Copeia, 2004(4), pp. 908–914

Photopic Spectral Sensitivity of Green and Loggerhead Sea

D. H. LEVENSON,S.A.ECKERT,M.A.CROGNALE,J.F.DEEGAN II, AND G. H. JACOBS

Flicker electroretinography (ERG) was used to examine the in situ photopic (cone- photoreceptor based) spectral sensitivities of Green and Loggerhead Sea Turtles. Both species were responsive to wavelengths from 440–700 nm, and both had peak sensitivity in the long wavelength portion of the spectrum (ϳ580 nm). For Logger- head Sea Turtles, no measurable responses were obtained below about 440 nm, whereas reliable signals were seen for Green Sea Turtles at wavelengths down to 400 nm. Both species exhibited significant declines in sensitivity below 500 nm. The overall shapes of the spectral sensitivity functions were similar for the two species. These results support previous findings that sea turtles have well-developed phot- opic visual systems. The characteristics of these spectral sensitivity functions indicate that both species possess multiple cone photopigment types, and these, in conjunc- tion with the presence of colored oil droplets, strongly imply a capacity for discrimination. Comparative evaluation suggests that these turtles have modified their visual pigments from those of their terrestrial relatives to better suit the am- bient conditions present in the shallow water, submarine environments that they typically inhabit.

ODERN sea turtles diverged from their wavelength sensitive visual pigments of marine M terrestrial and freshwater relatives rough- turtles toward shorter wavelengths. MSP also re- ly 150 million years ago (Pritchard, 1997). They veals that the light-absorbing oil droplets pre- live an almost exclusively marine existence, re- sent in marine cone photoreceptors are turning to the ocean within a few hours of different from those of terrestrial and freshwa- hatching and subsequently rarely returning to ter turtles (Granda and Haden, 1970; Granda land. Sea turtles are currently distributed world- and Dvorak, 1977). wide throughout the tropical and subtropical Although there is evidence that the visual oceans, with some species occasionally ranging sense is important to sea turtles throughout all into higher, more temperate latitudes. Sea tur- stages of their life cycle (Ehrenfeld and Carr, tles occupy a variety of ecologic niches. For in- 1967; Kingsmill and Mrosovsky, 1982; Lohmann stance, adult Green Sea Turtles (Chelonia mydas) et al., 1990), relatively little is known about their are generally found near shore feeding on plant in situ visual sensitivities; most previous work and algal matter, whereas others, such as adult has been directed at the individual photorecep- Loggerhead Sea Turtles (Caretta caretta) may tors. Because several conservation issues cur- stay farther offshore, diving deeper to forage on rently facing marine turtles can be related, at benthic invertebrates and fish (Bjorndal, 1997). least in part, to the effects of anthropogenic Anatomical examinations reveal that, in con- light sources, there is a particular need for a trast to terrestrial and freshwater turtles, the better understanding of the visual abilities of liv- of sea turtles have round lenses, much like ing turtles (e.g., Witherington, 1991; Witzell, those found in fish, to compensate for the loss 1999). As a step in this direction, we have used of corneal refraction under water (Walls, 1942; a noninvasive technique, rapid-flicker electro- Ehrenfeld and Koch, 1967; Northmore and retinography (ERG), to investigate the photopic Granda, 1991). The spectral sensitivity of ma- (cone-photoreceptor based) visual sensitivities rine turtles is also different from that of their of two marine turtle species, Green and Log- land-based relatives (Liebman and Granda, gerhead Sea Turtles. This type of ERG is partic- 1971; Granda and Dvorak, 1977). Microspectro- ularly relevant to behavioral/conservation is- photometric (MSP) evaluations of Green Sea sues, because it reflects the actual sensitivity of Turtle photoreceptors show that 11-cis retinal is the eyes of the animal, including the combined used as the light sensitive chromophore com- effects of the cone visual pigments, oil droplets, ponent of sea turtle visual pigments; land based and other sources of intraocular scattering and turtles typically use 3,4 di-dehydroretinal (Lieb- absorption (e.g. cornea, lens). Rapid-flicker man and Granda, 1971; Loew and Govardovski, ERG was chosen over the single flash ERG tech- 2001). This substitution has the effect of sub- nique previously used with Green Sea Turtles stantially shifting the sensitivity of the longer (Granda and O’Shea, 1972), because it is better

᭧ 2004 by the American Society of Ichthyologists and Herpetologists LEVENSON ET AL.—SEA TURTLE VISUAL PIGMENTS 909 suited to isolating cone photoreceptor respons- ments, the was stimulated with a train of es and thereby potentially providing a more ac- light pulses originating from a high-intensity curate representation of in situ photopic sensi- (50-W tungsten-halide lamp) grating mono- tivity. Furthermore, by conducting parallel ex- chromator having a half bandpass of 15 nm. periments with two species, we reasoned that, The light was imaged onto the retina in Max- because the individual cone photopigments of wellian view in the form of a spot subtending the Green Sea Turtle have been previously mea- 59 deg. The test light was temporally modulated sured, we could use the ERG measurements on with electromechanical shutters (Vincent Asso- Green Sea Turtles to draw more precise infer- ciates, Rochester, NY) as a square-wave pulse ences about the photoreceptor complements of having a 25% duty cycle so as to achieve any Loggerhead Sea Turtles. desired flicker rate. The fundamental frequency component of the ERG response was extracted MATERIALS AND METHODS by filtering and this signal was averaged over a total of 50 presentations. Spectral sensitivity Live adult (all greater than 30 years old) functions were measured using two techniques. Green and Loggerhead Sea turtles were exam- In the first case, a flicker photometric proce- ined at SeaWorld, San Diego, California. Re- dure was employed in which the responses to cordings were obtained from four Green Sea the test light and those given to an interleaved Turtles and six Loggerhead Sea Turtles. It was reference light (achromatic, 14 log photons/ not possible to determine the gender of some sec/sr) that illuminated the same region of the of the turtles, but at least one male and one retina and flickered at the same temporal fre- female were examined from each species. These quency were compared. Over successive presen- animals were maintained in captivity in seawater tations, the intensity of the monochromatic test exhibits before and after recording. All animal light was adjusted by changing the position of a husbandry and experimental procedures were 3.0-log unit neutral-density wedge until the light conducted according to protocols approved by produced a response equal to that given to the the SeaWorld Institutional Animal Care and Use fixed reference light. Repetition of this proce- Committee (IACUC) and were overseen by the dure for a range of different test wavelengths veterinary staff at SeaWorld. can be used to define a spectral sensitivity func- Photopic (cone-photoreceptor based) spec- tion ( Jacobs and Neitz, 1987). In a second set tral sensitivity was evaluated for each turtle in of measurements, spectral sensitivity functions vivo using flicker electroretinography (ERG). were similarly determined using a standard am- For this examination, animals were removed plitude-criterion method. In this case, the inten- from their holding pools and anesthetized with sity of the test light at each wavelength was ad- intravenous administration of ketamine (6.0–9.0 justed over successive presentations until it pro- mg/kg) and metatomadine (0.1 mg/kg) inject- duced a response with a constant amplitude of ed transdermally into the dilation of the exter- 3.2 ␮V. nal jugular vein at the base of the head. Once ERG temporal response functions were also anaesthetized, the turtles were positioned on a obtained. To accomplish this, the intensity of an slant board that was placed on an adjustable sur- achromatic (2850 K) flickering light was adjust- gical table, and the head position was stabilized ed to produce a response having a criterion am- through the use of padded restraints. Although plitude of 3.2 ␮V. This procedure was repeated the general anesthetic typically produced some for flickering lights varying in steps of 4 Hz degree of pupillary dilation, in some cases ad- from 4–40 Hz. For all of the spectral sensitivity ditional dilation was achieved by topical appli- and rate measurements, thresholds were deter- cation of atropine and ophthalmic neosyne- mined twice for each test condition and these phrine. The cornea was anesthetized by a topi- values subsequently averaged. All recordings cal application of proparacaine hydrochloride were made under moderate photopic illumina- (0.5%) prior to the installation of a bipolar con- tion produced by a mixture of indirect skylight tact-lens electrode of the Burian-Allen configu- and overhead fluorescent lighting that yielded ration. After the experiments were completed, an illuminance of 165 lux at the subject’s eye. the effects of the anesthesia were partially re- versed using atapamazole (0.1 mg/kg). In all RESULTS cases, full recovery was achieved without inci- dent. As recorded from the corneas of sea turtle The general technique used to record flicker eyes, flickering lights produced small but quite ERGs has been described in detail elsewhere reliable ERG signals. For example, Figure 1A ( Jacobs et al., 1996). In the present experi- shows a representative intensity/response func- 910 COPEIA, 2004, NO. 4

Fig. 1. (A) An example of a flicker ERG intensity/response function obtained from a Loggerhead Sea Turtle. The datapoints are mean amplitudes obtained from four presentations of an achromatic test light flickered at 20 Hz. The intensity of the stimulus is as specified at the cornea. The fitted line is a Michaelis- ϭ ␮ ϭ Menton function. The values of the three parameters for this fit are Vmax 22.9 V; k 15.2 log-photons/ sec/sr; ␩ϭ0.68. These three index, respectively, voltage at saturation, intensity required for half-maximum amplitude, and a slope parameter. (B) Photopic spectral sensitivity curves for Green and Loggerhead Sea Turtles obtained with the flicker-photometric ERG procedure described in the text. The datapoints are mean values for the numbers of animals specified and the error bars represent Ϯ 1 standard deviation. The data- points have been interconnected with straight lines. tion obtained from a Loggerhead Sea Turtle to amplitudes recorded under these flickering- 20 Hz flicker. The plotted points represent the light test conditions were modest in size (in the mean amplitudes recorded for four successive range of 20–50 ␮V), they were, as noted, highly presentations of the test light each of which in reliable; for example, the SD values for the re- turn consisted of 50 stimulus cycles. The line sponses of Figure 1 averaged less than 1 ␮V fitted through the datapoints was derived from across the full span of stimulus intensity. the Michaelis-Menton function, a metric typi- Figure 1B summarizes the spectral sensitivity cally used to account for intensity-response re- functions obtained from 10 sea turtles as deter- lationships for signals recorded early in visual mined with ERG flicker photometry using 20- systems, including photoreceptor responses re- Hz flicker. The functions for both species peak corded directly from cones of freshwater turtles at about 580 nm. The sensitivities of the two are (Granda and Dvorak, 1977). Although the peak indistinguishable from that point out to the lon- ger wavelengths. However, the sensitivity curve for the Loggerhead Sea Turtles falls off more steeply toward the short wavelengths than does the equivalent function obtained from the Green Sea Turtles. With this technique it proved impossible to make sensitivity measure- ments for wavelengths shorter than about 500 nm. Note that the individual variability for each species over this spectral range is quite small with SD values averaging 0.1-log unit or less. In an attempt to extend the spectral range of the spectral sensitivity functions, we also tested these same animals using the amplitude-criteri- on procedure. The results are shown in Figure 2, which again summarizes results obtained from the same 10 animals. With this procedure, it proved possible to obtain sensitivity measure- Fig. 2. Photopic spectral sensitivity curves for Green and Loggerhead Sea Turtles obtained from an ments from 700 nm well down into the short amplitude-criterion procedure. The test light was wavelengths (400 nm and 440 nm for the Green flickered at 20 Hz. Other details are the same as for and Loggerhead Sea Turtles, respectively). As Figure 1B. for the flicker photometric results, both species LEVENSON ET AL.—SEA TURTLE VISUAL PIGMENTS 911

show a sensitivity peak at about 580 nm with a flicker ERG more securely isolates signals from smooth (and equivalent) falloff in sensitivity to cones than the single-flash procedure, even the longer wavelengths. To the shorter wave- when the latter is conducted in a light-adapted lengths the shapes of the functions for the two eye. Thus, it is conceivable that some contribu- species are similar with a secondary peak at tions from rods are represented in the earlier about 520 nm and a region of near constant study’s spectral sensitivity results. The relatively sensitivity below about 500 nm. As in the flicker high frequency temporal responses of both spe- photometric spectral sensitivity functions, the cies (up to 36 Hz) support the conclusion that Loggerhead Sea Turtles had consistently lower our data are representative of cone photorecep- sensitivity to all of the test wavelengths shorter tor responses (see Jacobs et al., 1996). Perhaps than the principal peak. It is also apparent that more important is the great difference in age the variability among animals is larger for the of the turtles examined in the two experiments. shorter test wavelengths and that this is partic- In the earlier experiment, the turtles were very ularly marked for the Loggerhead Sea Turtles young (somewhere between two and 16 months at wavelengths shorter than 500 nm. Variability of age; Granda and O’Shea, 1972). There are within individuals remained relatively consistent not sufficient records available to age our sub- across the spectral range examined. jects accurately. The staff at SeaWorld indicates All of the above measurements were made at that they are all at least 30 years of age, and a single temporal frequency (20 Hz). To exam- perhaps some turtles are substantially beyond ine the effects of temporal rate on sea turtle that point. It is conceivable that with age the ERGs, we also measured thresholds for achro- ocular components of sea turtle eyes (cornea, matic lights across a range of temporal frequen- lens, etc.) become considerably less transmis- cies. For both species, temporal sensitivity was sive. In humans where age-related losses of oc- maximal over a relatively broad range extend- ular transmissivity have been extensively stud- ing from about 8–16 Hz. Sensitivity at 4 Hz was ied, these changes are often found to differen- only 0.25- to 0.5-log units below peak sensitivity. tially filter out short wavelength (␭Ͻ500 nm) At flicker rates above 12–16 Hz, sensitivity grad- energy (e.g., Weale, 1988). If this is also true for ually fell off to up to 36 Hz, where thresholds sea turtles, it might explain the differences in for both species were over 2.0-log units below short wavelength sensitivity seen in the two stud- peak values. At 40 Hz, no consistently reliable ies. In any case, the results of the two studies responses could be recorded and straight-line suggest there may be differences in short-wave- extrapolation of the frequency/sensitivity curve length sensitivity between young and aged sea suggests that 40 Hz represents the high-frequen- turtles. cy cutoff for both turtle species. For frequencies Earlier MSP measurements revealed the pres- greater than the peak, the sensitivity of the Log- ence of four types of photopigment in the ret- gerhead Sea Turtles was consistently (but not ina of the Green Sea Turtles: a rod pigment dramatically) lower than for the Green Sea Tur- with a 502 nm peak and three types of cone ␭ tles. This presumably reflects the lower sensitiv- pigment with respective peak values ( max)of ity of the former species to shorter test wave- 440, 502, and 562 nm (Liebman and Granda, lengths. 1971). As is typical of many , as well as a number of amphibians, monotremes and fishes, DISCUSSION the cone photoreceptors of the Green Sea Tur- tle also contain high-density oil droplets (Gran- Previous measurements of the spectral sensi- da and Haden, 1970). Because these oil drop- tivity of Green Sea Turtles have been made us- lets are interposed in the optical pathway to the ing a single-flash ERG technique (Granda and outer segments, if colored, they can serve to O’Shea, 1972). In both the dark- and light- spectrally filter incoming light. In the Green Sea adapted eye the spectral sensitivity functions Turtle there are three classes of oil droplets, had multiple peaks at about 600 nm, 520 nm, clear, yellow, and orange. They are selectively and 460 nm. The spectral sensitivities we mea- paired with the cone pigments to form what are sured for Green Sea Turtles are roughly similar potentially six spectrally discrete classes of re- to these earlier results, although the long wave- ceptor (Liebman and Granda, 1971). The net length peak is somewhat shorter in the present effect of these pairings is to effectively shift the ␭ ϳ measurements ( max 580 nm) and the short- spectral sensitivity of two of the cone classes to wavelength peak is much less clearly defined. longer wavelengths. As in Granda and O’Shea There are other differences between the two ex- (1972), the shifted positions of the two longer periments, two of which are potentially impor- wavelength peaks in the Green Sea Turtle ERG tant. The first is that the use of high frequency sensitivity curve reflect this (Fig. 2). 912 COPEIA, 2004, NO. 4

The spectral sensitivity functions obtained tion of sea turtle visual systems suggests that from Loggerhead Sea Turtles are similar in these animals have largely retained diurnally shape to those derived for Green Sea Turtles, adapted visual systems like those of their reptil- suggesting a similar cone pigment and oil drop- ian/avian relatives. Their broad spectral sensi- let complement in the two species. Direct com- tivity corresponds well with the type of light parisons can be made for one of the cone pig- available in relatively shallow, well-lit marine wa- ments in the two species. This is because, as not- ters, rather than that of the dim, nearly mono- ed above, the oil droplets function as long-pass chromatic deep oceanic water (Kirk, 1994). filters. The longest of these, the yellow droplets, They also have relatively small lenses (North- show no detectable absorption for wavelengths more and Granda, 1991) and cone-dominated longer than about 600 nm (Liebman and Gran- retinae with additional light filtering oil drop- da, 1971). Consequently, the long wavelength lets (Granda and Haden, 1970; Bartol and Mu- limb of the spectral sensitivity functions should sick, 2001). Even the very deep diving Leather- reflect principally the absorption properties of back Sea Turtle (Eckert et al., 1989) does not the longest of the cone pigments. To determine possess a particularly large lens, which might be the spectral position of this pigment, we shifted expected if these turtles were adapted for max- a standard photopigment absorption function imizing light capture (Northmore and Granda, (Govardovskii et al., 2001) along the wavelength 1991). axis to determine what pigment position best The presence of multiple functioning photo- accounted for the array of sensitivity values for receptor types also suggests that these turtles test lights of all wavelengths 600 nm and longer. have retained the ability to make color discrim- For the two estimates of sensitivity obtained for inations. Such abilities are lost in sensitivity Green Sea Turtles (Figs. 1, 2), these peaks were adapted marine mammals (Peichl et al., 2001; at 563 and 559 nm, respectively. These values Levenson and Dizon, 2003) and fish from deep- are very close to the position of the cone pig- er water habitats (e.g., Bowmaker et al., 1994; ment directly measured with MSP (562 nm). A Cowing et al., 2002) but are relatively common similar test of the two spectral sensitivities ob- in diurnally adapted fish, , and other rep- tained from Loggerhead Sea Turtles yielded es- tiles (Bowmaker, 1995; Yokoyama and Yokoya- timates of 562 and 563 nm. We conclude that ma, 1996). and the retinal circuitry these two species have in common their longest that supports that capacity have been extensive- cone pigment. Given the uncertainties pro- ly studied in freshwater turtles. Evidence sug- duced by oil droplet/pigment combinations de- gests that in these turtles the array of pigment scribed above, a similar comparison of other and oil droplet combinations and the neural cone pigment positions is not possible, al- support provide a multidimensional color vision though the general similarity of the shapes of system that is probably at least tetrachromatic in the spectral sensitivity functions strongly suggest nature (Neumeyer, 1998). Although both cone that they too are the same for these two sea tur- pigments and oil droplets differ for freshwater tles. and sea turtles, the presence of multiple pig- In general, the retinas of most turtles (Walls, ments and oil droplets in sea turtles strongly 1942; Granda and Dvorak, 1977), including the suggests that they are like their freshwater cous- marine species (Granda and Dvorak 1977; Bar- ins in enjoying a color vision capacity. The na- tol and Musick, 2001) are cone dominated, with ture of that capacity remains to be determined. cone:rod photoreceptor ratios of 2:1 or more All these observations suggest that the vision (Bartol and Musick, 2001). This is unlike other of sea turtles is primarily suited for use in phot- diving tetrapods, such as marine mammals that opic conditions. However, there is also reason typically have large, rod-dominated eyes to max- to conclude that the visual systems of sea turtles imize light capture, and a limited range of spec- have been modified for use in the marine en- tral sensitivity (Lavigne et al., 1977; Peichl et al., vironment. In comparison to closely related ter- 2001; Levenson and Dizon, 2003). Similarly, restrial turtles, both species of sea turtle exhib- many fish, particularly those inhabiting depths ited long wavelength sensitivity indicative of vi- visited by the deeper diving turtles (Ͼ 100 m), sual pigments that have been shifted toward the are strongly adapted to maximize light sensitiv- shorter wavelengths of light (␭ Յ 500 nm) typ- ity and exhibit evidence of reduced photopic ically prevalent in marine environments (Kirk, visual abilities (Lythgoe, 1979; Bowmaker, 1994). The cone pigments of the Green and 1995). This often includes a relatively narrow likely those of the Loggerhead Sea Turtles have ␭ range of spectral sensitivity in comparison to max 18 to 55 nm shorter in sensitivity than those similar, shallow water species (Bowmaker et al., of the land-based Red-Eared Slider (Trachemys 1994; Lythgoe et al., 1994). Qualitative evalua- scripta elegans; Liebman and Granda, 1971; Loew LEVENSON ET AL.—SEA TURTLE VISUAL PIGMENTS 913 and Govardovskii, 2001). Much of this sensitivity only be one of many factors to be considered change is undoubtedly related to a shift in chro- when examining the behavior of sea turtles or mophore. The essentially identical long wave- working to mitigate the effects of human activ- length sensitive pigments of Green and Logger- ities on sea turtle populations. head Sea Turtles suggest that both species, and perhaps then all marine turtles, have made the ACKNOWLEDGMENTS chromophore substitution to retinal from 3,4 di-dehydroretinal (Granda and Dvorak, 1977). Thanks to SeaWorld, San Diego, for their will- This same disparity is common between marine ingness to allow us to examine their animals and freshwater fish species; marine fishes typi- and to the SeaWorld animal husbandry staff for cally have retinal in their visual pigments and their skilled assistance in all aspects of the ex- the corresponding short wavelength shift in sen- periments (IACUC permit RR2001-15). Thanks sitivity (Bowmaker, 1995). also to W. Perrin, A. Dizon, P. Ponganis, G. The conclusion that sea turtle visual pigments Kooyman, and several anonymous reviewers for are well-suited for use in relatively well-lit, shal- critical reviews of earlier versions of the manu- low water marine environments concurs with script. This work was supported by a grant from the observed diving/foraging behavior of most the National Marine Fisheries Service, Honolu- species (Bjorndal, 1997). The photopic spectral lu, HI, to DHL and SAE. sensitivities of these sea turtles are clearly dif- ferent from those of the other diving tetrapod LITERATURE CITED groups, as they are different from their non- marine relatives. BARTOL,S.M.,AND J. A. MUSICK. 2001. Morphology In fact, the cone visual pigments of sea turtles and topographical organization of the retina of ju- are convergent in many ways with those of some venile Loggerhead Sea Turtles (Caretta caretta). Copeia 2001:718–725. of the tropical, shallow-water marine fish with BJORNDAL,K.A.1997. Foraging ecology and nutrition which they share habitat. Both have multiple of sea turtles, p. 29–50. In: Biology of sea turtles. P. pigment types and a broad range of sensitivity Lutz and J. A. Musick (eds.). CRC Press, Boca Ra- but are short-wavelength shifted in sensitivity ton, FL. when compared to similar species from fresh- BOWMAKER,J.K.1995. The visual pigments of fish. water/terrestrial habitats (Lythgoe et al., 1994; Prog. Retinal Eye Res. 15:1–31. Bowmaker, 1995; Losey et al., 2003). Indeed, ———, V. I. GOVARDOVSKII,L.V.ZUEVA,D.M.HUNT, considering the absence of reductions in phot- AND V. SIDELEVA. 1994. Visual pigments and the opic function for increased overall sensitivity photic environment: the cottoid fish of Lake Baikal. seen in deep water fish and mammals, one Vision Res. 34:591–605. COWING,J.A., S. POOPALASUNDARAM,S.E.WILKIE,J. might speculate that the visual sense may not be K. BOWMAKER, AND D. M. HUNT. 2002. Spectral tun- of great consequence to deep diving Logger- ing and evolution of short wave-sensitive cone pig- head and Leatherback Sea Turtles when they ments in cottoid fish from Lake Baikal. Biochem- venture to depths in excess of a few hundred istry 41:6019–6025. meters, as they sometimes do (Eckert et al., ECKERT,S.A.,K. L. ECKERT,P.PONGANIS, AND G. L. 1989; Bjorndal, 1997). This remains to be de- KOOYMAN. 1989. Diving and foraging behavior of termined. Leatherback Sea Turtles (Dermochelys coriacea). Can. However, it also important to consider the J. Zool. 67:2834–2840. ecological and behavioral ramifications of visual EHRENFELD,D.W.,AND A. CARR. 1967. The role of vision in the sea-finding orientation of the Green stimuli when considering the significance of the Turtle (Chelonia mydas). Anim. Behav. 15:25–36. sensitivity data presented here. The results from ———, AND A. L. KOCH. 1967. 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