Alan Henningsen

National Aquarium | NATIONALAQUARIUM · Biological Programs

Southern stingrays (Hypanus americanus) represent a multimillion dollar ecotourism operation in Grand Cayman, interacting with over a million visitors annually. Over 30 years of stingray provisioning by tour operators has provided a predictable aggregation at the Stingray City Sandbar (SCS). Despite potentially negative effects of provisioning and concerns about declining stingray numbers at SCS, there has never been a formal assessment of the aggregation. In the present study we analysed tagging data from 2002 to 2015 and established structured censuses monitoring the aggregation. The consistently female-dominated aggregation declined between 2008 and 2012, from >100 to <60 stingrays, but has increased since 2012, stabilising at ~90 stingrays. Female site fidelity was high, with ~20% of females resident for ≥10 years, compared with only 3 years for most males. Stingrays were also found to have growth rates similar to those in captivity. The results of the present study suggest the SCS aggregation is highly dependent on individuals arriving from the island-wide stingray population, susceptible to perturbation, and that successful management of activities at SCS will benefit from regular monitoring of the stingray aggregation. We chronicle the historical status of this well-known and economically valuable marine resource and provide suggestions applicable towards sustainable human–marine wildlife interactions for similar resources.

Using a novel set of 12 microsatellites, a captive, adult female swellshark Cephaloscyllium ventriosum that produced five pups via parthenogenesis is described; naturally occurring parthenogenesis has been observed in every vertebrate class with the exception of mammals. As demonstrated in this study, a captive environment is ideal for long-term monitoring of animals under controlled conditions, and easily allows the detection of particular facets of their biology.

A new marine leech is herein described from specimens infecting the external surfaces, including the mouth and cloaca, of the banded guitarfish, Zapteryx exasperata captured in the Gulf of California and eastern Pacific Ocean off the coast of San Diego, California. The leech is assigned to Austrobdella by possessing continuous contractile coelomic channels that lie outside the somatic musculature along the lateral edges of the urosome (marginal lacunae), clitellar gland cells densely packed in the urosome, 5 pairs of testisacs, and 6-annulate mid-body somites. The new leech is distinguished from its 6 congeners on the basis of body size (maximum 10 mm long) and shape (sub-cylindrical trachelosome distinctly demarcated from wider urosome that is ventrally flattened, convex dorsally, and narrowing toward caudal sucker that is narrow, 20ï€-25% of maximum body width), number of eyespots (2 pairs), shape and arrangement of the ovisacs (pyriform, and limited to somites XII/XIII), and characteristics of the mid-gut (1 pair of mycetomes, 6 pairs of simple thin-walled crop ceca, ventral postceca wanting, and 2 pairs of dendritic diverticula emerging from anterior portion of thick-walled intestine). The new species occurs in the northeastern Pacific Ocean on a benthic elasmobranch. Examination of host specificity for each Austrobdella species using the quantitative Index of Phylogenetic Host Specificity revealed that the new species is 1 of 4 oioxenous specialists in the genus and the remaining 3 congeners are relative generalists herein classified as euryxenous. This is the first time host specificity for members of the Piscicolidae has been quantitatively assessed. The analysis suggests that associations between marine leeches belonging in Austrobdella and their vertebrate hosts are driven by ecological influences rather than host taxonomic placement.

Sand tiger sharks, Carcharias taurus, are commonly maintained in large public aquaria throughout the world, but limited success has been achieved in captive reproduction. Successful captive reproduction in this species has only been documented in four institutions to date. In this investigation, steroid hormone assays in male sand tiger sharks were compared before and after dosing with a GnRH antagonist (Antide; Bachem, Inc., Torrance, CA). Three male sand tiger sharks were sampled serially for 12 months. All three sharks received two microsphere-encapsulated doses of Antide (0.185 and 0.225 mg·kg-1), 69 days apart. Serum samples were assayed for concentrations of the steroid hormones 17β-oestradiol, progesterone, testosterone, 5α-dihydrotestosterone, corticosterone, and the GnRH antagonist Antide via radioimmunoassay. The results obtained demonstrate cyclical patterns in the steroid profiles, and that mean Antide level peaked 33 and 27 days following each injection, respectively. Circulating Antide was detectable eight months after the final treatment. Contrary to the anticipated effect, however, concentrations of all five steroids increased immediately following initial administration of the antagonist. Although the lack of control subjects precludes solid conclusions regarding the effects of the antagonist upon steroid hormone levels, notable declines in the levels were observed concurrent with peak circulating Antide levels. Further, although we cannot attribute it to the antagonist, mean androgen levels declined more sharply following antagonist administration than those observed in a previous investigation in this group of male sharks. This is the first documented use of a GnRH antagonist in any chondrichthyan. Further research, including control subjects, is suggested to investigate the effects of the antagonist upon steroid hormones, reproductive cycles and behaviour.

Complete life history information is essential for effective population management, but little is known about the demographic characteristics of the southern stingray Dasyatis Americana. We describe life history characteristics of southern stingrays maintained in captivity from birth to 13 years. Size (disc width [DW]) at maturity ranged from 48 to 52 cm in males and from 75 to 80 cm in females; age at maturity was 3-4 years in males and 5-6 years in females. Individual growth was described using three models: the Gompertz function, von Bertalanffy growth function (VBGF), and logistic function. Analyses of DW at age and weight at age indicated that females were significantly larger at birth and reached larger maximum sizes than males. Because of the ability of the VBGF to fit the observed growth and that of previously reported maximum sizes, we favor its use to describe individual growth dynamics for this species. Using this model, we estimated that for males (n = 20), the asymptotic DW (DW ∞) was 67.4 cm, the von Bertalanffy growth coefficient (k) was 0.44 per year, and the predicted theoretical age at a DW of 0 cm (t 0) was -0.93 years. The corresponding estimates for females (n = 15) were a DW ∞ of 150.9 cm, a kvalue of 0.11 per year, and a t 0 of -1.61 years. The oldest southern stingrays in the study were a 12-year-old male and a 13-year-old female, and estimates of longevity were 7.9 years for males and 31.5 years for females. The sex ratio of neonates (n=453) did not differ significantly from 1:1. The life history characteristics derived from captive specimens indicate that southern stingrays are similar to other dasyatids in terms of growth and age at maturity.

Levels of reproductively-related steroids were determined in captive male sand tiger sharks, Carcharias taurus, maintained at two institutions: SeaWorld Adventure Park Orlando and the National Aquarium in Baltimore. Sexual conflicts were absent at the former, but were documented at the latter. Serum titers of 17β-estradiol, progesterone, testosterone, and 5α-dihydrotestosterone were determined via radioimmunoassay in adult male sharks from 1988 to 2000. Sampling overlap between the two institutions occurred for 3 months of the year, but steroid concentrations were compared only for April due to the occurrence of sexual conflicts in the sharks at the National Aquarium in Baltimore in that month. For April, testosterone and dihydrotestosterone were significantly higher in the SeaWorld males, and progesterone was significantly higher in the National Aquarium in Baltimore males, while estradiol was not significantly different. Steroid levels were also determined from serial samples taken monthly over 17 months from three male sharks and one female shark at the National Aquarium in Baltimore in 2001–2002 and were compared with corresponding observed sexual conflicts. The steroid levels obtained showed distinct annual hormonal cycles in the male sharks and corroborated a biennial cycle for the single serially-sampled female shark. Furthermore, the steroid levels for individual males correlated with sexual conflicts as well as their position within the male dominance hierarchy. As this species is depleted in some regions globally, insight into the steroid profile of mature sand tiger sharks is important for a greater understanding of the relationship between their reproductive physiology and behavior, and may aid in captive management and reproduction.

We report on three separate instances of protrusion of the valvular intestine in the smalltooth sawfish Pristis pectinata, compare pristid gastrointestinal anatomy and intestinal valve structure with those of other elasmobranchs, and discuss the relevance of anatomy and valve structure to the husbandry of captive specimens. Protrusion of the valvular intestine, or intestinal eversion, has been documented in carcharhinid sharks with scroll-type intestines. All three cases of protrusion in smalltooth sawfish in this report involved specimens in multispecies display facilities and ultimately resulted in mortality. These are the first documented cases of intestinal eversion in any species of elasmobranch with a conicospiral valvular intestine. The valvular intestine of sawfishes (family Pristidae) is of the conicospiral type, which is similar to that described in other batoid species. However, unlike many other sharks and batoids, which possess short, stout pyloric stomachs, the pyloric stomachs in the pristids we examined were long and similar to those of carcharhinid sharks. The ability to protrude the valvular intestine in elasmobranchs may depend upon both valve morphology and the length of the pyloric stomach. The details of the gastrointestinal anatomy may be useful for systematics but also may be relevant to the captive husbandry of carcharhinids and sawfishes.

Successful reproduction has been recorded in many different species of cartilaginous fish held in captivity, representing the various reproductive modes recorded in chondrichthyans. Documentation of behaviors of captive chondrichthyans has provided a foundation to our knowledge of reproductive behavior, as these interactions are rarely witnessed in the wild and difficult to infer from freshly caught wild specimens. Reproductive behavior often results in conspecific and interspecific conflicts. Conspecific sexual conflict may be consexual as well as intersexual. Although specific reproductive behaviors have The Elasmobranch Husbandry Manual: Captive Care of Sharks, Rays and their Relatives, pages 237-248.

Chondrichthyan reproduction is characterized by internal fertilization, diverse reproductive modes, complex reproductive cycles, late sexual maturity, iteroparity (several litters per lifetime), and small brood size. Embryonic development in elasmobranchs ranges from two months to at least two years, and generally proceeds uninterrupted, with the exception of those species in which embryonic diapause has been confirmed. Relatively little information on reproduction in captive elasmobranchs has been published. Information on reproduction from wild conspecifics is therefore useful in assessing reproductive potential in captive elasmobranchs. Reproduction in captive animals may provide insights into hormonal fluctuations, behavior, and maternal-brood relationships. Differences from wild conspecifics may result from constraints associated with the captive environment. Detailed, accurate information relating to reproductive biology and physiology should be collected from captive specimens, and disseminated via peer-reviewed publications. REPRODUCTION AND DEVELOPMENT Reproduction in chondrichthyans is variable in terms of the functional morphology of the reproductive tract, biology and behavior, embryonic development, and modes of embryonic nutrition. In general, the reproductive biology of elasmobranchs is characterized by: delayed sexual maturity, diverse modes of embryonic nutrition, different reproductive cycles, and low

Aspects of the reproductive biology of the Southern Stingray, Dasyatis americana, were determined from five captive adult females and their offspring. Mean size and weight of the neonates were 238.0 ± 1.6 mm disc width and 505.9 ± 10.7 g, respectively. Litter size (n = 47), which ranged from two to 10, averaged 4.2 ± 0.3 and varied directly with maternal size and indirectly with size and weight of neonates. Gestation (n = 47) ranged from 135 days to 226 days with a mean of 175.4 ± 4.1 days.

Chondrichthyans are a diverse group in terms of reproductive mode, which range from extended oviparity to placental viviparity. Although the reproductive biology of several species has been investigated, the reproductive physiology of only a few species has been reported. Only recently have the physiological factors of reproduction in cartilaginous fishes received attention. The information gained on reproductive cycles (both gonadal and uterine) has shown some similarities as well as differences between species. The serum levels of androgens, oestrogens, and progestins have been examined in several elasmobranch species and it has been shown that they are important in regulating key events in reproduction. The endocrine control of reproduction in elasmobranchs is more similar in many ways to higher vertebrates such as mammals than to teleosts. In general, the role of progesterone becomes more important than that of oestrogen in the transition from oviparity to viviparity. In addition, the roles of peptide hormones such as relaxin and the neurohypophysial hormones become increasingly important in viviparous species as in higher vertebrates. It is vital to understand the environmental and hormonal control of reproduction in elasmobranchs if more success is to be achieved in their reproduction in captivity. Knowledge gained from studies of the endocrine regulation of the reproductive cycle can be used to enhance the reproductive success of captive sharks, skates, and rays.

Historically, gymnurid rays have not done well in a captive environment. This report describes success in maintaining two specimens of the spiny butterfly ray, Gymnura altavela, in captivity. An aggressive husbandry protocol of tube feeding and force feeding maintained energy levels until the rays began to feed on their own. The rays used their pectoral fins to strike at food items, a behavior they may use in the wild to stun and capture prey. The first estimates of growth in captivity for any species of butterfly ray are given. Growth rates for the male averaged 0.063 mm/day (s.d.=0.030) and 10.253 g/day (s.d.=9.689), whereas growth rates for the female butterfly ray averaged 0.303 mm/day (s.d.=0.215) and 22.777 g/day (s.d.=15.2). Estimates of gross conversion efficiency (Kl) were calculated using the caloric values and known food intake. The estimates of Kl averaged 5.4% (s.d.=3.857) and 16.1% (s.d.=7.511) for the male and female, respectively, with a combined average of 10.8% (s.d.=7.95). These are the first estimates of Kl reported for any species of batoid using direct methods (growth rate and food intake). © 1996 Wiley-Liss, Inc.

Tonic immobility (TI), also known as animal hypnosis, has been observed in a wide variety of taxa and reported in all vertebrate classes with the exception of Agnatha. To date, TI has been reported in six species of elasmobranchs. Preliminary results are presented here for five species of galeomorph sharks, one species of squalomorph shark, and six species of batoids. Tonic immobility was induced in the leopard shark. Triakis semifasciata; the whitetip reef shark, Triaenodon obesus; the blacktip reef shark, Carcharhinus melanopterus; the Caribbean reef shark, Carcharhinus perezi; the swellshark, Cephaloscyllium ventriosum; the California round ray, Urolophus halleri; the shovelnose guitarfish, Rhinobatos productus; the clearnose skate. Raja eglanteria; the cownose ray, Rhinoptera bonasus; and the southern stingray, Dasyatis americana. The broadnose sevengill shark, Notorynchus cepedianus and the yellow stingray, Urolophus jamaicensis failed to exhibit the tonic immobility response, but only one individual of each species was tested. The average induction time ranged from 16.7 sec in the shovelnose guitarfish to 45.7 sec in the clearnose skate. Average duration times ranged from 34.3 sec in the clearnose skate to 274.0 sec in the Caribbean reef shark. Depending upon the species involved, TI has been used as an aid in a few husbandry and medical procedures in captive elasmobranches at the National Aquarium in Baltimore. These procedures have included gross examination, measuring lengths, tube feeding, and drawing blood via caudal venipuncture. Using tonic immobility during these procedures is beneficial as once induced, the subject's struggling is minimal and usually requires little restraint. © 1994 Wiley-Liss, Inc.

Abstract: Public aquariums have contributed to knowledge on elasmobranchs in various fields including diet, age and growth, bioenergetics, physiology, pathology, behavior, captive care, and population dynamics. Benefits of conducting research in public aquariums include: clear water, large tanks, species variety, and knowledge of husbandry. Limitations include: artificial habitats, possible modification of environmental cues (e.g., photoperiods, etc.), and insufficient replicates for adequate hypothesis testing. Although research in aquariums is continuing to increase, it appears to be restricted to relatively few institutions. We actively encourage aquariums to participate in elasmobranch research. We recommend cooperation between aquarists and colleagues at academic organizations to maximize the value of their respective skills. The ultimate aim of each study should be to publish results in peerreviewed journals or books, ensuring rigorous research practices and knowledge dissemination. Research activities will be of immediate benefit to the aquariums involved and ultimately aid in the conservation of elasmobranchs.