Nova Southeastern University NSUWorks

Oceanography Faculty Articles Department of Marine and Environmental Sciences

1-1-2013 The elY low Stingray, Urobatis jamaicensis (Chondrichthyes Urotrygonidae): A Synoptic Review Richard E. Spieler Nova Southeastern University, [email protected]

Daniel P. Fahy Nova Southeastern University

Robin L. Sherman Nova Southeastern University, [email protected]

James Sulikowski Nova Southeastern University

T. Patrick Quinn Nova Southeastern University

Find out more information about Nova Southeastern University and the Oceanographic Center.

Follow this and additional works at: http://nsuworks.nova.edu/occ_facarticles Part of the Marine Biology Commons

NSUWorks Citation Richard E. Spieler, Daniel P. Fahy, Robin L. Sherman, James Sulikowski, and T. Patrick Quinn. 2013. The eY llow Stingray, Urobatis jamaicensis (Chondrichthyes Urotrygonidae): A Synoptic Review .Caribbean Journal of Science , (1) : 67 -97. http://nsuworks.nova.edu/occ_facarticles/228.

This Article is brought to you for free and open access by the Department of Marine and Environmental Sciences at NSUWorks. It has been accepted for inclusion in Oceanography Faculty Articles by an authorized administrator of NSUWorks. For more information, please contact [email protected]. Caribbean Journal of Science, Vol. 47, No. 1, 67-97, 2013 Copyright 2013 College of Arts and Sciences University of Puerto Rico, Mayagu¨ ez

The Yellow Stingray, Urobatis jamaicensis (Chondrichthyes: Urotrygonidae): a synoptic review

Richard E. Spieler1,2,3,*, Daniel P. Fahy1,2, Robin L. Sherman4, James A. Sulikowski5, and T. Patrick Quinn1,6

1Oceanographic Center 2National Coral Reef Institute 3Guy Harvey Research Center Nova Southeastern University, 8000 North Ocean Drive, Dania Beach, Florida 33004 USA 4Farquhar College of Arts and Sciences, Nova Southeastern University, 3301 College Avenue, Fort Lauderdale, Florida 33314 USA 5Marine Science Center, University of New England, 11 Hills Beach Road, Biddeford, Maine 04005 USA 6Natural Resources Planning and Management Division, Broward County, 1 North University Drive, Plantation, Florida 33324 USA *Corresponding author. Tel: +1 9542623613 E-mail address: [email protected]

ABSTRACT.—The yellow stingray, Urobatis jamaicensis (Cuvier) has been the subject of a multitude of diverse studies on its natural history, morphology, and physiology. We have attempted here to briefly review all the studies on U. jamaicensis both published and unpublished with the goal of providing comparative information for researchers working on related species as well as to highlight areas of research requiring further investigation in this one.

KEYWORDS.—Anatomy, Ecology, Elasmobranch, Physiology, Reproduction, Stingray

Introduction males reached a maximum size of 398 mm TL (with a mean of » 325 mm). There are Urobatis jamaicensis (Cuvier), the yellow multiple publications listing 600 mm and stingray (Nelson et al. 2004) (Fig. 1), was orig- larger TL U. jamaicensis (Bigelow and inally described in 1816 as Trygon jamaicensis. Schroeder 1953; Lieske and Myers 1994; It has also been previously classified as McEachran and Fechhelm 1998; Parsons Trygonobatus torpedinus, Urolophus torpedinus, 2006). However, these appear to be based on Urobatis sloani, Urobatis vermiculatus, and an incorrect deduction of an ambiguous esti- Urolophus jamaicensis (Bigelow and Schroeder mate (“about 500 mm; tail 190 mm”; Fowler 1953); much of the literature refers to the latter 1945) or a misidentification. It would be a synonym. There are several phylogenetic considerably larger U. jamaicensisthanwe hierarchies currently proposed, the most have encountered. commonly accepted is: Class Chondrichthyes, Individual rays differ widely in color and Subclass Elasmobranchii, Order Myliobatiformes, pattern; the dorsal side of the disc typically Family Urotrygonidae; however, further revi- displays a reticulate dark greenish or sion should be expected (Nelson, 2006). brown pattern on a pale background, or a U. jamaicensis is a relatively small ray with close set pattern of minute white, yellow, or an average size of about 335 mm total length golden spots on a dark green or brown (TL) and 160 mm disc width (DW). Typical of background. The ventral side of the disc is elasmobranchs, females grow larger than males. lightly colored, uniformly yellowish or In our studies, with more than 500 animals, brownish-white (Bigelow and Schroeder the maximum size recorded was a female 1953). However, occasionally the ventral 480 mm TL (the mean was »345 mm); while side has the same pattern as the dorsum 67 68 R.E. SPIELER, ET AL.

Fig. 1. Urobatis jamaicensis: A. dorsal view of male; B. ventral view of female showing uncommon coloration of ventrum; C. on hardbottom; D. partially buried. either in a patchy distribution or restricted and Chaplin 1993; Hoese and Moore 1998; to the outer margins of the wings (Fig. 1). McEachran and Fechhelm 1998; McEachran The animals are found in shallow water and Carvalho 2002; Piercy et al. 2006b). (maximum reported depth 30 m) through- According to the IUCN Redlist report out most of the Greater Caribbean. They are (Piercy et al. 2006b) distribution is listed patchily distributed throughout their range, for all countries within the northern and but occasionally occur in relatively high southern limits of the species range. How- abundances (Bigelow and Schroeder 1953). ever, reports on abundance or even pres- For example, a study off Ft. Lauderdale, ence in many of these regions are typically Florida, tagged 108 individuals in an area of unverified and open to question. Although 2.7 + 0.4 km during 13 months of sampling the presumed range of U. jamaicensis is quite over a 14 month period without any single extensive, available data on distribution indi- recapture of a tagged or tag-site-scarred ani- cates that a complete absence or rare occur- mal (Sulikowski 1996). Presumably, this is rence is associated with several regions. not due to large migratory movements of Thus, a clear distribution pattern remains the animals such as those associated with uncertain. Populations of U. jamaicensis are reproduction in some other elasmobranchs most prevalent in South Florida (including (see Activity Patterns, below). Florida Bay and the Keys), Bahamas (north The geographic range of U. jamaicensis and central islands), Greater Antilles (west has previously been reported to occur of Mona Passage, including the Cayman from North Carolina to Brazil, includ- Islands), and Caribbean Mexico (Campeche, ing the Gulf of Mexico and widespread Yucatan, Quintana Roo, Cozumel) through throughout the Caribbean Sea (Bigelow and Belize. However, north of Jupiter Inlet on the Schroeder 1953; Robins et al. 1986; Bo¨hlke east coast of Florida and in waters of the A REVIEW OF UROBATIS JAMAICENSIS BIOLOGY 69 northern and western Gulf of Mexico begins of low blunt tubercles on the mid- U. jamaicensis is considered a rare tropical dorsum and re-curved thorns along dorsal stray (Robinson 1969; Gilmore et al. 1981; margins of the caudal fin. Larger adults Snelson and Williams 1981; Hoese and have the mid-dorsal tubercles to the orbits Moore 1998; Schmid et al. 1988; REEF 2009). and a lateral band of thorns over each shoul- In the Greater Antilles, reports are lacking for der. The ventrum remains smooth through- east of Mona Island across the Puerto Rican out life (Bigelow and Schroeder 1953). Plateau (Puerto Rico, Vieques, Culebra, St. The teeth of U. jamaicensis, apparently John, St. Thomas, Tortola, Virgin Gorda, and evolutionarily derived from denticles Anegada). Likewise, records from St. Croix, (Kemp 1999), number about 30 per row on Lesser Antilles (with the possible exception both the upper and lower jaws in about 5 of Grenada, Trinidad, and Tobago) and and 8 rows respectively. All rows are south of Venezuela (Guyane, Suriname, simultaneously functional. In females and Guyana, and Brazil) are either nonexistent or immature males, the teeth are closely questionable (Lowe-McConnell 1962; Dennis arranged and oval in shape with low cusps. et al. 2004, 2005; Menni and Stehmann 2000; In mature males the upper teeth are more Lasso et al. 2004; Nunes et al. 2005; Acevedo loosely spaced with high conical cusps that et al. 2007; Grijalba-Bendeck et al. 2007a, b; are slightly blunt at the end (Bigelow and REEF 2009). Further, there are few studies Schroeder 1953). This sexually dimorphic trait on temporal variation in abundance from is associated with reproductive behaviors and areas where the animals are prevalent. There likely functions to allow the male to maintain has been one report of a dramatic decrease in a grasp on the female during copulation (see sightings of yellow stingrays in the greater below). Sexually dimorphic dentition is a Caribbean area over a 14 year period (from common trait observed among batoids with sightings in 20.5% of dives to 4.7%); however, females exhibiting a smooth, molariform the trend was not consistent across all sur- shape, whereas male dentition consists of veyed regions (Ward-Paige et al. 2010). In sharp, recurved cusps (Bigelow and Schroeder some, U. jamaicensis’ distribution throughout 1953; Feduccia and Slaughter 1974; McCourt the Caribbean basin appears more restrictive and Kerstitch 1980; Taniuchi and Shimizu than previously considered and the patterns 1993; Nordell 1994; Kajiura and Tricas 1996). of biogeography and connectivity of this ani- Male Dasyatis sabina exhibit a seasonal tran- mal remain to be elucidated. sition in dentition; feminine-like teeth dur- U. jamaicensis has been the subject of a ing non-reproductive periods are replaced multitude of diverse studies on its natural by sharp cusps during the protracted mat- history, morphology and physiology. We ing season (Kajiura and Tricas 1996). The have attempted here to review all the studies re-curved condition of male U. jamaicensis on this animal of which we are aware, both dentition is static throughout the year; how- published and unpublished. Our goal is to ever, preliminary gross observations indi- summarize current knowledge of U. jamaicensis cate sharp cusps are more prominent during in order to provide comparative information periods of active breeding (Fahy unpub- for researchers working on related species lished). Additionally, increased incidence of as well as highlight areas of research requir- dermal bite wounds on females has been cor- ing further investigation in this one. related to male dentition and seasonal mating activity in D. sabina (Kajiura et al. 2000). Anatomy and Physiology Integument Caudal Spine The integument of U. jamaicensis,asin Urobatis jamaicensis typically has a single other batoids, is relatively thick and covered, venomous caudal spine (Fig. 2) which, like in part, with placoid scales or denticles many other stingrays, is shed periodically (Bigelow and Schroeder 1953; Kemp 1999). (Johansson et al. 2004; authors unpublished). At parturition, the skin is devoid of denticles. In a study off Seal Beach, California, natural However, shortly thereafter, development spine replacement occurred in U. halleri 70 R.E. SPIELER, ET AL.

Fig. 2. A) Transverse section of caudal spine of Urobatus halleri, illustrating enamel (E), dentine (D) and “poison gland” cell (PG) (minor modification of original by A. Paden from Daniel 1934). B) Three spines of U. jamaicensis, dorsal and ventral views of cleaned spines (left and center, respectively) and uncleaned spine with dried epidermal sheath (right). between August and October (Lowe et al. ranges from an itch to severe pain requir- 2007). During the period when the new spine ing medical treatment; again we write from is growing, the animal carries two spines and experience here. rarely three. Through most of the year, the spine has a strong attachment to the verte- Nervous System bral column and is not readily removed from Brain Morphology the tail. During these times, the spine will beartheentireweightoftheanimaloutof There has been little work on the ner- water and entanglements in nets are more vous system of U. jamaicensis.Walkerand likely to break the spine than pull it out. Dur- Sherman (2001) looked at gross morphology ing periods when the spine is being shed, it and there has been some abstracted, and is released with relative ease. The spine is unpublished, work on cerebellar function normally used in a stabbing motion that (Sherman et al. 2003). Like other stingrays, produces a puncture wound, although, if U. jamaicensis has a brain 3 to 10 times the the ray is lashing its tail about, a scalpel-like size of their sister groups, the electric rays, slash can be inflicted. This normally decep- guitarfish, and skates. The brain is well tively docile animal can stab its spine with developed and, relative to fishes, quite surprising speed, a fact which most research- large in proportion to body weight, rivaling ers working with it can attest to. We mammals in size (»1–2% bw) (Northcutt are unaware of studies on the toxin of the 1989; Walker and Sherman 2001). U. jamaicensis spine but it is likely similar to Gross morphology of the U. jamaicensis other stingrays. The toxin is a protein pro- brain is similar to the closely related duced in glandular tissue of the sheath, Dasyatids, including the presence of an within the ventrolateral grooves, that remains asymmetric cerebellum (Fig. 3). Like mam- behind in the wound rather than an injected mals, they also have a large, complex, three- venom (Fig. 2) (Russell 1959; Pedroso et al. lobed cerebellum. However, in U. jamaicensis, 2007). The pain produced by the toxin these lobes are completely separated. Thus, depends on the wound, and individual- the lobes can be individually manipulated specific responses to the envenomation, and to examine behavioral correlates of specific A REVIEW OF UROBATIS JAMAICENSIS BIOLOGY 71

Fig. 3. Dorsal and ventral view of brain with cranial nerves and major topography of Urobatis jamaicensis. Cranial Nerves: I-Olfactory, II-Optic, III-Oculomotor, IV-Trochlear, V-Trigeminal, VI-Abducens, VII-Facial, VIII- Auditory, IX-Glossopharyngeal, X-Vagus. Major Topography: ACc-Anterior caudal cerebellum, ARc-Anterior rostral cerebellum, CE-Cerebrum, H-Hypophysis, I-Inferior lobes of infundibulum, MO-Medulla oblongata, OL- Olfactory lobe, OpL-Optic Lobe, Pc-Posterior cerebellum, T-Tegmentum (from Walker and Sherman 2001). 72 R.E. SPIELER, ET AL. lobes. Some preliminary work examined the researchers, although the brain is readily function of these lobes. Cerebellar ablation accessed, the chondrocranium never repaired was performed on anesthetized animals by itself, and neither cements nor sutures ade- first creating a hinged window in the dorsal quately reattached an opened window. portion of the chondrocranium, using an Nonetheless, the large brain should make electric drill with a thin (0.1 mm) circular U. jamaicensis an interesting model for neuro- saw blade, exposing the midbrain. The three physiologists interested in fishes and the lobes of the cerebellum were identified and large cerebellum in this sedentary animal either the center lobe (n = 7) or caudal lobe begs further investigation. (n = 3) was removed. Following removal of the cerebellar lobe, the cartilaginous flap over Sensory Systems the window was closed with a single suture Vision and surgical adhesive, paraffin, or liquid W Band-Aid used to seal the cut edges. The Urobatis jamaicensis has the eyes located entire procedure, from anesthesia induction well up on the dorsum and somewhat pro- until completion of the surgery and resus- truding and periscopic in comparison to citation, took approximately 30 min. As other batoids. Presumably this protrusion controls, four animals were subjected to all allows the eyes to stay slightly above the the surgical procedures, but no brain tissue surface and provide vision when the ani- was removed. mals are buried (McComb and Kajiura Gross, reproducible behaviors were readily 2008). Like many other batoids, U. jamaicensis noted one day after surgery and did not has crescent shaped pupils and a pupillary improve over 3 weeks time (the longest operculum, a complex flap of iris tissue period an animal survived following lobe hanging over and partially covering the ablation). As noted in mammals, there pupil. The crescent-shaped pupil preserves appears to be a relationship between the a small depth of field, limits light flux to the cerebellum and voluntary coordination retina and decreases the effects of spherical and behavior in U. jamaicensis.Ablationof aberration inherent to the globular lens. The the center lobe caused a generalized pattern pupillary operculum effectively creates mul- of uncoordinated hyperactivity. When dis- tiple apertures, and thus multiple images, of turbed by gentle prodding, the animals objects lying either in front or behind the responded with an atypical rapid swimming plane of optical focus. This provides the ray to the surface, spinning, and often swim- with enhanced sensitivity to movement. In ming, momentarily, upside down and back- addition, the pupillary operculum may pro- wards (Sherman et al. 2003). These results, of vide a larger visual field than a circular pupil uncoordinated hyperactivity, would support of identical area and may also diminish the an inhibitory role for the center lobe of the effects of lens-induced spherical aberration cerebellum of U. jamaicensis similar to that (Murphy and Howland 1990). reported for the mammalian cerebellum (Ito McComb and Kajiura (2008) conducted et al. 1964). In sharp contrast, however, abla- an ecophysiology study on the visual field tion of the caudal lobe caused extreme leth- of four batoids, including U. jamaicensis. argy. The animals were unresponsive to They found that U. jamaicensis had a hori- prodding; even lifting by hand did not elicit zontal visual field of 360 and a vertical an escape response. Sham controls did not field of 264, thus the animals can see in all show any detectable difference in behavior directions with virtually no blind spots from non-operated controls. Both sham and except directly on top of their head (Fig. 4). non-operated controls spent most of the day However, horizontal binocular vision in buried in the sand substrate of the holding front of the animal was only 34. The tanks. None of the ablated animals buried authors deduced that given food acquisi- despite apparent attempts (i.e., forming shal- tion is primarily blind foraging in the low depressions). The study was ended pre- substrate, and likely not requiring great maturely due to technical difficulties with visual acuity, the binocular vision was ade- the aquarium facilities. As a caution to future quate for forward swimming. Further, they A REVIEW OF UROBATIS JAMAICENSIS BIOLOGY 73

Fig. 4. Horizontal and vertical visual fields and standardized convergence distance (cm) of Urobatis jamaicensis. Monocular and binocular visual fields are lightly and darkly shaded respectively (after McComb and Kajiura 2008). suggested the large horizontal and vertical ments of each holobranch are attached to an visual fields of this animal are associated interbranchial septum, which is attached to with a sedentary lifestyle and, likely, high both the dorsal and ventral surfaces of the predatory pressure. pharyngeal cavity. The interbranchial septa separate the gill pouches and are formed of Hearing skeletal (striated) muscle supported by carti- laginous rays. The gill arches contain a num- Casper and Mann (2006) examined hear- ber of small, coarse gill rakers that prevent ing thresholds of U. jamaicensis using audi- large particles from entering the gill pouch tory evoked potentials (AEP), essentially and possibly damaging the gill filaments. recording acoustic-stimuli-evoked poten- Sherman et al. (1995) examined two other tials from the brain. Test frequencies species of stingrays, in which the lamellar ranged from 100 to 2000 Hz. However, surface area utilized for gas exchange AEP were only obtained up to 1000 Hz. rangedfromtwotoseventimestheanimal’s The animals appeared to be most sensitive body surface area. They suggested that in at 300 and 600 Hz with a threshold of batoids, like other fishes, the ratio of gill sur- 139.45 dB and 140.23 dB re 1 mPa respec- face area to body surface area appears to be a tively. Like other elasmobranchs, or tele- function of the normal activity level of the osts lacking a swim bladder, U. jamaicensis animal being examined (Satchell 1962). For appears to have poor hearing abilities and example, a species that feeds high in the is limited to detecting particle motion and water column or migrates long distances will not sound pressure. have a higher gill surface area to body sur- Respiratory System face area ratio than a more sedentary animal. As in other batoid elasmobranchs, it Gross examination of the gills confirms appears U. jamaicensis’ water for respira- the basic structure of the gill arches in tion is primarily pumped through dorsally U. jamaicensis is similar to those of other located spiracles and, presumably, may sec- elasmobranchs. The hyoid arch supports a ondarily also be taken in through the mouth. single hemibranch. This single, anterior gill The water flows into each gill pouch, across is the first hemibranch. The posterior gill the lamellar surface, down a water chan- arches support the first, second, third and nel at the base of each filament, and out fourth holobranchs, respectively. The fila- through the gill slit on the ventral surface. 74 R.E. SPIELER, ET AL.

Respiratory water flow may be increased or onary arteries arising from the hypobrachial decreased, as needed, by muscular pumping arteries (Rogers et al. unpublished). Interest- (Donald 1988; Sherman 1998; Butler 1999). ingly, Olson et al. (2000) reported spontane- Constrictor muscles in the yellow ray cover ous contractions in the blood vessels from most of the head and gill region. They con- four elasmobranchs, two sharks and two sist of dorsal superficial constrictors that lie batoids, including U. jamaicensis. The authors dorsal to the gill pouches, and ventral super- noted that, in general, these contractions were ficial constrictors that lie ventrally between more prevalent in the sedentary batoids than the gill slits. The superficial constrictors in in the sharks and speculated that this might sharks compress the pharyngeal chamber, be due to a decreased utility of muscle pumps eject the water, and close the gill slits (Gilbert associated with this lifestyle. 1993; Ashley and Chiasson 1988). The simi- The conus arteriosus extends from the larity in these structures in stingrays sug- heart anteriorly to the end of the pericardial gests that they perform the same function. cavity. Beyond this point the vessel con- We are not aware of any work discussing a tinues as the ventral aorta, a median vessel tidal respiratory water-flow, in and out which gives off five pairs of afferent bran- through the spiracles. However, such an chial arteries leading to the gills. The fourth exchange would appear to be advantageous and fifth branchial arteries arise simulta- to an animal with ventral gill slits when bur- neously just anterior to the pericardial cav- iedinsandandmightbeaninterestingtopic ity at the point where the conus arteriosus for future research. joins the ventral aorta and serve the third and fourth holobranchs. The third afferent Cardiovascular System branchial artery serves the second holo- branch. The ventral aorta then extends Blood flow in elasmobranchs is a single without further branching to the level of circuit, flowing sequentially from the sinus the hyoid arch where it bifurcates, forming venosus to the atrium, the ventricle, the two stems which turn posteriorly. Each conus arteriosus, the ventral aorta, the gills, stem divides into two arteries, the first and then to systemic tissues and return (Tota second afferent branchials which lie on 1999). Hamlett et al. (1996c) examined the either side of the first gill pouch, the poste- anatomy, histology, and development of rior branch serving the first holobranch, and the three sets of cardiac valves in embry- the anterior branch serving the single onic and adult elasmobranchs, including hemibranch. Sherman and colleagues have U. jamaicensis. The sinus venosus is the first done several studies on the vascular structure heart chamber to receive venous blood, and of U. jamaicensis’ gills using corrosion casting. one-way flow is aided by a pair of sinoatrial In general, this animal’s gill structure resem- valves, which prohibit return flow of blood bles that noted in other elasmobranchs from the atrium into the sinus venosus.These (Donald 1988; Sherman 1998; Sherman and valves are simple flaps of tissue lacking papil- Spieler 1998; Sherman et al. 2001). However, lary muscles or chordae tendineae.Incontrast, some aspects of the arterio-arterial pathways as in higher vertebrates, the atrioventricular in Urolophus and Urobatis spp. gills differ valves, located between the atrium and the from that of teleosts and other elasmobranchs ventricle, have chordae tendineae,arecom- (Donald 1988; Sherman 1998). There is a more posed of linear arrays of collagen, and link extensive corpus cavernosum in the afferent cir- valve tissue to papillary muscles in the ventri- culation of Urobatis than that found in other cle. There are multiple rows of conal valves in groups. This corpus cavernosum is a well the conus arteriosus which prevent blood from developed structure into which blood flows reentering the ventricle. The conal valves from the afferent filament artery. From there, have chordae tendineae, but lack papillary mus- blood enters the lamellae through afferent cles. Preliminary work using mercox perfu- lamellar arterioles. Although the function of sion indicates the arterial blood supply to the the cavernous tissue has not been fully heart of U. jamaicensis is similar to other established, it may have a storage function, batoids (Prior and Marples 1945) with the cor- act to dampen the blood pressure pulse, or A REVIEW OF UROBATIS JAMAICENSIS BIOLOGY 75 serve as a hydrostatic skeletal structure. In gous to the septal corpora cavernosa found in addition to an enlarged corpus cavernosum, other elasmobranchs. Evidently, this arrange- additional, unique structural differences ment of vessels is not found in all batoids from other elasmobranchs include: 1) the lack because the vascular anatomy of some skates of a septal corpus cavernosum; 2) the existence lacks the vascular arcade; in Raja erinacea,and of a vessel, or vascular arcade, which con- R. clavata gill filament vasculature is similar to nects the afferent filament arteries near the that of selachians (Sherman et al. 2001). tip of the filament; 3) a channel, possibly an A non-gill secondary circulation has only extension of the afferent filament artery, at been identified in teleosts (Satchell 1991). the top of the filament corpus cavernosum However, there are interlamellar vessels in (Donald 1988; Sherman 1998). Donald (1988) the gills of U. jamaicensis that have been suggests the vascular arcade may be homolo- speculated to be part of a secondary,

Fig. 5. Example of an arterial cast of a yellow stingray, Urobatis jamaicensis (ventral view, in successive increasing magnification). Anastomosis between the fourth epibranchial arteries and the dorsal aorta is indi- cated by the arrow. DA-dorsal aorta; SC-subclavian; REB-right fourth epibranchial artery; LEB-left fourth epibranchial artery; CT-celiac trunk; AM-anterior mesenteric artery (from Basten et al. 2007). 76 R.E. SPIELER, ET AL. arterio-venous, circulatory system (Sherman and left epibranchial becomes the anterior 1998). Presumably, these secondary ves- mesenteric artery/posterior intestinal artery. sels empty into central veins of the head This vascular configuration appears to be such as the branchial and inferior jugular unique in elasmobranchs; the physiologic through which the blood/plasma is trans- function of this configuration is unclear, ported back to the heart. In U. jamaicensis, but it has been hypothesized to prevent a this system includes a series of intercon- large decrease in blood pressure that might necting vessels originating at arteriovenous occur at the juncture of the dorsal aorta and anastomoses from the efferent filament the subclavian arteries (Basten et al. 2007; artery and from some of the efferent lamel- 2009) (Fig. 5). lar arterioles. These post-lamellar arteriove- Blood to the spiral valve arises from the nous anastomoses supply blood to the central anterior mesenteric artery which feeds the venous sinus, a network of interconnecting spiral valve externally and from the ante- vessels that occupy the core of the filament rior intestinal artery which feed the spiral located between the corpus cavernosum and valve internally. Each of the 13 valves the efferent filament artery. This sinus is receives a direct arterial blood supply from connected to afferent and efferent compan- the anterior mesenteric artery. Venous ves- ion vessels that run parallel to the afferent sels lie above the arteries at each valve and and efferent filament arteries (Sherman 1998). anastomose, as do, apparently, all vessels These companion vessels are named for of the digestive tract in elasmobranchs, into their positions, not their functions, as both the hepatic portal vein (Daniel 1934; Mun˜oz- vessels serve to drain the blood and, possi- Cha´puli 1999; Maroni et. al. 2009). bly, lymphatic fluid from the central venous Other than some scattered work on sinustovenoussinusesinthegillarch reproductive organs (see below), little work (Metcalfe and Butler 1986). In teleosts, this has been done on arterial perfusion, or system was regarded as primarily lym- venous return, of the remaining organs of phatic until it was determined that its source U. jamaicensis. of blood is arterial and that red blood cells are sometimes passed through its vessels Digestive System (Satchell 1991). To conclude, most of the arterio-arterial gill anatomical structure in Gut U. jamaicensis has been worked out while much of the arterio-venous structure has Like many elasmobranchs, U. jamaicensis not. The physiological significance of many has a U-shaped stomach with a pyloric end of the structures of both systems remains to that enters a proximal (anterior) intestine then be elucidated. a spiral valve to a distal (posterior) intestine, Oxygenated blood flows from the gills rectum, and cloaca (Fig. 6). In extant fishes, via epibranchial arteries to systemic circu- the spiral valve is found in elasmobranchs lation. In most teleosts and elasmobranchs and some primitive families of Subclasses studies, the epibranchials join to form the Cladistia and Chondrostei. It functions in lieu dorsal aorta which gives rise to the subcla- of a small intestine and, by the addition of vian, anterior mesenteric, and gastric arter- internal structure, increases the surface area ies. However, with light and scanning allowing for increased area for digestion and electron microscopy of vascular corrosion absorption of nutrients. The spiral valve in casts, Basten et al. (2007; 2009) observed U. jamaicensis has 13 turns in an anterior ori- that the fourth epibranchial arteries do not ented conicospiral configuration (Holmgren merge completely with the dorsal aorta in and Nilsson 1999). Cestodes are routinely U. jamaicensis. Instead, they form a brief found in the spiral valves of elasmobranchs, anastomosis with a short vessel projecting including batoids, and U. jamaicensis is no ventrally from the dorsal aorta and main- exception. At least four species of tapeworms tain their integrity as separately distinct have been described from the spiral valves of vessels. Posterior to the anastomosis, the U. jamaicensis takeninJamaica(Kovacsand right epibranchial becomes the celiac trunk Schmidt 1980; Gardner and Schmidt 1984; A REVIEW OF UROBATIS JAMAICENSIS BIOLOGY 77

Fig. 6. Abdominal cavity of female Urobatis jamaicensis, with liver reflected.

Huber and Schmidt 1985). Additionally, the storage for periodic events (e.g., reproduc- digestive tract from specimens collected in tion, migration) and thus has little need for South Florida is often heavily invested with a large liver. un-identified nematodes (Quinn 1996; Fahy unpublished). Osmotic Regulation In its natural habitat, U. jamaicensis has Liver been collected in seawater (SW) that ranges Hepatosomatic indices (HSI; liver weight/ from 26% to 40% salinity (Yan˜ez-Arancibia body weight + 100) of U. jamaicensis are and Amezcua-Linares 1979). In order to test smaller than many other elasmobranchs the osmoregulatory capacity of this poten- including some other batoids. Sherman and tially euryhaline species, Sulikowski and Gilliam (1996) reported a mean HSI from 16 Maginniss (2001) characterized the water U. jamaicensis of 3.40 Æ 0.31 (mean Æ SE) and solute composition for plasma and a This was lower than free-swimming rays single intracellular compartment (erythro- (i.e., Aetobatus narinari, Rhinoptera bonasus) cytes) as a function of environmental salin- and is dramatically lower than the 20+% ity. In the laboratory, stingrays exhibited HSIs noted in some sharks (Kohler et al. rapid and significant increases in body 1996). The large HSI in elasmobrachs has mass upon exposure to stepwise seawa- been attributed to using the liver as a ter (33%) dilutions (82%, 74%, 66% SW). buoyancy organ as well as for food storage Average weight increases of 7-10% were (Bone and Marshall 1992). We suspect recorded within 24 h of exposure to the U. jamaicensis is a sedentary animal with three dilution steps. However, body fluid access to a relatively constant food supply recovery was generally achieved within 2- and does not require high levels of lipid 6 days for each of the three experimental 78 R.E. SPIELER, ET AL. groups. Likewise, changes in red blood cell urea across the RBC membrane of elasmo- (RBC) water content and mean corpuscular branchs, and it is most likely that urea levels Hb, indicative of erythrocyte swelling, sug- for erythrocytes and plasma in U. jamaicensis gested the stingray erythrocytes are regu- were nearly identical and exhibited compa- lated at a volume substantially less than a rable declines with environmental dilution passive RBC osmometer. Together, these (Walsh et al. 1994; Carlson and Goldstein 1997). data suggest that U. jamaicensis are capable Based on these results it would appear of extracellular and intracellular volume reg- that when exposed to mild or moderate ulation during hypo-osmotic exposure, espe- dilutions (82% and 74% SW), U. jamaicensis cially at lower salinities. regulate their body fluid compartments In 100% SW, stingray plasma was slightly slightly hyperosmotic to the external milieu hypo-osmotic to the external medium. by comparable reductions of the major elec- Although plasma osmolality decreased with trolytes and urea. With greater dilution hypo-osmotic exposure, the reductions were (66% SW), these elasmobranchs maintained not in proportion to the medium dilution. their hyperosmotic state by eliminating The measured plasma solutes also exhib- additional urea, while resisting further ited significant dilution-induced changes reductions of electrolytes (Sulikowski and in concentration, consistent with the corre- Maginniss 2001). Like many other marine sponding osmolality values. However, the elasmobranchs, the yellow stingray has a relative variations in plasma solutes were demonstrated capacity for survival and generally disproportionate and suggested acclimation in reduced salinity environ- regulation of the individual plasma solutes. ments (Lacy and Reale 1999). For example, in 82% SW, plasma Na, Cl, and urea were reduced 13%, 13%, and 21% below Reproductive System control levels, respectively; in 74% SW, the General corresponding values were 22%, 23%, and 25%, respectively. In the most dilute medium The gross and microscopic structure of (66% SW), further losses of the two primary the reproductive anatomy of U. jamaicensis electrolytes were curtailed. In fact, plasma was originally described by LaMarca (1961; concentrations of Na and Cl were reduced 1964) (gross structure: Figs. 7-10). More only 17% and 15%, respectively, below con- recently, several histological and ultra- trol levels. The animal’s lower limit of toler- structural examinations of specific repro- ance for extracellular ionic dilution may ductive structures (ovary, oviducal gland, occur within this concentration range. Solute uterus, and testis) have been conducted compensation for the transition from 74% to (Hamlett and Hysell 1998; Hamlett and Koob 66% SW was therefore achieved largely by 1999; Hamlett et al. 1996a; 1998; 1999a, b; further, and substantial, reductions of extra- 2005a, c). However, details on developmental cellular urea. In 66% SW, the plasma [urea] patterns of these structures throughout the of acclimated stingrays was reduced by 59% reproductive cycle are incomplete. Typical below control levels. Changes in plasma [K] among elasmobranchs, gonadal tissue is inti- and [Ca] were minor at each dilution. mately associated with lymphomyeloid tis- The three measured RBC cations (K, Na sue, forming the epigonal organs (LaMarca and Ca) exhibited similar responses to 1961; Hamlett et al. 1999c). In U. jamaicensis, environmental dilution and were reduced this gonadal-epigonal complex forms paired, by 12-16% in 82% SW and 32-37% in 74% dorsoventrally flattened and elongated organs SW, while in 66% SW, the electrolytes with morphological compensation due, pre- revealed a leveling-off effect which may sumably, to physical constraints of the visceral reflect the animal’s lower limit of tolerance anatomy within the coelomic cavity. At pre- for intracellular ionic concentration. Intra- sent, no studies have been conducted on cellular concentrations of urea have not steroidogenesis in U. jamaicensis; although, been reported for the yellow stingray. photoperiod, temperature, and the repro- However, the literature provides consider- ductive cycle have been correlated with cir- able support for the uniform distribution of culating levels of sex steroids in U. halleri. A REVIEW OF UROBATIS JAMAICENSIS BIOLOGY 79

Fig. 7. Reproductive organs of mature male Urobatis jamaicensis, with the left testis reflected to provide dorsal view of testicular lobes.

Androgens(testosteroneand11-ketotestosterone) the compound testis type described by Pratt were positively correlated with recrudes- (1988), with spermatocysts radiating both cence, with peaks at final sperm maturation outward from the germinal zone on the ven- and the onset of copulatory activity and neg- tral surface of each lobe and dorsally across the atively correlated with the photophase and diameter of the gonad (LaMarca 1961; Babel water temperature. Progesterone peaked at 1967). In U. jamaicensis, the germinal zone the time of ovulation, remained elevated consists of a testicular appendage that may through embryogenesis, and was positively be an exclusive structure of myliobatiform correlated with water temperature (Mull testicular morphology (LaMarca 1961, Lewis 2007; Mull et al. 2008). 1984). A condensed description of spermato- genesis (7 stages) has been reported with typ- Male Reproductive System ical patterns of elasmobranch spermatocyst/ The reproductive anatomy of male Sertoli cell development (Hamlett 1999). chondrichthyans (Figs. 7, 8) is structurally Variations have been observed in testicular more conserved than females (Hamlett lobate structure and efferent ductule devel- 1999). However, some variation exists in opment between conspecifics (LaMarca 1961; testicular structure and accessory glands, Babel 1967; Lewis 1984). In U. halleri, each with only minor differences in the extra- lobe consists of a permanent primary lobule testicular tract among species. Both testes and a transient secondary lobule (not present are equally developed and functional in during the quiescent phase of the reproduc- males; however the left testis is posteriorly tive cycle), with further subdivision of the folded conforming to the contours of the U- secondary lobule by connective tissue septae shaped stomach (LaMarca 1961). The paired that contain intermediate collecting ducts testes of U. jamaicensis are consistent with (Babel 1967; Mull 2007; Mull et al. 2008). 80 R.E. SPIELER, ET AL.

Fig. 8. Reproductive organs of mature male Urobatis jamaicensis, with testes removed.

In U. jamaicensis, testicular lobes persist branches of U. jamaicensis are confluent throughout the year (lacking a quiescent with degenerating spermatocysts during phase) with no indication of distinct pri- spermiation. The luminal epithelium of mary and secondary zonation (LaMarca both collecting and efferent ducts is identi- 1961; W. Hamlett personal communication) cal, consisting of a simple columnar epithe- possibly due to the biannual reproductive lium with elongated cilia. In U. jamaicensis, cycle (see below). Seasonal patterns of testic- the longitudinal ducts coalesce into a single ular development occur (indicating periods efferent duct that subsequently divides into of degeneration and recrudescence); how- 2-3 smaller branches, each branch sepa- ever, monthly histological examination of rately entering into the initial segment of the testes and reproductive tract is still the epididymis (LaMarca 1961). LaMarca required to determine production and stor- (1961) noted connective tissue septa that age of spermatozoa throughout the year partition the epididymis into two or three (LaMarca 1961; W. Hamlett personal com- rounded segments and identified two zones munication). U. jamaicensis exhibits a single (anterior and posterior) that vary in diame- longitudinal collecting duct supplied by ter and epithelia. The narrow diameter and interlobar collecting ducts, whereas U. halleri reduced lumen of the initial segment dis- displays individual longitudinal ducts asso- plays a high, irregular ciliated columnar ciated with each testicular lobe (LaMarca epithelium. The luminal diameter increases 1961; Babel 1967). These ventrally-located as the epididymis transitions into the termi- longitudinal ducts course through connec- nal segment, which is composed of a uni- tive tissue embedded within the testis- form, low ciliated cuboidal epithelium. The epigonal interface in both species (LaMarca external diameter of the epididymis gradu- 1961; Babel 1967; Lewis 1984). LaMarca ally increases as the convoluted tubule pro- (1961) reported that these smaller collecting gresses towards the terminal segment, and A REVIEW OF UROBATIS JAMAICENSIS BIOLOGY 81

Fig. 9. Reproductive organs of mature female Urobatis jamaicensis, with distended uteri and enlarged ova. eventually transitions into the larger and on the development of smooth muscle into more sinuous ductus deferens. The anterior mixed circular and longitudinal fibers that ductus deferens has a uniformly high, ciliated extend up into the connective tissue septa. columnar epithelium and is partially embed- Each transverse septum has an eccentric per- ded within the ventral tissue of Leydig’s foration with radially aligned smooth mus- gland (LaMarca 1961). Currently it is unclear cle that may regulate the spiraling luminal if Leydig’s gland tissue merely surrounds aperture throughout the seminal vesicle. portions of terminal segment or if excretory The seminal vesicle is considered a male ducts actually empty into the epididymal sperm storage site, and LaMarca (1961) has tract. LaMarca (1961) and Babel (1967) have suggested the arrangement of smooth mus- reported secretions from Leydig glands cle represents an ejaculatory mechanism empty solely into the ductus deferens proper during copulation. in U. jamaicensis and U. halleri,respectively. Although luminal fluids have not been Leydig glands consist of a series of convo- characterized throughout the genital ducts luted tubules with uniform columnar secre- of U. jamaicensis, continual absorption and tory epithelium and elongated cilia, similar seminal fluid modification has been reported to the upper epididymis. The tubules empty for Heterodontus portusjacksoni (Jones et al. into non-secretory collecting ducts prior to 1984; Jones and Lin 1993; Hamlett et al. discharging their contents into the extra- 1999b). Additionally, motility is enhanced in testicular tract. LaMarca (1961) referred to stepwise progression through the genital the enlarged S-shaped seminal vesicle as the tract with further transitions in sperm lumi- posterior ductus deferens or ampulla, and nal arrangement (Hamlett et al. 1999b). described low irregular folds of the mucosa LaMarca (1961) described varying columnar that form nearly transverse septa with cili- cell characteristics of luminal epithelia in ated columnar epithelium. He also remarked U. jamaicensis that are consistent with more 82 R.E. SPIELER, ET AL.

Fig. 10. Reproductive organs of a mature female Urobatis jamaicensis, with distended uteri (ovaries have been removed). recent descriptions of 2-3 cell populations The gland lumen consists of complex folds with varying distributions and functions (i.e. lined with simple columnar epithelium and a protein synthesis and secretion, absorption, surrounding layer of smooth muscle that and transport) (Botte et al. 1963; Jones and extends into mucosal folds (LaMarca 1961). Jones 1982; Jones and Lin 1993; Jones and Alkaline gland secretions are considered to Hamlett 2003; 2006; Jones et al. 2005). Acces- act directly on sperm motility and longevity sory glands in batoids have been variably with a potential function in the female repro- termed over the years and research directed ductive tract correlated with synthesis of a at morphological and functional characteris- relaxin-like molecule (Grabowski, et al. 1999; tics is lacking. The alkaline glands (formerly Lacy 2005). sperm sac) and clasper gland/sac (formerly LaMarca (1961; 1964) examined the struc- siphon gland/sac) are paired organs and ture of claspers and clasper glands of presumably assist in the transfer of sperma- U. jamaicensis including some histochemi- tozoa during coitus (LaMarca 1961; Babel cal analyses of clasper gland secretions. 1967; Lacy 2005). Alkaline glands are ven- Claspers are intromittent organs for inter- trally situated on the posterior aspect of each nal fertilization formed by developmental kidney and in stingrays the excretory duct is modifications of pelvic fin cartilages. In confluent with the terminal portion of the U. jamaicensis, these modifications consist of seminal vesicle (LaMarca 1961; Grabowski three connecting pieces, an appendix stem et al. 1999; Lacy 2005). Alkaline glands in and five fully-calcified segments (LaMarca U. jamaicensis are observed as small protuber- 1964). The diameter of the clasper tip is ances in immature specimens (LaMarca 1961) increased during copulation by flexion of a and are variably distended throughout the dilatator muscle to separate the terminal year in mature males (Fahy unpublished). cartilages and expand the hypopyle, thus A REVIEW OF UROBATIS JAMAICENSIS BIOLOGY 83 anchoring the clasper within the female clo- (subjacent to tunica albuginea) with simple aca. In U. jamaicensis, claspers are short and squamous epithelium and abundant lipid- stout, continually growing at an even rate like cells in the follicular wall. As follicles throughout sexual maturation. A viscous grow, a typical transitional gradient is white glycoprotein/phospholipid secretion observed for simple cuboidal (unilaminar) is produced within simple tubular glands, tissue in primary follicles (pre-vitellogenic), which radiate dorsally or dorso-laterally followed by stratification (multilaminar) from the secretory ridge (LaMarca 1964; and further development of columnar folli- Lacy 2005). Contraction of striated muscle cle cells. During initial stages of folliculo- that surrounds the organ expels secretory genesis, round lipid-like cells attain large products from the gland through a series of sizes, but eventually dissipate and vanish papillae (secretory openings) into the clasper prior to ovulation. A distinct zona pellicuda sac (Lacy 2005; Piercy et al. 2006a). Each is evident between the oocyte and follicle clasper gland papilla drains a series of cells. Follicular extensions extend across tubules which are lined with simple colum- the zona pellucida, indent the oolemma and nar epithelium via collecting ducts with form definitive transosomes during multi- pseudostratified epithelium (LaMarca 1964; laminar stages of follicle development Lacy 2005; Piercy et al. 2006a). The secretory (Hamlett et al. 1999c). openings are situated within the central lon- Ultrastructural observations of ovarian gitudinal groove of the organ with further folliculogenesis have described elaborate muscular contractions delivering secretions invaginations of the follicular epithelium into the clasper groove via an elongated slit along with subjacent portions of highly in the apopyle clasper segment (Lacy 2005). vascularized thecal tissue (Hamlett et al. Clasper gland secretions mix with spermato- 1999c). These inward folds initiate once ova zoaemittedfromthecloacaonceinsidethe attain diameters of 1.5 to 2.0 mm and are clasper groove (LaMarca 1964; Lacy 2005). In considered to increase surface area for a U. jamaicensis, the mixture of spermatozoa rapid and efficient transport of hepatically with clasper gland secretions produced derived yolk proteins during vitellogenesis. hyperactivity with motility persisting for These structures have also been described over 3 hours, whereas seawater mixing for other species of myliobatiform sting- entailed much lower activity for periods last- rays (Babel 1967; Lewis 1984; Teshima and ing only 15-20 minutes (LaMarca 1961; 1964). Takeshita 1992; Mull 2007) and are likely LaMarca (1964) proposed that clasper gland characteristic of the order. Although Babel secretions seal the clasper groove into a water- (1967) reports 24 months for egg develop- tight closed tube and also act as a medium for ment in U. halleri, a rapid onset of growth in sperm suspension and transport. the latter stages of gestation appears more characteristic of U. jamaicensis (Hamlett and Koob 1999; Hamlett et al. 1999c). Female Reproductive System LaMarca (1961) reported that specimens Females have two ovaries (Fig. 10) but collected during March and July displayed the right ovary is significantly reduced and all stages of oogenesis, including corpora production of mature ova is generally con- lutea, corpora albicans, and atretic follicles in sidered a sole function of the left ovary the left ovary. Corpora albicans and atretic (LaMarca, 1961; Fahy et al. 2007). However, follicles were often deeply embedded within Fahy et al. (2007) have reported enlarged epigonal tissue, whereas corpora lutea were vitellogenic oocytes from the right ovary of peripheral and described as large hollow two large females (single ovum »10 mm or structures with inward folded walls. Lewis larger). The germinal epithelium of the (1984) noted these observations were from ovary is simple cuboidal with rounded api- misidentified vitellogenic follicles, exhibiting ces and microvilli, overlying a moderately the above mentioned follicular epithelial dense layer of connective tissue (tunica folds. LaMarca (1961) also mentions small albuginea) (Hamlett et al. 1999c). Numerous ovawerepresentintherightovary,butdid primordial follicles are peripherally located not observe any glandular activity of atretic 84 R.E. SPIELER, ET AL. follicles as noted by Babel (1967) for to the lack of baffle plates associated with U. halleri. Hamlett et al. (1999c) reported both egg investment (this region of the OG in degeneration of atretic preovulatory follicles U. jamaicensis has been referred to as baffle and corpus luteum formation are observed zone equivalent) and a terminal zone is with an outer layer of vascularized thecal entirely absent (Hamlett et al. 1996a; 1998; cells surrounding a collapsed layer of lipid- 1999a). However, Fahy (unpublished) has rich granulosa cells. Babel (1967) mentioned repeatedly observed the presence of an iso- that large degenerate ova are often mistaken lated thin membranous casing from uteri for corpora lutea.Heproposedthatcorpora with recently ovulated eggs. Therefore, some lutea are derived solely from hypertrophy of form of a short-lived egg covering is likely theca externa cells within the collapsed folli- produced and warrants further investigation cle, whereas follicular folds and theca interna of OG structure and function in Urobatis.The tissue remain with the ovulated ovum. Thus, OG is typically considered the site of fertiliza- two distinct thecal layers (theca interna and tion (upper OG or uterine tube) and sperm theca externa) are observed for U. halleri, in storage (terminal zone) in elasmobranchs; contrast to the uniform layer of vascularized however, the unconfirmed egg investiture thecal cells reported for U. jamaicensis and lack of terminal zone storage tubules in (Hamlett et al. 1999c). The remaining female U. jamaicensis areuniquefeatures. reproductive tract (anteriad to posteriad) con- sists of paired ostia, uterine tubes, oviducal Maternal Anatomy glands, and uteri (Hamlett and Koob 1999; and Fetal Development Fahy et al. 2007). A common ostium is fused ventrally over the esophagus, with two later- In Urobatis, both uteri are functional, but ally distinct ostial openings (longitudinal with a unilateral dominance of the left slits) corresponding to individual uterine uterus (LaMarca 1961; Babel 1967; Fahy et al. tubes (anterior oviducts). Each uterine tube 2007). Uterine morphology corresponds with lumen is continuously disrupted into exten- mode of reproduction and the most signifi- sive longitudinal folds with ciliated columnar cant modification observed is the endometrial epithelium, interspersed with secretory cells proliferation of villous extensions, termed that often form basal secretory acini (Fahy, trophonemata. Like all myliobatiforms, in unpublished). Posteriorly, uterine tubes even- U. jamaicensis matrotrophic input of histotroph tually transition into slightly enlarged, bell- is supplied via trophonemata (termed, lipid shaped oviducal glands (LaMarca 1961; histotrophy) that provisions developing Hamlett and Koob 1999; Fahy et al. 2007). embryos beyond the initial egg investiture Typically, four histologically distinct zones (Hamlett 1986; Hamlett and Koob 1999; Hamlett et al 2005b, c). Corrosion casting (club, papillary, baffle, and terminal zones) (Basten 2007) confirmed the basic vascular characterize oviducal gland (OG) structure of structure noted with previous histological elasmobranchs. However, two visually dis- observations (LaMarca 1961; Hamlett and crete zones are grossly discernable from OG Hysell 1998; Hamlett et al. 2005b). A central in U. jamaicensis with further corroboration of artery bifurcates into two arterioles that run zonation from histochemical analyses (secre- parallel to each other down the edges of each tory granules are PAS (+) in anterior tubules villus and ramify into a capillary bed at the and PAS (-) in posterior tubules) (LaMarca distal end of the villus. The villus is com- 1961). The simplified OG of U. jamaicensis is prised of a network of web-like capillaries composed of a series of parallel tubular that wrap around the peripheral arterioles glands with secretory activity increasing and throughout the center of the villus. The adluminal and posteriad within the organ arterioles feed these capillaries through a (Hamlett et al. 1996a; 1998; 1999a; 2005a). series of connections along their length. Recently, Hamlett et al. (2005a) have reported Venous blood passes from capillaries into that the highly modified OG of U. jamaicensis collecting venules that channel blood into does not have club or papillary zones, thus the axial vein. While there does appear to be the ability to produce egg jelly is lost. Like- some variation in the density of the capil- wise, there is no egg-envelope produced due laries among trophonemata, no correlation A REVIEW OF UROBATIS JAMAICENSIS BIOLOGY 85 has been found between capillary density or Reproductive Cycle vessel shape and gestational stage (Basten The reproductive cycle of U. jamaicensis 2007). These observations may be indicative in coastal waters of South Florida has been of consistent development of trophonemata examined with field observations and in U. jamaicensis,associatedwithrepetitive monthly collections (Fahy 2004; Fahy et al. pregnancies throughout a female’s entire 2007; Fahy unpublished). Gravid females adult life. Dasyatis americana trophonemata, are visually conspicuous, displaying a con- have a transition from small capillaries with vex dorsum often with apparent movement overlying cuboidal epithelium during early of term-stage young. For short periods gestation to enlarged sinusoidal capillaries postpartum there is an obvious depression with simple squamous epithelium during or dorsal concavity with the skin stretched term stages (Hamlett et al. 1996b). The and loose in appearance. Gravid females enhanced vascularization combined with were observed year round, with two con- decreasing gas diffusion distances, were cor- secutive peaks in reproductive activity. related with increased oxygen demands of Examination of the reproductive tract indi- developing fetuses. Trophonemata secrete cated a protracted period of ovulation from uterine fluids (histotroph) composed of a January to April, and a second, more high organic content as nourishment for restricted, period of ovulation during developing embryos (Hamlett et al. 1993; August/September. The mean monthly 1996b; 2005c). However, ultrastructural com- peaks in maximum ovum diameter (MOD) parisons of secretory crypts of trophonemata corresponded with both periods of peak between near term D. americana and U. ovulation (Fahy unpublished). Addition- jamaicensis displayed dramatically fewer ally, all females observed midway through lipid droplets in Urobatis (Hamlett et al. both gestation periods (May and October, 2005c). Additional comparisons of the bio- respectively) were pregnant with subse- chemical composition of histotroph also quent periods of parturition between June demonstrated considerable differences: pro- and September (with a late July/early tein size (56.2 kDa and 85.6 kDa), protein August peak) and again between Novem- concentration (20.6 mg/ml and 9.5 mg/ml), ber and January. The bimodal overlap in total lipid content (3 mg/g and <0.5 mg/g), embryonic development with concurrent lipid composition (primarily triglycerides vs. vitellogenesis is further supportive of a primarily phospholipids), and fatty acid con- biannual reproductive cycle (Fahy et al. tent (ratio of saturated to unsaturated fatty 2007). Male stingrays exhibited maximal acids, 1: 1.5 and 12.5: 1) in D. americana and testicular development (i.e., elevated GSI U. jamaicensis,respectively(Hamlettetal. and prominent testicular lobes) 1-2 months 2005c). The lesser degree of lipid histotrophy prior to each ovulatory peak. This timing demonstrated by U. jamaicensis in compari- also corresponded with an increased occur- son with D. americana is noteworthy, since rence of female copulatory bite marks. The comparable levels of embryonic develop- increased prevalence of bite marks on post- ment are reported for both species (Hamlett partum females is suggestive of mating et al. 1996a; Hamlett et al. 2005c; Fahy et al. events closely following parturition sim- 2007). Preliminary wet weight determina- ilar to D. americana (Henningsen 2000; tions indicated U. jamaicensis is highly Chapman et al. 2003). matrotrophic with an approximate 4,600% A gestation rate of 5-6 months was increase in weight from mature ova to term observed for U. jamaicensis in South Florida fetus. This increase exceeds that reported for with a transitional overlap occurring between D. americana (3,750%) (Hamlett et al. 1996b; both cycles (i.e. ovulation and gestation) Fahy et al. 2007). Ongoing research is cur- (Fahy et al. 2007). There has been a previous rently examining the histotroph composition estimate of a 3-month gestation rate for and structure of trophonemata throughout U. jamaicensis; however, this was based upon gestation to clarify how U. jamaicensis Babel’s (1967) observed patterns for the con- achieves these results with a seemingly gener U. halleri (Hamlett 1999). Variable dilute histotroph. reports of maximum fecundity (3-5) for 86 R.E. SPIELER, ET AL.

U. jamaicensis have persisted throughout the months (LaMarca 1961; Yan˜ez-Arancibia and literature (Bigelow and Schroeder 1953; Amezcua-Linares. 1979; Young 1993; Piercy Hamlett 1999; McEachran and de Carvahlo et al. 2006b). LaMarca (1961) reported 2002, Piercy et al. 2006b). Recently, Fahy et al. that ovulation of U. jamaicensis in Bimini, (2007) reported a maximum uterine fecundity Bahamas, occurs over a wide period during (combined contents of both functional uteri) “early months of the year” (based upon of seven offspring. Brood size increased with ovarian condition and uterine embryo maternal size and was significantly higher sizes), with parturition occurring during during the spring/summer reproductive summer months (with mention of a single  cycle (X =3.1Æ 0.179 SE, range 1-7) compared term pup delivered during the month of  to the autumn/winter cycle (X =1.4Æ 0.110, March). Likewise, Piercy et al. (2006b) range 1-3) (Fahy et al. 2007). This seasonal reported parturition during the months of variation in uterine fecundity is further sup- June through August in the Bahamas. portive of a biannual cycle, rather than differ- Young (1993) proposed peak mating occurs ences in the reproductive cycles of separate during February/March in Belize, based on breeding populations. The transition from copulatory observations. Yan˜ez-Arancibia the initial cycle (both uteri typically active) to and Amezcua-Linares (1979) reported par- the second, less fecund cycle (only left uterus turition in the southern Gulf of Mexico typically active) is often represented by pres- occurred from May to October. Thus, most ence of ova in the left uterus and the right studies are in agreement on the timing of the uterus distended from recent parturition (D. initial reproductive cycle of U. jamaicensis. Fahy unpublished). However, additional work is required to Although both male and female U. verify the occurrence of a second cycle in jamaicensis exhibit biannual cycles of game- other portions of the species range. togenesis and breeding activity in South Florida, reproductive cycles among sting- Natural History rays vary with geographic location. Likely, Activity Patterns annual cycles involve various environmen- tal signals (i.e., temperature, salinity) as In general, U. jamaicensis have a demersal suggested for other species, to establish lifestyle. They are most often seen in sta- steroidogenic regulation of vitellogenesis, tionary positions and when seen moving it folliculogenesis, and gametogenesis and the is for short distances and less than a meter associated behavioral characteristics (Babel above the substrate (authors unpublished). 1967; Thorson 1983; Charvet-Almeida et al. Swimming appears to be done primarily by 2005; White and Dharmadi 2007; Mull et al. undulation of their pectoral fins, a locomo- 2008; Pierce et al. 2009). Reproductive peri- tory style displayed by other demersal odicity of the congener U. halleri is a well batoids (Rosenberger 2001; Schaefer and defined annual cycle among male stingrays Summers 2005; McComb and Kajiura 2008). with conflicting reports of synchronous Because the animals display nocturnal and asynchronous annual ovulatory cycles activity (see below), and most diving (and among females (Babel 1967; Mull et al. thus most sightings) is during the daylight 2008). Closely related species (Urotrygon hours, it may be that animals exhibit a spp.) with a more tropical distribution have pelagic behavior at night. However, all not displayed well-defined cycles (Tellez observations at nighttime are also consis- et al. 2006; Mejı´a-Falla and Navia 2007). tent with a demersal lifestyle (Fahy 2004). Studies in South Florida on U. jamaicensis In addition, U. jamaicensis have a lower (Fahy et al. 2007) were accomplished near hepato-somatic index than a pelagic sting- the northern extent of the species range. ray, a relatively low binocular overlap in Additional observations from several locales the horizontal visual field, and low lipid have also indicated that the primary repro- content in the chondocranium; all of these ductive season occurs from February to are adaptations associated with a demer- July; however, data collections from these sal lifestyle (Phleger 1988; Sherman and studies appear biased towards summer Gilliam 1996; McComb and Kajiura 2008). A REVIEW OF UROBATIS JAMAICENSIS BIOLOGY 87

Several recent studies, of other batoids, attachment to shallow water habitats using active tracking, passive monitoring (P. Lobel, personal communication). How- techniques and archival tags have estab- ever, intermittent tracking (over 2-7 days) lished long-term site fidelity, repetitive of several animals indicates U. jamaicensis seasonal movements or extensive periods activity spaces may be larger with animals of residency within limited areas (Hunter only using portions of their full range on a et al. 2005; Collins et al. 2007; Dewar et al. daily basis (Fahy 2004). Similarly, for U. 2008; Le Port et al. 2008). However, short- halleri in Southern California, patterns of term movements and seasonal patterns of sedentary behavior, with little movement, U. jamaicensis distribution have only been interspersed with periods of elevated activ- examined in a limited portion of the spe- ity were observed throughout the day. How- cies range (Sulikowski 1996; Fahy 2004). In ever, at night this activity was correlated South Florida, U. jamaicensis are perma- with ebbing tides and the influence of a nent residents throughout the year and heated effluent (Vaudo and Lowe 2006). Addi- primarily associated with hardbottom and tionally, U. halleri has been reported to move reef habitats (Sulikowski 1996; Fahy 2004). substantial distances (>30 km in 3 months) Movements over open sandy bottoms are after release (Russell 1955; Babel 1967; Vaudo highly directed transitions between adjacent and Lowe 2006). reef sites or brief forays with a subsequent In the Fahy (2004) study, bottom topog- return to previous hardbottom habitats (Fahy raphy had considerable influence on the unpublished).However,literaturefromother space utilization of U. jamaicensis, and locations has emphasized the importance movements varied with location in relation of seagrass habitats for pupping (Yanez- to proximity from the reef edge/sand Arancibia and Amezcua-Linares 1979; Piercy interface. Animals centrally located within et al. 2006b). consistent hardbottom displayed meander- Fahy (2004) examined the activity pat- ing movement patterns and continually terns and space utilization of U. jamaicensis returned to core areas. In contrast, sting- in coastal waters of southeast Florida via rays situated along the reef/sand interface active tracking of 17 adult stingrays. Sting- traveled along more linear pathways as rays were captured with handnets via defined by reef characteristics. Although SCUBA from shallow inshore hardbottom detailed analysis of habitat selection was communities in water ranging from 3-15 m not conducted, an apparent preference for of depth. Animals were anesthetized and hardbottom substrate was observed from tagged with external telemetry transmitters tracking data locations and by direct obser- attached by sutures to the epaxial muscula- vations during extended periods of inactiv- ture. After revival the stingrays were ity (Fahy 2004). However, longer term immediately returned to capture locations studies are necessary to determine the and monitored with a tracking receiver and repeatability of diel movements across directional hydrophone. Animals were multiple days to verify patterns of resi- tracked continuously for periods ranging dency and habitat utilization. Future active from (2-28 h); eight individuals were tracking, coupled with passive monitoring tracked for a full diel cycle (24 h). Activity techniques, would better establish the level spaces for both 95% Kernel Utilization Dis- of site fidelity displayed by U. jamaicensis tributions (KUD) and 50% KUD core areas and potentially characterize the existence were significantly larger during nocturnal of a home range. periods. Total (24 h) KUD were representa- Seasonal distribution was assessed to tive of confined activity spaces (mean = determine population residency within the 0.02 km2 +/– 0.01 SE) with linearity indices study site and ascertain the occurrence and and random walk analyses further demon- temporal patterns of onshore/offshore move- strating strong site attachment. Similarly, ments (Fahy 2004). Data on U. jamaicensis active tracking conducted in Belize demon- were extracted from several stationary visual strated short-range movements with fur- fish count studies (over 700 point counts) in ther evidence of a high degree of site Broward County, Florida, from January 1998 88 R.E. SPIELER, ET AL. to December 2003 and combined to deter- reef, hardbottom, and sea grass. They will mine abundance on each of the three coral- also bury themselves completely on sandy reef tracts (Baron et al. 2004; Ferro et al. 2005). bottoms and may lie concealed under rock The tracts lie parallel to the coast in progres- ledges (Fig. 1). When on the substrate they sively deeper water with increasing dis- often sit with the rostral portion of the disk tances from the shoreline. Data from these raised forming a cave-like area. It has been studies were tested for monthly and seasonal suggested this behavior is related to feed- differences as well as differences among reef ing and is used to attract invertebrates tracts. Analysis of seasonal distribution seeking refuge (Robins et al. 1986). How- established population residency was year- ever, we are unaware of any reports round with no indication of offshore emigra- documenting feeding from this position tion associated with water temperature or and startled rays will often swim away other environmental factors. However, this from a stimulus (e.g., diver) and assume conclusion requires further study as the the caving posture immediately on alight- Baron et al. (2004) and Ferro et al. (2005) stud- ing to the substrate. This might indicate the ies were concentrated on fish assemblages at behavior is related to respiration, but this hardbottom areas and were not designed requires further studies (Summers and specifically for addressing inshore/offshore Ferry-Graham 2001). movement. Thus, adjacent sand habitats were not sampled and may have been pre- Trophic Position ferred at different times of the year. Datasets on population structure from sev- U. jamaicensis, like its congener U. halleri, eral studies (Baron et al. 2004; Ferro et al. apparently obtains buried prey by 2005) and chance encounter/collecting data burrowing with its pectoral fins (Bigelow (Fahy unpublished) were analyzed in order and Schroeder 1953; Babel 1967). Mulvany to examine sexual segregation and ontoge- and Motta (2009) found U. jamaicensis and netic partitioning. The sex ratio was com- D. sabina would swim over presumably pared for differences monthly, seasonally, exposed live or dead prey and, using the and between reef tracts. Only spring obser- anterior pectoral fin margin, trap and repo- vations (March through May) evidenced a sition prey between the substrate and their statistically significant difference from a 1:1 body. Once the prey was near the mouth, ratio when females dominated the inshore ingestion was accomplished using suction visual observations (2.5F:1M; n=28). This and biting. observation of seasonal segregation was Bigelow and Schroeder (1953) reported that likely associated with the reproductive cycle the stomach of one specimen of U. jamaicensis (see below), as most females recorded during contained shrimp (Penaeus brasiliensis)andthe this period (15/20) were actively gestating. stomach of another contained bottom detri- Although few neonates were recorded in the tus. Yanez-Arancibia and Amezcua-Linares datasets, most observations occurred in shal- (1979), working in the Terminos Lagoon sys- low inshore water (< 6 m depth), suggesting tem in the Mexican province of Campeche, a nearshore pupping area with no indication examined the stomachs of 16 adult of an established nursery area as defined by U. jamaicensis; 11 (68.8%) had contents; the Heupel et al. (2007). Increased abundance remainder had empty stomachs. They and presence on the offshore reef among reported yellow stingrays consume different intermediate size classes (250-299 mm to types of crustaceans, polychaetes, mollusks, 300-349 mm) suggests a potential ontoge- amphipods, and stomatopods. The primary netic shift to deeper water by sub-adults food consisted of polychaetes, crustaceans, (Fahy 2004). and mollusks, with these three groups representing up to 82% of the diet. Quinn (1996) examined 31 U. jamaicensis Refuge throughout the year in South Florida. Their Cryptic coloration makes the animals dif- diet consisted primarily of polychaetes, crus- ficult to see in their natural habitats of coral taceans, nemerteans, sipunculids, nematodes, A REVIEW OF UROBATIS JAMAICENSIS BIOLOGY 89 and chaetognaths, with polychaetes and sonal communication). Although there are crustaceans comprising 67% of the stomach apparently no predators specializing on yel- contents by volume. Most of the remain- low stingrays we suspect they are com- ing stomach content volume consisted of monly taken by generalist fish, and possibly digested organic matter and unidentified bird, piscivores (Banks and Bostic 1966). vermiforms. There was no apparent differ- ence in diet between sexes, and seasonal Age and Growth changes in diet appeared to be limited to an increase in the proportion of polychaetes Sulikowski (1996) did some prelimi- found in the stomach during spring com- nary age and growth determinations on pared to fall. At the present, we are not U. jamaicensis. He looked at alizarin red aware of any studies on seasonal polychaete stained vertebral centra of 20 yellow stingrays abundances in South Florida. However, and examined opaque and translucent bands there are reports, from other areas, that of the corpus calcareum. He found a linear rela- suggested changes in polychaete abun- tionship exists between centrum diameter dance were correlated with changes in the and total length making this structure useful diet of demersal fishes (Nishikawa et al. 2000). for age estimation. Using marginal increment In conjunction with other, non-feeding- analysis and the von Bertalanffy growth related, studies it has been noted that equation he concluded the animals are rela- U. jamaicensis have also ingested dusky jawfish tively short-lived, 7-8 years maximum, and (Opistognathus whitehursti), a small (< 10 cm) achieve most (80%) of their annual growth tunnel/cave dweller (Fahy unpublished). during late spring through summer months. Similarly, Babel (1967) reported that bivalves, A study currently underway with a larger polychaetes, and crustaceans composed over sample size (100+ animals) likewise draws 94%ofthetotalfoodcontent,byvolume,for theconclusionofamaximumlifespanof7- U. halleri; however, bivalves were the most 8 years (B. Buskirk unpublished). A similar important single food class. In contrast, conclusion of an 8-year lifespan was reached Valadez-Gonza´lez et al. (2001) reported for congener U. halleri (Babel 1967); but other U. halleri fed primarily on stomatopods, crus- studies on that animal assessed the maximum taceans, and to a lesser extent on polychaetes age at 13-14 years (Hale et al. 2006; Hale and and fishes. The samples sizes for the stomach Lowe 2008). Not surprisingly for a short-lived content data of U. jamaicensis are small and animal, U. jamaicensis grow rapidly during caution should be taken in their interpreta- the first year of life. Approximately 150 mm tion. Nor are we aware of any studies on onto- TL at birth, they attain 200 mm TL by the geneticshiftsindietintheseanimals. second year (Yanez-Arancibia and Amezcua- Nonetheless, the differences among the diets Linares 1979; Sulikowski 1996; Basten 2007). in these studies lead us to conclude that at Yanez-Arancibia and Amezcua-Linares (1979) least these two urotrygonids are generalists have estimated U. jamaicensis is mature at and likely opportunistic feeders. 200 mm TL. However, LaMarca (1964) found Information on the predators of U. the smallest male with masses of spermato- jamaicensis is sparse. Nassau grouper, zoa in the intra-septal spaces of the seminal Epinephelus striatus, and lemon sharks, vesicle was 137 mm disk width (DW) (about Negaprion brevirostris, are mentioned in the 265 mm TL), and it was unclear if males were literature (Silva Lee 1974; Cortes and Gruber reproductively active until slightly larger. In 1990) and they have been found among the females, size at maturity still needs to be con- gut contents of other fishes (i.e., black grou- firmed by histological analysis of the repro- per, Mycteroperca bonaci; B. Buskirk, personal ductive tract (e.g. developed trophonemata) communication). U. jamaicensis has been as maternal indices are better estimates of the observed in the stomach contents of a female reproductive state than maturity Centrophorus sp. in deep waters off the determined solely by ovarian development northern coast of Jamaica. This is intriguing (Walker 2005). For example, in our studies as Centrophorus sp. were only collected at the smallest female observed in maternal depths of 450 m or greater (J. Morrissey per- condition measured 158 mm DW with a 90 R.E. SPIELER, ET AL. single 158 mm TL male embryo (Fahy et al. ing copulation (Dugger 1987); however, 2007). This is comparable in size to the due to Dugger’s (1987) initial misidenti- smallest gravid female (149 mm DW) of fication of the sexes this behavior requires U. halleri in Babel’s (1967) study. additional confirmation. Furthermore, the female’s need to bite and to effectively Courtship maintain a grasp during coitus is question- able due to sex-specific tooth morphology. There is apparently little written about We found no reports of studies examining courtship behavior in U. jamaicensis. Issues the possible effects of male biting on female of attraction, rejection, or acceptance are reproductive behavior (i.e., enhancing recep- obviously dealt with by this species, but it tivity) or physiology (i.e., stimulating repro- is unclear how. We have observed females ductive processes). Because biting appears to fleeing from males, as well as ganging invariably be associated with copulation, this behavior, where multiple males attempt to may be a fertile area for research. mate with a single female. It is also appar- ent that there is some attractant, likely pher- omonal, emitted by the females, as males Pupping and Nursery Habitat will converge from a distance on a female. Specific requirements of the nursery habi- Equally likely, electroreception is used for tat of U. jamaicensis are unclear. Nearshore short-distance orientation as it is in U. halleri pupping is apparent, but the cryptic nature (Sisneros and Tricas 2002). We assume the and small size of neonates has made for few mating drive in males is strong, as we have field observations. In the Terminos Lagoon noted, on several occasions, a recently cap- (Campeche, Mexico), U. jamaicensis is consid- tured male attempting to copulate with a female while both were contained in a small ered rare throughout most of the year; how- mesh dive bag carried by a diver. However, ever increased prevalence of gestating other than what can be inferred from these females and neonates during the rainy season anecdotal observations, nothing is known (May–October) in seagrass has suggested the about the proximal physiological mecha- importance of this habitat as a primary pup- nisms involved in copulation. ping area (Yan˜ez-Arancibia and Amezcua- Linares 1979). Parturition has also been observed in seagrass beds in the Bahamas Copulatory Behavior (Piercy et al. 2006b). Interestingly, small The copulatory behavior of U. jamaicensis aggregations of predominantly gestating is typical of most stingrays (McCourt and females have also been observed beneath Kerstitch 1980; Dugger 1987; Young 1993; mangrove trees (apparently only those occu- Nordell 1994; Chapman et al. 2003). Male pied by nesting egrets) during summer individuals orally grasp a female’s pectoral months in Jamaica (J. Morrissey perso- margin and rotate to a ventrum to ventrum nal communication). In Broward County, position and insert the ipsilateral clasper Florida, where there is minimal seagrass or into the female’s cloaca. The male bite and mangroves at the shoreline, pregnant females hold is forceful and mating wounds and and neonates of U. jamaicensis are found on scars are common on the pectoral margin hardbottom habitat. Together, these observa- of females. Multiple males are often seen tions appear to indicate some aspect of shal- crowding mated pairs or exhibiting follow- low nearshore habitat in general, rather than ing behavior (Dugger 1987; Young 1993; a specific habitat type (e.g., seagrass, man- authors unpublished), suggestive of the grove, hardbottom) is required for pupping. polyandrous breeding strategy exhibited However, more data are required to conclu- by D. americana (DeLoach 1999; Chapman sively determine the existence of a nursery et al. 2003). Young (1993) reported copula- area for this animal. tion is brief (4 min) with similar reports for congeners U. concentricus (McCourt and Anthropogenic Interactions Kerstitch 1980) and U. halleri (Nordell 1994). Female U. jamaicensis have also been There is little literature dealing directly reported to simultaneously bite males dur- with human/U. jamaicensis interaction. A REVIEW OF UROBATIS JAMAICENSIS BIOLOGY 91

Because of the stingray’s abundance in some within the fetal spiral valve intestine has inshore areas there are multiple reports of assisted in staging developing embryos U. jamaicensis injuring bathers and fishers (Harms et al. 2004). These radiographic fea- (Bigelow and Schroeder 1953). Possibly in tures are prominent during early stages some areas (e.g., Broward County, Florida; and diminished in term stage fetuses. Jamaica) the high abundance of U. jamaicensis Tonic immobility (TI) can be induced in is related to a paucity of large benthic many animals, including elasmobranchs, piscivores due to overfishing (Ferro et al. and can be used as an aid in some sampling 2005), this contention receives a measure of procedures (e.g., body measurements, tak- support from the fact that the dramatic ing blood or tissue samples). There is one decrease in U. jamaicensis in the Florida Keys report on tonic immobility in elasmo- over a 14 year span can be correlated to an branchs that included a preliminary exami- increase in population of Goliath grouper, nation of urotrygonids. The author was Epinephelus itajara, (Ward-Paige et al. 2010). able to induce tonic immobility in a single However, other possible anthropogenic fac- male specimen of U. halleri by placing the tors cannot be discounted for changes in animal in a horizontal inverted position, U. jamaicensis abundances e.g., habitat destruc- but was not successful in inducing TI in a tion, harvest (Ward-Paige et al. 2010). female U. jamaicensis (Henningsen 1994). There is one study that used U. jamaicensis However, as the author pointed out, this is as the experimental animal for bioassay of too small of a sample size to draw firm Tributyltin oxide (TBTO). TBTO is the main conclusions and more research is required. constituent of tin-based antifouling marine paint used on the hulls of ships to prevent Conclusion the growth of fouling organisms. This study investigated the toxicity and accumulation Urobatis jamaicensis is a small batoid with of tin in the gill tissue of U. jamaicensis after a widespread range within the greater acute exposure to TBTO. Results indicated Caribbean area; it is relatively abundant in U. jamaicensis are hypersensitive to TBTO patchy distribution and is relatively easy to exposure. The gills showed a distorted, maintain in captivity. These characteristics, swollen epithelium with exfoliation following among others, make it a good research sub- acute exposure to as little as 0.05 mg/L TBTO ject. When the problems of captive breeding and tissues of treated animals contained a sig- are resolved, this animal, with its rapid nificantly increased tin concentration as com- breeding cycle, should provide an excellent pared to controls. There was also evidence of model in efforts to understand elasmobranch induction of the stress proteins Hsp 70 and functional morphology and behavior. HO1. 4-Hydroxynonenol (4HNE) and adduct The studies cited here offer some insight formation evidence that membrane degrada- into the natural history, ecology, nervous/ tion was a result of lipid peroxidation sensory system, respiration, reproduction, (Dwivedi and Trombetta 2006). Because vasculature, osmoregulation, and digestion U. jamaicensis appears to be relatively seden- of U. jamaicensis. We were able to find little, tary, not migratory, and found abundantly in if any, literature on a number of organ sys- some near-shore environments, it may prove tems in U. jamaicensis (i.e., skeletal, muscu- to be a likely candidate to examine biological lar, endocrine, and immune systems) and uptake of onshore generated pollutants. for these we refer the reader to the general, Captive breeding of U. jamaicensis has or system-specific, literature on batoids occurred, but with limited survival of off- and elasmobranchs. spring due to unsuccessful parturition and high rates of neonate mortality. Several Acknowledgements.—We thank the many procedures have been incorporated to man- students of the Oceanographic Center who ually and pharmacologically induce partu- have aided us in field and laboratory stud- rition (Stamper et al. 1998; Hanna 2004; ies of the yellow stingray over the years Harms et al. 2004). The novel use of radio- and an anonymous reviewer who provided opaque concretions (calcium apatite) stored extensive critical and insightful comments 92 R.E. SPIELER, ET AL. on an earlier draft of this paper. Funding of W. C. Hamlett, 174-197. Baltimore: The Johns our stingray studies has come from diverse Hopkins University Press. sources but primarily from: the National Botte, V., G. Chieffi, and H. P. Stanley. 1963. Histolog- ical and histochemical observations on the male Coral Reef Institute (NCRI), the Guy Harvey reproductive tract of Scyliorhinus stellaris, Torpedo Research Institute and NSU President’s marmorata and T. torpedo. Pubbl. Staz. Zool. Napoli Faculty Research and Development Grants. 33:224-242. This is publication number 112 of the NCRI. Carlson, S. R., and L. Goldstein. 1997. Urea transport across the cell membrane of skate erythrocytes. J. Exp. Zool. 277:275-282. References Casper, B. M., and D. A. Mann. 2006. Evoked potential audiograms of the nurse shark (Ginglymostoma Acevedo, K., J. Boho´rquez-Herrera, F. Moreno, C. cirratum) and the yellow stingray (Urobatis Moreno, E. Molina, M. Grijalba-Bendeck, and P. jamaicensis). Environ. Biol. Fish. 76:101-108. Go´mez-Canchong. 2007. Tiburones y rayas Chapman, D. D., M. J. Corcoran, G. M. Harvey, (Subclase Elasmobranchii) descatados por la flota S. Malan, and M. S. Shivji. 2003. Mating behavior de arrastre camaronero en el Caribe de Columbia. of southern stingrays, Dasyatis americana (Dasyatidae). Acta Biol. Columb. 12(2):69-80. Environ. Biol. Fish. 68:241-245. Ashley, L. M., and R. B. Chiasson. 1988. Laboratory Charvet-Almeida, P., M. L. Goes de Araaujo, and M. anatomy of the shark (5th ed.). Dubuque: Wm. C. Pinto de Almeida. 2005. Reproductive aspects of Brown Publishers. freshwater stingrays (Chondrichthyes: Potamotry- Babel, J. S., 1967. Reproduction, life history, and ecol- gonidae) in the Brazilian Amazon basin. J. North- ogy of the round stingray, Urolophus halleri,Cooper. western Atlantic Fish. Sci. 35:165-171. Calif. Fish Game, Fish. Bull. 137. Collins, A. B., M. R. Heupel, and P. J. Motta. 2007. Banks, R. C., and D. L. Bostic. 1966. A record of sting- Residence and movement patterns of cownose rays ray predation by the brown pelican. Condor. 68(5): Rhinoptera bonasus within a south-west Florida 515-516. estuary. J. Fish Biol. 71:1159-1178. Baron, R. M., L. K. B. Jordan, and R. E. Spieler. 2004. Cortes, E., and S. H. Gruber. 1990. Diet, feeding habits Characterization of the marine fish assemblage and estimates of daily ration of young lemon associated with the nearshore hardbottom of sharks, Negaprion brevirostris (Poey). Copeia 1990(1): Broward County, FL, USA. Estuar. Coast. Shelf S. 204-218. 60(3):431-443. Daniel, J. F., 1934. The Elasmobranch Fishes (3rd ed.). Basten, B. L., 2007. The microvascular anatomy of fetal Berkeley: University of California Press. respiration in the U. jamaicensis (Urobatis DeLoach, N., 1999. Reef Fish Behavior: Florida, jamaicensis). (M.S. Thesis) Nova Southeastern Uni- Caribbean, Bahamas. Jacksonville: New World Pub- versity Oceanographic Center, Dania Beach, Florida, lications, Inc. USA. 75pp. Dennis, G. D., D. Hensley, P. L. Colin, and J. J. Basten, B. L., R. L. Sherman, A. Lametschwandtner, Kimmel. 2004. New records of marine fishes from A., and R. E. Spieler. 2007. A unique arterial anas- the Puerto Rican Plateau. Caribb. J. Sci. 40(1):70-87. tomosis among the efferent epibranchial arteries Dennis, G. D., W. F. Smith-Vaniz, P. L. Colin, D. A. and the dorsal aorta in the yellow stingray, Hensley, and M. A. McGhee. 2005. Shore fishes Urobatis jamaicensis: a preliminary examination. from islands of the Mona Passage, Greater Antilles Microsc. Microanal. 13(Suppl 2):498-499. with comments on their zoogeography. Caribb. J. Basten, B. L., R. L. Sherman, A. Lametschwandtner, Sci. 41(4):716-743. and R. E. Spieler. 2009. A unique vascular configu- Dewar, H., P. Mous, M. Domeier, A. Muljadi, J. Pet, ration among the efferent branchial arteries and and J. Whitty. 2008. Movements and site fidelity of splanchnic arteries in the yellow stingray, Urobatis the giant manta ray, Manta birostris, in the Komodo jamaicensis. Microsc. Microanal. 15(3):194-196. Marine Park, Indonesia. Mar. Biol. 155:121-133. Bigelow, H. B., and W. C. Schroeder. 1953. Fishes of the Donald, J. A. 1988. The innervation of the gills of the Western North Atlantic. Sawfishes, guitarfishes, stingarees Urolophus mucosus and U. paucimaculatus skates, rays and chimaeroids. Memoirs of the Sears (Urolophidae, Elasmobranchii). Comp. Biochem. Foundation for Marine Research 1(2):416-427. Physiol. 90C:165-171. Bo¨hlke, J. E., and C. C. G. Chaplin. 1993. Fishes of the Dugger, A. J., 1987. Mating stingrays. Sea Frontiers Bahamas & Adjacent Waters (2nd ed.). Austin, TX: 33:352-354. University of Texas Press. Dwivedi, J., and L. D. Trombetta. 2006. Acute toxicity Bone, Q. and N. B. Marshall. 1992. Buoyancy. In Biol- and bioaccumulation of tributyltin in tissues of ogy of Fishes, eds. Q. Bone, and N. B. Marshall, 63- Urolophus jamaicensis (Yellow Stingray). J. Toxicol. 81. Glasgow: Blackie Academic and Professional, Env. Heal. A 69(14):1311-1323. an imprint of Chapman and Hall. Fahy, D. P. 2004. Diel activity patterns, space utiliza- Butler, P. J. 1999. Respiratory System, In Sharks, Skates, tion, seasonal distribution and population struc- and Rays: The Biology of the Elasmobranch Fishes, ed. ture of the yellow stingray, Urobatis jamaicensis A REVIEW OF UROBATIS JAMAICENSIS BIOLOGY 93

(Cuvier, 1817) in South Florida with comments on Fishes, ed. W. C. Hamlett, 444-470. Baltimore: The reproduction. (M.S. Thesis) Nova Southeastern Johns Hopkins University Press. University Oceanographic Center, Dania Beach, Hamlett, W. C., A. M. Eulitt, R. L. Jarrell, and M. A. Florida, USA. Kelly. 1993. Uterogestation and placentation in Fahy, D. P., R. E. Spieler, and W. C. Hamlett. 2007. elasmobranchs. J. Exp. Zool. 266:347-367. Preliminary observations on the reproductive cycle Hamlett, W. C., and M. K. Hysell. 1998. Uterine special- and uterine fecundity of the yellow stingray, Urobatis izations in elasmobranchs. J. Exp. Zool. 282:438-459. jamaicensis (Elasmobranchii: Myliobatiformes: Hamlett, W. C., M. Hysell, M. Jezior, T. Rozycki, N. Urolophidae) in Southeast Florida, U.S.A. Raffles B. Brunette, K. Tumilty. 1999a. Fundamental zonation Zool. suppl. 14:131-139. in elasmobranch oviducal glands. In Proc. 5th Indo- Feduccia, A., and B. H. Slaughter. 1974. Sexual dimor- Pac. Fish Conf., Noume´a, 1997, eds. B. Se´ret, and J. Y. phism in skates (Rajidae) and its possible role in Sire, 271-280. Paris: Soc. Fr. Ichtyol. differential niche utilization. Evolution 28:164-168. Hamlett, W. C. M. K. Hysell, T. Rozycki, N. Brunette, Ferro, F. M., L. K. J. Jordan, and R. E. Spieler. 2005. K. Tumilty, A. Henderson, and J. Dunne. 1999b. Spatial variability of the coral reef fish assemblages Sperm aggregation and spermatozuegmata forma- offshore Broward County, Florida. NOAA Tech. tion in the male genital ducts in the clearnose Memo. NMFS-SEFSC-532. skate, Raja eglanteria.InProc. 5th Indo-Pac. Fish Fowler, H. W. 1945. A study of the fishes of the south- Conf., Noume´a, 1997, eds. B. Se´ret, and J. Y. Sire, ern piedmont and coastal plain. Acad. Nat. Sci. 281-291. Paris: Soc. Fr. Ichtyol. Phila., Monogr. 7 (401pp, citation is on page 265). Hamlett, W. C., M. Jezior, and R. Spieler. 1999c. Ultra- Gardner, S. L., and G. D. Schmidt. 1984. Discobothrium structure analysis of folliculogenesis in the ovary caribbensis sp. N., a Lecanicephalidean cestode of the yellow spotted stingray, Urolophus jamaicensis. from a yellow-spotted stingray, Urolophus jamaicensis, Ann. Anat. 181:159-172. in Jamaica. J. Parasitol. 70(2):303-304. Hamlett, W. C., D. P. Knight, M. Jezior, K. Kamm, and Gilbert, S. G. 1993. Pictorial anatomy of the Dogfish. K. Mitchell. 1996a. Ultrastructure of the oviducal Seattle: University of Washington Press. gland in the yellow spotted ray, Urolophus Gilmore, R. G., Jr., C. J. Donohoe, D. W. Cooke, and jamaicensis. Summer Meeting of the Anatomical D. J. Herrema. 1981. Fishes of the Indian River Society of Great Britain and Ireland, Belfast, North- Lagoon and adjacent waters, Florida. Harbor Branch ern Ireland, J. Anat. 188:224-245. Foundation, Tech. Rept. 41:1-64 Hamlett, W. C., D. P. Knight, T. Koob, M. Jezior, T. Grabowski, G. M., J. G. Blackburn, and E. R. Lacy. Luong, T. Rozycki, N. Brunette, and M. Hysell. 1999. Morphology and epithelial ion transport of 1998. Survey of oviducal gland structure and func- the alkaline gland in the Atlantic stingray (Dasyatis tion in elasmobranchs. J. Exp. Zool. 282:399-420. sabina). Biol. Bull. 197:82-93. Hamlett, W. C., D. P. Knight, F. T. V. Pereira, J. Steele, Grijalba-Bendeck, M., C. Polo-Silva, and A. P. Acero. and D. M. Sever. 2005a. Oviducal glands in 2007a. Una aproximacio´n a la abundancia de los chondrichthyans. In Reproductive Biology and Phy- batoideos capturados artesanalmente en Santa Marta logeny of Chondrichthyes, ed. W. C. Hamlett, 301- (Colombia). Boletin De Investigaciones Marinas Y 335. Enfield: Science Publishers, Inc. Costeras, Colombia 36(1):251-268. Hamlett, W. C., and T. J. Koob. 1999. Female reproduc- Grijalba-Bendeck, L. M., J. Bohorquez-Herrara, P. tive system. In Sharks, Skates, and Rays: The Biology Gomez, K. K. Acevedo-Urzola, and C. Moreno. of Elasmobranch Fishes, ed. W. C. Hamlett, 398-443. 2007b. Tiburones y rayas (Subclase Elasmobranchii) Baltimore: The Johns Hopkins University Press. descartados por la flota de arrastre camaronero en Hamlett, W. C., G. Kormanik, M. Storrie, B. Stevens, dos zonas del mar Caribe de Colombia. Acta biol. and T. I. Walker. 2005b. Chondrichthyan parity, Columb. 12(2):69-80. lecithotrophy and matrotrophy. In Reproductive Hale, L. F., J. V. Dudgeon, Z. Andrew, A. Z. Mason, Biology and Phylogeny of Chondrichthyes,edW.C. and C. G. Lowe. 2006. Elemental signatures in the Hamlett, 395-434. Enfield: Science Publishers, Inc. vertebral cartilage of the round stingray, Urobatis Hamlett, W. C., J. A. Musick, A. M. Eulitt, R. L. Jarrell, halleri, from Seal Beach, California. Environ. Biol. and M. A. Kelly. 1996b. Ultrastructure of uterine Fish. 77:317-325. trophonemata, accommodation for uterolactation Hale, L. F., and C. G. Lowe, 2008. Age and growth of and gas exchange in the southern stingray, Dasyatis the round stingray Urobatis halleri at Seal Beach, americana. Can. J. Zool. 74:1417-1430. California. J. Fish Biol. 73(3):510-523. Hamlett, W. C., F. J. Schwartz, R. Schmeinda, and Hamlett, W. C. 1986. Prenatal nutrient absorptive E. Cuevas. 1996c. Anatomy, histology, and devel- structures in selachians. In Indo-Pacific Fish Biology: opment of the cardiac valvular system in elasmo- Proceedings of the second International Conference on branchs. J. Exp. Zool. 275:83-94. Indo-Pacific Fishes, eds. T. Uyeno, R., Arai, T. Hamlett, W. C., R. E. Spieler, D. P. Fahy, and E. E. Taniuchi, and K. Matsura, 333-344. Tokyo: Ichthy- McKee. 2005c. Uterolactation by trophonemata in ological Soc. Japan. the yellow stingray, Urobatis jamaicensis. XVIII Hamlett, W. C., 1999. Male reproductive system. In International Symposium on Morphological Sci- Sharks, Skates, and Rays: The Biology of Elasmobranch ences, Belgrade, Serbia, and Montenegro. 94 R.E. SPIELER, ET AL.

Hanna, L. 2004. Yellow stingrays. Conserving the Cape Jones, C. J. P., T. I. Walker, J. D. Bell, M. B. Reardon, Fear, A semi-annual publication of the North Carolina C. E. Ambrosio, A. Almeida, and W. C. Hamlett. Aquarium at Fort Fisher (Winter 2003-04) 1(2):2-3. 2005. Male genital ducts and copulatory append- Harms, C. A., K. E. Linder, M. H. Fatzinger, B. A. ages in chondrichthyans. In Reproductive Biology Wolfe, K A. Spaulding, and G. A. Lewbart. 2004. and Phylogeny of Chondrichthyes: Sharks, Batoids and Apatite concretions in spiral valve of yellow sting- Chimaeras, ed. W. C. Hamlett, 361-393. Enfield, NH: ray (Urobatis [Urolophus] jamaicensis) fetal pups. In Science Publishers, Inc. 29th Annual Eastern Fish Health Workshop, March 22- Kajiura, S. M., A. P. Sebastian, and T. C. Tricas. 2000. 26, 2004, ed. R. C. Cipriano, 29. Atlantic Beach: Dermal bite wounds as indicators of reproductive North Carolina. seasonality and behavior in the Atlantic stingray, Henningsen, A. D. 1994. Tonic immobility in 12 elas- Dasyatis sabina. Environ. Biol. Fish. 58:23-31. mobranchs: Use as an aid in captive husbandry. Kajiura, S. M., and T. C. Tricas. 1996. Seasonal dynam- Zoo. Biol. 13(4):325-332. ics of dental sexual dimorphism in the Atlantic Henningsen, A. D. 2000. Notes on reproduction in the stingray, Dasyatis sabina. J. Exp. Biol. 199:2297-2306. southern stingray, Dasyatis americana (Chondrichthyes: Kemp, N.E., 1999. Integumentary system and teeth. In Dasyatidae) in a captive environment. Copiea 2000(3): Sharks, Skates, and Rays: The Biology of Elasmobranch 826-828. Fishes, ed. W. C. Hamlett, 43-68. Baltimore: The Heupel, M. R., J. K. Carlson, and C. A. Simpfendorfer. 2007. Shark nursery areas: Concepts, definition, Johns Hopkins University Press. characterization and assumptions. Mar. Ecol. Prog. Kohler N. E., J. G. Casey, and P. A. Turner. 1996. Ser. 337:287-297. Length-length and length-weight relationships for Hoese, H. D., and R. H. Moore. 1998. Fishes of the Gulf 13 shark species from the Western North Atlantic. of Mexico, Texas, Louisiana, and adjacent waters. Col- NOAA Tech Memo NMFS NE 110:1-22. lege Station: Texas A &M University Press. Kovacs, K. J., and G. D. Schmidt. 1980. Two new spe- Holmgren S. and S. Nilsson. 1999. Digestive System. In cies of cestode (Trypanorhyncha, Eutetrarhynchidae) Sharks, Skates, and Rays: The Biology of Elasmobranch from the yellow-spotted Stingray, Urolophus jamaicensis. Fishes, ed. W. C. Hamlett, 144-173. Baltimore: The P. Helm. Soc. Wash. 47:10-14. Johns Hopkins University Press. Lacy, E. R. 2005. Alkaline glands and clasper glands of Huber, P. M., and G. D. Schmidt. 1985. Rhinebothrium batoids. In Reproductive Biology and Phylogeny of biorchidum n. sp., a Tetraphyllidean cestode from a Chondrichthyes: Sharks, Batoids and Chimaeras,ed. yellow-spotted stingray, Urolophus jamaicensis,in W. C. Hamlett, 336-360. Enfield, NH: Science Pub- Jamaica. J. Parasitol. 71(1):1-3. lishers, Inc. Hunter, E., A. A. Buckley, C. Stewart, and J. D. Lacy, E. R, and E. Reale. 1999. Urinary system. In Metcalfe. 2005. Migratory behaviour of the thorn- Sharks, Skates, and Rays: The Biology of Elasmobranch back ray, Raja clavata, in the southern North Sea. J. Fishes, ed. W. C. Hamlett, 353-397. Baltimore: The Mar. Biol. Assoc. U. K. 85:1095-1105. Johns Hopkins University Press. Ito, M., M. Yoshida, and K. Obata. 1964. Monosynaptic LaMarca, M. J., 1961. The anatomy of the reproductive inhibition of the intracerebellar nuclei induced system of the yellow stingray, Urolophus jamaicensis from the cerebellar cortex. Experientia 20:575-576. (Cuvier). (Ph.D. Dissertation) Cornell University, Johansson, P. K. E., T. G. Douglass, and C. G. Lowe. Ithaca, New York, USA. 2004. Caudal spine replacement and histogenesis LaMarca, M. J., 1964. Functional anatomy of the in the round stingray, Urobatis halleri. Bull. Southern clasper and clasper gland of the yellow stingray, California Acad. Sci. 103:115-124. Urolophus jamaicensis. J. Morphol. 114:303-324. Jones, C. J. P., and W. C. Hamlett. 2003. Glycosylation Lasso, C. A., J. I. Mojica, J. S. Usma, J. A. Maldonado- of the male genital ducts and spermatozuegmata Ocampo, C. DoNascimiento, D. C. Taphorn, F. formation in the clearnose skate Raja eglanteria. Provenzano, O. M. Lasso-Alcala´, G. Galvis, L. Histochem. J. 34:601-615. Va´squez, M. Lugo, A. Machado-Allison, R. Royero, Jones, C. J. P., and W. C. Hamlett. 2006. Ultrastructure C. Sua´rez, and A. Ortega-Lara. 2004. Peces de la of the male genital ducts of the clearnose skate Raja cuenca del rı´o Orinoco. Parte I: Lista de especies y eglanteria. J. Exp. Zool. 305A:1018-1029. distribucio´n por subcuencas. Biota Colombiana Jones, N., and R. C. Jones. 1982. The structure of the 5(2):95-158. male genital system of the Port Jackson shark, Le Port, A., T. Sippel, and J. C. Montgomery. 2008. Heterodontus portusjacksoni, with particular refer- Observations of mesoscale movements in the ence to the genital ducts. Aust. J. Zool. 30:523-541. short-tailed stingray, Dasyatis brevicaudata from Jones, R. C., N. Jones, and D. Dkakiew. 1984. Lumi- New Zealand using a novel PSAT tag attachment nal composition and maturation of spermatozoa method. J. Exp. Mar. Biol. Ecol. 359:110-117. in the male genital ducts of the Port Jackson Shark, Lewis, T. C., 1984. The reproductive anatomy, sea- Heterodontus portusjacksoni. J. Exp. Zool. 230:417-426. sonal cycles, and development of the Atlantic sting- Jones, R. C., and M. Lin. 1993. Structure and functions ray, Dasyatis sabina (LeSueur) (Pisces, Dasyatidae) of the genital ducts of the male Port Jackson from the Northeastern Gulf of Mexico. (Ph.D. Dis- shark, Heterodontus portusjacksoni. Environ. Biol. sertation) Florida State University, Tallahasse, Fish. 38:127-138. Florida, USA. A REVIEW OF UROBATIS JAMAICENSIS BIOLOGY 95

Lieske, E., and R. Myers. 1994. Coral reef fishes. Indo- yellow stingray (Urobatis jamaicensis). SICB Meet- Pacific and Caribbean including the Red Sea (Collins ing, Boston MA, Jan. 3-7, 2009. Pocket Guide). London: HarperCollins Publishers. Mun˜oz-Cha´puli, R., 1999. Circulatory system: Anat- Lowe, C. G., G. J. Moss, G. Hoisington, IV, J. J. Vaudo, omy of the peripheral circulatory system. In Sharks, D. P. Cartamil, M. M. Marcotte, and Y. P. Skates, and Rays: The Biology of Elasmobranch Fishes, Papastamatiou. 2007. Caudal spine shedding peri- ed. W. C. Hamlett, 198-217. Baltimore: The Johns odicity and site fidelity of round stingrays, Urobatis Hopkins University Press. halleri (Cooper), at Seal Beach, California: Implica- Murphy, C. J., and H. C. Howland. 1990. The func- tions for stingray-related injury management. Bull. tional significance of crescent-shaped pupils and mul- Southern California Acad. Sci. 106(1):16-26. tiple pupillary apertures. J. Exp.Zool. 256(suppl. 5): Lowe (McConnell), R. H. 1962. The fishes of the British 22-28. Guiana continental shelf, Atlantic coast of South Nelson, J. S., 2006. Fishes of the world (4th ed.). Hoboken, America, with notes on their natural history. NJ: John Wiley and Sons, Inc. J. Linn. Soc. Lond. 44:669-700. Nelson, J. S., E. J. Crossman, H. Espinosa-Pe´rez, L. T. Maroni, K., R. E. Spieler, and R. L. Sherman. 2009. A Findley, C. R. Gilbert, R. N. Lea, and J. D. Williams, preliminary comparison of the vasculature of the 2004. Common and Scientific Names of Fishes spiral valve in the yellow stingray, Urobatis from the United States Canada and Mexico 6th ed. jamaicensis, and the North American paddlefish, Amer. Fish. Soc. Special Publication 29. Polyodon spathula. Microsc. Microanal. (In press). Nishikawa, J., T. Sonoda, I. Sakurai, M. Seto, and McComb, D. M., and S. M. Kajiura. 2008. Visual fields S. Nakao. 2000. Diet of demersal fishes and of four batoid fishes: a comparative study. J. Exp. macrobenthos in the coastal water off Tomakomai, Biol. 211:482-490. Hokkaido. Bull. J. Soc. Sci. Fish. [Nippon Suisan McCourt, R. M., and A. N. Kerstitch. 1980. Mating Gakk.] 66(1):33-43. behavior and sexual dimorphism in dentition in Nordell, S. E., 1994. Observations of the mating behav- the stingray Urolophus concentricus from the Gulf ior and dentition of the round stingray, Urolophus of California. Copeia 1980(4): 900-901. halleri. Environ. Biol. Fish. 39:219-229. McEachran, J. D., and M. R. de Carvalho. 2002. Northcutt, R. G. 1989. Brain variation and phylo- Urotrygonidae. In The living marine resources of genetic trends in elasmobranch fishes. J. Exp. Zool. the western central Atlantic, Volume 1: Introduc- 2 (Supp.):83-100. tion, mollusks, crustaceans, hagfishes, sharks, Nunes, J. L. S., Z. S. de Almeida, and N. M. Piorski. batoids, fishes, and chimaeras, ed. K. E. Carpenter, 2005. Raias capturadas pela pesca artisanal em 572-574. Rome: FAO Species Identification Guide aguas rasas do Maranha˜o. Brasil. Arqivos de for Fishery Purposes and American Society of Ich- Ciencias do Mar, Fortaleza 38:49-54. thyologists and Herpetologists Special Publication Olson, K. R., M. E. Forster, P. G. Bushnell, and D. W. No. 5, Food and Agriculture Organization of the Duff. 2000. Spontaneous contractions in elasmo- United Nations. branch vessels in vitro. J. Exp. Zool. 286:606-614. McEachran, J. D., and J. D. Fechhelm. 1998. Fishes of the Parsons, G. R., 2006. Sharks, Skates, and Rays of the Gulf of Mexico, Volume 1: Myxiniformes to Gasteros- Gulf of Mexico: A Field Guide. Jackson, MS: teiformes. Austin, TX: University of Texas Press. University Press of Mississippi. Mejı´a-Falla, P. A., and A. F. Navia. 2007. Life history Pedroso, C. M., C. Jared, P. Charvet-Almeidab, M. P. aspects of round stingrays Urotrygon rogersi of the Almeidac, D. G. Neto, M. S. Lira, V. Haddad, Jr., Pacific Ocean off Columbia.[abstract] 23rd Ann. K. C. Barbaro, and M. M. Antoniazzi. 2007. Mor- Meet. AES, St. Louis, Missouri. phological characterization of the venom secretory Menni, R. C., and F. W. Stehmann. 2000. Distribution, epidermal cells in the stinger of marine and fresh- environment and biology of batoid fishes off water stingrays. Toxicon 50:688-697. Argentina, Uruguay and Brazil: a review. Rev. Phleger, C. F., 1988. Bone lipids of Jamaican reef Mus. Argent. Cienc. Nat. (Nueva Ser.) 2(1):69-109. fishes. Comp. Biochem. Physiol. 90B(2):279-283. Metcalfe, J. D., and P. J. Butler. 1986. The functional Pierce, S. J., S. A. Pardo, and M. B. Bennett. 2009. anatomy of the gills of the dogfish (Scyliorhinus Reproduction of the blue-spotted maskray canicula). J. Zool. 208:519-530. Neotrygon kuhlii (Myliobatoidei: Dasyatidae) in Mull, C. G. 2007. Environmental and endocrine regu- south-east Queensland, Australia. J. Fish Biol. 74(6): lation of seasonal reproduction in round stingrays 1291-1308. (Urobatis halleri). (M.S. Thesis) California State Uni- Piercy, A., J. Gelsleichter, and F. F. Snelson, Jr. 2006a. versity, Long Beach, California, USA. Morphological changes in the clasper gland of the Mull, C. G., C. G. Lowe, and K. A. Young. 2008. Pho- Atlantic stingray, Dasyatis sabina, associated with toperiod and water temperature regulation of sea- the seasonal reproductive cycle. J. Morphol. sonal reproduction in male round stingrays 267:109-114. (Urobatis halleri). Comp. Biochem. Physiol. Part A Piercy, A. N., F. F. Snelson, Jr., and R. D. Grubbs. 151:717-725. 2006b. Urobatis jamaicensis. In IUCN 2008. 2008 Mulvany, S. L., and P. J. Motta. 2009. Feeding kinemat- IUCN Red List of Threatened Species. . Downloaded on 01 May 2009. 96 R.E. SPIELER, ET AL.

Pratt, H. L. 1988. Elasmobranch gonad structure: a jamaicensis (Urolophidae), by SEM observations of descriptive survey. Copeia 1988(3):719-729. resin casts. Ital. J. Zool. 65(suppl):431-434. Prior, M. L., and B. J. Marples. 1944-1945. A compara- Sherman, R. L., J. Sulikowski, and R. E. Spieler. 2001. tive account of the vascular system of certain Similarities and differences in fine gill vasculature rajiform fishes. Trans. Royal Soc. New Zealand,74(4): among some batoid elasmobranchs. Proc. Soc. Inte- 343-358. grative Comp. Biol., 4-7 Jan, Chicago, IL. Quinn, T. P. 1996. Diet and seasonal feeding habits of Silva Lee, A. F., 1974. Habitos alimentarios de la the yellow stingray, Urolophus jamaicensis. (M.S. cherna criolla Epinephelus striatus Bloch y algunos Thesis) Nova Southeastern University Oceano- datos sobre su biologia. Academia de Ciencias de graphic Center, Dania Beach, Florida, USA. Cuba, Instituto de Oceanologia, Serie Oceanologica REEF. 2009. Reef Environmental Education Founda- No. 25, La Habana, Cuba. tion Volunteer Survey Project Database. World Sisneros, J. A., and T. C. Tricas. 2002. Neuroethology Wide Web electronic publication. www.reef.org, and life history adaptations of the elasmobranch date of download (04 May 2009). URL: http:// electric sense. J. Physiol. 96:379-389. www.reef.org/db/reports/dist/species/TWA/172/ Snelson, F. F., Jr., and S. E. Williams. 1981. Notes on 2007-01-01/2009-05-06. the occurrence, distribution, and biology of elas- Robins, C. R., G. C. Ray, and J. Douglass. 1986. Peterson mobranch fishes in the Indian River lagoon system, Field Guide Series: A Field Guide to Atlantic Coast Florida. Estuaries 4(2):110-120. Fishes, North America., Boston: Houghton Mifflin Stamper, M. A., G. A. Lewbart, and A. Wrangell. 1998. Company Manually induced parturition of two yellow spot- Robinson, M. C. 1969. Elasmobranch records and ted stingrays (Urolophus jamaicensis) with dysto- range extension for the Texas Gulf Coast. Tex. cias. Annual Conference, American Association of J. Sci. 21(2):235-236. Zoo Veterinarians, 1998. Rosenberger, L.J., 2001. Pectoral fin locomotion in Sulikowski, J. 1996. A preliminary study of the pop- batoid fishes: undulation versus oscillation. J. Exp. ulation density, size distribution, age and growth Biol. 204:379-394. of the stingray, Urolophus jamaicensis, in South- Russell, F. E., 1955. Multiple caudal spines in the round eastern, Florida. (M.S. Thesis) Nova Southeastern stingray, Urobatis halleri. Calif. Fish Game 41(3): University Oceanographic Center, Dania Beach, 213-217. Florida, USA. Russell, F. E. 1959. Stingray injuries. Public Health Rep. Sulikowski, J. A., and L. A. Maginniss. 2001. Effects of 74(10):855-859. environmental dilution on body fluid regulation in Satchell, G. H. 1962. Intrinsic vasomotion in the dog- the yellow stingray, Urolophus jamaicensis. Comp. fish gill. J. Exp. Biol. 39:503-512. Biochem. Physiol. 128A:223-232. Satchell, G. H. 1991. Circulation through special Summers, A. P., and L. A. Ferry-Graham. 2001. Venti- regions. In Physiology and Form of Fish Circulation. latory modes and mechanics of the hedgehog 89-226. Cambridge: Cambridge University Press. skate, Leucoraja erinacea: testing the continuous Schaefer, J. T., and A. P. Summers. 2005. Batoid wing flow model. J. Exp. Zool. 204(9):1577-1587. skeletal structure: novel morphologies, mechanical Taniuchi, T., and M. Shimizu. 1993. Dental sexual implications, and phylogenetic patterns. J. Morphol. dimorphism and food habits in the stingray 264:298-313. Dasyatis akajei from Tokyo Bay, Japan. Nippon Schmid, T. H., L. M. Ehrhart, and F. F. Snelson, Jr. Suisan Gakk. 59:53-60. 1988. Notes on the occurrence of rays Te´llez, L., C. Vargas, and M. Grijalba-Bendeck. 2006. (Elasmobranchii, Batoidea) in the Indian River Algunosaspectosbiolo´gicos de Urotrygon venezuelae lagoon system, Florida. Fla. Sci. 51:121-128. Schultz, 1949 (Elasmobranchii, Rajiformes, Sherman, R. L., 1998. Fine structure of the gill vascula- Urolophidae), capturada en playa Salguero, Santa ture of the yellow stingray (Urolophus jamaicensis). Marta, Caribe de Colombia. Rev. UDCA Actualidad & (M.S. Thesis) Nova Southeastern University Divulgacio´nCientı´fica 9(2):75-87. Oceanographic Center, Dania Beach, Florida, USA. Teshima, K, and K. Takeshita. 1992. Reproduction of Sherman, R. L., J. W. Barnes, J. P. Huston, and R. E. the freshwater stingray, Potamotrygon magdalenae Spieler. 2003. The yellow stingray, Urobatis taken from the Magdalena River System in jamaicensis, as a model for studying cerebellar func- Colombia, South America. Bull. Seikai Natl. Fish. tion in vertebrates. J. Fish Biol. 63:256-257. Res. Inst. 70:11-27. Sherman, R. L., and D. S. Gilliam. 1996. Hepato- Thorson, T. B. 1983. Observations on the morphology, somatic indices and lifestyles in some batoids elas- ecology and life history of the euryhaline stingray, mobranchs. Fla. Sci. 59(4):275-278. Dasyatis guttata (Bloch and Schneider) 1801. Acta Sherman, R. L., C. A. Nelson, R. Hueter, and R. E. Biol. Venezuelica 11(4):95-125. Spieler. 1995. Preliminary examination of gill sur- Tota, B. 1999. Heart. In Sharks, Skates, and Rays: The Biol- face area in two batoid elasmobranchs. Am. Zool. ogyofElasmobranchFishes, ed. W. C. Hamlett, 238- 35(5):118A. 272. Baltimore: The Johns Hopkins University Press. Sherman, R. L., and R. E. Spieler. 1998. Examination of Valadez-Gonza´lez, C., B. Aguilar-Palomino, and S. gill vasculature of the yellow stingray, Urolophus Herna´ndez-Va´zquez. 2001. Feeding habits of the A REVIEW OF UROBATIS JAMAICENSIS BIOLOGY 97

round stingray Urobatis halleri (Cooper, 1863) Ward-Paige, C. A., R. A. Myers, C. Pattengill- (Chondrichthyes: Urolophidae) from the continen- Semmens, and H. K. Lotze. 2010. Spatial and tal shelf of Jalisco and Colima, Mexico. Cienc. Mar. temporal trends in yellow stingray abundance: 27(1):91-104. evidence from diver surveys. Environ. Biol. Fish Vaudo, J. J., and C. G. Lowe. 2006. Movement patterns (in press). of the round stingray Urobatis halleri (Cooper) near White, W. T., and Dharmadi. 2007. Species and size a thermal outfall. J. Fish Biol. 68:1756-1766. compositions and reproductive biology of rays Walker, B. K., and R. L. Sherman. 2001. Gross brain (Chondrichthyes, Batoidea) caught in target and morphology in the yellow stingray, Urobatis non-target fisheries in eastern Indonesia. J. Fish jamaicensis. Fla. Sci. 64(4):246-249. Biol. 70:1809-1837. Walker, T. I. 2005. Reproduction in fisheries science. Yan˜ez-Arancibia, A., and F. Amezcua-Linares. 1979. In Reproductive Biology and Phylogeny of Ecologı´adeUrolphus jamaicensis (Cuvier) en Chondrichthyes, Sharks, Batoids, and Chimaeras, ed. Laguna de Te´rminus un sistema estuarino del W. C. Hamlett, 81-127. Enfield,NH: Science Pub- golfo sur del Golfo de Me´xico (Pisces: lishers, Inc. Urolophidae). An. Centro Cienc. Del Mar y Limnol., Walsh, P. J., C. M. Wood, S. F. Perry, and S. Thomas. Univ. Nal. Auton. Mexico 6(2):123-136. 1994. Urea transport by hepatocytes and red blood Young, R. F. 1993. Observation of the mating behavior cells of selected elasmobranch and teleost fish. of the yellow stingray, Urolophus jamaicensis. Copeia J. Exp. Biol. 193:321-335. 1993(3):879-880.