REEXAMINATION OF EYE DESIGN IN THE CLASSIFICATION OF STOMATOPOD CRUSTACEANS Christine Harling

JOURNAL OF CRUSTACEAN BIOLOGY, 20(1): 172 185, 2000 REEXAMINATION OF EYE DESIGN IN THE CLASSIFICATION OF STOMATOPOD CRUSTACEANS Christine Harling Sussex Centre for Neuroscience, University of Sussex, Falmer, Brighton, BN1 9QG, United Kingdom (e-mail: c.harling@sussex.ac.uk) ABSTRACT At least 7 distinct eye types have evolved in the Stomatopoda. This reflects adaptations to the wide range of habitats and depths in which stomatopods occur. However, there are some species for which eye design does not correlate with environmental factors. The distribution of certain eye types in taxonomically unrelated groups suggests that their occurrences result from convergent evolution. The current classification of stomatopods into five superfamilies is not supported by eye design. Polyphyly in the Gonodactyloidea is proposed. Eye structure cannot be used as a taxonomic character to superfamily or family level in stomatopods, but is helpful in the diagnosis of genera and species. A few genera and species can be distinguished from their eye design alone. A variety of apposition and superposition optics has evolved among crustacean taxa. Crustaceans are ubiquitous in aquatic environments, and there is an accordingly diverse range of visual adaptations to suit many different habitats, whether they be intertidal or abyssal, benthic or pelagic. Once evolved, eye structure is generally a stable character and the occurrence of a particular eye type in many different groups is likely to indicate a shared ancestry. Accordingly, eye design is often an informative character in crustacean taxonomy. For example, reflecting superposition optics are found in penaeid, caridean, and stenopid shrimps and prawns, supporting their grouping into the Suborder Natantia. Eye structure does not support the Reptantia or Anomura, both of which include species of varying eye types (Fincham, 1980). Stomatopods have compound apposition eyes of an unusual design. Their eyes are notable both for their diverse corneal shapes and for the complexity of the internal structure. A stomatopod eye is usually distinguishable from any other crustacean eye by the presence of a midband. The term midband is a loose description and refers to the central rows of enlarged ommatidia. The midband ommatidia may or may not be morphologically and functionally distinct from those in the peripheral retina. In many stomatopods in the superfamilies Gonodactyloidea and Lysiosquilloidea, the midband is composed of six rows. Four of these rows have an unusual tiered retina containing multiple classes of photoreceptive pigment and also up to four classes of photostable carotenoid filters (Marshall et al., 1991b). There is behavioral evidence that stomatopods can distinguish colors (Marshall et al., 1996). The remaining two rows of the midband are specialized for the reception of polarized light. Stomatopods in the superfamily Squilloidea do not have these adaptations for color vision. The external and internal eye morphology of stomatopods is subject to considerable variations throughout the group (Manning et al., 1984a; Marshall et al., 1991a, b; Marshall and Land, 1993a, b). Externally, variations are apparent in the corneal shape, facet size and shape, and the number of midband rows. Manning et al. (1984b) observed that four distinct eye types have evolved within the Stomatopoda, each characteristic of one of the four superfamilies. Members of the Lysiosquilloidea and Gonodactyloidea had six rows of ommatidia in the midband. Gonodactyloids had square corneal facets in the midband rows, whereas those in lysiosquilloids were hexagonal. Squilloids had two midband rows and in bathysquilloids the midband was absent. However, this study was a preliminary investigation, with conclusions based on observations of only 18 species. Since that study was made, several new species of stomatopods have been recognized. Their taxonomy has been subjected to a number of reviews and a fifth superfamily, the Erythrosquilloidea (Manning and Camp, 1993), has been set up. The distribution of eye types among the new taxa has not yet been assessed. Moreover, the study was made before recent research into the structure and 172

HARLING: EYE DESIGN IN STOMATOPOD CRUSTACEANS 173 function of the stomatopod midband. It is now known that the color vision apparatus in the midband rows varies in its complexity, and that species with superficially similar eye types may differ in their retinal structure (Cronin et al., 1994a, b). The number of classes of photosensitive pigments present, and the number, position, and length of the color filters may vary. The number of rows in the midband and their specializations is potentially a very informative character in stomatopod classification, since it is likely to reflect evolutionary radiation and adaptation. To establish such a relationship, there is a need to thoroughly investigate correlations between eye structure and ecological factors such as depth and substrate. The cornea shape and surface structure depend on ambient light conditions and behavior patterns (Abbott et al., 1984). Most species conform to expectations, i.e., those from shallow, clear water have the largest pseudopupils and small corneal facets, reflecting high acuity but low sensitivity. There are a number of anomalous species, for example, Echinosquilla guerinii White, from dimly lit habitats, which has unexpectedly small corneal facets. In species thus far studied, the complexity of the color vision system also relates to the spectral quality of the surrounding water (Cronin et al., 1993). New information regarding the stomatopod midband now needs to be incorporated with other aspects of stomatopod eye design relevant to taxonomic studies. It is apparent that a comprehensive survey of external and internal eye morphology is required to assess the value of old and new characters in stomatopod taxonomy across a much larger sample of species than considered in previous studies. This study is an extensive review of variations in the eye characters used in stomatopod classification and a preliminary survey of several new characters. The taxonomic level at which different eye characters are most appropriately used will be considered. Eye design is undoubtedly of importance in stomatopod taxonomy, but the way in which it is used in classifications needs to be thoroughly described. MATERIALS AND METHODS The external eye structure was examined in representatives of 99 genera, included in each of the eighteen families and five superfamilies of stomatopods. The eye size, cornea shape, and midband organization were noted for each species. Actual eye size was taken as the measurement across the widest axis of the cornea. The obtain comparable data, eye size was also calculated as a percentage of body length. Measurements of body length were taken along the dorsal midline from the tip of the rostrum to the apices of the submedian teeth of the telson. The eyes of a selection of species were also examined from wax-embedded sections taken through transverse and longitudinal axes to investigate the cellular organization of the retina, with particular attention to the midband region. As far as possible, sectioning was performed on fresh material, but many results were obtained from older, preserved material. A comparison of freshly fixed, year-old and ten-year-old material from a well-studied gonodactyloid species, Neogonodactylus oerstedii, showed that long-term preservation in 70% ethanol has little impact on the basic cellular structure of the eye. The material for this study included specimens from the collections of the Natural History Museum, London; the National Museum of Natural History, Smithsonian Institution, Washington, D.C.; the Zoological Museum, University of Copenhagen; the Muséum national d Histoire naturelle, Paris; and the Australian Museum, Sydney. RESULTS Eye size in a sample of stomatopods is shown in Table 1. Measurements have been recorded as an index of the body length in or- Table 1. Eye size in stomatopods. All measurements taken from mature males. S.F. = superfamily; B = bathysquilloidea; G = Gonodactyloidea; L = Lysiosquilloidea; S = Squilloidea; E = Erythrosquilloidea. Body Cornea Cornea length/ length length body length Species S.F. (mm) (mm) 100 Bathysquilla microps B 165 4.0 2.4 B. crassipinosa B 151 5.4 3.6 Altosquilla soelae B 101 2.9 2.9 Indosquilla manihinei B 160 4.3 2.7 Erythrosquilla megalops E 105 9.2 8.8 Eurysquilla sewelli G 32 1.9 5.9 Manningia pilaensis G 64 2.4 3.8 Odontodactylus scyllarus G 162 5.7 3.5 Hemisquilla ensigera G 128 6.1 4.8 Pseudosquilla oculata G 30 1.5 5.0 Pseudosquillopsis lessoni G 62 3.3 5.3 Parasquilla ferussacii G 110 4.2 3.8 Faughnia serenei G 82 3.4 4.1 Neogonodactylus oerstedii G 53 1.8 3.4 Echinosquilla guerinii G 74 2.4 3.2 Lysiosquilla maculata L 217 8.2 3.8 L. maculata L 289 9.2 3.2 Heterosquilla tricarinata L 73 2.5 3.4 Heterosquilloides insignis L 52 3.2 6.2 Allosquilla africana L 46 2.5 5.4 Alachosquilla vicina L 43 1.8 4.2 Coronis scolopendra L 45 1.6 3.6 Clorida microphthalma L 32 0.9 2.8 Harpiosquilla raphida S 277 11.9 4.5 Squilla mantis S 157 6.9 4.4

174 JOURNAL OF CRUSTACEAN BIOLOGY, VOL. 20, NO. 1, 2000 Fig. 1. Bathysquilloid eyes. A, Bathysquilla crassispinosa, right eye; B, transverse section through right eye of B. crassispinosa with a diagrammatic representation of the arrangement of retinular cells R1 7. der to allow an objective comparison of the eye size in different species. Observations on the external and internal features of stomatopod eyes show that the variations in eye design within each superfamily are wider than previously recognized. Bathysquilloidea The four members of this superfamily have a very similar eye structure. The eyes are small in size. In Bathysquilla microps, Altosquilla soelae, and Indosquilla manihinei, the cornea width is ~2.4 2.9% of the body length. Bathysquilla crassispinosa has larger eyes of 3.6% of the body length (Fig. 1a). The cornea may be globular or bean-shaped and, unlike other stomatopods, the ommatidia are not organized into regular rows. As in many other deep-water crustaceans, the cornea is heavily sclerotinized, with the result that, externally, the facets are barely discernible. There is no evidence of a midband or of any functionally distinct portions in the retina. Sections taken through the eyes of B. crassispinosa are comparable to those from the periphery of a typical species of Gonodactylus. The retinular cells R 1 7 conform to the typical configuration of stomatopods (Fig. 1b), although, as in some squilloids, the rhabdom from the eighth retinular cell is absent. There is a substantial layer of distal pigment just below the level of the crystalline cones. Erythrosquilloidea The superfamily Erythrosquilloidea is currently represented by only a single species, Erythrosquilla megalops. This species has very large eyes approaching 9% of the body length. In shape, the bilobed cornea resembles that of the genus Lysiosquilla, but the midband is apparently absent. Unfortunately, this species is known only from the male holotype and a thorough investigation of eye structure is not possible at present. Squilloidea The basic eye structure is consistent throughout the 160+ species in this large superfamily. In most genera, the cornea is broadly bilobed as in Squilla mantis (Fig. 2a).

HARLING: EYE DESIGN IN STOMATOPOD CRUSTACEANS 175 Fig. 2. Squilloid eyes. A, Squilla mantis, right eye; B, Clorida microphthalma, right eye; C, Crenatosquilla oculinova, right eye; D, transverse section through the two midband rows and peripheral retina in Natosquilla investigatoris. M.B. = Midband.

176 JOURNAL OF CRUSTACEAN BIOLOGY, VOL. 20, NO. 1, 2000 Eye size is generally between 4% and 6% of the body length. Certain species such as Clorida microphthalma (Fig. 2b) and Crenatosquilla oculinova (Fig. 2c) have an unusual cornea shape. In C. microphthalma, the cornea is very much reduced in size and appears out of proportion with the enlarged, bulb-shaped eyestalk. The crown-shaped cornea of Crenatosquilla is perhaps the most unusual eye shape of any crustacean. A midband is present in all squilloid species, apparent only as two central rows of ommatidia. As in Natosquilla investigatoris (Fig. 2d), the midband is evident in longitudinal section as two rows whose optical axes are perpendicular to the plane of the cornea. The rows adjacent to the midband are skewed toward it, so that at the level of the retina there is a clear gap between the midband and the periphery. There is no evidence of differentiation, such as tiering of the retinal cells, in the midband rows. Lysiosquilloidea In the Lysiosquilloidea the eyes are typically broadly bilobed or globular with a sixrow midband of hexagonal or rounded facets. The corneal facets and crystalline cones in rows two and four of the midband are usually smaller than in the other midband rows (Fig. 3a). Notable exceptions to this rule are Allosquilla africana and Heterosquilloides. Allosquilla is a monotypic genus, currently placed in the family Nannosquillidae. Allosquilla africana has a midband of two rows and exceptionally large eyes for that family (5.4% of the body length compared with only 3.6% in Coronis scolopendra, another nannosquillid). As in the bathysquilloids, the eyes of Allosquilla have a thickened cornea and an abundance of dark screening pigment just below the level of the crystalline cones (Fig. 3b). All three species in the genus Heterosquilloides have a two-row midband. On first inspection, the midband appears to be formed of four rows due to extreme inward skewing of ommatidia in the rows immediately adjacent to the midband (Fig. 3c). In longitudinal sections, it is apparent that midband is formed of only the two central rows (Fig. 3d). Other lysiosquilloid genera may also have atypical eyes, but the scarcity of specimens has precluded a verification of this by sectioning. Externally, Acoridon and Parvisquilla appear to have a midband of fewer than six rows. Paracoridon may also have a reduced midband. Gonodactyloidea This is the most diverse of the superfamilies in terms of eye design. The most common gonodactyloid eye type has a globular or bean-shaped cornea, and a midband of six, equally sized rows with rectangular facets. The morphological differentiation of the midband ommatidia from those in the periphery can be clearly seen in transverse section, especially in species with large eyes such as Hemisquilla ensigera (Fig. 4a). Most genera in two families, Parasquillidae and Eurysquillidae, do not have typical gonodactyloid eyes: (1) Parasquilla and Faughnia (Parasquillidae). The cornea is asymmetrically bilobed with the medial lobe broadly rounded and the lateral lobe more protruding and globular in shape (Fig. 4b). The midband is composed of only two undifferentiated rows of ommatidia. The corneal facets are hexagonal, giving a closer resemblance to members of the Squilloidea rather than to the gonodactyloid type. Species of Faughnia have more distal pigment than those of Parasquilla, giving the eyes a darker appearance. (2) Pseudosquillopsis (Parasquillidae). The four species in Pseudosquillopsis have a particularly unusual eye design. The cornea shape is similar to that of Parasquilla, but this time there are three rows in the midband (Fig. 4c, d). This is a condition not seen in any other stomatopod. The midband rows have an identical structure to those in the periphery. (3) Manningia and Coronidopsis (Eurysquillidae). These two closely related genera have an extremely bilobed cornea with the result that each hemisphere of each eye is almost globular. The midband is composed of only two rows. Again, an abundance of distal pigment in the eye gives them a very dark, almost black, coloration when preserved in alcohol (Fig. 4e). The appearance of the eyes in live animals is unrecorded. (5) Eurysquilla (Eurysquillidae). This is currently a somewhat heterogeneous group and on the basis of eye design alone, the genus divides into two distinct groups. One group of species comprises E. foresti (Fig. 4f), E. veleronis, E. delsolari, E. leloueffi, E.

HARLING: EYE DESIGN IN STOMATOPOD CRUSTACEANS 177 Fig. 3. Lysiosquilloid eyes. A, Lysiosquilla maculata, longitudinal section showing midband of right eye. Note the reduced size of crystalline cones in rows 2 and 4 (rows oriented dorsal (top) to ventral); B, Allosquilla africana, longitudinal section through left eye. The midband is composed of two rows. There is an abundance of dark pigment below the crystalline cones and surrounding the rhabdoms; C, Heterosquilloides insignis, external view of left eye. The midband appears to have four rows; D, Heterosquilloides insignis, longitudinal section through left eye. The midband is actually formed only of two rows of ommatidia. M.B. = Midband. galathae, E. pumae, E. sewelli, E. plumata, and E. maiguensis. All these have eyes resembling those of a typical lysiosquilloid. The midband is composed of six rows, but the facets are rounded and of smaller size in rows 2 and 4. The cornea may be bilobed or have a flattened, rounded shape in this group. The second, smaller group of species contains E. chacei, E. crosnieri, E. holthuisi, and E. pacifica. These have a strongly bilobed cornea re-

178 JOURNAL OF CRUSTACEAN BIOLOGY, VOL. 20, NO. 1, 2000 Fig. 4. Gonodactyloid eyes. A, transverse section through the midband in Hemisquilla ensigera; B, left eye of Parasquilla ferrusacii; C, right eye of Pseudosquillopsis lessonii; D, longitudinal section through right eye of P. lessonii; E, eyes of Manningia australiensis; F, corneal facets of Eurysquilla foresti. Those in rows 2 and 4 of the midband are reduced in size. M.B. = Midband.

HARLING: EYE DESIGN IN STOMATOPOD CRUSTACEANS 179 Table 2. Table summarizing midband size in stomatopod taxa. (G) = Gonodactyloidea, (L) = Lysiosquilloidea, * = external observation only. Number of midband rows 0 2 3 6 Bathysquilloidea Squilloidea Pseudosquillopsis Gonodactyloidea *Erythrosquilloidea Parasquilla (G) (G) and Faughnia (G) Lysiosquilloidea Manningia (G) Coronidopsis (G) (Except those Eurysquilla spp. (G) indicated Allosquilla (L) otherwise). Heterosquilloides (L) *Acoridon (L) *Parvisquilla (L) sembling that of Manningia. On external examination, the midband consists of only two rows, although this is unconfirmed by sectioning. DISCUSSION The observations made here are not in full agreement with previous studies. Contrary to Manning et al. (1984b), this study finds that more than four distinct eye types have evolved in the Stomatopoda. Furthermore, the use of eye design, particularly the midband arrangement, as a taxonomic character at superfamily level is not supported. At present, the Bathysquilloidea can be defined by the absence of a midband, although Erythrosquilla may yet prove to share this condition. Eye design is consistent throughout the Squilloidea, where the midband is always formed of two rows. This state, however, cannot be used to define the Squilloidea, since it is also present in members of the Gonodactyloidea and Lysiosquilloidea. In these two superfamilies, a six-row midband is typical of most members, but this is not present in all species. Table 2 summarizes midband size across all stomatopod groups. This study demonstrates that accurate information on the eye characters currently used in stomatopod taxonomy cannot be obtained from external observations alone. Heterosquilloides provides a good example of the need to thoroughly investigate the eye structure by sectioning before reaching conclusions regarding the midband construction. Due to extreme inward skewing of the rows of ommatidia immediately adjacent to the midband, Heterosquilloides appears outwardly to have four midband rows. In transverse and longitudinal section, it becomes clear that there are only two rows in the midband, which, unusual for a lysiosquilloid, are unspecialized. Evolutionary Origins of Stomatopod Eye Types Although the fossil history of stomatopods can be traced back to their emergence around three hundred million years ago, the five extant lineages, as they are currently recognized, diverged only one hundred million years ago (Manning, 1968). A common ancestry must be assumed for the Gonodactyloidea and Lysiosquilloidea, since it is unlikely that such a complex eye would have evolved independently in each group. The six-row midband typical of most gonodactyloids and lysiosquilloids would have been established before their divergence. The presence of a two-row midband in members of both lineages is, therefore, an effect of convergent regressive evolution. If this regression has occurred independently in gonodactyloid and lysiosquilloid species, it follows that the simple eyes of the squilloids may have similar origins. Rather than representing a primitive state, prior to the evolution of the six-row midband (Cronin et al., 1993), it may instead be a more recent adaptation. Pseudosquillopsis presents a puzzling case. The midband is formed of three rows but, as in the Squilloidea, these rows are undifferentiated with respect to those in the periphery. In evolutionary terms, it is difficult to determine the relationship between this condition and either a two- or six-row state. If the two-row midband is the primitive state, there would be no obvious advantage in adding a third, unspecialized row. Functionally, a six-

180 JOURNAL OF CRUSTACEAN BIOLOGY, VOL. 20, NO. 1, 2000 Table 3. Typical depth ranges and habitats for stomatopod taxa. Data quoted are from the world catalog of the Stomatopoda (Müller, 1994). Genus/species Known depth range (meters) Habitat information Bathysquilloidea Bathysquilla microps 500 1,519 soft, level substrates B. crassispinosa 200 350 on outer continental Altosquilla soelae 400 456 shelf and continental Indosquilla manihinei 420 580 slope Erythrosquilloidea Erythrosquilla megalops 75 175 unrecorded Gonodactyloidea Neogonodactylus intertidal 10 coral reef Hemisquilla ensigera 20 200 sandy mud Faughnia 70 385 mud/shingle Parasquilla 20 700 mud/sand Pseudosquillopsis intertidal 100 sand and cobbles/sea-grass beds/mud Echinosquilla guerinii 40 100 coral reef Pseudosquilla ciliata intertidal 110 reef-flats/sea-grass beds Manningia intertidal 100 rocky reef/sand Coronidopsis 15 100 mud and sand Eurysquilla chacei 419 fine sand Eurysquilla galatheae 10 100 fine sand Lysiosquilloidea Acoridon manningi 95 100 continental shelf Coronida intertidal 70 rubble Parvisquilla <10 in nonliving bases of corals Allosquilla africana 130 230 clayey silt Coronis scolopendra intertidal 2 littoral mudflats Acaenosquilla 55 100 gravel Heterosquilloides 90 510 mud Lysiosquilla sulcata intertidal 20 coarse sand in reef lagoon Squilloidea Squilla mantis 5 320 (usually <120) muddy sand Crenatosquilla oculinova 0 23 coral rubble row midband is divided into rows one to four for color vision, and rows five and six for polarization vision (Marshall, 1988). If the visual system of the midband was reduced to two rows, it would seem logical that rows one to four would be lost. In Pseudosquillopsis the loss of only three rows and the lack of specializations in the remaining three rows are perplexing. Pseudosquillopsis and other parasquillids are probably an intermediary lineage between the gonodactyloids and squilloids. The threerow midband of Pseudosquillopsis is a relic of the transition in eye design between these two groups, but it is unclear how that transition may have proceeded. Stomatopod Eyes and Habitat Table 3 shows the known depth range and habitat for a sample of stomatopod genera and species. The majority of the Gonodactyloidea are found in reef habitats in clear, shallow water. They defend crevices in the coral structure or excavate holes in the gravel under rocks. Exceptions are Hemisquilla, which constructs burrows in soft sandy substrates, and also members of the families Parasquillidae and Eurysquillidae, notable also for their atypical eyes. The Lysiosquilloidea are typically found in depths of 10 50 m and most prefer soft substrates. Some of the Coronididae are reef-dwelling; Coronida is found in large recesses and among rubble, and Parvisquilla inhabits the abandoned burrows of boring worms deep within coral heads. The Squilloidea construct burrows in soft sand, silt, or mud substrates. Most occupy deeper water than the Lysiosqulloidea, with the result that their surrounding water is generally dimmer and more turbid. Little is known about the ecology of the Bathysquilloidea. All inhabit deep water, from 100 m down to 2 km, and are thought to prefer soft substrates. Most of the species with a simpler eye design are from deep water. Their eyes are of-

HARLING: EYE DESIGN IN STOMATOPOD CRUSTACEANS 181 ten large as in Bathysquilla crassispinosa, Erythrosquilla megalops, and Allosquilla africana. These three are found in the 100 350 m depth range where vision is still an important sense. As would be expected, the eyes of the deepest-living species, B. microps (600 1,500 m), are considerably smaller. In Parasquilla, Faughnia, Allosquilla, and Heterosquilloides, the deviation from the characteristic gonodactyloid/lysiosquilloid eye type is appropriate for the depth ranges at which they live. In most cases, stomatopod eyes reflect adaptations to the surrounding environment, but there are a number of exceptions where that correlation is not immediately obvious. Crenatosquilla oculinova is an unusual squilloid species that lives among shell, rock, and rubble in shallow, bright water. As in all squilloids the midband is composed of two unspecialized rows. On first consideration, this would seem to put C. oculinova at a disadvantage when compared to other stomatopod species in the same habitat that have more complex eyes. However, C. oculinova is a nocturnal species and its eye design is thought to optimize light capture and rangefinding in dim light (Schiff and Manning, 1984). Pseudosquillopsis is present in the intertidal and subtidal zones, very rarely below 30 m. It excavates short burrows under rocks or cobbles on the sea bed. In southern California, its range overlaps that of another gonodactyloid, Hemisquilla ensigera. This is normally found in deeper water, around 20 40 m, on flat, featureless sand or mud substrates. Hemisquilla has the typical gonodactyloid eye with a six-row midband. From a comparison of the two species, the three-row midband of Pseudosquillopsis apparently does not reflect an adaptation to environmental light levels or substrate features. Coronidopsis and Manningia frequently occur in shallow water or even intertidal habitats, and yet have abandoned the specialized parts of the midband which would enhance vision in bright light. Perhaps the eyes seen in the Parasquillidae and Eurysquillidae illustrate an ancient evolutionary and taxonomic separation from the other gonodactyloids rater than adaptations to current circumstances. If their ancestors once had color vision, this has been lost, perhaps as a consequence of a reduction in ambient light levels long ago. Once the color vision system was lost, it did not reevolve in genera such as Pseudosquillopsis and Manningia after a subsequent move back to clearer water. The eye design of stomatopods is clearly highly variable, showing a wide range of adaptations to their particular environments. The importance of vision in the life-style of stomatopods has allowed for substantial investment in the evolution of optics that fulfill individual requirements. Visual pigment diversity in stomatopod eyes implies that their evolution was rapid (Cronin et al., 1996). The range of adaptations was probably established a long time ago and has persisted until today. If eye design stabilized after the initial rapid evolution, this may help to explain why the eyes of some stomatopods do not seem to be ideally suited to their environment. Stomatopod Eyes and Taxonomy In most crustacean groups, eye design is evolutionarily stable and can be treated as a reliable character for establishing taxonomic relationships (Fincham, 1980). The presence of the same eye type in different taxonomic groups suggest an ancestral affinity, present before their divergence and persisting afterward. Stomatopod eyes do not appear to be as stable, and there are many examples of convergence in eye evolution. On the basis of eye design, this study does not support the current division of stomatopods into five superfamilies. The variations in external eye design are such that this cannot be used as a defining character to superfamily or even family level. The distinguishing eye types for each superfamily proposed by Manning et al. (1984a, b) should be considered a general trend rather than an absolute characteristic. However, stomatopod eyes provide many useful characters that may be used in the definition of species and genera. With the omission of Eurysquilla, external eye design is consistent at genus level. A revision of Eurysquilla into two or three new genera would resolve this one exception. There is some justification for splitting the genus Eurysquilla on the basis of eye design and of other characters. The proposed group, including E. crosnieri, E. pacifica, E. chacei, and E. holthuisi, possesses an unusual uropod with

182 JOURNAL OF CRUSTACEAN BIOLOGY, VOL. 20, NO. 1, 2000 a row of spinules along the inner margin. Except for E. maiguensis, this feature is absent in the second group of species. The Gonodactyloidea is especially heterogeneous with respect to eye design and on this evidence alone it could be construed as a polyphyletic group. The absence of a specialized retina in the midband of the Paraquillidae (Parasquilla, Faughnia, and Pseudosquillopsis) and some Eurysquillidae distinguishes them from other gonodactyloids. In this respect, they have a closer affinity with the Squilloidea. There is a strong argument for removing the Parasquillidae and Eurysquillidae from the Gonodactyloidea and placing them in their own respective superfamilies. At a lower taxonomic level, the position of Allosquilla as a member of the Nannosquillidae also needs to be reconsidered. The other 14 genera of nannosquillids have eyes of a very different type, with a rounded, flattened cornea and a six-row midband. The morphological features that define the Nannosquillidae, i.e., an ovate endopod on the walking legs and a proximal fold on the uropodal exopod, are weak characters and may merely reflect convergence. In terms of the form of its raptorial claw and telson, Allosquilla shares some affinities with the Heterosquillidae, especially Heterosquilloides, and might be transferred to this or to its own monotypic family. The existence of so much variation in eye design, even between closely related species, means that, in stomatopods, this feature is not a stable character on which to base a higher taxonomic structure. Further analysis of phylogenetic relationships within the Gonodactyloidea, taking other morphological characters into account, may help to determine whether there is any real justification in further fragmenting the higher taxonomy of stomatopods. Although stomatopod eye design is not useful in their classification to superfamily or family level, it is still an important character to consider in the definition of genera and species. Many stomatopods have highly distinctive eyes and may be distinguished by this feature alone. When describing a stomatopod, the following characters should be considered in the diagnosis: (Characters 1 3 are evident from an examination of an intact eye. Characters 4 6 may be determined by simple histological procedures. Other internal features of the eyes, such as diversity of visual pigments, are more difficult to utilize, since their measurement often requires complex techniques). (1) Cornea shape. At least five distinct cornea shapes can be defined: a, Globular or bean-shaped, e.g., Gonodactylus and Odontodactylus; b, Rounded and flattened, e.g., Eurysquilloides and Nannosquilla; c, Symmetrically bilobed, e.g., Squilla and Lysiosquilla; d, Asymmetrically bilobed, e.g., Parasquilla; and e, Extremely bilobed, e.g., Acoridon and Coronidopsis. (2) Number of rows in the midband. In known species, there are examples of two-, three- and six-row midbands or the midband may be absent. A caution regarding the measurement of midband size should be reiterated at this point; although the number of rows is usually apparent externally, this needs to be confirmed by sectioning before using it as a defining character. For example, Heterosquilloides appears to have four rows in the midband, but histological examination shows that there are in fact only two. With very small eyes, such as those of Coronida, the midband can only be seen clearly in section. (3) Shape of corneal facets. These are square in gonodactyloids with the exception of the Eurysquillidae and Parasquillidae. Members of these two families have hexagonal or rounded facets as in the Lysiosquilloidea and Squilloidea. (4) Presence of a distal pigment just below the level of the crystalline cones. Many squilloids and lysiosquilloids have a certain amount of distal pigment in the eyes (Marshall et al., 1991b). In live animals, the pigment is green or yellow and iridescent and may be involved in camouflage or in excluding light from the retina to produce a sharper field iris for each rhabdom. A pigment in this position is present in a number of species that typically live in the 50 150-m depth range. It is particularly noticeable in Allosquilla, Manningia, Coronidopsis, and Faughnia. The color of this pigment has not been observed in live animals, but in preserved specimens the eyes are dark brown or black. The function of this pigment in these species is speculative, since a pigment that excludes light from the retina at that depth does not seem advantageous.

HARLING: EYE DESIGN IN STOMATOPOD CRUSTACEANS 183 Fig. 5. The seven eye types in stomatopods as typified by: A, Type 1 Cornea globular, midband absent, e.g., Bathysquilla crassispinosa; B, Type 2 Cornea bilobed, midband absent, e.g., Erythrosquilla megalops; C, Type 3 Cornea bilobed, midband of two rows, e.g., Squilla empusa; D, Type 4 Cornea extremely bilobed, midband of two rows, e.g., Allosquilla africana; E, Type 5 Cornea asymmetrically bilobed, midband of three rows, e.g., Pseudosquillopsis lessonii; F, Type 6 Cornea globular, midband of six rows, e.g., Odontodactylus scyllarus; G, Type 7 Cornea bilobed, midband of six rows, e.g., Lysiosquilla maculata. (5) Tiering of the retina in rows 1 4 of the midband. In species with a six-row midband, the tiered retina of rows 1 4 is evident in transverse sections from the different configurations of retinular cells R1 7. (6) The number, color, and size of carotenoid filters in rows 2 and 3 of the midband. These are best described from fresh, frozen sections and have not been considered in detail here. Previous studies have shown that filter characteristics are correlated with depth and habitat. For example, in a shallow-water gonodactyloid such as Chorisquilla trigibbosa, there are two yellow filters in row two and a pink and a purple filter in row three (Marshall et al., 1991b). In species that inhabit a greater range of depths, e.g., Odontodactylus scyllarus, the filters are longer and red in row three. In lysiosquilloids, the proximal filter is frequently absent in one or both of the rows. Identifying Stomatopods by Their Eyes It is not possible to construct a key based on eye design that includes all stomatopods, although there are a number of species, or groups of species, for which eye type is an important distinguishing feature. Of the characters described above, characters 1 and 2 are the most useful for distinguishing among

184 JOURNAL OF CRUSTACEAN BIOLOGY, VOL. 20, NO. 1, 2000 stomatopod taxa. On the basis of these two characters only, seven distinct eye types may be described (Fig. 5) that give a general guide to recognizing some stomatopod groups: Type 1 Midband absent, cornea globular. Bathysquilloidea. Type 2 Midband absent, cornea bilobed. Erythrosquilloidea. Type 3 Midband consisting of two rows, cornea bilobed. Squilloidea, Parasquilla (Gonodactyloidea), Faughnia (Gonodactyloidea), and Heterosquilloides (Lysiosquilloidea). In squilloids, the two rows of ommatidia adjacent to the midband usually have very small facets, whereas in Parasquilla and Heterosquilloides they are of the same size as those in the midband. Externally, Heterosquilloides appears to have four rows in the midband. Parasquilla and Faughnia may be distinguished by the characteristic asymmetrical shape of the cornea. Type 4 Midband consisting of two rows, cornea extremely bilobed. Allosquilla (Lysiosquilloidea), Manningia (Gonodactyloidea), and Coronidopsis (Gonodactyloidea). (Also Paracoridon, Acoridon, and Parvisquilla (Lysiosquilloidea); Eurysquilla crosnieri, E. pacifica, E. chacei, and E. holthuisi (Gonodactyloidea) subject to confirmation). Manningia and Coronidopsis are easily distinguished by the dense layer of distal pigment in the eye which gives a black appearance. Type 5 Midband consisting of three rows, cornea asymmetrically bilobed. Pseudosquillopsis (Gonodactyloidea). Type 6 Midband consisting of six rows, cornea globular or slightly bilobed, midband facets square and rows two and four of equal size to rows one and three. Gonodactylidae, Protosquillidae, Odontodactylidae, Pseudosquillidae, Takuidae, Alainosquillidae, and Hemisquillidae (Gonodactyloidea). These groups may be further separated on the basis of variations in the shape of the cornea and also by the structure of the retina. For example, the cornea in the Odontodactylidae is almost spherical, whereas in other families the eyes tend to be tall and bean-shaped or cylindrical (Manning et al., 1984a). Hemisquilla lacks the proximal filter classes in rows two and three of the midband, while Echinosquilla (Protosquillidae) lacks the proximal row three class (Cronin et al., 1994a). Type 7 Midband consisting of six rows, cornea bilobed or rounded and flattened, midband facets hexagonal or rounded. The facets of rows 2 and 4 are smaller than those of rows 1 and 3. Eurysquilla veleronis, E. delsolari, E. leloueffi, E. galathae, E. pumae, E. sewelli, E. foresti, E. plumata, E. maiguensis, Sinosquilla, and Eurysquilloides (Gonodactyloidea). Also included are lysiosquilloids, except those mentioned above. ACKNOWLEDGEMENTS I thank Prof. Michael Land for helpful criticism and Julia Horwood for assistance with histology. This work was supported by grants from the B.B.S.R.C. and the Natural History Museum, London. LITERATURE CITED Abbot, B. C., R. B. Manning, and H. Schiff. 1984. An attempt to correlate pseudopupil sizes in stomatopod crustaceans with ambient light conditions and behavior patterns. Comparative Biochemistry and Physiology A 78: 419 426. Cronin, T. W., N. J. Marshall, and R. L. Caldwell. 1993. Photoreceptor spectral diversity in the retinas of squilloid and lysiosquilloid stomatopod crustaceans. Journal of Comparative Physiology A 172: 339 350.,, and. 1994a. The intrarhabdomal filters in the retinas of mantis shrimps. Vision Research 34: 279 291.,, and. 1996. Visual pigment diversity in two genera of mantis shrimps implies rapid evolution (Crustacea: Stomatopoda). Journal of Comparative Physiology A 179: 371 384.,,, and N. Shashar. 1994b. Specialisation of retinal function in the compound eyes of mantis shrimps. Vision Research 34: 2639 2656. Fincham, A. A. 1980. Eyes and classification of malacostracan crustaceans. Nature 287: 729 731. Manning, R. B. 1968. A revision of the family Squillidae (Crustacea, Stomatopoda), with descriptions of eight new genera. Bulletin of Marine Science 18: 105 142., and D. K. Camp. 1993. Erythrosquilloidea, a new superfamily, and Tetrasquillidae, a new family of stomatopod crustaceans. Proceedings of the Biological Society of Washington 106: 85 91., H. Schiff, and B. C. Abbot. 1984a. Cornea shape and surface structure in some stomatopod Crustacea. Journal of Crustacean Biology 4: 502 513.,, and. 1984b. Eye structure and the classification of stomatopod Crustacea. Zoologica Scripta 13: 41 44. Marshall, N. J. 1988. A unique colour and polarisation vision system in mantis shrimps. Nature 133: 557 560., and M. F. Land. 1993a. Some optical features of the eyes of stomatopods: 1. Eye shape, optical axes and resolution. Journal of Comparative Physiology A 173: 65 582., and. 1993b. Some optical features of the eyes of stomatopods: 2. Ommatidial design, sensitivity, and habitat. Journal of Comparative Physiology A 173: 583 594., J. P. Jones, and T. W. Cronin. 1996. Behavioural evidence for colour vision in stomatopod crus-

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