Comparative visual function in four piscivorous fishes inhabiting Chesapeake Bay

Waters of different types differentially scatter and absorb down-welling light, affecting their spectral bandwidth (color) and intensity (brightness). Pure natural waters and clear pelagic seas maximally transmit short wavelength (blue) light, whereas coastal waters are most deeply penetrated by intermediate (green) wavelengths. Estuarine and many fresh waters maximally transmit longer (yellow–red) wavelengths due to increasing concentrations of phytoplankton, yellow products of vegetative decay (Gelbstoff), and suspended particulates that scatter, absorb and more rapidly attenuate light (Lythgoe, 1975; Lythgoe, 1988; Jerlov, 1968). Fishes have radiated into a wide range of aquatic photohabitats possessing complex photic properties, exposing their visual systems to a myriad of selective pressures (Levine and MacNichol, 1979; Collin, 1997). The visual systems of fishes have thus evolved to generally reflect the characteristics of aquatic light fields in their specific microhabitats and macrohabitats (Guthrie and Muntz, 1993).

Estuarine and near-coastal waters represent some of the most dynamic aquatic photohabitats on Earth. Luminous and chromatic properties of these waters vary on temporal and spatial scales ranging from milliseconds to decades, and millimeters to kilometers (e.g. Schubert et al., 2001; Harding, 1994). This extensive variability is due to vertical mixing, stratification, wave activity, clouds and weather, sunrise and sunset, seasonal solar irradiance, phytoplankton dynamics, as well as anthropogenically induced processes such as eutrophication and sedimentation (McFarland and Loew, 1983; Wing et al., 1993; Schubert et al., 2001; Gallegos et al., 2005; Kemp et al., 2005). Furthermore, at midday, a fixed point in an estuary can range widely in luminous and chromatic properties due to tidal and freshwater inputs along salinity gradients. Flood tides push relatively well-lit green coastal waters into estuaries, while falling ebb tides draw highly attenuating, very turbid riverine waters through the estuary and out to sea (e.g. Bowers and Brubaker, 2004).

The visual systems of fishes inhabiting highly productive and frequently turbid coastal waters must balance luminous sensitivity, resolution, contrast perception and rapid adaptation to dynamic light conditions depending on evolutionary pressures and phylogenetic constraints (Dartnall, 1975; Levine and MacNichol, 1979). The eyes of diurnal predatory fishes typically use rod photoreceptors during scotopic (dim/dark) conditions and cone photoreceptors under photopic (bright) conditions, the latter potentially differing in number, the pigments they contain, and their spectral position depending on phylogeny, species' lifestyle and optical microhabitat (Lythgoe, 1979; Crescitelli, 1991; Levine and MacNichol, 1979). At the cost of acuity, luminous sensitivity can be extended under dim conditions by widening pupils, increasing spatial and temporal summation, and even reradiating light through retinal media to maximize photon capture (Warrant, 1999). However, unavoidable tradeoffs between luminous sensitivity and resolution limit the plasticity of optical responses to widely ranging photic conditions (Warrant, 1999).

Many shallow-dwelling piscivores have large, broadly tuned and highly resolute eyes, foraging visually when light is not limiting because a wider breadth of information is rapidly available through this sensory channel relative to other modalities (Hobson et al., 1981; Guthrie and Muntz, 1993; Rowland, 1999). Paradoxically, many fishes that inhabit productive but turbid estuaries rely on vision to detect their predators, prey and mates (Abrahams and Kattenfield, 1997; Engström-Östa and Candolin, 2007). The visual range of fishes is constrained when the luminous and chromatic properties of light are limiting due to changing diel light conditions or via scattering and absorption by suspended materials. Degradation of optical conditions affects predators and prey asymmetrically. Mild turbidity may enhance prey contrast, but piscivory is inhibited under adverse optical conditions via the reduction of ambient light intensity and contrast degradation, with the ultimate effect of decreasing effective visual fields and increasing search time (Vogel and Beauchamp, 1999; Utne-Palm, 2002). Simultaneously, turbidity enhances cover and foraging opportunities for planktivorous species that are released from predation by piscivores [i.e. ‘turbidity as cover hypothesis’ (Gregory and Northcote, 1993)]. Piscivores may therefore be forced to abandon visual foraging for less-efficient encounter-rate feeding and to shift from pelagic to benthic prey when optical conditions are greatly degraded (Grecay and Targett, 1996a; Grecay and Targett, 1996b; De Robertis et al., 2003). Such foraging shifts may tip the competitive predatory balance in an ecosystem from visually feeding piscivores to tactile and chemoreceptive foragers, with potentially cascading effects (Carpenter and Kitchell, 1993; Aksnes and Utne, 1997). Additionally, degradation of the chromatic and luminous properties of light fields can affect the distribution and movements of predatory fishes (McFarland, 1986), interspecific and intraspecific communication (Siebeck et al., 2006), reproductive habits and speciation (Seehausen et al., 1997), as well as vulnerability to fishing gear (Loesch et al., 1982; Walsh, 1991; Buijse et al., 1992).

In summary, because predation by visually foraging piscivorous fishes can affect the structure and function of aquatic communities (Paine, 1966; Northcote, 1988), changes in the visual environment may thus have far-reaching effects on coastal ecosystems and their management through light-induced changes in picscivore behavior (Aksnes, 2007). However, visual function of coastal piscivorous fishes has received relatively little attention despite their importance to both commercial and recreational fisheries. We therefore used corneal electroretinography (ERG) to assess the absolute sensitivities, temporal properties and chromatic sensitivities of four piscivores common to coastal waters of the western North Atlantic. Optical conditions in key mid-Atlantic estuaries such as Chesapeake Bay have changed dramatically over the past century due to industrialization, population expansion, eutrophication and sedimentation (Jackson, 2001; Kemp et al., 2005), with unknown consequences for predation, mating and other activities involving vision because so little is known of the visual function of this estuary's diverse fish fauna. A previous investigation of fish visual ecophysiology (Horodysky et al., 2008) applied comparative methods to assess the visual function in five phylogenetically related fishes that use different optical microhabitats in Chesapeake Bay. Using the same experimental setup and methods, we investigated the converse question, assessing the visual systems of four coastal western North Atlantic piscivores with different phylogenies that use similar microhabitats, bear similar trophic ecologies, or both (Fig. 1). We sought mechanistic insights into how biotic and abiotic processes influence relationships between form, function and the environment in the visual systems of coastal marine fishes.

Striped bass (Morone saxatilis Walbaum 1792), bluefish (Pomatomus saltatrix Linnaeus 1766), summer flounder (Paralichthys dentatus Linnaeus 1766) and cobia (Rachycentron canadum Linnaeus 1766) were all captured by standard hook and line fishing gear (Table 1). Animals were maintained in recirculating 1855 l aquaria on natural ambient photoperiods at 20±1°C (winter) or 25±2°C (summer). Fish were fed a combination of frozen Atlantic menhaden (Brevoortia tyrannus), squid (Loligo sp.) and commercially prepared food (AquaTox flakes; Zeigler, Gardners, PA, USA).

Experimental and animal care protocols were approved by the College of William & Mary Institutional Animal Care and Use Committee (protocol no. 0423) and followed all relevant laws of the United States. Fish were removed from holding tanks, sedated with an intramuscular (i.m.) dose of ketamine hydrochloride (Butler Animal Health, Middletown, PA, USA; 30 mg kg⁻¹), and immobilized with an i.m. injection of the neuromuscular blocking drug gallamine triethiodide (Flaxedil; Sigma, St Louis, MO, USA; 10 mg kg⁻¹). Drugs were re-administered during the course of experiments as required. Following initial drug injections, fish were moved into a light-tight enclosure and placed in a rectangular 800 mm×325 mm×180 mm Plexiglas tank with only a small portion of the head and eye receiving the light stimulus remaining above the water. Subjects were ventilated with filtered and oxygenated sea water (1 l min⁻¹) that was temperature controlled (20±2°C) to minimize the potentially confounding effects of temperature on ERG recordings (Saszik and Bilotta, 1999; Fritsches et al., 2005). Fish were dark adapted for at least 30 min prior to any measurements (see Horodysky et al., 2008).

Experiments were conducted during both day and night to control for any circadian rhythms in visual response (McMahon and Barlow, 1992; Cahill and Hasegawa, 1997; Mangel, 2001). We defined ‘day’ and ‘night’ following ambient photoperiods. At the conclusion of each experiment, fish were euthanized via a massive overdose (~300 mg kg⁻¹) of sodium pentobarbital (Beuthanasia-D, Schering-Plough Animal Health Corp., Union, NJ, USA).

Whole-animal corneal ERGs were conducted to assess the absolute sensitivities, temporal properties and spectral sensitivities. Teflon-coated silver–silver chloride electrodes were used for recording ERGs. The active electrode was placed on the corneal surface and a reference electrode was placed subdermally in the dorsal musculature. ERG recordings and stimulus presentations were controlled using software developed within the LabVIEW system (National Instruments, Austin, TX, USA).

Absolute luminous sensitivities were assessed via intensity–response (V/logI) experiments described previously (Horodysky et al., 2008). Briefly, six orders of magnitude of stimulus intensity were presented to subjects using appropriate combinations of Kodak Wratten 1.0 and 2.0 neutral density filters (Eastman Kodak Co., Rochester, NY, USA) via an Advanced Illumination SL-2420-WHI white LED light source that had a working range of roughly three log₁₀ units, and a maximum output intensity of 1585 cd m⁻². Light intensities were calibrated with a research radiometer (model IL 1700, International Light, Inc., Newburyport, MA, USA). V/logI experiments progressed from subthreshold to saturation intensity levels in 0.2 log unit steps. At each intensity step, ERG b-waves were recorded from a train of five 200 ms flashes, each separated by 200 ms rest periods. This process was repeated three times, recorded and normalized to the maximum voltage response (V_max). Mean V/logI curves for each species were created by averaging the V/logI curves of individuals of that species. Interspecific comparisons of relative luminous sensitivity were made at stimulus irradiances eliciting 50% of V_max (referred to as K₅₀). Dynamic ranges, defined as the log irradiance range between the limits of 5–95% V_max (sensuFrank, 2003), were calculated separately for day and night experiments.

The temporal resolution of sciaenid visual systems was assessed via flicker fusion frequency (FFF) experiments using the white light LED source described above and methods developed by Fritsches and colleagues (Fritsches et al., 2005). Sinusoidally modulated white light stimuli ranging in frequency from 1 Hz (0 log units) to 100 Hz (2.0 log units) were presented to subjects in 0.2 log unit frequency steps, repeated three times at each frequency, and averaged for each subject. Light stimuli were presented for 5 s, followed by 5 s of darkness. Seven total FFF experiments were conducted for each subject: one at 25% (I₂₅) of maximum stimulus intensity (I_max) from the V/logI curve, and one at each log₁₀ step interval over six orders of magnitude of light intensity. A subject's FFF threshold at a given intensity was determined by analyzing the power spectrum of the averaged responses from 1 to 100 Hz and comparing the power of the subject's response frequency (signal) with the power of a neighboring range of frequencies (noise). Diel and interspecific comparisons were conducted on the FFF data at I_max and I₂₅. The FFF at I_max was considered to be the probable maximum FFF attainable by the visual system of a given species, and FFF at I₂₅ to be a proxy for ambient environmental light intensity (Horodysky et al., 2008).

Intraspecific diel differences in spectral sensitivity curves were assessed by subtracting the day and night curves and calculating confidence intervals (CI) of the resulting difference curve. In this analysis, positive values corresponded to increased day sensitivity; negative values indicated increased nocturnal sensitivity. Significant differences in spectral sensitivity were defined where the mean±CI of difference curves did not encompass zero.

To form hypotheses regarding the number and spectral distribution of pigments potentially contributing to piscivore spectral ERG responses, we fitted the SSH (Stavenga et al., 1993) and GFRKD (Govardovkii et al., 2000) vitamin A1 rhodopsin absorbance templates separately to the photopic spectral sensitivity data (Horodysky et al., 2008). A range of possible conditions was considered: 1–3 α-band rhodopsins, 1–3 α-band rhodopsins with a single β-band on any pigment, and 1–3 α-band rhodopsins with multiple β-bands. For a given species, condition and template, models of summed curves were created by adding the products of pigment-specific templates and their respective weighting factors. Estimates of the unknown model parameters (λ_max values and their respective weighting proportions) were derived by fitting the summed curves to the ERG data using maximum likelihood.

White light-evoked ERG b-wave responses of the four piscivores increased non-monotonically with stimulus intensity to maximum amplitudes (V_max) of 30–400 μV, then decreased at intensities above those at V_max (Fig. 2), presumably due to photoreceptor saturation and a lack of pigment regeneration. The K₅₀ values of V/logI curves differed significantly among species (F_3,16=18.83, P<0.0001) and between diel periods (F_1,16=44.23, P<0.0001). The interaction between species and diel period was also significant because of diel differences in K₅₀ values of pelagic piscivores but not for benthic summer flounder (F_1,16=11.18, P<0.0003). Tukey's post-hoc comparisons revealed that the mean photopic K₅₀ values of summer flounder were significantly left-shifted (0.5–1.8 log units, P<0.05) relative to the other piscivores, indicating higher sensitivity to dim light. Mean photopic dynamic ranges of the four species, defined as 5–95% of V_max, varied between 1.84 and 3.35 log units and scotopic dynamic ranges between 2.34 and 3.32 log units. Dynamic ranges varied significantly among the species (F_3,16=11.18, P<0.0003) and diel periods (F_3,16=36.43, P<0.0001); however, the significant interaction term (F_3,16=6.57, P<0.005) compromised interpretation. Pelagic piscivores generally had narrower photopic dynamic ranges with varying degrees of diel differences, contrasting with the broader, diel-invariant dynamic range of benthic summer flounder.

Piscivore FFF values (Fig. 3) varied significantly among the four species (F_3,20=9.82, P<0.003), with benthic summer flounder having significantly lower values than pelagic piscivores. FFF increased with increasing intensity (i.e. greater at I_max than at I₂₅; F_1,67=75.46.27, P< 0.001). Likewise, FFF values were significantly higher during the day than at night (F_1,67=75.46.27, P>0.001). This difference was most pronounced in cobia and striped bass. Interaction terms were not significant.

Piscivore photopic spectral sensitivities generally spanned 400–600 nm, with cobia having the narrowest spectral range (Fig. 4). Striped bass were a clear exception, exhibiting a high sensitivity to longer wavelengths (650 nm and above). Striped bass and bluefish demonstrated a significant nocturnal short wavelength shift, while cobia and summer flounder exhibited no such shifts (Fig. 4).

Given our data, maximum likelihood estimation using published SSH and GFRKD rhodopsin templates suggested that most of the Chesapeake Bay piscivores have multiple pigment mechanisms (Fig. 5). Striped bass (SSH; λ_max=542, 612 nm) and summer flounder (GFRKD; λ_max=449, 524 nm) photopic spectral sensitivities were consistent with the presence of two α-band vitamin A1 pigments (Table 2). In contrast, bluefish were fitted with four rhodopsins (GFRKD; λ_max=433, 438, 507, 547), and the cobia spectral sensitivity curve was fitted by a single rhodopsin (SSH) centered at 501 nm.

The number, properties and distribution of photoreceptor cells in fish visual systems, their luminous sensitivities, chromatic sensitivities and photopigments, and correlations to the photic properties of habitats have received rigorous attention in the literature (McFarland and Munz, 1975; Dartnall, 1975; Levine and MacNichol, 1979; Bowmaker, 1990; Parkyn and Hawryshyn, 2000). The functional characteristics of the visual systems of fishes generally reflect the aquatic light fields they inhabit, within ecological and phylogenetic constraints (Guthrie and Muntz, 1993). Luminous and chromatic sensitivities as well as temporal and spatial properties of fish visual systems are therefore useful metrics to describe the functions and tasks of aquatic visual systems (Lythgoe, 1979; Warrant, 1999; Marshall et al., 2003).

The range of light from which visual information can be obtained is extended in fishes with duplex retinae that use cone cells under photopic (bright) conditions and rod cells during scotopic (dim/dark) conditions (Lythgoe, 1979; Crescitelli, 1991). Piscivore luminous sensitivities, evidenced by the K₅₀ points and dynamic ranges of V/logI curves, are comparable to those of other Chesapeake Bay fishes (Horodysky et al., 2008) and a range of freshwater and marine teleosts (Naka and Rushton, 1966; Kaneko and Tachibana, 1985; Wang and Mangel, 1996; Brill et al., 2008). Coastal and estuarine piscivores demonstrated less luminous sensitivity than deep sea fishes (Warrant, 2000) and mesopelagic arthropods (Frank, 2003). In fact, striped bass, bluefish and cobia, which frequently forage in shallow coastal and estuarine waters, had fairly high K₅₀ values (~1–2 log cd m⁻²) and very narrow dynamic ranges, similar to those observed in black rockfish (Sebastes melanops), a coastal Pacific sebastid (2.0 log cd m⁻²) (Brill et al., 2008). These three pelagic piscivores demonstrated significant diel shifts in luminous sensitivity, presumably as a result of retinomotor movements (Ali, 1975). In daylight, the luminous sensitivities of striped bass, bluefish and cobia were substantially more right-shifted (i.e. less sensitive), with narrower dynamic ranges and larger diel shifts, than those of pelagic-foraging sciaenid fishes from the same estuary (Fig. 6) (Horodysky et al., 2008). The K₅₀ values of benthic summer flounder (0.14–0.17 log cd m⁻²), were similar in magnitude and relative diel invariance to those of demersal Pacific halibut (Hippoglossus stenolepis: 0.14–0.15 log cd m⁻²) (Brill et al., 2008) and benthic foraging sciaenids (−0.24–0.30 log cd m⁻²) (Horodysky et al., 2008) (Fig. 7). The luminous sensitivities of coastal flatfishes, and of other benthic foragers, tend toward the more sensitive end of an emerging continuum for coastal fishes, consistent with their use of low light habitats. In contrast, shallow-dwelling diurnal piscivores have lower but more plastic luminous sensitivities, consistent with hunting in extensively variable photic habitats.

Temporal properties of coastal piscivore visual systems are also comparable to those of a range of diurnal freshwater and marine fishes, closely matching species-specific visual requirements and tasks (Warrant, 2004). The FFF of the four piscivores predictably increased with light intensity (sensuCrozier et al., 1938), as was observed in sciaenid fishes (Horodysky et al., 2008). The benthic summer flounder, however, had significantly lower FFF at I₂₅ than the three pelagic piscivores, consistent with the use of comparatively deeper and dimmer waters by this flatfish. Daytime FFF at I₂₅ ranged little among the three pelagic piscivores (47–50 Hz), but cobia and bluefish attained these values at intensities ~1 order of magnitude lower than striped bass, suggesting that the latter may be more light-limited or may forage on more active prey in clearer waters that the former species. Maximum FFFs, which reveal the scope of the visual system when light is not limiting, were lowest for flounder, intermediate for bluefish and highest for cobia and striped bass. Predators that forage on rapidly swimming prey in clear and bright conditions, such as yellowfin and bigeye tunas (Thunnus albacares and T. obesus, respectively), have high FFFs and low spatial summation of photoreceptors [60–100 Hz; evoked potentials (EP) (Bullock et al., 1991); ERGs (Brill et al., 2005)]. In contrast, nocturnal species and those that forage in dim light, such as broadbill swordfish and weakfish (Xiphias gladius and Cynoscion regalis, respectively), have low FFFs and high spatial summation of photoreceptors [ERGs (Fritsches et al., 2005; Horodysky et al., 2008)]. Cobia and striped bass maximum FFF were therefore comparable to those of epipelagic scombrids, those of bluefish were similar to most sciaenids (~50–60 Hz) and freshwater centrarchid sunfishes (51–53 Hz), while those of flounder were analogous to crepuscular-foraging weakfish (42 Hz) [ERGs (Crozier et al., 1936; Crozier et al., 1938; Horodysky et al., 2008); EP (Bullock et al., 1991)]. Collectively, maximum FFFs of benthic and nocturnal species in coastal and estuarine waters are lower than those of daytime foraging pelagic species (Figs 6 and 7). We caution that the above metanalysis may be limited by differences in ecosystems as well as experimental and analytical techniques among these many studies, but consider the collective synthesis to be consistent with ecologies of the species discussed.

Chromatic properties of the visual systems of piscivores can likewise be placed in the context of fishes from this and other ecosystems. Coastal fishes are generally sensitive to a shorter subset of wavelengths than many freshwater fishes and a longer range of wavelengths than coral reef, deep sea and oceanic species (Levine and McNichol, 1979; Marshall et al., 2003). For maximum sensitivity in an organism's light microhabitat, scotopic (rod-based) pigment absorption spectra should match the ambient background to optimize photon capture [‘Sensitivity Hypothesis’ (Bayliss et al., 1936; Clark, 1936)]. Maximal contrast between an object and the visual background is provided by a combination of matched and offset visual pigments [‘Contrast Hypothesis’ (Lythgoe, 1968)]. Fishes that possess multiple spectrally distinct visual pigments likely use both mechanisms, depending on the optical constraints of their specific light niches (McFarland and Munz, 1975). Western North Atlantic piscivores demonstrated broad, species-specific responses to wavelengths ranging from the blue (~440 nm) to the yellow–orange (600–650 nm) end of the spectrum (Fig. 4). Responses blue-shifted nocturnally in striped bass and bluefish, whereas cobia and flounder showed no diel shifts. Coastal and estuarine fishes are commonly dichromats possessing short wavelength visual pigments with λ_max values ranging from 440 to 460 nm and intermediate wavelength pigments with λ_max values of 520 to 540 nm (Lythgoe and Partridge, 1991; Lythgoe et al., 1994; Jokela-Määttä et al., 2007; Horodysky et al., 2008).

Chromatic sensitivities of the four piscivores indicate species-specific pigment mechanisms based on a comparison of rhodopsin templates fitted to our ERG data and published microspectrophotometry (MSP) estimates of pigment λ_max for the species (Table 2). The ERG data of juvenile cobia were consistent with a single rhodopsin pigment. Although it is unclear whether this condition remains throughout ontogeny in the species, monochromacy occurs in other large aquatic predators including cetaceans, phocids and elasmobranchs such as the sandbar shark (Peichl et al., 2001; Litherland, 2009). Striped bass and summer flounder appear to have two visual pigments while bluefish appear to have four (Levine and MacNichol, 1979; Miller and Korenbrot, 1993; Jordan and Howe, 2007). Template fitting procedures may not extract the exact λ_max values from prior MSP studies due to potential differences in habitats, experimental error in ERG and/or MSP experiments, the generally poor performance of rhodopsin templates at short wavelengths (Govardovskii et al., 2000), or a combination of these factors. ERG is well suited for comparative investigations of vision and form–function relationships in fishes (Ali and Muntz, 1975; Pankhurst and Montgomery, 1989) and measures summed retinal potentials that account for any filtration by ocular media, which MSP does not (Brown, 1968; Ali and Muntz, 1975). Selective isolation of individual mechanisms and behavioral experiments may help determine the functions of multiple cone mechanisms (Barry and Hawryshyn, 1999; Parkyn and Hawryshyn, 2000); however, cone morphologies, their photopigments and distributions were beyond the scope of our study. Comparison of MSP estimates with those resulting from the rhodopsin template fitting procedures (Horodysky et al., 2008) suggest that the latter provides useful comparative insights into visual systems with few, fairly widely spaced visual pigments. The procedure does, however, risk mischaracterizing λ_max in species with many closely spaced pigments and/or when underlying data are sparse and fitting procedures balance optimization and parsimony.

Collectively, the luminous, temporal and chromatic properties of the visual systems of coastal and estuarine fishes are consistent with inferences based on ecology and lifestyle (this study) (Horodysky et al., 2008). The eyes of daytime-active pelagic piscivores, such as striped bass, bluefish and sciaenid spotted seatrout (Horodysky et al., 2008) have fast temporal resolution, limited photopic luminous sensitivity and broadly tuned chromatic sensitivity, consistent with foraging on fast-moving planktivorous fishes in well-lit waters (Fig. 6). Daytime active pelagic piscivores, such as striped bass and spotted seatrout, enhance resolution at the expense of luminous sensitivity during daylight hours, but increase nocturnal sensitivity, presumably at the expense of acuity, to match their diurnal light niches (Horodysky et al., 2008). In contrast, deeper-dwelling piscivores, such as summer flounder and weakfish, have comparatively slower, more sensitive vision, higher spatial summation and reduced acuity (K. Fritsches, personal communication) (Warrant, 1999; Horodysky et al., 2008). These species exhibit few diurnal differences in visual properties (Figs 6 and 7), presumably because their light niches are consistently dim.

Increasing turbidity asymmetrically affects the distances over which conspecifics, predators and prey interact. For encounter-rate feeders (i.e. many larvae and planktivores), turbidity resuspends forage and may serve as cover, decreasing sighted distances and increasing escape rates from predatory attacks (Utne-Palm, 2002). Benthic foragers are typically well adapted to low-light ambient conditions typical of turbid habitats, and many also feature enhancement of other sensory modalities to increase prey detection (Huber and Rylander, 1992). Conversely, reductions in ambient light intensity and veiling effects impede the ability of low-sensitivity, high-contrast piscivore visual systems to view fast-moving planktivorous prey against strongly turbid backgrounds (De Robertis et al., 2003; Thetmeyer and Kils, 1995; Turesson and Bronmark, 2007). Moderate turbidity may actually improve the contrast of prey against estuarine backgrounds (Utne-Palm, 2002), but the visual systems of striped bass and bluefish require bright light for optimal function and should thus be frequently disadvantaged in coastal habitats rendered highly turbid by human activities. Anthropogenic light pollution in coastal habitats may, however, extend the duration of photopic vision and thus visual foraging via general illumination of the night sky in urbanized areas (sensuMazur and Beauchamp, 2006), and by constraining nocturnal foraging arenas to small, highly illuminated point sources such as dock and bridge lights. Human impacts may thus be ecologically structuring factors in coastal ecosystems that both benefit and impede visually feeding piscivores, with turbidity further exerting contradictory and asymmetric effects on different trophic levels and life stages (Utne-Palm, 2002).

Optical conditions in coastal and estuarine waters are complex and have changed dramatically over the past century due to human activities (Kemp et al., 2005), with potentially large consequences for visually foraging piscivores. Characterizing visual function of nearshore fishes is a first step, but many questions remain on topics such as ambient light levels in specific light niches (Marshall et al., 2006) as well as light threshold effects on predator–prey interactions (Mazur and Beauchamp, 2003; De Robertis et al., 2003), reproduction (Engström-Östa and Candolin, 2007), and fishery gear interactions (Buijse et al., 1992). The effects of ambient light fields on the reflectance of conspecifics, prey and competitors, encounter and reaction distances, and the manner in which these change in space and time should also be investigated to gain insight into visual systems and tasks for a species (Levine and MacNichol, 1979; Johnsen, 2002). Comparative approaches investigating the form–function–environment relationships between sensory ecophysiology, behavioral ecology and ecosystem dynamics are thus important to mechanistically link processes from the cellular to the individual to the population level to support better management of aquatic resources.

We thank Captain S. Wray, J. Lucy, J. Smith and P. Lynch, and the vessels Bada Bing and Sea Beaver, for their assistance collecting study animals. M. Patterson, S. Johnsen and L. Litherland kindly provided comments on earlier drafts of this manuscript. K. Fritsches and L. Litherland patiently provided assistance with lamp calibrations and electroretinographic experiments, and M. Luckenbach, R. Bonniwell and S. Fate provided logistical assistance and extreme flexibility in support of these experiments. Assistance with animal husbandry was graciously provided by A. Buchheister, P. Lynch, C. Magel, S. Musick, T. Nania, L. Rose and J. Woodward. This research was funded by the Virginia Sportfish Development Fund, Virginia Marine Resources Commission. Partial support was also provided by the National Marine Fisheries Service and by an award to A.Z.H. from the International Women's Fishing Association. E.J.W. is grateful for the ongoing support of the Swedish Research Council (VR). This is VIMS contribution number 3064.