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Hidden in plain sight: The ecology and physiology of organismal transparency.

Sonke Johnsen (*)

Abstract. Despite the prevalence and importance of transparency in organisms, particularly pelagic species, it is a poorly understood characteristic. This article reviews the current state of knowledge on the distribution, ecology, and physical basis of biological transparency. Particular attention is paid to the distribution of transparent species relative to their optical environment, the relationship between transparency and visual predation, the physics of transparency, and what is known about the anatomical and ultrastructural modifications required to achieve this condition. Transparency is shown to be primarily a pelagic trait, uncommon in other aquatic habitats and extremely rare on land. Experimental and theoretical studies in terrestrial, freshwater, and marine ecosystems have shown that transparency is a successful form of camouflage, and that several visual adaptations seem to counter it. The physical basis of transparency is still poorly understood, but anatomical observations and mathematical mo dels show that there are various routes to transparency. Future avenues for research include examination of the ultrastructure and optical properties of transparent tissue, exploring the link between transparent species and special visual modifications in the species they interact with, and analysis of the evolution of transparency using comparative methods.

Introduction

Transparency is a fascinating and surprisingly common characteristic that has received little attention because the majority of transparent species are found only in the pelagic regions of the open ocean. In these regions, however, the prevalence and diversity of transparent species is remarkable, ranging from the relatively well-known medusae and ctenophores to transparent polychaetes, gastropods, and fish (Fig. 1). Transparency is one of the few forms of camouflage possible in a habitat with no surfaces to match or hide behind. It is also the only form of camouflage, and one of the few adaptations, that involve the entire organism. Although the importance of transparency has been mentioned many times by pelagic ecologists, it is a relatively unstudied characteristic (Hardy, 1956; Fraser, 1962; McFall-Ngai, 1990; Meyer-Rochow, 1997).

This review synthesizes the current knowledge on the distribution, ecology, and physical basis of biological transparency. It is divided into five sections. The first section reviews the phylogenetic distribution of transparent species. The second section reviews and attempts to explain the relationship between transparent species and their optical environment. The third section links transparency to visibility; reviews terrestrial, freshwater, and marine studies of transparency and visual predation, including the use of special visual adaptations; and lists known active uses of transparency. The fourth section presents the underlying optical principles of transparency and then applies these principles to the various anatomical and ultrastructural modifications seen in transparent tissues. The final section suggests several avenues for future research.

Phylogenetic Distribution

The phylogenetic distribution of transparent animals is diverse, uneven, and strongly influenced by environment. Although significant levels of tissue transparency are found in a wide array of organisms (Figs. 1, 2), most transparent species are found in the following 10 groups, all of which are pelagic: cubozoans, hydromedusae, non-beroid ctenophores, hyperiid amphipods, tomopterid polychaetes, pterotracheid and carinariid heteropods, pseudothecosomatous pteropods, cranchiid squid, thaliaceans, and chaetognaths. Most benthic, neustonic, and terrestrial groups have very few transparent members, although there are exceptions.

The following phyletic review of transparency was compiled with the aid of specialists in different taxa and environments (see acknowledgments) and is subject to several constraints. First, because nearly all small, unpigmented objects are transparent (for reasons described later), this section considers only species with transparent regions larger than 5 mm. Therefore certain phyla (e.g., Rotifera, Gastrotricha) and most larvae and freshwater taxa are not covered. Second, because aquatic species from transparent groups that are found at aphotic depths tend to be strongly pigmented (usually red, orange, or black) (Hardy, 1956; Herring and Roe, 1988), only terrestrial taxa and aquatic taxa at euphotic and dysphotic depths are considered. Euphotic and dysphotic regions possess enough solar radiation for photosynthesis and vision, respectively. In the clearest waters, the lower bounds of the two regions are 200 and 1000 m. Finally, infaunal or endoparasitic species, in which transparency could not have any optic al function (e.g., Echiura, Sipuncula, Nematomorpha), are not covered.

Eight phyla--Porifera, Nematoda, Pogonophora, Onycophora, Brachiopoda, Bryozoa, Platyhelminthes, and Echinodermata--appear to have no transparent adults. The first seven of these are exclusively benthic, neustonic, or terrestrial (Faubel, 1984; May, 1994). Echinodermata is benthic with few exceptions (Miller and Pawson, 1990). Possible examples of transparency in these phyla, such as hexactinellid sponges and certain benthopelagic holothurians (e.g., Peniagone diaphana, Irpa ludwigi) are better described as unpigmented and translucent (i.e., milky) rather than transparent.

With the exception of the beroids, ctenophores at euphotic and dysphotic depths are generally transparent (Mayer, 1912; Harbison et al., 1978). Guts, papillae, and other small features are sometimes strongly pigmented, and the comb rows iridesce in directional illumination, but the bulk of the body is often extraordinarily transparent. Beroid ctenophores tend to be opaque, due to the presence of thousands of giant muscle fibers within the mesoglea (Hernandez-Nicaise, 1991), though smaller specimens of certain species (e.g., Beroe gracilis) can be transparent.

Transparency in the Cnidaria is mostly found in cubozoans, hydromedusae, and siphonophores. Cubozoans are all highly transparent (Matsumoto, 1995). Hydromedusae tend to be highly transparent, though often with pigmented guts or gonads (Russell, 1953; Kramp, 1959) (Fig. lA). Siphonophores follow a similar pattern with the exception of neustonic species (e.g., Physalia), which are often blue, and members of the benthic family Rhodaliidae, which are opaque (Totton, 1965; Herring, 1967; Pugh, 1983). Scyphozoans, in contrast and for unknown reasons, are generally opaque and pigmented (Mayer, 1910; Russell, 1970; Wrobel and Mills, 1998). No anthozoans are transparent.

Among the Annelida, transparency is found only among the pelagic polychaetes (Fig. lE). Five phyllodocidacean families (Alciopidae, Lopadorrhynchidae, Pontodoridae, Tomopteridae, and Typhloscolecidae) and two flabelligerid families (Flotidae and Poeobiidae) are dominated by transparent species (Uschakov, 1972; Glasby et al., 2000). The degree of transparency varies between the different families, with the tomopterids and alciopids highly transparent and the flabelligerids less so. The remaining pelagic family, Isopilidae, apparently does not have transparent members (Uschakov, 1972; Glasby et al., 2000).

Several genera of polystiliferous pelagic nemerteans are transparent (Pelagonemertes, Pilonemertes) (P. Roe, California State University Stanislaus, pers. comm.). However, pigmented food in their highly branched guts often seriously reduces any cryptic benefit. No species of benthic nemerteans is known to be transparent (Roe, pers. comm.).

Transparency in the Mollusca is complex. Although the phylum as a whole is overwhelmingly benthic and opaque, it contains several pelagic groups that are dominated by transparent species (Van der Spoel, 1976; Lalli and Gilmer, 1989). The Mollusca also contains pelagic groups that are entirely opaque, and at least one transparent benthic genus. The Aplacophora, Monoplacophora, Polyplacophora, Bivalvia, and Scaphopoda are exclusively benthic and opaque. Among gastropods, the exclusively pelagic pterotracheid and carinariid heteropods, pseudothecosomatous pteropods, and phylliroid nudibranchs are highly transparent (Figs. 1F, L). However, the janthinid snails, atlantid heteropods, euthecosomatous and gymnosomatous pteropods, and glaucid nudibranchs are all opaque, despite also being pelagic taxa (Van der Spoel, 1976; Lalli and Gilmer, 1989). Benthic gastropods are opaque, with the exception of several species of the nudibranch Melihe, which have transparent oral hoods that are used to catch crustaceans (Von W. K jerschow-Agersborg, 1921). Among cephalopods, transparency is found only in octopus and squid. Although no benthic octopi are transparent, the pelagic families Amphitretidae and Vitreledonellidae are highly transparent (Ijema and Ikeda, 1902; Joubin, 1918) (Fig. 1B). None of the genera of the four families of the pelagic argonautoid octopods are transparent, and the pelagic Bolitaenidae are better described as translucent (Nesis, 1982). The benthopelagic cirrate octopods are all opaque and often strongly pigmented. Among the exclusively pelagic squid, only the Cranchiidae and small specimens of certain chiroteuthids (e.g., Chiroteuthis) display any significant transparency. Vampyroteuthis and the Sepioidea are opaque.

Species in the Chaetognatha are pelagic and highly transparent, with the exception of the benthic Spadellidae and certain species at the lower end of the dysphotic zone (Fig. 1G). The spadellids are opaque due to the presence of transverse muscles and pigmentation (Bone and Duvert, 1991).

With the exception of the wings of certain satyrid and ithomiid butterflies and sphingid moths (e.g., Greta oto, Cephonodes hylas) (Papageorgis, 1975; Yoshida et al., 1997) (Fig. 1C) and the large pelagic larvae of certain freshwater insects (e.g., Chaoborus), transparency in the Arthropoda appears to be limited to aquatic crustaceans. As in the Mollusca, the distribution of transparency in crustaceans is complex, with many major groups containing both transparent and non-transparent forms. The only group that is truly dominated by transparent forms is the exclusively pelagic Hyperiidea (Amphipoda) (Bowman and Gruner, 1973; Vinogradov et al., 1996). The hyperiids, which are commensal on gelatinous zooplankton (Madin and Harbison, 1977; Laval, 1980), can be extraordinarily transparent and often have special modifications to increase their transparency (e.g., Land, 1981; Nilsson, 1982). The generally benthic or terrestrial groups (e.g., Decapoda, Gammaridea, Cirripedia, Stomatopoda, Isopoda) are primarily opaqu e, but with many exceptions among pelagic and benthopelagic subgroups (e.g., some Pasiphaeaid shrimp, various species of cleaner shrimp, the sergestid Lucifer, the isopod Astacilla, the phyllosoma larvae of Palinurus, the anemone shrimp Periclirnenes) (Fig. IJ). As is true of cnidarians and ctenophores, many transparent pelagic crustaceans have red-pigmented guts and gonads, particularly at dysphotic depths (Hardy, 1956; Herring and Roe, 1988). Transparency is fairly common in freshwater crustaceans, but only a few species, mostly highly modified cladocerans, are larger than 5 mm (e.g., Leptodora, Bythotrephes) (Fig. 1C).

Most transparent urochordates are found in the exclusively pelagic Thaliacea, which comprises the pyrosomids, salps, and doliolids (Godeaux et al., 1998). Pyrosomids are opaque, while salps and doliolids, excepting large individuals of Thetys vagina, are highly transparent. Among the exclusively benthic Ascidea, transparency is observed in several genera of the order Enterogona (e.g., Ciona, Clavelina), some of which are predatory (e.g., Megalodicopia hians) (Sanamyan, 1998). The larvaceans generally have small opaque bodies and long transparent tails, but with few exceptions (e.g., Bathochordeus) are smaller than 5 mm (L. P. Madin, Woods Hole Oceanographic Institution, pers. comm.) (Fig. 1I).

Although adults in the Hemichordata are infaunal and opaque, the larval form of Planctosphaera pelagica has a diameter of 25 mm and is highly transparent (Hart et al., 1994) (Fig. 1D). This organism, known only in this form, appears to have a prolonged larval stage and is well adapted to a pelagic existence.

No tetrapod chordate is transparent, but a number of fish arc. Transparent adults are scattered throughout marine and freshwater teleosts, but are common only in the freshwater family Ambassidae (glassfish) (Johnson and Gill, 1995). Commonly known examples from other families include the glass catfish Kryptopterus bicirrhis (Siluridae) and Parailia pellucida (Schilbeidae), the cardinalfish genus Rhabdamia (Apogonidae), the clingfish Alabes parvulus (Cheilobranchidae), and the glass knifefish Eigenmannia virescens (Sternopygidae) (Briggs, 1995; Ferraris, 1995; Johnson and Gill, 1995). In addition, the pelagic larvae of many freshwater and marine fish are often highly transparent (Breder, 1962; Meyer-Rochow, 1974) (Fig. 1K). The most striking of these are the leptocephalous larvae of elopomorphs. These leaf-shaped larvae incorporate gelatinous material in their bodies and quickly grow to lengths of up to 50 cm (Pfeiler, 1986). Most larval fish lose their transparency upon metamorphosis, some within 24 hours. Th e only possible tetrapod candidates, the glass frogs (Centrolenidae), have transparent skin on their ventral side, but opaque organs and a strongly pigmented dorsal surface (reviewed by McFallNgai, 1990).

Transparency and Environment

As can be seen from Figure 2 and the previous section, transparency has evolved multiple times and is almost exclusively a pelagic trait. Organismal transparency (rather than simply ocular) is extremely rare on land, rare in the aquatic benthos, uncommon in aphotic regions, somewhat more common in dysphotic and neustonic habitats, and ubiquitous at euphotic depths in clear water. The rarity of terrestrial transparency is probably due to the low refractive index of air, the presence of gravity, and high levels of ultraviolet radiation. The distribution of transparency in aquatic habitats appears to be correlated with the distribution of successful visual predation and crypsis strategies.

Terrestrial transparency

The extreme rarity of terrestrial transparency is probably due to the problem of reflections. The invisibility of a transparent object depends in part on the difference between its refractive index and the refractive index of the surrounding medium. A large difference causes surface reflections that substantially increase visibility. For example, an ice sculpture, while transparent, is highly visible due to surface reflections. At normal incidence, the fraction of incident light that is reflected (R) is

R = [([n.sub.1] - [n.sub.2]/[n.sub.1] + [n.sub.2]).sup.2] (1)

where [n.sub.1] and [n.sub.2] are the refractive indices of the object and the surrounding medium. The refractive index of biological tissue is roughly proportional to density and ranges from 1.35 (cytoplasm) to about 1.55 (densely packed protein) (Charney and Brackett, 1961; Chapman, 1976). The refractive index of seawater depends on temperature and salinity, but is about 1.34. For these values, the surface reflection of a transparent organism in air (2%-5%) is roughly 10-fold to 2000-fold greater than its surface reflection in seawater (0.001%-0.7%). Although some nongaseous compounds with refractive indices slightly less than that of seawater exist (e.g., trifluoroacetic acid, n = 1.28), the refractive index of water is the lower limit for biological materials. Therefore successful crypsis using transparency is unlikely in terrestrial habitats. Other likely contributing factors are the increased levels of ultraviolet radiation on land, which require protective pigmentation, and the need for supporting skel etal structures that are often opaque.

Distribution of aquatic transparency

Transparency is common in pelagic species at euphotic and dysphotic depths. Almost all non-transparent pelagic taxa are either camouflaged by small size (e.g., atlantid heteropods, euthecosomatous and gymnosomatous pteropods, glaucid nudibranchs, copepods, ostracods) or mirrored surfaces (e.g., fish, cephalopods), or are protected by fast swimming speeds (e.g., fish, cephalopods, shrimp) or chemical or physical defenses (e.g., scyphozoans, janthinid snails, Nautilus) (Hamner, 1996). The primary explanation for the prevalence of transparency in this environment is that it is the only form of camouflage in the pelagic realm that is successful from all viewpoints and at all depths. Cryptic coloration (e.g., countershading) is generally successful only from a given viewpoint and at a given depth (Munz and McFarland, 1977; Johnsen, 2002). Mirrored sides are successful at euphotic and upper dysphotic depths and for most viewpoints, although not from directly above or below (Herring, 1994; Denton, 1990). Counterillu mination tactics are metabolically expensive and successful only during moonlit nights or at dysphotic depths.

The relative rarity of transparency in benthic and neustonic habitats is puzzling. Both benthic and neustonic species tend to be pigmented to match the surface below them--benthic animals matching the substrate and neustonic species matching the upwelling radiance (deep blue in oceanic water, brown in shallow freshwater) (David, 1965; Herring, 1967; Cheng, 1975; Guthrie, 1989). The rarity of transparency in benthic habitats is possibly due to two factors. First, pigmentation may be less costly to the animal than transparency, since it requires fewer modifications. However, a varied background requires the ability to detect and match a range of patterns and colors, a process done automatically by transparency camouflage. A second possibility is that even perfectly transparent objects tend to cast highly conspicuous shadows, due to distortion of the light by the higher refractive index of the tissue. These shadows, invisible in pelagic habitats, may render transparency ineffective for benthic species.

Neither of these factors, however, can account for the relative rarity of transparency in neustonic species. The two major hypotheses for the pigmentation of neustonic species are photo-protection and crypsis (Herring, 1967; Zaitsev, 1970). Although ultraviolet (UV) radiation is quite high at the surface of any aquatic habitat, there is no evidence that the pigmentation in neustonic species absorbs strongly at UV wavelengths. In addition, there are compounds, such as mycosporine-like amino acids, that strongly absorb at UV but not visible wavelengths (Karentz et al., 1991). The fact that neustonic pigmentation often matches the upwelling radiation strongly suggests that at least part of its function is crypsis. However, the blue or brown pigmentation is successfully cryptic only from above, or possibly from the side (Munz and McFarland, 1977; Johnsen, 2002), whereas neustonic individuals are most likely to be viewed from below. From this angle, any individual is silhouetted by the bright downwelling light, re ndering cryptic coloration useless. Predation from above (e.g., avian) appears to mostly involve larger species (Zaitsev, 1970). As Herring (1967) concluded, no functional explanation of pigmentation in neustonic species is entirely satisfactory, and more data on the UV absorption of the pigments and the structure of the neustonic food web is needed.

As mentioned above, transparent species are rare at aphotic depths, generally being replaced by species with whole-body red or black pigmentation (Hardy, 1956; Herring and Roe, 1988; McFall-Ngai, 1990). At these depths, visual predation by solar light is sometimes replaced by visual predation based on directed bioluminescence. Because the spectra of photophores are generally void of red wavelengths (Widder et al., 1983), neither red nor black surfaces can be seen by bioluminescent "searchlights." If the red or black coloration absorbs more than 99.5% of the directed bioluminescence, it may be more cryptic than transparency because even a perfectly transparent object causes surface reflections. However, because the reflected light is a small fraction of a dim source, the background light levels must be extremely low for the reflection to be visible. For example, the radiant intensity of the suborbital photophores of the Panama snaggletooth (Borostomias panamensis) is on the order of [10.sup.10] photons * [s.sup.-1] * [sr.sup.-1] (Mensinger and Case, 1997). If this light strikes a transparent individual with a refractive index of 1.37 (10% protein), one can determine from equation (1) that about 0.01% of the photons are reflected back to the viewer. Therefore the background light levels must be [10.sup.6] photons * [s.sup.-1] or lower. For upward viewing this occurs at about 750 m in oceanic water (using absorption and attenuation values from the equatorial Pacific (Barnard et al., 1998) and radiative transfer software (Hydrolight 4.1, Sequoia Scientific)). At these depths, horizontal and upward radiances are 3% and 0.5% of the downward radiance (Denton, 1990), so the equivalent depths for successful viewing using horizontal and downward bioluminescence are 650 and 600 m. For viewers with brighter bioluminescent "searchlights" or targets with higher refractive index, the depths are less. For example, the chitinous cuticle of a transparent hyperiid amphipod (n = 1.55) reflects 0.5% of the light and would be visible a t 625, 525, and 475 m for upward, horizontal, and downward-directed bioluminescence, respectively. Truly opaque objects, such as guts and digestive organs, reflect a much higher percentage of light and are visible at even shallower depths. This may explain why many opaque and high refractive index organs are pigmented at shallower depths than those at which whole-body pigmentation is observed.

Visibility and Visual Predation

Although some transparent species may only have trophic interactions with blind taxa, the majority either prey on or are preyed upon by at least some species with well-developed visual systems (Harbison et al., 1978; Alldredge and Madin, 1982; Alldredge, 1984; Madin, 1988; Lalli and Gilmer, 1989; Pages et al., 1996; Baier and Purcell, 1997; Madin et al., 1997; Purcell, 1997; Harbison, unpublished literature review of gelatinivory in vertebrates). Since transparent animals are often more delicate and less agile than their visually orienting predators or prey, their success in predator/prey interactions with these animals depends critically upon their visibility and in particular their sighting distance (the maximum distance at which they are detectable by an animal relying on visual cues). Prey with short sighting distances reduce their encounters with visually orienting predators (Greene, 1983). "Ambush" predators (e.g., medusae, siphonophores, cydippid ctenophores) with short sighting distances increase thei r chances of entangling visually orienting prey before being detected and avoided. Raptors (e.g., chaetognaths, heteropods) with short sighting distances increase their chances of getting within striking distance without being detected.

Transparency and contrast

The visibility of a transparent individual generally depends more on its contrast than on its size (Mertens, 1970; Hemmings, 1975; Lythgoe, 1979). The inherent contrast (contrast at zero distance) at wavelength [lambda] is defined as

[C.sub.o]([lambda]) = [L.sub.o]([lambda]) - [L.sub.b]([lambda])/[L.sub.b]([lambda]), (2)

where [L.sub.o],([lambda]) is the radiance of the object and [L.sub.b]([lambda]) is the radiance of the background, both viewed a short distance from the object (Hester, 1968; Mertens, 1970; Jerlov, 1976). The absolute value of contrast decreases exponentially with distance according to

\C([lambda])\ = \[C.sub.o]([lambda])\ * [e.sup.([K.sub.L]([lambda])-c([lambda]))d], (3)

where \C([lambda])\ is the absolute value of apparent contrast at distance d from the object, [K.sub.L]([lambda]) is the attenuation coefficient of the background radiance, and c([lambda]) is the beam attenuation coefficient of the water (adapted from Mertens, 1970; Lythgoe, 1979). The maximum distance at which the object is still detectable is

[d.sub.sighting]([lambda])=ln(\[C.sub.o]([lambda])\/[C.sub.min]([lamb da]))/c([lambda]) - [K.sub.L]([lambda]), (4)

where [C.sub.min]([lambda]) is the minimum contrast threshold of the viewer. An animal can indirectly affect c([lambda]]) - [K.sub.L]([lambda]) by moving into a different water type or controlling the angle from which it is viewed, but it can only directly decrease its sighting distance by decreasing its inherent contrast. The inherent contrast of a transparent organism from an arbitrary viewpoint depends on its light-scattering properties and the characteristics of the underwater light field (Chapman, 1976), so it is difficult to model exactly. In general, however, pelagic objects have the greatest sighting distances when viewed from below, and are often viewed from this angle (Mertens, 1970; Munz, 1990; Johnsen, 2002). The transparency, T([lambda]), of an object is the fraction of light of wavelength [lambda] that passes unabsorbed and unscattered through it. Therefore, for the upward viewing angle

T([lambda]) = [L.sub.o]([lambda])/[L.sub.b]([lambda]), \[C.sub.o]([lambda])\ = 1 - T([lambda]),

and [d.sub.sighting]([lambda]) = ln(1 - T([lambda])/[C.sub.min]([lambda])/c([lambda]) - [K.sub.L]([lambda]). (5)

Thus, the relationship between transparency and sighting distance is not linear and depends also on the contrast sensitivity of the viewer. Optimal minimum contrast thresholds have been determined for man (0.01), cat (0.01), goldfish (0.009-0.05), cod (0.02), rudd (0.03-0.07), roach (0.02), and bluegill (0.003-0.007) (Lythgoe, 1979; Douglas and Hawryshyn, 1990). It is important to note, however, that because these values depend on many aspects of the experimental situation (e.g., temperature, target size, position of stimulus on retina, whether one eye or two was used, assessment method), they are not directly comparable (Douglas and Hawryshyn, 1990). For example, the minimum contrast threshold increases as the light level decreases. For example, the minimum contrast threshold of cod (Gadus morhua) increases from 0.02 at the surface to nearly 0.5 at 650 m in clear water ([10.sup.-7] W [sr.sup.-1] [m.sup.-2] (Anthony, 1981). Therefore, animals that are detectable near the surface may become undetectable at dept h.

Empirical studies

The only empirical research on terrestrial transparency is a study on predation of neotropical butterflies showing that transparent species were mostly found near the ground, where they were presumably maximally cryptic (Papageorgis, 1975). A subsequent study, however, did not confirm this (Burd, 1994).

Most of the research on the relationship between transparency and visual predation has been performed in freshwater systems. Early studies by Zaret (1972) on fish predation on two morphs of transparent daphnia (Ceriodaphnia cornuta) showed that predation was higher on the morph with larger eyes. When the "small-eye" morph was then fed India ink, creating a "super eye spot" in the gut, the predation preferences of the fish switched. Zaret also found that the small-eye morph had a greatly reduced reproductive potential and hypothesized that it was maintained in natural populations due to its reduced visual predation pressure. Later Zaret and Kerfoot (1975) showed that predation on a different transparent cladoceran (Bosmina longirostris) did not depend on body size but on the size of the opaque eye spot; they concluded that the important variable in visual predation was not body size, as previously assumed, but apparent body size. This conclusion has been supported by several subsequent studies (e.g., Confer et al., 1978; Wright and O'Brien, 1982; Hessen, 1985). Kerfoot (1982) measured the transparency, palatability, and sighting distances (for pumpkinseed fish) of several species of transparent freshwater zooplankton and found that transparency was correlated with palatability and inversely correlated with sighting distance. He proposed that visual predation by freshwater fishes has driven zooplankton in two opposing directions--palatable groups being selected for decreased visibility through decreased size, increased transparency, or both; unpalatable groups being selected for increased visibility through increased size, intense pigmentation, or both. O'Brien and Kettle (1979) examined the countervailing selective pressures of tactile predation (selecting for large prey) and visual predation (selecting for small prey) on two species of Daphnia. They found that these species increased their actual size, but not their apparent size, by developing morphs with large transparent armored sheaths. Giguere and Northcote (1987) repeated the India ink studies of Zaret (1972) in a more natural way by examining the effect of a full gut on the predation of transparent prey. They found that ingested prey increased the predation of Chaoborus larvae by 68% and suggested that this increased risk was at least partially responsible for the sinking of the animals after nocturnal feeding.

In contrast to the relatively abundant freshwater studies, fewer feeding studies on transparency exist for marine ecosystems. Tsuda et al. (1998), in a feeding study similar to Giguere and Northcote's, found that predation on transparent copepods roughly doubled when their guts were full; he also suggested that predation risk due to gut visibility may be an important factor contributing to vertical migration in transparent zooplankton. Brownell (1985) and Langsdale (1993) both found that eye pigmentation significantly increased the vulnerability of transparent fish larvae to predation. Thetmeyer and Kils (1995) examined the effect of attack angle on the visibility of transparent mysids to herring predators and found that they were most visible when viewed from above or below and least visible when viewed horizontally. Finally, Utne-Palm (1999) found that the sighting distances for transparent copepods (to goby predators) were significantly lower than the sighting distances for pigmented copepods.

Most of the research on transparency in marine ecosystems has concentrated on physical measurements of transparency and modeling its relationship to visibility. Greze (1963, 1964) was the first to describe the importance of transparency in visual predation. Using relatively crude equipment, he measured the average transparency of various dinoflagellates, siphonophores, copepods, and larvaceans and presented a model, which, unfortunately, was inaccurate, relating the measurements to sighting distance. Using a spectrophotometer, Chapman (1976) measured the transparency of several medusae (Polyorchis, Chrysaora, Aurelia) as a function of wavelength (from 200 to 800 nm). He found that transparency was relatively constant over the visual and infrared range and then dropped dramatically at ultraviolet wavelengths. Chapman also modeled the relationship between transparency, reflectivity, and visibility as a function of viewing angle, showing that the visibility of any object that is not 100% transparent depends stro ngly on the viewing angle and the underwater radiance distribution. Forward (1976), in a study of shadow responses in crab larvae, measured the transparency of the larvae's ctenophore predator, Mnemiopsis leidyi, and showed that the ctenophores were sufficiently opaque to cause a defensive response in individuals below them. More recently, Johnsen and Widder (1998, 2001) measured the ultraviolet (280- 400 nm) and visible (400-700 nm) transparency of 50 epipelagic and mesopelagic Atlantic species from seven phyla (Cnidaria, Ctenophora, Annelida, Mollusca, Crustacea, Chaetognatha, Chordata) and modeled the relationship between transparency and sighting distance using analyses similar to those given in the previous section. They found that transparency is generally constant over the visual range, with longer wavelengths slightly more transparent. Deepwater animals tended to have constant and high transparency at UV wavelengths, whereas near-surface animals showed rapidly decreasing and low transparency in the UV . The relationship between transparency and visibility was complex and depended strongly on the contrast sensitivity of the viewer. Many mesopelagic animals were found to be far more transparent than necessary for complete invisibility.

Visual adaptations to increase contrast of transparent animals

The importance of transparency in predator/prey interactions is also demonstrated by the special visual adaptations seen in pelagic animals. The three best studied of these are UV vision, polarization vision, and viewing at certain angles. In addition to their possible other functions, all three of these can "break" the camouflage of transparency.

UV vision (documented down to ~320 nm) has been demonstrated in many aquatic species; it has been conservatively estimated that there is sufficient UV light for vision down to 100 m in clear ocean water (reviewed by Losey et al., 1999, and Johnsen and Widder, 2001). Visual pigments with UV sensitivity have been found in dozens of species of marine and freshwater fish (reviewed by Douglas and Hawryshyn, 1990; Jacobs, 1992; Goldsmith, 1994; and Johnsen and Widder, 2001). Among arthropods, UV vision has been demonstrated in stomatopods, cladocerans, copepods, decapods, and horseshoe crabs (Wald and Krainin, 1963; Marshall and Oberwinkler, 1999; Flamarique et al., 2000). Finally, and surprisingly, UV sensitivity is found in at least one mesopelagic alciopid polychaete and four mesopelagic decapod crustaceans (Wald and Rayport, 1977; Frank and Case, 1988).

Three primary functions for UV vision have been hypothesized (Losey et al., 1999): (1) intraspecific communication, (2) enhanced detection of opaque prey (silhouetted against the relatively bright UV background), and (3) enhanced detection of transparent prey. Due to higher light scattering or the presence of UV-protective compounds, many visibly transparent tissues are opaque at UV wavelengths (Douglas and Thorpe, 1992; Thorpe et al., 1993; Johnsen and Widder, 2001). Several researchers have hypothesized that UV vision is primarily used to improve detection of transparent prey (Loew et al., 1993; Cronin et al., 1994; McFarland and Loew, 1994; Loew et al., 1996; Sandstroem, 1999), and Browman et al. (1994) have shown that the presence of UV light improves the search behavior of certain UV-sensitive zooplanktivorous fish. The presence of UV sensitivity in planktivorous but not in non-planktivorous life stages of salmonids (reviewed by Tovee, 1995) and the correlation between UV vision and planktivory in coral reef fish (Mc-Farland et al., unpubl. data) suggest that UV vision is often used to increase the contrast of transparent planktonic prey.

Therefore, near-surface transparent species may have to satisfy the conflicting selective pressures of camouflage and protection from radiation damage. The increased visibility due to photo-protective carotenoid and melanin pigmentation in high-UV freshwater environments has been studied for many years (Hairston, 1976; Luecke and O'Brien, 1981, 1983; Byron, 1982; Hobaek and Wolf, 1991; Hansson, 2000; Miner et al., 2000). These studies have shown several novel solutions, such as inducible pigmentation mediated by the relative levels of UV radiation and visual predation, restriction of pigmentation to vital organs, and the use of a photoprotective compound that also decreases visibility. Only two studies have examined marine systems (Morgan and Christy, 1996; Johnsen and Widder, 2001), and only the latter has explored the effect of nonvisible UV protective pigments on UV visibility. In this study, near-surface zooplankton displayed significantly greater UV absorption than deep-dwelling zooplankton, but the effe ct of UV absorption on UV visibility was less than expected because the measured UV absorption was generally significantly greater in the UVB than in the UVA (where UV vision occurs), and because the highest UV absorption was often found in less transparent individuals.

The conflict between UV protection and UV concealment may have important ecological implications in light of reports of decreasing ozone levels at polar, temperate, and tropical latitudes and concomitant increases in UVB radiation (measured at l0%-20% per decade at temperate latitudes) (Solomon, 1990; Smith et al., 1992; Stolarski et al., 1992). A responsive increase in UV-protective pigmentation (at either an individual or population level) increases visibility at UV and possibly visible wavelengths, potentially resulting in increased predation or decreased feeding success. A responsive increase in depth may decrease access to prey, phytoplankton, or warmer water. Given the importance of transparent zooplankton to the trophic ecology of the pelagic realm (e.g., Madin et al., 1997; Purcell, 1997), either response may have significant effects.

A second visual adaptation that can increase the contrast of transparent predators or prey is polarization vision. Underwater light is polarized, particularly in the horizontal direction (Waterman, 1981). A transparent object can affect this polarization in two ways: it can depolarize it entirely or, if the object is birefringent, it can rotate the plane of polarization (Lythgoe and Hemmings, 1967; Fineran and Nicol, 1978). Either change is potentially detectable by a polarization-sensitive visual system (Fig. 3), which may explain the prevalence of polarization sensitivity in underwater crustaceans and cephalopods (Waterman, 1981). Despite the enormous potential of this field, only one study has tested this possibility (Shashar et al., 1998). This study showed that squid (Loligo pealei) preferentially attacked birefringent plastic beads over non-birefringent beads, although they were otherwise indistinguishable.

The final adaptation is behavioral rather than physiological and relies on the special optical properties of the airwater interface. Due to refraction at the water's surface, the hemispherical sky is compressed into a region 97 0 across, known as Snell's window. Any transparent object just outside the edge of this window is more conspicuous because it refracts and reflects some of the light from within the window, but is seen against the relatively dark background of water outside the window (Lythgoe, 1979). As with polarization sensitivity, this contrast enhancer, while potentially quite important, has only been tested once. Janssen (1981) showed that the attack angles of the blueback herring (Alosa aestivalis) were closely distributed around the outside edge of Snell's window.

Active uses of transparency

Although transparency seems to be primarily designed for passive crypsis, a few examples exist of more active uses of this trait. The physonect siphonophores Athorybia rosacea and Aglama okeni are mostly transparent, but they have pigmented regions mimicking copepods and larval fish that are apparently used as lures (Purcell, 1980, 1981). Therefore, animals approaching the small lures cannot detect the large individual that is also present. Other siphonophores appear to have exploited temporal changes in transparency for defense. The calycophoran siphonophores Hippopodius hippopus and Vogtia are normally transparent, but they rapidly become opaque when disturbed, presumably as a defensive startle response (Mackie, 1996).

The Physical Basis of Transparency

General principles

Transparency differs from other forms of crypsis and most adaptations in general in that it involves the entire organism. Therefore, many or all the tissues must be specialized for transparency. How this is achieved and how the modifications are compatible with life are only just beginning to be understood. The following sections explain the physics of transparency and then discuss the few theoretical and fewer empirical biological studies that have been performed.

An organism or tissue is transparent if it neither absorbs nor scatters light (Kerker, 1969). The majority of organic molecules do not absorb visible light (Tardieu and Delaye, 1988), and measurements of the wavelength dependence of light attenuation in 52 species of transparent zookplankton show no evidence of visible absorption bands in the transparent regions (Chapman, 1976; Johnsen and Widder, 1998, 2001). Therefore, except for necessarily opaque tissues (e.g., gut, retina) and the special case of UV transparency, the primary barrier to transparency in organic tissue appears to be light scattering.

Scattering is caused by discontinuities in refractive index. A nonabsorbing substance with a homogeneous refractive index is transparent. Biological tissue has many refractive-index discontinuities, due to the varying proportions and densities of its components. For example, the refractive index of lipids is higher than that of cytoplasm (Meyer, 1979). Therefore, plasma membranes, lipid droplets, and organelles with extensive folded membranes (e.g., mitochondria, Golgi apparatus, and endoplasmic reticulum) have a higher refractive index than the surrounding cytoplasm. Organelles with dense protein concentrations, such as peroxisomes and lysosomes, also have a higher refractive index than the surrounding cytoplasm, as do nuclei, due to their high concentrations of nucleic acids. Even gelatinous organisms containing large amounts of water have sufficient complexity to scatter light, as evidenced by their opacity after death. In addition to these internal discontinuities, there is also the large discontinuity de fined by the surface of the organism. As a photon passes through regions of different refractive indices, its direction is altered. Given enough direction changes, the tissue, though nonabsorbing, will be opaque. Common examples of nonabsorbing, highly scattering, opaque substances are milk, clouds, snow, and the sclera (white) of the eye.

Therefore, transparent animals must be adapted to scatter as little light as possible. Because the refractive indices of organic molecules are generally closely correlated with density (Ross, 1967), chemical adaptations are unlikely, and the problem is essentially a structural one.

Anatomical adaptations

Although most of the adaptations for transparency are observable only at the electron microscopy level, some are visible to the naked eye. These can be divided into the cloaking of tissues that cannot be made transparent and body flattening (Fig. 4).

Eyes and guts cannot be made transparent. Eyes must absorb light to function and guts are betrayed by their contents, since even transparent prey become visible during digestion. The eyes of transparent animals have been camouflaged in various ingenious ways. Many hyperiid amphipods have enormous eyes, covering most of their head, and could be betrayed by their large, pigmented retinas. However, the retinal signature is masked using either of two strategies. In some hyperiids (e.g., Phronima), the light is directed from the large eyes to highly compact retinas using transparent fiber optic cables of complex optical design (Land, 1981; Nilsson, 1982) (Fig. 4B). Conversely, the retina of the hyperiid Cystisoma is thinned, expanded, situated directly behind the cornea, and therefore indistinct (Fig. 4A). Many transparent molluscs camouflage their eyes with mirrors, because mirrors in the open ocean reflect only more ocean and so are invisible (Herring, 1994). Others, particularly the transparent cranchiid squid, use counterillumination to mask the shadows of their eyes seen from below (Fig. 4D) (Voss, 1980). Land (1992) suggested that the elongated eyes of transparent octopi function to minimize the shadow of the eye from below. A final adaptation that has not been explored is the separation of the eyes using long stalks (e.g., cranchiid and phyllosoma larvae), thereby minimizing the characteristic signature of two eyes side by side (Fig. 4F).

Similarly ingenious adaptations exist for minimizing the visibility of the opaque guts. Many transparent animals have elongated, vertically oriented, and sometimes reflective guts, including pterotracheid heteropods, cranchiid squid, transparent octopi, and hyperiid amphipods (Seapy and Young, 1986; Land, 1992; Vinogradov et al., 1996; Young et al., 1998). The shape and orientation minimizes the profile of the gut when viewed from above or below. The reflective coating minimizes the contrast of the gut when viewed from other angles. Seapy and Young (1986) showed that pterotracheids and cranchiids actively maintained the vertical orientation of their guts while altering the orientation of their bodies (Fig. 4C, D). A converse approach, seen in many salps, ctenophores, and medusae, is the possession of compact, spherical guts. Although not as cryptic from below, a sphere has the minimum average projected area when averaged over all potential viewing angles (Johnsen and Widder, 1999). Finally, as is found in eye s, the shadows of the opaque guts of certain species are masked using counterilluminating bioluminescence. For example, the mostly transparent midwater shrimp Sergestes similis masks the shadow of its digestive organs in this fashion (Warner et al., 1979).

Many guts of transparent animals, if not mirrored, are pigmented. This is hypothesized to mask the presence of bioluminescent prey but may also serve as cryptic coloration, particularly since the color often approximates the optimally cryptic shade for a given depth (Johnsen, 2002).

Finally, some animals simply ingest substances that remain clear. The highly transparent larva of the phantom midge (Chaoborus) sucks out clear fluids from its prey (Kerfoot, 1982). Therefore, the gut remains transparent and does not need to be camouflaged.

Light attenuation in tissue, whether due to absorption or scattering, is exponential. For example, if a 1-cm-thick section of tissue is 60% transparent, then 2 cm is 36% transparent, and 3 cm is 22% transparent. Conversely, a 1-mm-thick section of the same tissue is 95% transparent. Therefore, transparency can be achieved through extreme body flattening. This adaptation has the additional advantage of also camouflaging the animal when it is observed edge-on. Flattening is observed in many transparent animals including cestid ctenophores, phylliroid nudibranchs, many freshwater cladocerans, hyperiid amphipods, phyllosoma and stomatopod larvae, and the leptocephalous larvae of fish (Mayer, 1912; Zaret, 1981; Pfeiler, 1986; Lalli and Gilmer, 1989; Vinogradov et al., 1996) (Fig. 4E, F). In certain cases, the flattening is extreme. The phyllosoma larvae of Palinurus are about 50 mm across and less than 1 mm thick (Fig. 4F). In many cases, body flattening may serve additional functions, such as more efficient swimm ing in fish and phylliroid nudibranchs, or increased surface area for gas exchange in cestid ctenophores.

Transparency and ultrastructure

The primary modifications for transparency, however, are ultrastructural and can only be seen with electron microscopy. The modifications depend on the tissue, which can be divided into three groups: external surface, extracellular matrix, and cellular tissue.

As mentioned above, the external surface of even a perfectly transparent organism reflects light due to the change in refractive index. These reflections can be reduced or eliminated by covering the surface with submicroscopic protrusions (Miller, 1979; Wilson and Hutley, 1982). Because the protrusions are submicroscopic, they do not scatter light, but instead mimic a material of an intermediate refractive index. At the tips of the protrusions, the refractive index is that of the external medium. At the base, the index is that of the organism. At intermediate heights, the index varies smoothly and depends on the relative projected areas of the protrusions and the external medium (Fig. 5). These structures, known as "moth eye" surfaces, are found on the eyes of certain, particularly nocturnal, lepidopterans, dipterans, and caddisflies, where they are believed to camouflage the large eyes and increase sensitivity (by reducing reflected light) (reviewed by Miller, 1979; Parker et al., 1998). They are also found on the wings of transparent lepidopterans, and in certain species (e.g., Cephonodes hylas) have been shown to reduce their visibility (Yoshida et al., 1997).

The transparency of many extracellular tissues may depend on the counterintuitive notion that, although a completely homogeneous refractive index is sufficient for transparency, it is not always necessary. A transparent tissue can have components with many different refractive indices, so long as the average refractive index is constant over distances equal to half the wavelength of the incident light or more (Benedek, 1971). More precisely, scattering and light attenuation are low if the spatial distribution of refractive index has no Fourier components with wavelengths greater than one half the wavelength of light. This low scattering is due to extensive destructive interference of the scattered light from the various scatterers. What is observed instead is a slower speed of light through the material. In short, scattering (in the presence of heavy destructive interference) is the source of refractive index. In glass, for example, each of the various molecules scatter light, but due to destructive interfere nce no scattered light is observed and the beam is not attenuated. This theory has been invoked to explain the transparency of the mammalian cornea and lens (Benedek, 1971; Tardieu and Delaye, 1988; Vaezy and Clark, 1994). In both tissues, a substance with a high refractive index (collagen fibers in the cornea and crystalline proteins in the lens) is embedded within a substance with a low refractive index. The substance with the high refractive index is packed so densely that steric and other repulsive interactions force a local ordering of the scatterers (Tardieu and Delaye, 1988). The ordering exists only over distances on the order of several diameters of the scatterers, but it is sufficient to drastically reduce scattering. In the case of N identical scatterers, the total scattering cross-section, [C.sub.total], is given by

[C.sub.total] = [NC.sub.sca]S([phi]), (6)

where [C.sub.sca] is the scattering cross-section of an individual scatterer, [phi] is the volume concentration of the scatterers ([V.sub.scatterers]/[V.sub.total]), and S([phi]) is the structure factor. The structure factor gives the amount of reduction in total scattering due to destructive interference caused by local ordering. In general, S([phi]) is complex or unknown (see Benedek, 1971), but in the simpler case of small scatterers (radius [less than or equal to] 70 nm) it is

S([phi]) = [(1 - [phi]).sup.4]/1 + 4[phi] + 4[[phi].sup.2] - 4[[phi].sup.3] + [[phi].sup.4]

(Delaye and Tardieu, 1983). (7)

A concentration of scatterers of 30% reduces the total scattering to 10% of the value calculated under the assumption of no destructive interference of scattered light. A concentration of 60% reduces the scattering to less than 1% of the value calculated assuming no destructive interference. Figure 6 shows the total scattering cross-section of a solution of small particles plotted against their volume concentration. As the volume concentration increases there are more scatterers, but also more destructive interference. The maximum light scattering occurs at 13% concentration and then decreases as the concentration increases (see Benedek (1971) and Tardieu and Delaye (1988) for further details). This theory has been experimentally confirmed using solutions of lens proteins (Bettleheim and Siew, 1983). The solution becomes cloudier with increasing concentration, until a volume concentration of about 13%, after which it becomes clearer.

Many extracellular and some cellular tissues (e.g., muscle) of transparent o rganisms may meet these requirements. Although studies of the extracellular matrices and muscle of transparent animals are fairly rare, ultrastructural data exist for hydromedusae, siphonophores, ctenophores, chaetognaths, transparent ascidians, pyrosomas, doliolids, and salps (De Leo et al., 1981; Weber and Schmid, 1985; Franc, 1988; Hernandez-Nicaise, 1991; Shinn, 1997; Hirose et al., 1999). The fact that all of these appear homogeneous under light microscopy strongly suggests that they have few Fourier components greater than one half the wavelength of light. However, rigorous analyses have not been performed.

Although the above theory may explain the transparency of extracellular structures, it cannot adequately account for the transparency of cellular tissue. Reduction of scattering by destructive interference relies on dense packing of similar objects. In the two cases where this theory has been successfully applied (lens and cornea), the tissues are highly simplified. The mammalian lens, in particular, has been drastically modified for transparency (Goldman and Benedek, 1967; Philipson, 1973; Tardieu and Delaye, 1988). Most of the lens cells lack nuclei, mitochondria, and other organelles and, in fact, are little more than containers for dense concentrations of a few different proteins. The cells rely entirely on the surrounding cells for metabolic support and maintenance. Similarly, the cornea is a tightly packed array of collagen fibers with very few support cells and cannot maintain itself. These modifications are obviously incompatible with life when employed throughout an entire organism.

The only investigation of the basis of transparency in more complex cellular tissue is a theoretical treatment by Johnsen and Widder (1999). This study assumed that a cell requires given total volumes of various components. It then determined how to apportion, distribute, and shape the volumes to minimize light scattering. The study found that the size of the components was most important, followed by the refractive index and, distantly, by the shape (Fig. 7; Table 1). A similar analysis was performed assuming that a cell requires a given total surface area of certain components, with similar results. Because a group of smaller particles within a wavelength of light of each other behave roughly like one larger particle (Thiele, 1998), clustering particles can change the total amount of scattering. For example, if several lysosomes have radii near the critical radius (see Fig. 7; Table 1), they can be clustered to reduce the total amount of light scattering. Shape is surprisingly unimportant. For particles sma ller than the wavelength of light, shape is irrelevant (Johnsen and Widder, 1999). For larger particles, the change in scattering as an object shifts from needle-shaped to disk-shaped is quite small relative to the enormous changes due to size (Fig. 7B).

Table 2 lists the predictions for actual cell components to scatter a minimum amount of blue-green light. For each component, a range of size and refractive index is given. All the components are considered to be primarily bound by constant-volume constraints, with the exception of mitochondria. Since mitochondrial functioning depends heavily on membrane surface, it is considered to be bound by constant-surface-area constraints (see above). The refractive index of the cytoplasm is assumed to be 1.35. The refractive indices of the components are highly approximate and based on values of 1.62 for protein, 1.49 for lipid, and 1.34 for saline. In cases where a given prediction cannot be applied (e.g., dividing a nucleus into smaller nuclei, changing the shape of a microtubule), no prediction is made. All predictions assume that the size and refractive index of a given component must remain within the range given. None of these predictions have been tested, although the morphological techniques are relatively straightforward.

In summary, although the physics of light scattering is well understood, the field of organismal transparency is still in its infancy. The few theoretical and empirical studies suggest that there are several routes to transparency, many of which probably operate concurrently. For example, the transparency of leptocephalous larvae may be due to body flattening, ordered packing within the gelatinous core, a very thin muscle layer, and possibly modifications within the cellular tissue itself. Other animals, such as phyllosoma larvae, may rely entirely on their extreme flattening. However, the actual modifications and their proximate and ultimate costs are, for the most part, unknown.

Future Directions

Transparency is currently a field with more questions than answers. Almost every major aspect of its study is a fruitful avenue for future research, but several topics are critical for future understanding of this adaptation. First, the structural predictions must be tested using morphological and optical measurements of transparent tissue. The unlikely possibility that organic molecules in transparent organisms have altered their refractive indices needs to be tested. More images of transparent animals under UV and polarized light are needed to evaluate the hypotheses of special camouflage breakers in planktivores, as are more feeding studies in both freshwater and marine ecosystems. Finally, as more phylogenies of pelagic groups become available, comparative methods should be used to explore the evolution of this extraordinary trait.

Acknowledgments

I thank the following for information on the transparency of specific groups: Martin Angel, Daphne Fautin, Tamara Frank, Steven Haddock, Richard Harbison, Peter Herring, Dina Leech, Laurence Madin, Marianne Moore, Karen Osborn, David Pawson, Pamela Roe, Clyde Roper, Michael Vecchione, Janet Voight, and Edith Widder. I also thank Ken Halanych and Yale Passamaneck for pointing out relevant phylogenetic literature and software, and Kristina Fjeld, Tamara Frank, and Laurence Madin for a critical reading of the manuscript. The images for Figures 1, 3, and 4 were generously provided by Tamara Frank, Steven Haddock, Jeff Jeffords, Laurence Madin, Nadav Shashar, and Edith Widder. This work was funded in part by grants to SJ from The Rinehart Coastal Research Center, the Reuben F. and Elizabeth B. Richards Endowed Fund, the Penzance Endowed Fund, and the Grayce B. Kerr Fund. This is contribution number 10555 of the Woods Hole Oceanographic Institution.

Received 30 May 2001; accepted 30 August 2001.

(*.) Current address: Biology Department, Box 90338, Duke University, Durham, NC 27708. E-mail: sjohnsen@duke.edu

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[Figure 6 omitted]

[Figure 7 omitted]
Table 1

Ultrastructural predictions for transparent cellular tissue: the left
column lists the various parameters in order of their importance to
tissue transparencey; the right column lists the predictions for the
given parameter under a constant volume constraint; particles are
considered clustered if they are within a wavelength of light of each
other

          Parameter                            Predictions

Size of particles into which         Particles will have radii either
 substance is subdivided              greater or less than 100 nm
Clustering or dispersion of          Small particles with be dispersed;
 particles                            large particles will be clustered
Refractive index of particles        All particles will have relative
                                      refractive indices
Shape for particles with radii less  Particle shape will be arbitrary
 than the wavelength of light
Shape for particles with radii       Predictions are highly case-
 comparable to the wavelength of      specific
 light
Shape for particles with radii       Particles will be spherical
 greater than the wavelength of
 light
Table 2

Predictions for a typical cell that scatters a minimum amount of light:
the predictions cover the shape, distribution (many and small, few and
large), and refractive index of the cellular components

         Component             Constraint          Size

Actin filaments, intermediate  Volume        4 nm, 5 nm, 12 nm
filaments, microtubules

Ribosomes                      Volume              15 nm


Transport vesicles             Volume            15-50 nm



Lysosomes, peroxisomes         Volume         0.1-0.25 [mu]m



Lipid droplets                 Volume          0.1-10 [mu]m




Mitochondria                   Surface area    0.25-10 [mu]m



Nucleus                        Volume           1.5-5 [mu]m


Large vacuole                  Volume           5-15 [mu]m




         Component               Index

Actin filaments, intermediate  1.55-1.62
filaments, microtubules

Ribosomes                      1.55-1.62


Transport vesicles             1.49-1.62



Lysosomes, peroxisomes         1.49-1.62



Lipid droplets                 1.49-1.62




Mitochondria                   1.42-1.49



Nucleus                        1.42-1.49


Large vacuole                  1.34-1.62




         Component                   Predictions

Actin filaments, intermediate  Shape: not applicable
filaments, microtubules        Distribution: dispersed
                               Refractive index: low
Ribosomes                      Shape: arbitrary
                               Distribution: dispersed
                               Refractive index: low
Transport vesicles             Shape: arbitrary
                               Distribution: many, small, and
                               dispersed
                               Refractive index: low
Lysosomes, peroxisomes         Shape: difficult to predict
                               Distribution: many, small, and
                               dispersed
                               Refractive index: low
Lipid droplets                 Shape: arbitrary (if droplets are
                               large, then spherical)
                               Distribution: many, small, and
                               dispersed
                               Refractive index: low
Mitochondria                   Shape: difficult to predict
                               Distribution: many, small, and
                               dispersed
                               Refractive index: low
Nucleus                        Shape: spherical
                               Distribution: not applicable
                               Refractive index: low
Large vacuole                  Shape: spherical
                               Distribution: few, large, and
                               clustered
                               Refractive index: low
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