Comparative Visual Function in Predatory Fishes from the Indian River Lagoon Author(S): D
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Comparative Visual Function in Predatory Fishes from the Indian River Lagoon Author(s): D. Michelle McComb, Stephen M. Kajiura, Andrij Z. Horodysky, and Tamara M. Frank Source: Physiological and Biochemical Zoology, Vol. 86, No. 3 (May/June 2013), pp. 285-297 Published by: The University of Chicago Press Stable URL: http://www.jstor.org/stable/10.1086/670260 . Accessed: 16/07/2013 16:00 Your use of the JSTOR archive indicates your acceptance of the Terms & Conditions of Use, available at . http://www.jstor.org/page/info/about/policies/terms.jsp . JSTOR is a not-for-profit service that helps scholars, researchers, and students discover, use, and build upon a wide range of content in a trusted digital archive. We use information technology and tools to increase productivity and facilitate new forms of scholarship. For more information about JSTOR, please contact [email protected]. The University of Chicago Press is collaborating with JSTOR to digitize, preserve and extend access to Physiological and Biochemical Zoology. http://www.jstor.org This content downloaded from 152.3.102.242 on Tue, 16 Jul 2013 16:00:41 PM All use subject to JSTOR Terms and Conditions 285 Comparative Visual Function in Predatory Fishes from the Indian River Lagoon D. Michelle McComb1,* Introduction Stephen M. Kajiura2 Teleost fishes represent a speciose vertebrate lineage that ra- Andrij Z. Horodysky3 diated into distinct aquatic habitats that present unique diver- Tamara M. Frank4 gent light qualities (Jerlov 1968). Selective pressure on the pi- 1Harbor Branch Oceanographic Institute at Florida Atlantic scine eye has resulted in an extensive array of both 2 University, Fort Pierce, Florida 34946; Biological Sciences, morphological and physiological adaptations to maximize vi- Florida Atlantic University, Boca Raton, Florida 33431; sual function under differing light conditions. Morphological 3 Marine and Environmental Science, Hampton University, adaptations—including eye size, eye position, lens composition, 4 Hampton, Virginia 23668; Nova Southeastern University retinomotor movement, and reflective retinal media—have Oceanographic Center, Dania Beach, Florida 33004 been correlated to aspects of life style and habitat niche (Collin and Marshall 2003). Furthermore, the growth of the teleost eye Accepted 2/15/2013; Electronically Published 4/5/2013 throughout life allows for dynamic physiological adaptations to the prevailing aquatic light field throughout ontogeny (Zaun- reiter et al. 1991; Stearns et al. 1994; Schwab 2012). The maximum transmission of light occurs at shorter wave- ABSTRACT lengths in deep-sea and clear open ocean environments (blue), Visual temporal resolution and spectral sensitivity of three at intermediate wavelengths in coastal waters (green), and at coastal teleost species (common snook [Centropomus undeci- longer wavelengths in estuarine and freshwater environments malis], gray snapper [Lutjanus griseus], and pinfish [Lagodon (yellow-red; Jerlov 1968). For mobile species that utilize several distinct habitats, maintaining optimal visual performance over rhomboides]) were investigated by electroretinogram. Temporal the full range of ambient light conditions is nearly impossible, resolution was quantified under photopic and scotopic con- and unavoidable physiological trade-offs exist between visual ditions using response waveform dynamics and maximum crit- sensitivity and resolution. For instance, absolute sensitivity of ical flicker fusion frequency (CFF ). Photopic CFF was sig- max max the eye may increase in low-light or turbid conditions to max- nificantly higher than scotopic CFF in all species. The max imize photon capture but requires a reduction in temporal snapper had the shortest photoreceptor response latency time resolution (Warrant and Locket 2004). For species that do not (26.7 ms) and the highest CFF (47 Hz), suggesting that its max possess mobile pupils or other mechanisms to increase sensi- eyes are adapted for a brighter photic environment. In contrast, tivity, reducing temporal resolution is analogous to holding a the snook had the longest response latency time (36.8 ms) and shutter open longer on a camera, resulting in an increase in lowest CFFmax (40 Hz), indicating that its eyes are adapted for absolute sensitivity of the eye. The temporal and spatial prop- a dimmer environment or nocturnal lifestyle. Species spectral erties of visual systems in fish vary depending on ecological responses ranged from 360 to 620 nm and revealed the presence constraints and light qualities of the habitat. of rods sensitive to dim and twilight conditions, as well as Teleosts possess rod photoreceptors that confer sensitivity multiple cone visual pigments providing the basis for color and and resolution in low-light conditions and may possess single, contrast discrimination. Collectively, our results demonstrate double, and twin cone photoreceptors for bright conditions. differences in visual function among species inhabiting the In- The possession of multiple cone types allows for behavioral dian River Lagoon system, representative of their unique ecol- color discrimination (McFarland and Munz 1975). Extensive ogy and life histories. research has linked ambient environmental light and fish pho- toreceptor sensitivity. The sensitivity hypothesis proposed by Clarke (1936) states that rod-based photoreceptor sensitivity will match the ambient microhabitat spectra to maximize pho- ton capture in lower light conditions. The contrast sensitivity hypothesis (Lythgoe 1968) states that maximum contrast of objects against a background is achieved by the presence of * Corresponding author; e-mail: [email protected]. matched and slightly offset visual pigments and is the principal evolutionary driver and utility of color vision (Wallace 1891; Physiological and Biochemical Zoology 86(3):285–297. 2013. ᭧ 2013 by The University of Chicago. All rights reserved. 1522-2152/2013/8603-2104$15.00. Walls 1942; Marshall et al. 2003). The twilight hypothesis (Lyth- DOI: 10.1086/670260 goe 1968; Munz and McFarland 1973, 1977; McFarland 1991) This content downloaded from 152.3.102.242 on Tue, 16 Jul 2013 16:00:41 PM All use subject to JSTOR Terms and Conditions 286 D. M. McComb, S. M. Kajiura, A. Z. Horodysky, and T. M. Frank predicts that sensitivity of rod photoreceptors in fish will match were revived, rehabilitated, and released back into the wild the more narrow range of environmental spectra during dusk under Florida Fish and Wildlife guidelines. and dawn, thus enhancing vision during a biologically active period of heightened predation. Experimental Setup In this study, we test the predictions of these hypotheses by characterizing the spectral sensitivities and response dynamics The temporal resolution and spectral sensitivity of the pho- of three teleost fish species that inhabit the Indian River Lagoon, toreceptors were electrophysiologically determined using an Florida. The Indian River Lagoon is North America’s most electroretinogram (ERG) technique. Experimental animals were biodiverse estuarine ecosystem, with habitats comprised of sea- anesthetized with tricaine methanesulphonate (MS-222; grass flats, mangrove forests, and salt marshes that provide 1 : 15,000 wt : vol). After respiration ceased (2–4 min), animals nursery and shelter to more than 700 fish species (Gilmore et were quickly transferred to an acrylic experimental tank (79 al. 1981, 1983; Mulligan and Snelson 1983; Tremain and Adams cm # 39 cm # 11 cm) and secured with Velcro straps to a 1995). Decades of anthropogenic stressors have altered water submerged plastic stage. Animals were immediately fitted with clarity and quality in the lagoon (Sigua and Steward 2000; Sigua an oral ventilation tube that delivered a recirculating mainte- and Tweedale 2004). Reduced visibility can negatively impact nance dose (1 : 20,000 wt : vol) of MS-222 over the gills; flow foraging success of visual predators, necessitating a switch to was confirmed with a dye test. The experimental tank was less efficient and energetically costly encounter-rate feeding placed within a Faraday cage and light eliminated by creating (Grecay and Targett 1996). Alterations in predatory foraging a dark room frame using black plastic sheeting. The animals’ strategies can ultimately alter fish community structure (See- eyes were allowed to dark-adapt for a minimum of 45 min. All hausen et al. 1997; Helfman et al. 2009; Montan˜o 2009). Be- necessary adjustments in the dark were made under dim red cause of alterations within this ecosystem and management light. The water was aerated throughout the trial, and water plans to increase viability of game fish populations, a com- temperature was maintained between 24Њ and 25ЊC. parative assessment of visual performance of predatory and ERGs were recorded by placing a tungsten microelectrode prey species within the Indian River Lagoon was warranted. (5–7 MQ; FHC, Brunswick, ME) subcorneally in the submerged The objective of this study was to determine whether the eye, while grounding the body with an AgCl wire. The signals visual performance of three teleost species from the Indian were amplified (#1,000–10,000) and filtered (low cutoff, 0.1 River Lagoon correlated with aspects of their habitat and ecol- Hz; high cutoff, 15 kHz) with a microelectrode amplifier (Xcell- ogy. Temporal resolution and spectral sensitivity were deter- 3; FHC), used together with a high-impedance probe to min- mined for two visually oriented predators and their shared prey: imize electrode polarization artifacts. The