located off the campus of California State University, Long Beach. Swim-through tests were conduci .zd on the horn shark (Heterodontus francisci) and swell shark (Cephaloscyllium ventriosum). The sharks, while swimming normally around the tank, were directed through test “blocks” of seawater with a known concentration of uniformly dispersed repellent chemical. Any unconditioned responses were noted.

PALEOECOLOGY OF THE MIOCENE SHARKTOOTH HILL BONEBED, SOUTHERN CALIFORNIA

The middle Miocene marine Sharktooth Hill Bonebed (12-15 mya) in the Southern Central Valley of California contains a high concentration of fossil vertebrates. Many marine mammals, a few marine turtles and birds, about 30 species of sharks and rays, and about 25 species of bony fishes have been identifikd. A remarkable, uniformly dense concentration of bones covers at least 30 sq km. and does not have any satisfying analogs on the sea floor of today. The shark and fish remains represent a diverse mixture of larger temperate and tropical species, including the genera Heterodontus, Hexanchus,Galeocerdo, Carcharhrinus, Caranx Semicossyphus, Oplegnathus, Thunnus,Paralichthys, Diodon, Xiphias, and Stereolepis collectlvely these genera reflect a strong temperate and antitropical element (based on the distribution of these taxa today). They also indicate land areas near deep marine waters in an area influenced by both temperate and tropical conditions. A microfauna of fish remains is beginning to be identified.

FRESHWATER ADAPTATION IN ELASMOBRANCHS

Elasmobranchs are predominantly marine animals, but a number of species are known to be adapted in various degrees to life in entirely fresh water. Complete transition from a marine to a freshwater existence requires change in a number of functions, especially in the osmo-regulatory process and reproduction.

Variois stages of the transition in each of these functions will be illustrated by several variously freshwater-adapted species that I have been studying during the past 25 years: (1)Carcharhinus leucas, the bull shark, in the Lake Nicaragua-Rio San Juan system, (2)Pristis perotteti, the large-tooth sawfish, in the same system, (3) Dasyatis guttata, a fully euryhaline stingray of the Caribbean coast of South and Central America, (4) Dasyatis garouaensis, of the Benue and Niger rivers of Nigeria and Cameroon, and (5) several species of freshwater stingrays (family Potamotrygonidae) of South American river systems.

TONIC IMMOBILITY IN JIJVENILE SANDBAR SHARKS,CARCHARHINUS PLUMBEUS (NARDO, 1827) (PISCES, CARCHARHINIDAE)

Tonic immobility was investigated in 22 female and 11 male juvenile sandbar sharks,Carcharhinus plumbeus (Nardo, 1827). Immobility was induced by grasping the sharks by the posterior margin of the first dorsal fin and the caudal peduncle, inverting the animal and holding it towards the bottom of the test tank. After a brief struggle, the body tone of the animal relaxed (the “limp” response) and it was released. This “limp” response was used as the criterion for the occurrence of ionic immobility since motionlessness always followed its occurrence. This relationship was found to be statistically significant (Chi-square=33.0, P> 0.001). The probability of the occurrence of tonic immobility was significantly lower in males than in females (Chi-square = 9.01, P 0.005). The mean number of trials to induce tonic immobility was 2.3. The variances for induction time (in set) were significantly different for males and fermales. Mean induction time for males was 39.3 sec and the mean induction time for females was 38.1 sec. The mean duration for an episode of tonic immobility was 88 sec.

THE U.S. NAVY AND SHARK RESEARCH: AN OVERVIEW

For over a quarter century, the U.S. Navy has supported research on sharks relative to the problems sharks cause. While primary effort has focused on basic research, applied studies have been supported on repellents, deterrents or anti-shark weapons. Support of basic science has included the organization and funding of scientific conferences to review problems of shark-human interactions and to summarize our understanding of sharks. Research on elasmobranch systematics and taxonomy was supported concurrently with efforts to document the shark attack problem in the International Shark File. ONR support of research on the sensory biology, physiology and behavior of sharks has resulted in increased understanding of their sensory capabilities, behavior patterns and distribution. As knowledge of sharks has increased, many of the shark-related problems for the U.S. Navy have been solved or changed. For example, today there is more concern about protection of vulnerable instrumentation since solutions for the protection of humans appear to be adequate. On the other hand, because sharks possess well developed sensory capabilities, basic research projects on elasmobranchs will continue to be considered for support by ONR.