© 2001 by The Society for Integrative and Comparative Biology
Ontogeny of Vision in Marine Crustaceans1
1 Department of Biological Sciences, University of Maryland Baltimore County, Baltimore, Maryland 21250
2 Department of Biology, Franklin and Marshall College, Lancaster, Pennsylvania 17604
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Marine crustaceans present an extremely interesting set of examples in which to examine visual development and metamorphosis. Larvae of these animals are almost always planktonic, living in the light field of open waters. The presence of a simple, predictable photic environment, the relatively basic visual requirements of larvae, and the need to remain transparent to reduce predation lead to the use of a single eye type throughout all marine crustacean larvae. Adult crustaceans, on the other hand, use a greater diversity of optical designs than all other animals combined, occupy habitats from the deep sea to mountaintops, and have very complex visual systems and behaviors. Thus, visual development varies tremendously among modern Crustacea. In this brief review, we consider the structure and development of marine crustacean eyes, focusing on optics, retinal design, and metamorphosis of the visual pigments.
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INTRODUCTION |
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When animals live in very different environments during different stages of their development, and their sensory requirements change, their sensory systems are obligated to undergo considerable reorganization as ontogeny proceeds. Such is the case with the great majority of marine crustacean species, which almost always pass through a planktonic larval existence before metamorphosing to benthic or nektonic adult forms. Frequently, the habitats of larvae and adults differ greatly from each other in the structure of the visual world, as well as in the intensity and spectral distribution of the illumination.
Perhaps even more significantly, the visual tasks of larvae and adults rarely have much in common. Larval vision is primarily concerned with orientation in the water column, vertical migration, and avoidance of predators (Forward et al., 1984
; Tankersley et al., 1995). Adult vision is employed for far more elaborate tasks in addition to these: navigation, prey recognition and capture, spatial vision, mate selection, and communication (see reviews of Wehner, 1981; Cronin, 1986). Consequently, adult eyes are often quite unlike those of the larvae (for an example drawn from the stomatopods, see Fig. 1). Even when adult and larval crustaceans inhabit the same environments (as in the case of mesopelagic shrimps, such as the oplophorids), the adult visual system is far more complex than what exists in the larval stages and demands specialized ocular adaptations.
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In this review, we will focus primarily on crustacean taxa that include large, powerful marine animals as adults: decapods and stomatopods. Less is known of larval sensory development in other crustaceans, many of which undergo direct development and thereby avoid the challenge of metamorphosis in any case. Our focus will be on the structure and function of the eyes of planktonic crustacean larvae, as these seem to be similar throughout the group, and on some of the changes that must occur as the eye takes on the structure and functions required by the adult.
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STRUCTURE OF CRUSTACEAN LARVAL EYES |
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Throughout the euphausiids, decapods, and stomatopods, larvae invariably possess compound eyes, which are naturally complicated structures. Making such an eye presents a planktonic crustacean larva with an impossible dilemma: the primary passive defense of plankton is transparency, but photoreceptors by definition must absorb light and thereby sacrifice transparency (see Nilsson, 1996
for discussion). The problem is compounded by the need to shield the independent optical units of the eye to preserve some level of optical independence between them and to reduce off-axis stimulation. This screening requires additional light-absorbing material, decreasing transparency yet further. Crustacean larvae respond in the simplest possible way to this challenge; they condense their retinas to a tiny clump in the eye's center, packing the visual and screening pigments into a compact mass. The optical design of a compound eye that permits the smallest retinal radius is the apposition type, so it is not surprising that this is the optical plan used in all larval crustacean compound eyes (Fincham, 1984; Nilsson, 1983; Nilsson et al., 1986; Cronin, 1986; Douglas and Forward, 1989; Gaten, 1998).
Each photoreceptor unit in an apposition compound eye receives input through a single optical system. With proper design (Nilsson, 1983), the optics can be isolated in each ommatidium without shielding and thus remain transparent, as their function is only to refract light onto the receptors. In crustacean larval eyes, the receptor array is tightly bunched into a sphere surrounding the geometrical center of the eye. This array consists of radially oriented photoreceptors (rhabdoms) separated by screening pigment. As mentioned above, the screening pigment is essential; otherwise, the rhabdoms would receive light from all directions, destroying any spatial information. The pigment must lie not only alongside receptors, but also underneath them to prevent light entering from the "wrong" end.
The compact nature of the photoreceptor mass requires the pigment screen to be extremely dense, as very short optical paths separate receptors from each other. Consequently, the retina, while tiny, offers extreme contrast against any bright background. Many larval species have evolved further specializations that reduce the retina's visibility even more. Retinas of zoea larvae of both decapods and stomatopods have an iridescent pigment layer overlying the outer surface, giving the eyes a golden, greenish, or shiny blue appearance when viewed under magnification (see Jutte et al., 1998a). The reflection must be produced by the structural organization of the pigment layer, as also occurs in some adult stomatopods (Marshall et al., 1991). In the larvae, this reflective layer can act to camouflage the dark retina, replacing by reflection the light normally passing from behind the eye that was absorbed by the retinal pigments. Additionally, the retinal screening pigments themselves can be increased in transparency. For instance, in the retinas of some larval stomatopods, patches of a clear, yellow pigment are located between the rhabdoms (Jutte et al., 1998a). The absorption spectrum of this pigment is very similar to that of the visual pigment, implying that it absorbs light that otherwise might excite the receptors. Thus, the yellow pigment confers some degree of transparency to the eye while absorbing light in the critical spectral regions where the photoreceptors must be screened.
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PIGMENTS IN CRUSTACEAN LARVAL EYES |
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Like the compound eyes of adult crustaceans, larval eyes contain several types of pigments. As just described, many of these serve to control the distribution of light within the retina or to reduce the retina's contrast against the background. Similar sets of pigments are used in larval and adult eyes: brown granular ommochromes, reddish or orange pigments in oil droplets, green pigment mixed in with the reflecting pigment, and the yellow material used as a semitransparent screen (Cronin et al., 1995
; Jutte et al., 1998a). Ommochromes and yellow, orange, or red pigments are common in adult crustacean eyes as well (Marshall et al., 1999), so the larvae are not unusual. Based on their characteristic spectral shapes, many of the colored pigments are probably carotenoids, although this has not been confirmed biochemically. In the stomatopods, which as adults use colored pigments extensively to tune photoreceptor spectral sensitivity (Marshall et al., 1991; Cronin et al., 1994a), some of these larval pigments may be ontogenetic (and potentially evolutionary) precursors of the filter pigments later seen in the mature retina. We will return to this point when we discuss metamorphosis of the retina.
Of course, the retina must also include the photosensitive visual pigments, the molecular photoreceptors that take part in the first stages of vision. It is not particularly difficult to prepare larval retinas for microspectrophotometry; even though the eyes themselves are small, photoreceptors themselves cannot be commensurately reduced in scale because of limitations imposed by the physical properties of light. Thus, larval rhabdoms are several microns in diameter, large enough for microspectrophotometric work. Larval visual pigments have been thereby characterized in several stomatopod and decapod species (see Fig. 2, Table 1). Their spectral features identify them as typical rhodopsins, usually with middle-wavelength spectral placement (maximum absorption between 450 and 500 nm). So far, only a single spectral class of visual pigment has been found in any given species. Studies of larval photobehavior do suggest that more than one spectral type of receptor may contribute to phototaxis (Forward, 1987), and ultraviolet (or short-wavelength) vision is common in adult crustaceans (e.g., Cummins and Goldsmith, 1981; Martin and Mote, 1982; Cronin et al., 1994c; Marshall and Oberwinkler, 1999), so it seems quite likely that some larval species will be found to have two (or more) spectral photoreceptor classes in their retinas.
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FUNCTION OF LARVAL VISUAL SYSTEMS |
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The simple observation that crustacean larvae have paired, stalked compound eyes (e.g., Fig. 1A), rather than the simple ocelli found in many holoplankton, implies that vision is a critical sensory modality in these animals. In the vast majority of crustacean species that undergo metamorphosis, larvae are planktonic for at least some period of development. While they occupy the plankton, they must feed, avoid predators, travel to a location where they can successfully metamorphose, and choose a precise habitat within which to complete metamorphosis. Vision has been demonstrated to play a role in all these tasks except for feeding, where only a few equivocal results have been obtained (see Cronin and Forward, 1980
). The compound eye, with almost omnidirectional coverage of the visual world, may be required to provide correct and accurate directional cues for larval orientation.
Larval photoreception plays a primary role in depth maintenance and vertical migration of larvae, both in the ocean and in coastal/estuarine habitats (Cronin and Forward, 1986). However, larval responses are not simple phototaxes. Instead, in coastal waters, responses to light are modulated by other environmental influences, such as pressure, salinity, or temperature. These responses typically act in a negative-feedback system to assist in depth maintenance, and are often modulated during larval ontogeny to bring the larva into the appropriate body of water for correct retention or dispersal, depending on the requirements of the particular larval stage (see Sulkin, 1984; Forward et al., 1984, 1995). Thus, responses of early-stage larvae often disperse them, while later stages, or postlarvae, have responses that bring them near potential adult habitats. Most current knowledge applies to coastal species with benthic adult stages, and it would be exciting (though challenging) to see this work extended to larvae of mesopelagic or deep-sea species.
As metamorphosis approaches, postlarval photobehavior takes on new roles. In crabs, transport to the general area where the transition to the adult stage occurs continues to involve modulation of photoresponses by environmental chemical and physical cues, but the actual settlement onto a particular substrate where the molt to the juvenile state occurs also can involve photoresponses. Animals typically become photonegative when in the correct chemical environment, where they drop to the bottom and commence benthic existence (Forward et al., 1995; Tankersley et al., 1995). Less is known about larval photobehavior in other crustaceans, but virtually all species are faced with the problem of open-water navigation, and it is a safe bet that vision plays a role in this.
The involvement of vision in predator evasion by crab larvae is well established (Forward, 1976, 1977). Species commonly initiate strongly photonegative swimming when the intensity of light decreases, such as would occur when a predator passes overhead; the behavior is known as the "shadow response." The speed of swimming and its accurate orientation should provide effective escape from drifting predators, and possibly from more active planktivores as well.
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ONTOGENY AND METAMORPHOSIS OF CRUSTACEAN COMPOUND EYES |
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Marine crustacean larvae clearly depend on their well-developed eyes for survival; nevertheless, these eyes are poorly suited for the mature stages that appear following metamorphosis. Nevertheless, in crustaceans the adult eye is almost always derived directly from that of the pre-existing larva. This requires extensive remodeling of the structure, as the adult eye often has fundamentally different optics and a far more complex retina. New visual pigments may also be expressed in the adult retina as adaptations to its changed environment or more highly developed visual system. We will consider each of these metamorphic events in turn.
Ontogeny of optical design
The optical mechanisms used by adult crustaceans are extremely varied, and involve more functional designs than are found in all other animals combined (see Land, 1981; Cronin, 1986; Nilsson, 1989). Crustaceans that have apposition compound eyes as adults, like some crabs, may simply continue to use the larval design with few modifications. But it is far more common for the adult type to incorporate optics that are not only different from those of the larvae, but even for which there is no obvious functional intermediate between larval and adult type (such as the transition to superposition optics; see Nilsson, 1983, 1989; Nilsson et al., 1986; Gaten, 1998). In stomatopods, adults do have apposition eyes, but the plan of the adult eye is so different from the larval eye that none of the actual lenses or other optical elements are carried through metamorphosis.
Nilsson (1983) pointed out that the transparent compound eyes of euphausiid and decapod crustacean larvae are in fact pre-adapted to serve either apposition optics, refracting superposition optics, or reflection superposition optics in adults. Thus, the problem of passing through nonfunctional intermediates does not occur during expansion of the eye. Unexpectedly, even juvenile mysids, which are never planktonic, have similar optics to those of larval euphausiids and decapods, and form refracting superposition eyes in adults (Nilsson et al., 1986). In all these animals, the larval eye continues to exist as part of the adult eye, although the number of ommatidia in the adult compound eye far exceeds the larval quantity (Fincham, 1984; Douglas and Forward, 1989; Meyer-Rochow, 1975). As development proceeds in species with reflecting superposition eyes as adults (a design requiring square ommatidia), the facet shapes gradually square off from their originally hexagonal outlines. Similar events occur in the eyes of mesopelagic shrimps, such as the oplophorids (Gaten and Herring, 1995).
More extreme events occur during the late stages of development of bresiliid shrimps (and probably other crustaceans) that occupy deep, benthic habitats (for example, Mid-Atlantic Ridge hydrothermal vents) as adults. Postlarvae settling at the vents have reasonably normal ommatidia, with layered rhabdoms, standard crystalline cones, and faceted external corneas reflective of the zoeal apposition eye (Gaten et al., 1998). However, as the animal matures at the vents, imaging apposition eyes are sacrificed for absolute sensitivity and replaced by naked retina eyes (see Jinks et al., 1998). Optics and eyestalks are traded for smooth corneas backed in some species by extensively hypertrophied retinas (e.g., Rimicaris exoculata; Van Dover et al., 1989; O'Neill et al., 1995; Nuckley et al., 1995; and Chorocaris; Lakin et al., 1997; Kuenzler et al., 1997). In R. exoculata, the retina extends dorso-posteriorly to form a large eye on the dorsal carapace (Van Dover et al., 1989; O'Neill et al., 1995) that appears well-suited for detection of the dim photon fluxes characteristic of hydrothermal vent systems. To increase absolute sensitivity, the screening pigment cells that optically isolate the rhabdoms of imaging retinas are replaced in R. exoculata and Chorocaris by modified pigment cells containing a colloidal suspension that acts to diffuse (rather than absorb) light throughout the retina. In another vent shrimp, Alvinocaris markensis, the adult eyes are degenerate with little evidence of a retina beneath the smooth cornea (Wharton et al., 1997). Preliminary studies of the ontogeny of vision in the Pacific hydrothermal vent crab Bythograea thermydron suggest a similar progression from a larval apposition eye to a hypertrophied, high-sensitivity naked retina eye in settlement-stage juvenile crabs (Markley et al., 2000). Populating sparsely distributed hydrothermal venting systems presents challenges of dissemination and settlement for larvae and post-larval propagules. The metamorphosis of eye and retinal structure observed in these animals from a planktonic imaging system to a high-sensitivity photon detector may contribute to successful settlement at the vents.
While larval eyes of decapods and euphausiids commonly continue to exist as parts of the adult eyes, in stomatopods the larval optics are literally shoved aside and a whole new optical system emerges in a single step at the molt to the postlarva (Morgan and Provenzano, 1979; Provenzano and Manning, 1978; Williams et al., 1985; Hamano and Matsuura, 1987; Cronin et al., 1995). This radical event is required because the optical organization, particularly the ommatidial arrangement, of the adult eye differs entirely from the simple spherical array found in the larvae (Figure 1; see also Manning et al., 1984; Marshall, 1988). Furthermore, as will be discussed later, the retina of adult mantis shrimps contains numerous specialized features not present in the larvae. In these animals, the adult eye forms from the larval eye, but none of the photoreceptors and associated optical elements survive to adulthood.
Ontogeny of the retina
In euphausiids and decapods, since the larval retina persists as part of the adult eye, the photoreceptor array is preserved. Normally, new ommatidia are added at the dorsal margin of the eye, and thus the retina gradually enlarges with growth of the eye at each successive molt. Thus, in some parts of the retina the larval rhabdoms are incorporated into the receptor array. As the eye grows (and in some cases transforms its optics), the rhabdoms may change their size and relative arrangements, but they remain functional (see Fincham, 1984).
Such is not the case with the stomatopods. Here, the larval retina is the typical spherical array, but from the postlarva on, the eyes develop 3 functional regions, occupied by an unequalled diversity of photoreceptor classes and specializations (Manning et al., 1984; Marshall, 1988; Cronin and Marshall, 1989). Among these are a huge proliferation of visual pigments and the appearance of photostable, colored filter pigments in the rhabdoms (Marshall et al., 1991; Cronin et al., 1994a). Together, these specializations produce a unique complex of narrowly tuned spectral receptor classes, highly suitable for true color vision (Marshall et al., 1996; Chiao et al., 2000). Main rhabdoms (i.e., those composed of retinular cells numbered 1 through 7) of adults contain up to 10 different visual pigments (some species, for example Squilla empusa, have only one such pigment, but this is exceptional; see Cronin, 1985). The larval retina, in contrast, has a single visual pigment in all main rhabdoms (Table 1). Stomatopod larvae inhabit coastal or pelagic waters, and thus experience similar habitats across species, but the adults encounter a much more diverse set of photic environments, and have extremely varied sets of visual pigments (Cronin et al., 1994b, 2000). Basically, the adult retina seems to be a completely new structure.
Ontogeny confirms this. In the eyes of final planktonic stages of stomatopod larvae, the future adult-type retina develops adjacent to the larval retina, and at the molt to the postlarva, the optical and retinal arrays of the adult eye suddenly appear (Williams et al., 1985; Cronin et al., 1995). While the visual pigments of postlarvae have not been characterized, the filters in the retina are identical to those of the adults in the same species, and it seems probable that the postlarval retina changes only in its proportions during successive molts to the mature adult stages. The filter pigments may have their precursors in the yellow, orange, or red pigments of the larval retina, as the spectral properties of these larval materials (which originally had the function of screening photoreceptors, not tuning them) resemble those of the retinal pigments used later on as filters. Early in postlarval life, the larval retina persists adjacent to the new adult-type retina, although it probably does not contribute to vision, but it rapidly degenerates (Williams et al., 1985; Cronin et al., 1995). In their formation, as in many other characteristics, stomatopod eyes are very unlike those of other crustaceans.
Ontogeny of visual pigments
Being planktonic, larval crustaceans exist in the photic environment of open water, and one might expect them to have visual pigments typifying open-water organisms. Pelagic species, such as the larvae of open-ocean adults, could have visual pigments that are blue-shifted relative to larvae of coastal or estuarine habitats (see Lythgoe, 1979). There is also the possibility that new visual pigments are expressed after metamorphosis, when the adult occupies a habitat with different photic properties than the larva's; in other words, a physiological metamorphosis might occur in parallel with anatomical events. Many vertebrates change their visual pigments during ontogeny, both by changing chromophores attached to the same opsin (see Lythgoe, 1979) or by expressing new suites of opsins following metamorphosis (Evans et al., 1993; Loew and Sillman, 1993). Fortunately, a small but diverse data set has now been collected for crustaceans, permitting a preliminary examination of these questions (Table 1).
Current data provide at least a suggestion of a correlation between habitat and visual pigment absorption (here given by 
max, the wavelength of maximum absorption). The most coastal species, Squilla empusa (stomatopod) and Callinectes sapidus (blue crab), have visual pigments with peak absorption beyond 500 nm, while the island or open-ocean species of Pullosquilla (stomatopod, 2 species) or Bythograea thermydron (hydrothermal vent crab) have the shortest-wavelength pigments. Larvae of the stomatopod Gonodactylaceus mutatus (formerly Gonodactylus aloha) live along coasts or near islands, and their visual pigment absorbs maximally between those of the other 2 groups. There is, therefore, some suggestion of tuning of visual pigments to environments.
The issue regarding the metamorphosis of visual pigments is more complicated. In most species that have only a single visual pigment in main rhabdoms as adults, the larval pigment appears to be identical to that of the adult. The stomatopod species, Squilla empusa, illustrated in Figure 2, provides an excellent example of this; its adult visual pigment was described by Cronin (1985), and we here present new data obtained from larvae of this species. The template spectra (Stavenga et al., 1993) that fit these two visual pigments differ in max by only 2 nm (507 vs. 509 nm), suggesting that the same pigment is actually present at both life stages. Similarly, in the blue crab Callinectes sapidus, identical pigments are found in the megalopal retina (unfortunately, zoea larvae have not yet been studied) and in the adult (Table 1, see also Cronin et al., 1995). Since most brachyurans have only one main-rhabdom visual pigment (Cronin and Forward, 1988), it may be most common for crab larvae and adults to share the same visual pigment. The hydrothermal vent crab, Bythograea thermydron, would thus be an exception, as preliminary data suggest that the larval and adult stages express different visual pigments (Table 1). This may reflect the very different habitats of these two life stages (pelagic vs. deep hydrothermal vents), and further work on this species or other deep-sea species with pelagic larvae should be very interesting.
Many mantis shrimps present results that are more difficult to interpret. In some, like the case already mentioned for Squilla empusa where the adult retina is rather simple, there appears to be no change of visual pigment. However, most stomatopod species have many classes of visual pigments in the adult retina, so it is not always easy to know whether the larval pigment appears again in the adults; there is so much opportunity for a near-match that small differences are difficult to evaluate. Cronin et al. (1995) concluded that in Gonodactylaceus mutatus the larval pigment is lost at metamorphosis. In the other two stomatopod species included in Table 1, there do appear to be some pigments in the adults that are similar to the larval pigment. Here, the question of metamorphosis awaits resolution using genetic approaches that examine whether the similar visual pigments are based on opsins with different amino acid sequences. In all of the work included in Table 1, the visual pigment templates that fit the larval (and adult) data the best are based on retinal1, with no evidence that any chromophore shift occurs at metamorphosis. It is likely that all marine crustaceans build their visual pigments using this chromophore (see Goldsmith and Cronin, 1993).
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SUMMARY AND CONCLUSIONS |
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The spectacular diversity of eye types of adult marine Crustacea does not appear in their larval eyes, all of which have a transparent apposition design. The ontogenetic appearance of the adult types from the same morphological source provides fascinating examples of evolutionary inventiveness and ontogenetic flexibility. We have shown here how well the larval design meets the ecological and behavioral requirements of crustacean larvae, and how this design can provide a base from which to develop the adult eye. During their development, some crustaceans simply enlarge the larval eye, adding ommatidia as the animal grows. Others entirely discard the larval apparatus, literally pushing it aside and replacing it with a new optical and retinal array. As the photic environments of larvae and adults change, so do the pigments in the eyes of many species, including the visual pigments of photoreceptors. Only a few crustacean species have been studied in detail throughout morphological and physiological metamorphosis, and the research topic holds many, many interesting questions for future students of development, neuroethology, and visual ecology.
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ACKNOWLEDGMENTS |
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Many individuals contributed to the ideas of this paper; we particularly wish to thank R.L. Caldwell, R.B. Forward, Jr., M.F. Land, J. Marshall, and D-E. Nilsson for enlightening discussions over the years. We also thank D. Pales and P. Rutledge for help with preparing the scanning electron micrographs, J. Welch for collecting larvae of Squilla empusa for microspectrophotometry, and C. Epifanio and G. Perovich for collecting larvae and adults of Bythograea thermydron. This work is based on research supported by the NSF, most recently under Grant Number IBN-9724028, and by Franklin and Marshall College.
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FOOTNOTES |
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1 From the Symposium Ontogenetic Strategies of Invertebrates in Aquatic Environments presented at the Annual Meeting of the Society for Integrative and Comparative Biology, 3–7 January 2001, at Chicago, Illinois.
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References |
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