Electrosensory System
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3044 The Journal of Experimental Biology 212, 3044-3050 Published by The Company of Biologists 2009 doi:10.1242/jeb.028738 Functional consequences of structural differences in stingray sensory systems. Part II: electrosensory system Laura K. Jordan1,*, Stephen M. Kajiura2 and Malcolm S. Gordon1 1Ecology and Evolutionary Biology, University of California at Los Angeles, 621 Charles E. Young Drive South, Los Angeles, CA 90095, USA and 2Biological Sciences, Florida Atlantic University, 777 Glades Road, Boca Raton, FL 33431, USA *Author for correspondence ([email protected]) Accepted 6 July 2009 SUMMARY Elasmobranch fishes (sharks, skates and rays) possess highly sensitive electrosensory systems, which enable them to detect weak electric fields such as those produced by potential prey organisms. Different species have unique electrosensory pore numbers, densities and distributions. Functional differences in detection capabilities resulting from these structural differences are largely unknown. Stingrays and other batoid fishes have eyes positioned on the opposite side of the body from the mouth. Furthermore, they often feed on buried prey, which can be located non-visually using the electrosensory system. In the present study we test functional predictions based on structural differences in three stingray species (Urobatis halleri, Pteroplatytrygon violacea and Myliobatis californica) with differing electrosensory system morphology. We compare detection capabilities based upon behavioral responses to dipole electric signals (5.3–9.6 μA). Species with greater ventral pore numbers and densities were predicted to demonstrate enhanced electrosensory capabilities. Electric field intensities at orientation were similar among these species, although they differed in response type and orientation pathway. Minimum voltage gradients eliciting feeding responses were well below 1 nV cm–1 for all species regardless of pore number and density. Supplementary material available online at http://jeb.biologists.org/cgi/content/full/212/19/3044/DC1 Key words: batoid, elasmobranch, electroreception, prey detection, Urobatis halleri, Myliobatis californica, Pteroplatytrygon violacea. INTRODUCTION detection capabilities of species with quantified morphological The first paper in this two part series reported relationships of form differences. Carcharhinid and sphyrnid sharks with similar pore and function of the mechanosensory lateral line canal system in three densities yet different pore numbers showed similar behavioral- stingray species; in the present study we explore similar relationships response thresholds to dipole electric fields (Kajiura and Holland, in the electrosensory system to further understand how these 2002). Benthic-feeding elasmobranchs typically have high animals use sensory modalities other than vision to capture prey in electrosensory pore numbers and densities whereas pelagic species their ventral mouths. Like the lateral line canal system, the have a lower pore number and density with more similar dorso- electrosensory system is highly modified in batoid fishes. In ventral distributions (Raschi, 1986; Kajiura, 2001; Raschi et al., stingrays the canals extend over the ventral body surface and out 2001; Cornett, 2006; Jordan, 2008). toward the wing tips with increased density surrounding the mouth The present paper reports differing behavioral responses to (Chu and Wen, 1979; Raschi, 1986; Jordan, 2008). Electric signals electric signals in three Eastern Pacific stingray species with have a short range relative to visual and olfactory signals and provide significant differences in sensory morphology. Ventral directional information for locating buried prey and directing the electrosensory pore numbers range from 1200±27 and 1425±41 in mouth strike to ingest prey. Previous studies of elasmobranchs have Urobatis halleri and Myliobatis californica, respectively, to just demonstrated feeding responses to weak electric signals (Kalmijn, 553±26 in Pteroplatytrygon violacea (Jordan, 2008). The density 1971; Kalmijn, 1978; Kalmijn, 1982; Tricas, 1982; Johnson et al., of pores within the ventral pore field in the two benthically feeding 1984; Tricas and McCosker, 1984; Blonder and Alevizon, 1988; species is more than three times that of the pelagic stingray P. Kajiura and Holland, 2002; Whitehead, 2002); however, detection violacea (Jordan, 2008). While factors such as canal length and capabilities have rarely been related to interspecific anatomical convergence ratios also influence sensitivity, high ventral differences. electrosensory pore numbers and densities may provide enhanced The electrosensory system in marine elasmobranchs consists of electro-sensitivity to benthic-feeding elasmobranchs; therefore, we pores at the skin’s surface, which lead through canals to sensory hypothesize that both U. halleri and M. californica will demonstrate cells located in ampulla clusters in the head (Chu and Wen, 1979; greater resolution in locating weak dipole electric signals relative Raschi, 1986; Tricas, 2001). This system enables detection of weak to the pelagic stingray P. violacea. electric fields such as those generated by living organisms, which can be mimicked using dipole electrodes (Kalmijn, 1971; Kalmijn, MATERIALS AND METHODS 1982; Tricas, 1982; Johnson et al., 1984; Tricas and McCosker, Experimental animals 1984; Haine et al., 2001; Kajiura and Holland, 2002). Despite The experimental animals and study design are described in detail considerable interspecific variation in the number, density and in part I (Jordan et al., 2009) and are briefly outlined here. Twenty- distribution of electrosensory pores, few studies have compared the five round stingrays Urobatis halleri Cooper [12 females, 13 males; THE JOURNAL OF EXPERIMENTAL BIOLOGY Stingray sensory function part II 3045 disc width (DW)=9.5–24.0 cm], six pelagic stingrays nesting multiple observations for each individual within each Pteroplatytrygon violacea Bonaparte (five females, one male; species. Variation in body size was standardized in statistical DW=49.5–60.0cm) and 14 bat rays Myliobatis californica Gill (five comparisons by centering the mean body size for each species. females, nine males; DW=26.5–38.5cm) were held at Wrigley Differences were considered significant at P<0.05. Marine Science Center (WMSC) on Santa Catalina Island, CA, USA The frame immediately preceding the initiation of the orientation (33°30Ј18.52ЉN, 118°30Ј36.32ЉW) in 2.4m diameter, 1m deep response to the electric signal was saved and analyzed using outdoor fiberglass tanks with flow through ambient seawater ranging ImageJ. The distance and angle from the center of the electrode to from 18 to 25°C at 35p.p.t. Rays were held for a total of 3–5 weeks the nearest ampulla cluster, located just posterior to the spiracle, and tested in behavioral trials only after normal feeding was were measured (Fig.1). The angle relative to the dipole axis was observed in the holding tank, usually within one week after capture. calculated as the difference between the dipole angle and the All work with these animals was done during June through to orientation angle (Fig.1). The electric field strength (E) at the point September of 2006 and 2007 according to approved IACUC of orientation was calculated using the following equation: protocols at both USC and UCLA. Species were studied at the same E=ρId/πr3cosθ, where ρ is the resistivity of seawater (Ωcm), I is time of year to avoid effects of breeding season (Sisneros and Tricas, the current (A), d is the dipole separation distance (cm), r is the 2000). distance from the dipole center (cm) and θ is the orientation angle relative to the dipole axis in degrees (Kalmijn, 1982). The resistivity Study design varied between 18.9 and 21.9Ωcm with fluctuations in temperature The experimental tank was fitted with an apparatus consisting of a and salinity. In most cases the approach consisted of a right or left 1ϫ1m acrylic plate with 6mm holes fitted with polyethylene tubing turn; however, when the animal was on a straight trajectory toward (Tygon, Akron, OH, USA) underneath [see fig.1 in part I (Jordan the dipole center the initial response was to brake with the pectoral et al., 2009)]. Four dipole electrodes, with a 1cm dipole separation and pelvic fins to allow a bite at the electrode. The frame distance, were connected to underwater electric cables (Impulse immediately preceding the brake response was analyzed. Only initial Enterprise, San Diego, CA, USA) and a 9V battery source with responses where the ray initiated a right or left turn are included in controls to adjust the current, which was monitored by an ammeter interspecific comparisons, although rays occasionally made more in series (Meterman 35XP, Everett, WA, USA), and a switch to than one turn to approach the center of the electrode and in some activate one of four electrodes at a time following Kajiura and cases they passed over the dipole center and reversed backwards Holland (Kajiura and Holland, 2002). The tank contained no metal prior to biting. Responses were ranked from 1 to 5 for increasing and sat on a wooden platform for isolation from confounding electric intensity, where 1=slight pause and 5=bite, as described for water signals. jets in part I (Jordan et al., 2009). No zero response rank was included as rays rarely approached an active electrode without exhibiting a Behavioral experiments response. Prior to each trial, food was withheld for 1–2 days until rays showed Initial responses to electric