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Visual Biology of Hawaiian Coral Reef Fishes. II. Colors of Hawaiian Coral Reef Fish

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Visual Biology of Hawaiian Coral Reef Fishes. II. Colors of Hawaiian Coral Reef Fish Copeia, 2003(3), pp. 455–466 Visual Biology of Hawaiian Coral Reef Fishes. II. Colors of Hawaiian Coral Reef Fish N. J. MARSHALL,K.JENNINGS, W. N. MCFARLAND, E. R. LOEW, AND G. S. LOSEY The colors of 51 species of Hawaiian reef fish have been measured using a spec- trometer and therefore can be described in objective terms that are not influenced by the human visual experience. In common with other known reef fish populations, the colors of Hawaiian reef fish occupy spectral positions from 300–800nm; yellow or orange with blue, yellow with black, and black with white are the most frequently combined colors; and there is no link between possession of ultraviolet (UV) re- flectance and UV visual sensitivity or the potential for UV visual sensitivity. In con- trast to other reef systems, blue, yellow, and orange appear more frequently in Hawaiian reef fish. Based on spectral quality of reflections from fish skin, trends in fish colors can be seen that are indicative of both visually driven selective pressures and chemical or physical constraints on the design of colors. UV-reflecting colors can function as semiprivate communication signals. White or yellow with black form highly contrasting patterns that transmit well through clear water. Labroid fishes display uniquely complex colors but lack the ability to see the UV component that is common in their pigments. Step-shaped spectral curves are usually long-wave- length colors such as yellow or red, and colors with a peak-shaped spectral curves are green, blue, violet, and UV. HE reasons why reef fish are so colorful ful discussion, see Endler, 1981, 1984), or dis- T have been the subject of speculation since ruption (Cott, 1940), aposomatism (Ehrlich et Darwin’s time (Darwin, 1859; Longley, 1917a; al., 1977), temperature control (Fox and Vevers, Lorenz, 1962), with the Hawaiian Islands and 1960). Some coloration could result from phy- their reef fish having been particularly closely logenetic constraint or a nonfunctional meta- scrutinized (e.g., Longley, 1918; Lorenz, 1962; bolic byproduct (Longley, 1917a,b; Fox and Vev- Barry and Hawryshyn, 1999). When faced with ers 1960). All of these possibilities are rendered the many colors of reef fish, it is tempting to more complex by the ability of almost all reef describe them using our human eyes. This can fish to change color on one or more of a num- lead to erroneous conclusions if we then try to ber of time scales from subsecond to ontoge- draw behavioral or physiological conclusions netic (Townsend, 1929; Crook, 1997a,b). Here based on this experience (Cuthill et al., 1999). we describe only the spectral distribution and Reef fish visual systems (Losey et al., 2003) and frequency of the most commonly seen colors of their light environment (Marshall et al., 2003) 51 species of Hawaiian reef fish and attempt to are quite different from ours, and the way they place this body of data in the context of previ- see their own colors must necessarily be quite ous work. different from the way we see them. Here we Use of the human visual system to describe attempt a general description of a variety of Ha- color and its uses can be very misleading (Ben- waiian reef fish colors that is independent of nett et al., 1994; Cuthill et al., 1999; Endler, human perceptual experience. Marshall et al. 1990). This is well illustrated by a consideration (2003) use this and other data to begin to mod- of the ultraviolet (UV) part of the spectrum to el the design of reef fish colors and vision. which most mammals, including humans, are These are early steps in the study of the visual relatively insensitive ( Jacobs, 1993) but which ecology of reef fish, and therefore we try to may play an important role in processes such as draw some general conclusions that we hope sexual selection (Andersson and Amundsen, will be of use in future work. 1997; Andersson et al., 1998; Bennett et al., Coral reef dwellers are certainly one of the 1996), camouflage (Lavigne, 1976; Shashar, most colorful and varied assemblages of ani- 1994), and food choice (Church et al., 1998). mals. Reasons suggested for the ‘‘bright’’ col- UV is of primary interest in this paper. It is im- oration of reef fish include territorial marking portant to realize, however, that just because we (Lorenz, 1962), sexual display (Thresher, 1984), do not see it, UV is not necessarily more im- camouflage through object or background portant to animals that do see it than is any oth- matching (Randall and Randall, 1960; for a use- er spectral region. q 2003 by the American Society of Ichthyologists and Herpetologists 456 COPEIA, 2003, NO. 3 Approximately half of the species of reef fish- spectrometer, or ‘‘Sub-Spec,’’ an Andor Tech- es examined to this date are largely insensitive nology submersible spectrometer that is fully to UV based on ocular media transmission mea- described in Marshall (1996, 2000a). These in- surements (Thorpe et al., 1993; Siebeck and struments and their use are detailed elsewhere Marshall, 2001; Losey, et al., 2003). Although (Endler, 1990; Marshall, 1996, 2000b). the remainder may allow UV to reach the retina The sampling area of the Sub-Spec spectrom- and be detected, the value of UV-sensitive vision eter, which could be as small as 0.3 mm2 (de- to such fishes is unclear. Therefore, it is impor- pending on the range to the object being mea- tant to examine functional and ecological dif- sured) was visualized through a sighting optic ferences between reef fishes that do and those that is much like the viewfinder for a single lens that do not detect UV. This is particularly in- reflex (SLR) camera but with a sampling fiber- triguing for body colors and color patterns be- optic embedded centrally in the mirror-plane of cause it raises the possibility of a communica- the optical system. The light reflected from a tion channel open only to species with UV visual colored area on a fish was sampled through the sensitivity and closed to all others. fiber optic and stored by the spectrometer. With S2000 measurements, the bare end of a fiber MATERIALS AND METHODS optic probe attached to the spectrometer was placed close to the fish at a 458 angle so that it All fish were caught using hand nets and bar- sampled from that colored region alone. Each rier nets or, occasionally, rod and line either by measurement was an average of three to 10 sam- researchers or local tropical fish suppliers. Fish ples of the same colored zone on the fish. De- were housed in marine aquaria at the Hawai’i tailed descriptions of spectrometers in general Institute of Marine Biology, University of Ha- and their design are available at the Ocean Op- wai’i, on Coconut Island, Kaneohe Bay. Fish col- tics website: www.Oceanoptics.com. ors were occasionally measured in situ or in Sampling color patches on a fish is a subjec- small aquaria but normally out of water. Efforts tive process in the choice of color patches to were made to reduce stress (and in some cases sample. We strove to include all qualitatively dif- the resulting color change) by anaesthetizing ferent hues. Toward this goal, we also used a fish with MS222 or clove oil or by removing UV-sensitive camera to image each fish to reveal them from the water for only a few seconds for possibly inconspicuous UV reflecting areas. De- measurement. They were placed in cloth soaked tails of UV camera design are found in Marshall in seawater and the skin was kept wet during (1996) and Losey et al. (1999a). measurements. For most species, results of this technique are equivalent to those when fish are Definition of color categories and spectral shapes.— kept in water (Marshall 1996, 2000a), and mea- The same 21 human-subjective color categories surements made out of water allow more exact- identified in Marshall (2000a) are used here to ing optical alignment with small spots and provide labels and ease description and com- stripes. Clove oil occasionally results in fish tak- parison of reef fish colors, not for quantitative ing on a dark coloration after several minutes, purposes. Colors discussed in relation to these so we made measurements before this com- specific categories are written in italics: color menced. Some species (the rapid color chang- without UV-Blue, Green, Yellow, Orange, Brown/Ol- ers such as some balistids and pomacentrids, for ive, Red, Blue/Red, Blue/Far-Red, Magenta, Black, example) changed color too rapidly and fre- Labriform-Green Complex; UV containing colors— quently for us to be confident that we were mea- UV, White, Violet, Blue-UV, Blue-UV-Hump, Green- suring their ‘‘normal’’ coloration. Data from UV, Yellow-UV, Orange-UV, Red-UV, Blue/UV/Red such fish were discarded. Whether this was the Labriform-Purple Complex. These categories are case for other fish was judged subjectively (by based on the appearance of the color to us and us closely examining fish in and out of water) the shape of the spectrum of the color (Fig. 1). and it remains possible that we overlooked For example, both Red and Red/UV may appear some colors that ‘‘disappear’’ or change without identical to our visual system; however Red/UV our knowledge or are outside of the range of contains a second region of reflectance in the human vision. Attention should be paid to such UV. Good examples of Yellow/UV and Orange/UV problems in more detailed descriptions of in- can be seen in Figure 1B. dividual species in future work.
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