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Factors Affecting Counterillumination As a Cryptic Strategy

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Factors Affecting Counterillumination As a Cryptic Strategy Reference: Biol. Bull. 207: 1–16. (August 2004) © 2004 Marine Biological Laboratory Propagation and Perception of Bioluminescence: Factors Affecting Counterillumination as a Cryptic Strategy SO¨ NKE JOHNSEN1,*, EDITH A. WIDDER2, AND CURTIS D. MOBLEY3 1Biology Department, Duke University, Durham, North Carolina 27708; 2Marine Science Division, Harbor Branch Oceanographic Institution, Ft. Pierce, Florida 34946; and 3Sequoia Scientific Inc., Bellevue, Washington 98005 Abstract. Many deep-sea species, particularly crusta- was partially offset by the higher contrast attenuation at ceans, cephalopods, and fish, use photophores to illuminate shallow depths, which reduced the sighting distance of their ventral surfaces and thus disguise their silhouettes mismatches. This research has implications for the study of from predators viewing them from below. This strategy has spatial resolution, contrast sensitivity, and color discrimina- several potential limitations, two of which are examined tion in deep-sea visual systems. here. First, a predator with acute vision may be able to detect the individual photophores on the ventral surface. Introduction Second, a predator may be able to detect any mismatch between the spectrum of the bioluminescence and that of the Counterillumination is a common form of crypsis in the background light. The first limitation was examined by open ocean (Latz, 1995; Harper and Case, 1999; Widder, modeling the perceived images of the counterillumination 1999). Its prevalence is due to the fact that, because the of the squid Abralia veranyi and the myctophid fish Cera- downwelling light is orders of magnitude brighter than the toscopelus maderensis as a function of the distance and upwelling light, even an animal with white ventral colora- visual acuity of the viewer. The second limitation was tion appears as a black silhouette when viewed from below addressed by measuring downwelling irradiance under (Johnsen, 2002). This is particularly disadvantageous be- moonlight and starlight and then modeling underwater spec- cause an object is detectable at a far greater distance when tra. Four water types were examined: coastal water at a viewed from below than when viewed from any other angle depth of 5 m and oceanic water at 5, 210, and 800 m. The (Mertens, 1970; Johnsen, 2002). Aside from extremely appearance of the counterillumination was more affected by transparent tissue, which is not easy to achieve in larger the visual acuity of the viewer than by the clarity of the species with complex tissues, the way to overcome this water, even at relatively large distances. Species with high disadvantage is for the ventral surface to emit light that visual acuity (0.11° resolution) were able to distinguish the matches the downwelling light in intensity, spectrum, and individual photophores of some counterilluminating signals angular distribution. Indeed, this solution is nearly ubiqui- at distances of several meters, thus breaking the camouflage. tous in nontransparent mesopelagic species, particularly in Depth and the presence or absence of moonlight strongly crustaceans, fish, and squid (Young and Roper, 1976; Her- affected the spectrum of the background light, particularly ring, 1977, 1985; Widder, 1999). near the surface. The increased variability near the surface Counterilluminating species have evolved complex strat- egies to match the intensity, spectrum, and angular distri- bution of the downwelling light (Denton et al., 1972; Young Received 15 December 2003; accepted 17 April 2004. and Mencher, 1980; Herring, 1983; Widder, 1999). One * To whom correspondence should be addressed. E-mail: sjohnsen@ duke.edu aspect that is poorly understood, however, is the spatial Abbreviations: MTF, modulation transfer function; OTF, optical transfer distribution of the photophores (Young and Roper, 1976). function; PSF, point spread function. While some species (e.g., the cookie cutter shark Isistius 1 2 S. JOHNSEN ET AL. brasiliensis) have many small photophores that evenly illu- viewer’s eye. The water and associated particulates poten- minate the ventral surface, most have a smaller number of tially dim and blur the image, and the acuity of the eye isolated photophores that produce uneven illumination (e.g., determines the resolution of the perceived image. Fig. 2d). Thus, even if the photophores match the spectrum The effect of the first factor is generally modeled in the and intensity of the downwelling light perfectly, the coun- following way. First, the optical effects of the water on the terilluminator will be visible when viewed at a distance that image of a point source are calculated. The image of a point allows these individual sources to be discerned. To inves- source is known as the point spread function (PSF) (Mertens tigate this problem, the effects of the intervening water and and Replogle, 1977). The point source is then convolved the viewer’s visual acuity on the perceived image of the with a given image to determine the appearance of the counterillumination must be understood. image after it passes through the water. In a convolution, This study examines the effects of underwater light scat- each point in the image is replaced by its product with the tering and visual acuity on the perceived images of coun- point spread function (Fig. 1). Fortunately, this computa- terillumination signals. The effects are modeled with Monte tionally expensive procedure can be streamlined using the Carlo methods and image transfer theory, using data col- convolution theorem, which states that for any two images lected from water types ranging from shallow coastal water I1 and I2, the convolution of I1 with I2 is equal to the inverse to the deep mesopelagic zone (800 m). Three visual sys- Fourier transform of the product of the Fourier transforms tems, with high, medium, and low acuity, are also exam- of the two images: that is, ined. The goal is to determine under which conditions ϭ ᏲϪ1͓Ᏺ͑ ͒ ⅐ Ᏺ͑ ͔͒ counterilluminators are still visible and what implications I1*I2 I1 I2 , (Fig. 1) (Equation 1) this has for both camouflage and visual detection under Ϫ where * denotes convolution, and Ᏺ(I) and Ᏺ 1(I) are the low-light conditions. Fourier and inverse Fourier transforms of an image I (Good- man, 1996). Let I be the image of the counterillumination, Materials and Methods 1 and I2 be the point spread function. Substituting into equa- General principles of image transfer tion (1) gives The perceived image of a counterilluminating animal image*PSF ϭ ᏲϪ1͓Ᏺ͑image͒ ⅐ Ᏺ͑PSF͔͒. (Equation 2) viewed from a distance is affected by three factors: absorp- tion and scattering by the water and the acuity of the The Fourier transform of the point spread function is gen- Figure 1. The convolution of image 1 and image 2 (denoted by the “*” operator) can be calculated by multiplying the Fourier transforms of the two images and then calculating the inverse Fourier transform of the product. PROPAGATION AND PERCEPTION OF BIOLUMINESCENCE 3 erally referred to as the optical transfer function (OTF). Due tion transfer function (MTF), is often also calculated. The to the convolution theorem, the OTF of a whole system is MTF is quite useful because it gives the fraction of remain- simply the product of the OTFs of the various components ing image contrast as a function of spatial frequency. For in the system (Goodman, 1996). Thus, for this study example, MTF(4) ϭ 0.5 implies that 50% of the original image contrast remains for detail that has a spatial fre- image ϭ ᏲϪ1͓Ᏺ͑image ͒ ⅐ OTF ⅐ OTF ͔, final initial water eye quency of 4 cycles per degree. (Equation 3) where image is the perceived image and OTF and final water Images examined OTFeye are the optical transfer functions of the water and eye respectively. A final, convenient implication of the Images of the ventral bioluminescence of two counter- convolution theorem is that the OTF of x meters of optically illuminating species were used: (1) the enoploteuthid squid homogeneous water is equal to the OTF of 1 meter of water Abralia veranyi (Ru¨ppell, 1844) (eye-flash squid), and (2) to the xth power. Thus, one need only calculate the PSF for Ceratoscopelus maderensis one distance. This property, known as the linearity assump- the myctophid fish (Gunther, tion, does not hold in extreme cases (e.g., very large x), but 1864) (horned lanternfish) (Fig. 2A, B). The two were is appropriate for the situations examined in this study chosen to provide a range of photophore spacing. Counter- (Jaffe, 1992). The equation for underwater image transfer is illumination in A. veranyi is finely detailed; that of C. then maderensis is relatively coarse (Fig. 2C, D). A. veranyi was collected at depth, using the Johnson-Sea-Link research ͑ ͒ ϭ ᏲϪ1͓Ᏺ͑ ͒ ⅐ ͑ ͒x ⅐ ͔ imagefinal x imageinitial OTF1 OTFeye , submersible fitted with 11-liter acrylic plastic cylinders with (Equation 4) hydraulically activated, sliding lids. C. maderensis was col- lected at night, using an opening/closing Tucker trawl 2 where imagefinal(x) is the perceived image viewed from a (4.3-m opening, 1⁄4 inch knotless nylon mesh) fitted with a distance of x meters, and OTF1 is the optical transfer func- thermally insulated collecting container. Specimens were tion of the water over a distance of 1 meter. manually stimulated to bioluminesce, and then were re- Although Eq. (4) correctly describes the propagation of a corded with a Dage ISIT image-intensified video camera (A. two-dimensional image, it requires modification when used veranyi) or Intevac GenIISys image intensifier system and in the context of counterillumination, because the back- CCD video camera (C. maderensis). Images that show how ground radiance is affected by the entire three-dimensional the counterilluminating animals appear from below (Fig. light field and changes as the viewer moves down and away 2E, F) were created by combining the bioluminescence from its target. From Mertens (1970), the degradation of images with silhouettes of the animals obtained from nor- contrast of a large image underwater (i.e., the OTF at zero mal illumination photographs (taken immediately after the spatial frequency) is intensified images).
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