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AMER. ZOOL., 30:175-188 (1990) Crypsis in the Pelagic Environment1 MARGARET J. MCFALL-NGAI Department of Biological Sciences, University of Southern California, Los Angeles, California 90089-0371 SYNOPSIS. Pelagic aquatic environments differ from terrestrial environments in being three-dimensional and relatively homogeneous, rather than two-dimensional and heterogeneous. The present paper examines the causes and consequences of these differences in the context of their influence on the interactions of animals with environmental light. Particular emphasis is placed on light as a determinant of effective modes of crypsis in the two different habitats. The terrestrial world has selected for the expression of crypticity in the form of superficial color patterns. The heterogeneity of this habitat has resulted in evolutionary divergence of these superficial color patterns, often in very closely-related animals. In contrast, in the homogeneous pelagic aquatic habitats, evolutionary convergence on three main forms of crypsis is evident: (1) transparency; (2) reflection of most, if not all visible wavelengths; and, (3) ventral bioluminescence as counterillumination; thus, to be cryptic most animals in these habitats use one or a combination of these modalities to variously transmit, reflect or mimic environmental light. In the present paper, special attention is given to transparency as the most prevalent, yet least understood, of these mechanisms that are used in predator-prey interactions. these animals, such a phenomenon can be considered a kind of "photomorphogeneAn examination of books and research publications on animal coloration and sis," a term thus far only applied to plants. crypsis reveals the absence of any serious In contrast, the whole body morphology treatment of the vast aquatic pelagic envi- of most terrestrial animals results primarily ronment and the selection pressures that from selection pressures imposed by gravsuch an environment has imposed on ani- ity (Little, 1983; Hildebrand et al, 1985; mals in terms of cryptic body form (Poul- Radinsky, 1987), and crypticity is usually ton, 1890; Pycraft, 1925; Elton, 1939; Cott, only "skin deep." To develop these ideas 1957; Wickler, 1968; Edmunds, 1974; within the specific context of this sympoOwen, 1980). This omission is a reflection sium, I would like to: (1) contrast the ecoof the limited extent to which we recog- logically relevant properties of light in the nize, much less understand, the mecha- aquatic and terrestrial environments, and nisms by which animals have become the role of these properties in the selection cryptic 'within the three-dimensional, ho- of the different kinds of crypsis observed mogeneous nearshore and oceanic envi- in the two environments; (2) discuss examronments. It should be clear, then, that an ples of convergent evolution in the three important question to be addressed is this: most prevalent light dependent cryptic How is crypsis achieved in the pelagic envi- mechanisms in the pelagic zone: bioluronment and what are the antipredation minescence, reflectivity, and transparency; strategies available to animals in this iso- and, 3) consider in depth the phenomenon of transparency, the least understood yet tropic (Hutchinson, 1961) environment? probably the most significant of cryptic The present paper examines the concept mechanisms in aquatic habitats. that selection for crypticity in aquatic light fields is a prime determinant of the whole THE QUALITY OF LIGHT IN THE body morphology, and often the anatomy, TERRESTRIAL AND AQUATIC WORLDS of animals in the pelagic zones. Among To understand trends in the relationship between light and modes of animal crypsis 1 From the Symposium on Concepts of Adaptation in in the pelagic portions of the ocean or the Aauatic Animals: Deviationsfrom the Terrestrial Paradigm presented at the Annual Meeting of the American terrestrial world, we must first compare and Society of Zoologists, 27-30 December 1988, at San contrast the nature of the quality of light Francisco, California. that animals experience in the two enviINTRODUCTION 175 176 TABLE 1. MARGARET J. MCFALL-NGAI Factors affecting light quality in different en- vironments. Terrestrial Abiotic Medium — Dissolved materials — Suspended particles — Biotic Bacteria — Plants + Animals — Relative stability* high Benthic aquatic + + + Nearshore Oceanic pelagic pelagic + + + + — — + + — + + + + — low to low to high high high * Stability of all factors as a function of time and space. ronments. Special attention is given to those features that appear to directly influence expression of differential cryptic patterns. The depth of the habitats A considerable difference exists in the distance over which light travels through the terrestrial and aquatic realms. In the terrestrial world, the biosphere is vertically compressed upon the surface to a thin veneer rarely more than 50 m deep. Only birds and insects operate within the fluid that is air, and generally only transiently. Under these circumstances, a major theme of selection has been concerned with interactions of the organisms with the substrate, rather than with the fluid environment, a condition analogous to only the benthic portions of the aquatic world. In contrast, the aquatic environment in some places extends as deep as 11,000 m (Sverdrup et al., 1942). A set of niches is created, that have no true analogue in the terrestrial world, in which the organisms interact throughout their entire life history within the fluid environment, often miles away from the substrate. Abiotic and biotic influences on light quality As it passes through the biosphere, light will be variously transmitted, absorbed, reflected or scattered (Campbell, 1981; Kirk, 1983). The interplay of these processes results in a set of ecologically relevant properties characteristic of a given location, that include the light's intensity, color, angular distribution and polarization. The features of the environment that modulate these properties can be divided into abiotic and biotic influences (Table 1). (1) Medium effects.—As sunlight passes through the earth's atmosphere, it is attenuated through scattering by air molecules, dust, water molecules, and through absorbtion by dust, water vapor, ozone, carbon dioxide and oxygen. Thus, the earth is subject to two light sources, direct solar radiation and diffuse hemispherical sky light produced by scattering (McCartney, 1976). However, over the relatively short distances of the terrestrial biosphere, the magnitude of these processes is negligible, and the light quality is little changed. In contrast, water itself significantly influences the quality of environmental light over very short distances (Jerlov, 1976; Kirk, 1983; Wheeler and Neushul, 1981). In pure water, light intensity decreases logarithmically with increasing distance from the source and the spectrum is narrowed by absorbance of short, ultraviolet and long visible wavelengths of the spectrum, resulting in a predominance of blue light at depth. Light attenuation in the sea occurs over considerable distances, creating a photocline divided into the euphotic, dysphotic and aphotic zones, which are denned on the basis of light quantity (Marshall, 1980). The euphotic zone extends to a depth of about 200 m in the clearest of oceanic waters and is defined as that area where there is sufficient light for net photosynthetic production. In the dysphotic zone, which extends from about 200 m down to about 1,000 m, some light is still present but it is insufficient for effective photosynthesis. Here the quality of surface-derived light is essentially predictable because its intensity, spectral composition and angular distribution change in a regular way both diurnally and with the phases of the moon (Jerlov, 1968). The aphotic zone, which encompasses the majority of the earth's biosphere, extends from about 1,000 to over 11,000 m, with an average depth of 4,000 m over the abyssal plains. In the CRYPSIS IN THE PELAGIC ENVIRONMENT 177 aphotic zone, surface-derived irradiation restrial and nearshore aquatic worlds, phohas been completely attenuated, and the tosynthetic eucaryotes exert the most sigonly ambient light is bioluminescent in ori- nificant potential and actual biotic effects gin. on light quality. In tropical rain forests, the (2) Dissolved substances and suspended par-light is attenuated by plant life often by ticles in nearshore pelagic environments.— over 99% as it travels from the top of the While the water itself may be the only or canopy to the forest floor (Chazdon and most important determinant of light qual- Fetcher, 1984). While some of the green ity in open ocean environments, nearshore light is reflected or transmitted (Loomis, pelagic environments are influenced by a 1965; Smith, 1986), chlorophylls and number of abiotic and biotic factors. One carotenoids of plants absorb much of the of the most important abiotic factors is the visible spectrum, except in the far red presence of soluble and suspended, organic wavelengths (between 700 and 800 nm) and inorganic, light-absorbing material in (Smith, 1986). the medium (Jerlov, 1968, 1976). In the In nearshore aquatic environments, terrestrial world, particles suspended in air there are two distinct forms of plant life (dust storms, volcanic ash, smog, etc.) are that affect light processes in different ways: both ephemeral in time and limited in (1) benthic macroalgae (kelp) and seaspace. This low density medium cannot grasses, which are most often associated support particulate material for protracted with the substrate; and (2) phytoplankton periods. In contrast, in nearshore pelagic (suspended unicellular algae). The presence environments, the suspended particles, of kelp in the environment can reduce light because of the viscosity and density of the incidence on the benthos by 90% or more aquatic medium, can persist for extended (Neushul, 1971; Reed and Foster, 1984), periods of time. However, their geograph- but the effects of the water itself on the ical extent may be quite variable and epi- spectral quality of the light often override sodic, depending upon such factors as the the absorbance, transmission and reflecamount of terrestrial runoff, local wave tion by kelp fronds themselves. In contrast, energy and the distance from shore. Thus, phytoplankton blooms are diffuse and can the influence of these abiotic factors on reach densities at which they may affect not light quality is also quite variable. only light intensity but also the color of the (3) Bacterial blooms.—The biotic influ- light in much the same way as bacteria and ences that are known to affect light quality suspended inorganic particulates can (Kiein nearshore areas include the presence of fer and Austin, 1974; Kirk, 1983; Atlas and bacteria, photosynthetic eucaryotes (phy- Bannister, 1980). toplankton, macroalgae, and seagrasses), Although the spatial distribution of phoand animals. Because bacteria require an tosynthetic organisms may affect light aqueous medium in which to grow, bac- quality in both terrestrial and aquatic nearterial blooms do not occur in air. However, shore environments, there is a major difin freshwater and marine lakes (Truper and ference in the time scale over which plant Genovese, 1968; Matsuyama and Shi- biomass persists in the two environments. rouzu, 1978; Hamner et al., 1982), as well In much of the terrestrial world, the caras the surface film of the open ocean bon in plant material is stably fixed for (Lapota et al., 1988), visibly dense popu- periods of tens to hundreds of years. Even lations of bacteria can occur where nutrient in the temperate zones, which experience and physical conditions are favorable for seasonal fluctuations in the amount of growth. These bacterial blooms can be sta- foliage, the patterns of carbon fixation are ble or stochastic, and in some cases have some of the most predictable of all patterns been shown to affect the light transmit- in the biological world. In contrast, while tance and spectral quality markedly (Ham- a kelp forest community also may persist ner et al, 1982). for many years, the time scale of major phytoplankton blooms often is on the order (4) Photosynthetic eucaryotes: Consideration of time and space scales.—In both the ter- of days. Plankton blooms are an important, 178 MARGARET J. MCFALL-NGAI although unpredictable influence on the light regime of nearshore pelagic waters. Under proper environmental conditions, phytoplankton blooms can typically cover hundreds of square kilometers to a depth of 10 m, appearing and disappearing within a period of a few days to weeks (Brink et al, 1981; Kirk, 1983). A notable exception to the transient and often unpredictable plankton blooms of the temperate zones are the predictable, seasonal blooms of algae in the Antarctic sea ice during austral spring (Lewis and Weeks, 1970; Sullivan and Palmisano, 1981; Palmisano and Sullivan, 1983), a time when pack ice can cover 10% of the world's oceans (Ainley et al., 1986). Algae grow to high density in the layers of ice that interface with the water column. The sea ice and its associated community form a kind of firmament over the fluid environment affecting the intensity and spectral quality of the light below (SooHoo et al., 1987; Palmisano et al., 1987). Light is attenuated to such a degree at these times, with underice irradiances usually less than 1% of the surface (Sullivan et al., 1983), that certain nonvertically migratory mesopelagic species occur in ice-covered surface waters (Ainley et al., 1986). The seasonal patterns of these areas are quite stable and predictable, and thus reminiscent of the terrestrial temperate deciduous forests. variable, depending on their abundance and distribution within any given area. Nevertheless, where major terrestrial plants occur they are stable and predictable in both time and space. With the exception of the Antarctic, both benthic and pelagic nearshore areas experience a very wide variety of unpredictable influences on light quality. THE INFLUENCE OF LIGHT QUALITY ON THE EXPRESSION OF CRYPSIS To understand how light quality will influence crypticity, we must consider the use of cryptic patterns within the context of predator-prey interactions. In Feder and Lauder's book Predator-Prey Relationships (1986), Endler divides the successful predation event into five stages: 1) detection by the predator's sensory system; 2) identification of the cue as a potential prey item; 3) approach; 4) subjugation; and, 5) consumption. In each one of these stages, a variety of defense mechanisms have evolved in prey organisms to avert a successful predation event. For visually orienting predators, the characteristics of environmental light regime will influence most significantly the detection, identification and approach stages. Crypsis is one of the best documented prey mechanisms for avoiding detection by predators using visual cues. This strategy works by reducing the signal(5) The secondary effects of zooplankton graz- to-noise ratio of the prey's image in the ing.—Recently it has been demonstrated predator's visual field (Endler, 1986). by Huntley and co-workers (1987) that Within this context, Endler distinguishes grazing zooplankton within the water col- two kinds of crypsis: 1) masquerade, in umn also can have an indirect but signifi- which the animal resembles an object that cant effect on the light quality in the water is not normally eaten; and 2) eucrypsis, by influencing the density of phytoplank- where the animal resembles a random samton. Comparable effects exhibited by non- ple of the background in which it resides. aquatic animals are rare and transitory Crypsis in terrestrial and benthic events (e.g., locust swarms). aquatic habitats In summary, the terrestrial and open ocean pelagic environments have in comAs biologists we are well aware of the mon that their light quality is affected pri- variety of studies of animal crypsis that have marily by a single component; however, in been reported from terrestrial and nearthe terrestrial world that component is shore benthic aquatic environments (Poulplant abundance, while in the pelagic ocean ton, 1890; Pycraft, 1925; Elton, 1939; Cott, it is the medium itself. Thus, the light qual- 1957; Wickler, 1968; Edmunds, 1974; ity in the open ocean is most influenced by Owen, 1980; Endler, 1978, 1981, 1984; a constant, intrinsic condition, while in the Wicksten, 1983; Greene, 1989). Examples terrestrial world, the influence of plants is of both masquerade and eucrypsis can be CRYPSIS IN THE PELAGIC ENVIRONMENT found in both of these two habitats. Animals in benthic nearshore habitats express similar strategies to those of terrestrial animals; however, these benthic animals experience a wide array of abiotic and biotic influences on light quality (Wicksten, 1983). Thus, these compounding factors have been integrated into the resulting selection of cryptic body coloration. For example, because red light is filtered out with depth in the water column, a red crustacean that would be conspicuous against its background in air is a camouflaged shade of gray in its natural environment. While there is this difference in the variety of influences, cryptic color patterns reflect the interaction of the animals with a solid surface both on the land and in the nearshore benthos, and are divergent and variable because of the heterogeneity of the substratum. Under these circumstances, divergence of color pattern among closely-related species is not uncommon, and reflects differential attempts to either appear as something inedible or match a random sample of their heterogeneous habitat. 179 ment, the three-dimensional, homogeneous pelagic world appears to have selected for the convergent evolution among disparate phyla (from cnidarians to chordates and crustaceans) of three fundamental strategies of eucrypsis: transparency, reflectivity and luminescence. To reduce the signal-to-noise ratio, the organism's body form resembles a random sample of a homogeneous habitat by variously transmitting, reflecting, or mimicking the quality of the ambient photic environment itself. All three mechanisms are used by animals in the pelagic aquatic environments (Marshall, 1971), resulting in morphologies and behavior that rarely if ever made the water-to-land transition. Although the offshore and nearshore pelagic environments differ in their predictability and stability, these strategies often are possible in both environments because they are a response to the photic environment itself and not to the interaction of the animal with the substratum. (2) Biogeographic trends in pelagic cryptic- ity.—Patterns in the use of these three modes of crypsis in any given animal are Crypsis in the pelagic zone related to 1) the biogeography of the species Hamner and co-workers (1975) and Zaret and, 2) characteristics of the biology of the (1975), studying marine and freshwater animal, such as size and life history stratsystems, respectively, analyzed antipreda- egy. In clear oceanic waters, where the light tory strategies in pelagic habitats. In both quality is relatively predictable and stable, environments, four types of antipredation certain biogeographic trends in the occurmechanisms were recognized: 1) time and rence of bioluminescence, reflectivity and space (e.g., vertical migration); 2) body-size; transparency are apparent (Fig. 1). 3) visibility; and, 4) behavior (e.g., schoola. The oceanic euphotic zone. Diurnally ing). Of these categories, visibility is that in the euphotic zone, transparency is the strategy with which detection and, hence, dominant mechanism and all phyla have crypsis is of greatest significance. transparent representatives. Reflectivity is (1) Evolutionary and morphological conse- also a conspicuous mode in the euphotic quences.—There are two important and zone and is best exemplified by schooling distinctive characteristics of cryptic adap- fishes. Often these fishes will be countertations in the isotropic, pelagic environ- shaded, with the dorsum dark and the venment. Firstly, convergent evolution of sim- trum light, to camouflage from above and ilar cryptic mechanisms by phylogenetically below. Because ambient light levels are so different organisms is common, and sec- high in this portion of the ocean, the use ondly, morphological adaptation often of bioluminescence is precluded during the involves the entire anatomy, rather than day as a form of camouflage. simply the adoption of superficial colorb. The oceanic dysphotic zone. The ation patterns. As opposed to divergence dysphotic zone is characterized by the into a vast number of superficial cryptic prevalence of bioluminescence as a cryptic coloration patterns as in the two-dimen- mechanism (Herring, 1978). Examples of sional, heterogeneous terrestrial environ- this kind of adaptation are particularly 180 MARGARET J. MCFALL-NGAI ency, reflectivity and luminescence, which use or mimic light in the environment, are TRANSPARENCY not adaptive in this habitat. REFLECTIVITY EUPHOTtC btolumlnescence Into this seemingly simple set of trends is woven a number of other factors, such 100 as diurnal photic cycle and life history strategy of the individual. At night, the transparency reflectivity DYSPHOTIC photic quality of the upper waters is altered, BIOL.UUNESCENCE such that there is no longer a euphotic zone. Under these circumstances, the use of bioluminescence can be effective right up to woo the surface of the open ocean, and many transparency animals vertically migrate into these areas A PHOTIC reflectivity btolumlnescence at night (Vinogradov, 1968; Robison, 1972), effectively counterilluminating against moonlight and starlight. Further, FIG. 1. Relative importance of the major crypticity whether or not these traits are found within modes characteristic of the pelagic zones of the open a certain individual is a function of a numocean. Capital letters signify dominance of a mode; lower case letters signify that such a mode is of lesser ber of organismal factors including life history strategy. For instance, some fish species importance. have transparent larval stages that, upon prevalent among midwater fishes, cepha- metamorphosis, become reflective, counlopods and Crustacea, all of which often tershading members of the euphotic zone; express their light as serial, ventral pho- other species migrate down to the mesotophores. In these areas of the ocean, pelagic zone to become bioluminescent ambient light quality is attenuated enough counterilluminating fishes (Greenwood, and stable enough to have selected for the 1975). Another strategy, common among expression of ventral luminescence, which larval fishes and small crustaceans, is to have is thought to be used to mimic downwelling most parts of the body transparent, and to light to camouflage the silhouette in a make reflective those portions where behavior called counterillumination transparency cannot be maintained (e.g., (Clarke, 1963; McAllister, 1967). Coun- the enteric tract). Further, many luminesterillumination is considered analogous to cent systems are composed of photogenic countershading. A number of studies on tissue, either autogenic or bacterial, that is the animals in this environment have shown complemented by reflectors and transparthat their luminescence systems produce ent lenses (Herring, 1978). These highly light similar in color, angular distribution complex luminescence systems often and intensity to that of light in the meso- involve large portions of the anatomy and pelagic zone (Denton et al., 1972; Young, morphology of the animal. 1977; Latz and Case, 1982). The anatomy d. Nearshore pelagic environments. of the predator visual systems in the meso- While trends in the use of transparency, pelagic zone suggests that acuity is low reflectivity and bioluminescence such as (Munk, 1966); thus, the serial photophores those described above may occur in the might be perceived as one continuous dif- open ocean, in nearshore pelagic environfuse glow against dim downwelling envi- ments similar patterns are not so clearly ronmental light. discernable. Transparency and reflectivity c. The oceanic aphotic zone. In the are the primary modes of crypsis in these aphotic zone, where solar illumination is waters, while bioluminescence is comparabsent, animals are most often black or red atively rare. Where it does occur, camou(Marshall, 1971), colors that would most flaging luminescence in nearshore animals effectively absorb point sources of biolu- (primarily fishes and cephalopods) is often minescent light produced by potential characterized by an internal, bacterial light predators. The cryptic modes of transpar- organ. One striking example of this can be CRYPSIS IN THE PELAGIC ENVIRONMENT found in leiognathid fishes, a group of approximately 25 species of nearshore perciforms. These fishes inhabit the shallow, low visibility waters along coastlines of the Indo-West Pacific province. Bioluminescence produced by a single internal, bacterial light organ is used in a wide variety of behavioral displays, one of which is counterillumination (McFall-Ngai and Dunlap, 1983). In these fishes much of the anatomy is recruited into the counterillumination camouflaging mechanism. Light produced by the symbiotic bacteria in a circumesophageal light organ is reflected off a silvery-surfaced gas bladder (McFallNgai, 1983a) into nearly transparent hypaxial musculature and through precisely oriented guanine platelets in the skin (McFall-Ngai, 19836). The systems work in concert to produce a ventral luminescent glow that camouflages the fish from below. The resultant ventral glow can be controlled at each level of the light organ system, producing a variable mottled effect. Such a display in these waters of variable optical quality might be considered analogous to the phenomenon of disruptive coloration (Morin, 1983). TRANSPARENCY AS A CRYPTIC MECHANISM IN PELAGIC ENVIRONMENTS Reviews on the subject of cryptic mechanisms rarely include coverage of pelagic animals, and when they do, they concentrate on bioluminescence and reflectivity. Transparency as a cryptic mechanism is almost totally neglected, even though it is probably the dominant form of crypsis in the aquatic environment and biosphere. For this reason, I believe it deserves special attention within the context of this symposium. There are three biologically relevant questions that I will review and explore: 1) What factors render cryptic transparency specific to the pelagic, aquatic environment; or stated from another viewpoint, why is transparency not used extensively in the terrestrial environment as a camouflaging mechanism? 2) What is the evidence that transparency is used by pelagic organisms as a form of camouflage in 181 response to predator/prey interactions? 3) What do we know about the biochemical and developmental mechanisms by which transparency is both achieved and maintained? Transparency as an aquatic-specific characteristic Probably the two most important differences between the aquatic and terrestrial worlds that would influence the expression of transparency are 1) refractive indices of air and water, and 2) the amount of incident ultraviolet light penetrating these two different media. Because animals are largely water, the refractive indices of their tissues could theoretically approach that of water itself (1.34 at 20°C; Maurice, 1957), and, thus, be very different from that of air (1.00 at 20°C) (Jerlov, 1976). As light travels from the surrounding water into the aquatic animal's tissue, the incident angle would be little changed and, if there are no scattering or absorbing elements, the animal would appear transparent. The significant difference in the refractive index of air and the terrestrial animal's tissues creates an easily perceived outline, and is probably the single most important factor that precludes the achievement and use of transparency in the morphology of most nonaquatic animals. Whereas differences in medium refractive index produce an optical constraint, the damaging effects of ultraviolet light on biological systems (Ichihashi and Ramsay, 1976; Rothman and Setlow, 1979; Kantor et al., 1980) create a biochemical limitation on the expression of transparency by terrestrial organisms. The general absence of transparency among nonaquatic animals may be considered indirect evidence of a limitation overcome in only a few exceptional cases. A search of the literature reveals few examples in which the majority of the body of a terrestrial animal is transparent or nearly transparent, with some indication that the transparency is used in crypsis. In one instance, some species of the small glass frogs of the family Centrolenidae, which occur in the rainforests of Central and South America, are often nearly transparent (McDiarmid, 1975), but 182 MARGARET J. MCFALL-NGAI only from a ventral view. Dorsally, these frogs are pigmented (Schwalm et al., 1977). It is believed that the dorsal pigmentation and ventral transparency work in concert to provide effective camouflage in the frog's environment. The second example of terrestrial use of transparency comes from a study of tropical rainforest butterflies. Papageorgis (1975) found that assemblages of butterflies stratify by wing color in the Peruvian rainforests. The various color patterns appear to be used by the butterflies to effect crypsis during flight under the differing light regimes from the top of the canopy to the forest floor. This is also the only example that appears in the literature of terrestrial crypsis in three-dimensional space. The butterfly assemblage closest to the forest floor is almost entirely transparent, camouflaging them within the large patches of filtered light characteristic of that portion of the rainforest. As with the glass frog, the butterflies are in an area of greatly attenuated ambient sunlight. Furthermore, while transparency in insect wings is not uncommon, the analysis of the color patterns of these butterflies appears to be the only really good study of insects where transparency statistically correlated with predator avoidance. Although some ultraviolet light does penetrate into water (Jerlov, 1976; Baker and Smith, 1982), a good deal of it is filtered out within a few meters of the surface, so that organisms living some distance below the surface do not experience the deleterious effects of high-energy irradiation. However, other evidence that the presence of ultraviolet light precludes transparency comes from the studies of marine fish larvae and invertebrates that occur in surface waters where UV irradiation can be substantial. H u n t e r s al. (1981) showed that entirely transparent larvae, such as those of the anchovy, Engraulis mordax, do not survive well when experimentally exposed to ultraviolet light. These findings are correlated with the fact that the larval development of these fishes is restricted to months of the year when incident solar irradiation is sub-maximal. Fish species (such as certain atherinid species) with larvae that are at the water's surface during times of high incident ultraviolet radiation have distinct dorsal pigmentation and, under experimental conditions, resist ultraviolet light damage (Moser, 1982). There have also been a number of studies of the effects of UV on freshwater and marine invertebrates. In freshwater copepods, the presence of carotenoids has been implicated as photoprotection against high energy solar irradiation (Hairston, 1976, 1978, 1979). Further, Jokiel (1980) showed that certain epifaunal species on coral reefs occur only in shaded areas and are killed either when moved to sunlit areas on the reef or are experimentally exposed to UVrich light fields. Species that occur in highly lit areas of the reef have protective pigmentation. Transparency in predator-prey interactions No organism is completely transparent, and the degree of transparency among pelagic species varies over a wide range (Hamner, 1974; Chapman, 1976a, b; Greze, 1964a, b). In addition, the extent to which an increase in transparency translates into a significant advantage in predator-prey interactions is difficult to ascertain. However, as Hamner (1974) points out, anything that reduces the contrast and brightness of the animal would make it more difficult to see and would, in the context of predator-prey interactions, be an advantage. (1) Morphological and behavioral evidence.—There are only a few examples in the literature that transparency is an important mode of crypsis in predator-prey interactions. In analyses of aggressive mimicry in siphonophores, Purcell (1980) describes two species that appear to use transparency to enhance predatory success. The siphonophores Agalma okeni and Athorybia rosacea are highly transparent, except for nematocyst batteries that mimic the appearance of a copepod and a larval fish, respectively. It is hypothesized that the copepod-mimics attract potential prey to the otherwise invisible siphonophores (Purcell, 1980; Mackie et al., 1987). CRYPSIS IN THE PELAGIC ENVIRONMENT Observations of another siphonophore, the Mediterranean species Hippopodius hippopodus (Mackie and Mackie, 1967; Bassot et al., 1978), revealed reversible-blanching behavior. Upon stimulation, the animal changes from almost completely transparent to a milky white in 1-2 sec. If the animal is then left undisturbed, transparency is restored in 15-30 min. The behavior is effected by the control of the movement of granules contained in the mesoglea. When Hippopodius is transparent, these granules are punctate, and upon stimulation, the granules disperse through the mesoglear matrix, rendering the siphonophore visible. Although these studies concentrated on the mechanism of the reversible blanching, Mackie hypothesized that transparency confers an advantage on the siphonophore by making it invisible to potential prey, while the blanching creates a large visible object that will be avoided by fishes and other animals that could potentially damage this delicate animal. Morphological correlates for the use of transparency in predator-prey interactions can also be found among larval fishes. A wide variety of fishes are transparent during their pelagic larval and juvenile stages (Breder, 1962; Meyer-Rochow, 1974; Lasker, 1982). Upon metamorphosis onto the two-dimensional environment of the reef, the fish lose their transparency and assume coloration that renders them cryptic against the substratum. One striking example of this phenomenon occurs in the postlarval or "acronurus" stage of the acanthurid surgeonfishes (Randall, 1961; Thresher, 1984). During this stage, which immediately precedes settlement on the reef, individuals averaging roughly 20 to 25 mm are virtually transparent except for their silvery gut tract. Upon settlement, they transform to a fully pigmented adult fish within as little as 24 hr. While the biochemical and structural mechanisms underlying this process are not understood, the resulting phenomenon suggests that transparency is a developmentally programmed cryptic adaptation used specifically during the larval and postlarval stages of these fishes. 183 (2) Ecological correlates.—Direct evidence that prey visibility is important in predation in pelagic environments has been obtained from studies of crustacean species in freshwater lakes (Zaret, 1975; Kerfoot, 1980; Lazzaro, 1987). For many years, either body size (Brooks and Dodson, 1965; Brooks, 1968) or behavior (Jacobs, 1965) of the prey had been the focus of studies on cues used by fish predators. However, more recent analyses show that, at least in some species, the most important factor is the overall visibility of the prey (Zaret, 1972; Mellors, 1975; Zaret and Kerfoot, 1975; Confer et al, 1978). Zaret (1972) compared rates of predation on two daphnia morphs that are of the same size, but which differ in visibility due to the absolute size of the eyespot. In laboratory experiments, he offered these two morphs in differing mixtures to a known fish predator and found that the predator preferentially selected the large-eyed morph in higher proportion than would be predicted by their proportion in the mixture. Further, he changed the visibility of the small-eyed type by feeding them India ink to create a "super-eye" spot, which was now larger than the eye of the naturally large-eyed type. Under these conditions, the predators preferentially selected organisms with the artificially-produced super eye. These findings were supported by Zaret in a field study in collaboration with Kerfoot (Zaret and Kerfoot, 1975), which showed that when predators are absent, average eye size is always significantly larger. Further, Mellors (1975) investigated predation on daphnia bearing ephippia, pigmented envelopes on the dorsum containing resting eggs. These structures, produced in the Spring and Fall, go through a tanning process prior to release from the maternal daphnia. Mellors found that the more visible ephippial daphnia had higher predation rates than non-ephippial individuals of the same species. Because the ingested eggs survive passage through the gut of the predators, Mellors concluded that this system aids in dispersal. Further, Confer et al. (1978) showed that daphnia with high concentrations of hemoglobin were more likely prey 184 MARGARET J. MCFALL-NGAI TABLE 2. Ways by which animals achieve transparency. Reduced chromophore content High water content Low tissue complexity At least one dimension small Regular arrangement of components than transparent daphnia. These studies all show that, in at least some systems, zooplankton predation is positively associated with their relative degree of transparency. How is transparency achieved and maintained? which it occurs may lend some insight (Table 2). These conditions have proven to be a complex interrelationship of body size, water content, tissue complexity, and the arrangement of the anatomical components of the system. High water content is characteristic of the tissues of many transparent cnidarians and ctenophores, which can attain very large sizes. Much of the body mass of a medusa is represented by the mesoglea, a primarily acellular, watery tissue. In measurements of transparency in these animals, Chapman (1976a, b) found that the mesoglea transmits nearly all of the incident light and the very thin layer of ectodermal cells that overlies the mesoglea is where some light loss occurs. However, more complex animals, with more tissue types and without mesoglea, cannot attain large size and transparency simply by depending on the wateriness of their tissues. John Tyler Bonner's new Quanta within the spectral range of visible light can only be efficiently absorbed by a few specialized biological molecules, such as carotenoids and chlorophylls. These molecules have extended pi-electron systems that promote electronic excitation within the energy range of visible light book, The Evolution of Complexity by Means (Needham, 1974). Most cell constituents, of Natural Selection (1988), includes estisuch as nucleic acids, proteins, carbohy- mates of the number of cell types in organdrates and lipids, cannot themselves absorb isms from one, in unicellular animals, to quanta in the visible wavelengths. Thus, about 55 in the squid and 120 in verteone way to reduce visibility is to limit the brates. It seems logical that the more comnumber of absorbing molecules or pig- plex the animal, the more different types ments. However, transparency of a system of tissues must be adapted for specific funccan also be compromised by the scattering tions, and the more difficult it would be to of light. When the constituents of cells are achieve overall body transparency. One way organized into more complex structures, to get around this problem is to be small such as membranes and organelles, and in at least one dimension. The leptocephthese cells become organized into tissues, alus larvae of eels may have body lengths scattering becomes significant. If a struc- and depths of up to several hundred milturally complex or large animal is to attain limeters and achieve transparency by being transparency, it must conquer this prob- leaf-like (i.e., small in width) (Meyerlem. The problem is further exacerbated Rochow, 1974). A great majority of the because cell constituents and their orga- transparent species of the higher phyla are nization are subject to perturbation by small in overall body size. environmental stresses such as temperaIn addition to these mechanisms, transture and pressure. Therefore, the orga- parency can be achieved through the regnization of such structures to achieve trans- ular arrangement of cellular components. parency is also likely to be perturbed by The most notable cases of transparency such stresses, and the adaptation to differ- occur in the dioptric apparati of the eye ent environments must be not only bio- (the lens and cornea), which are thought chemical (Hochachka and Somero, 1984), to achieve transparency in this manner (Cox but also morphological. et ai, 1970; Delaye and Tardieu, 1983). Our understanding of how transparency Chapman (1976a, b) has suggested that ceris achieved and maintained is poor. How- tain transparent animals, such as chaetoever, an analysis of those conditions under gnaths, may also have some precision in 185 CRYPSIS IN THE PELAGIC ENVIRONMENT the arrangement of tissue components to promote transparency. Transparent animals, like all organisms, must tolerate environmental and physiological stress. The degree to which such stresses may compromise transparency itself is an area that has not been explored. However, a large body of literature does exist indicating that animals in stressful habitats have metabolic machinery that is adapted to work optimally under the set of environmental conditions that they experience (Hochachka and Somero, 1984). As ambient conditions move away from this preferred temperature/pressure range, biological molecules, particularly proteins, will cease to function properly and, eventually, denature and precipitate. Whereas no data are available on how such processes would influence transparency of pelagic animals, some data do exist on the influence of temperature on transparency in one tissue: the vertebrate eye lens. In a recent, yet unpublished study, we analyzed the resistance of lenses and their constituent proteins to temperature stress (McFall-Ngai et al., in preparation). The study included ingroups and outgroups within all the vertebrate classes, including organisms with preferred body temperatures that ranged from 2° to 39°C. Our results showed a strong positive correlation between both the retention of transparency of the whole lens and the solubility of its constituent proteins, and the preferred body temperature of the animal. Though much more complex, the transparent bodies of pelagic animals may be similarly adapted to a certain range of environmental conditions. TERRESTRIAL PELAGIC AQUATIC PHYSICAL CHARACTERISTICS OF THE PHOTIC ENVIRONMENT 2-D, heterogenous 3-D. homogenous long-term, predictable transient, stochastic BIOLOGICAL CONSEQUENCES FOR CRYPTIC PATTERNS primarily divergent primarily convergent transparency, blolumlnascance. and r«fl«ctMty superficial only whole body and superficial 'PHOTOMORPHOGENESIS' FIG. 2. Summary of the physical differences in the light quality in the terrestrial and aquatic realms, and the biological consequences of these differences in the selection of crypticity. with the casual observations of many marine biologists that transparent organisms often become opaque just before death, strongly suggests that the transparency is maintained by active physiological means. CONCLUSIONS Although crypsis has been a widely studied phenomenon in terrestrial and benthic aquatic habitats, its involvement in predator-prey interactions in the pelagic environment is poorly understood. Intrinsic differences exist between the expressions of cryptic body form, because of the nature of the light environment experienced by The loss of transparency as a result of animals in these various habitats (Fig. 2). physiological stress has been well docu- The light environment of the pelagic zones mented in cataractogenesis of the verte- has selected for the convergent evolution brate eye lens (Bloemendal, 1981). Whereas of transparency, reflection of all wavepelagic animals have been little studied in lengths, and bioluminescence as crypticity this regard, Hamner (1984) reports the loss strategies in a wide variety of pelagic phyla. of transparency in krill, Euphausia superba, Of these modes, transparency is probably as a result of parasitism. 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