Optics, Range-finding, and Neuroanatomy of the Eye of a Mantis , mantis (Linnaeus) (Crustacea: Stomatopoda: )

HELGA SCHIFF, BERNARD C. ABBOTT, and RAYMOND B. MANNING

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Robert McC. Adams Secretary Smithsonian Institution SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY • NUMBER 440

Optics, Range-finding, and Neuroanatomy of the Eye of a , Squilla mantis (Linnaeus) (Crustacea: Stomatopoda: Squillidae)

Helga Schiff, Bernard C. Abbott, and Raymond B. Manning

SMITHSONIAN INSTITUTION PRESS City of Washington 1986 ABSTRACT Schiff, Helga, Bernard C. Abbott, and Raymond B. Manning. Optics, Range-finding, and Neuroanatomy of the Eye of a Mantis Shrimp, Squilla mantis (Linnaeus) (Crustacea: Stomatopoda: Squillidae). Smithsonian Contri- butions to Zoology, number 440, 32 pages, 19 figures, 1 table, 1986.—Optical and histological studies have been carried out on the eye of the Mediterranean mantis shrimp Squilla mantis (Linnaeus), with emphasis on correlation of observations based on the different methodologies. The ommatidia have acceptance angles of 2.4°, comparable to those of other compound eyes, but the wide apertures, 20°, of the cornea-cone units apparently are an adaptation to the dimly lit natural habitat of the . Skewing of optical axes in the ommatidia of the double cornea suggests that each eye is capable of distance perception. Three systems of tangential nerve fibers in the lamina connect sets of cartridges in specific arrays. Giant fiber trees extend throughout the medulla externa. The medulla interna also contains large, extensively branched, integrating fibers. All ganglia, at least up to the medulla interna, are structurally divided into an upper and a lower half and contain large integrating fibers connecting the two halves. Optical findings are correlated with histological findings.

OFFICIAL PUBLICATION DATE is handstamped in a limited number of initial copies and is recorded in the Institution's annual report, Smithsonian Year. SERIES COVER DESIGN: The coral Montastrea cavernosa (Linnaeus).

Library of Congress Cataloging in Publication Data Schiff, Helga. Optics, range-finding, and neuroanatomy of the eye of a mantis shrimp, Squilla mantis (Linnaeus) (Crustacea, Stomatopoda, Squillidae). (Smithsonian contributions to zoology ; no. 440) Bibliography: p. Supt. of Docs, no.: SI 1.27:440 I. Squilla mantis—Physiology. 2. Squilla mantis—Anatomy. 3. Eye. 4. Vision. 5. Crus- tacea— Physiology. 6. Crustacea—Anatomy. I. Abbott, Bernard C. II. Manning, Ray- mond B. III. Title. IV. Series. QL1.S54 no. 440a 591s [595.3'843] 86-600006 [QL444.M375] Contents

Page Introduction 1 Acknowledgments 4 Techniques 4 Abbreviations 6 Results 6 General Description of the Cornea 6 Shape of Cone and Rhabdom 8 Optical Axes 10 Acceptance Angles and Light Transmission 11 The Lamina 14 General Organization 14 Retina-Lamina Projection 14 Receptor Terminals in the Cartridges 16 Tangential Connections 18 Blood Supply of the Lamina 20 The Medulla Externa 20 The Medulla Interna 23 Higher Order Ganglia 23 Summary 23 Discussion 25 Literature Cited 29

111

Optics, Range-finding, and Neuroanatomy of the Eye of a Mantis Shrimp, Squilla mantis (Linnaeus) (Crustacea: Stomatopoda: Squillidae)

Helga Schiff, Bernard C. Abbott, and Raymond B. Manning

Introduction should be capable of stereoscopic vision in the The vision scientist G.A. Horridge prefaced horizontal plane. In the same year, Parker (1891) his account of the eye of Odontodactylus scyllarus surveyed eyes and included an ac- (Linnaeus, 1758) by calling it "the most amazing count of the eye of Gonodactylus bredini Dingle, compound eye" (Horridge, 1977a: 15). He com- 1969 (as G. chiragra (Fabricius, 1781)), showing mented that both Odontodactylus and its relative that the cornea was divided into two halves by a Gonodactylus "have remarkable eyes." Land longitudinal band of specialized cells. Ciaccio (1984:427) noted that stomatopod eyes are "the (1894) studied the anatomy of the eye of a most specialised and intriguing apposition eyes Squilla. The physiology of the eye of Squilla in the Crustacea," and commented that a striking mantis was investigated by Demoll (1909), and in feature of stomatopod eyes was their size. We the same year Lo Bianco (1909) carried out an arejust beginning to understand how remarkable ecological study of Squilla mantis. Giesbrecht the eyes of stomatopods really are. (1910) provided a detailed account of the anat- Until recently, the eyes of stomatopods and omy and development and, to a more limited vision in these have received very little extent, observations on the behavior of several attention from biologists. In the late 1800's, Ex- Mediterranean stomatopods, primarily Squilla ner (1891) studied the eyes of Squilla mantis mantis. During the following half century sto- (Linnaeus, 1758) and concluded that each eye matopod vision was studied only occasionally, e.g., the investigations of Hanstrom (1931, Helga Schiff Dipartimento di Informatica, Universita degli Studi 1934). These early investigations on stomatopod di Torino, Via Valperga Caluso 37, 10125 Torino, Italy; Ber- nard C. Abbott, Department of Biological Sciences, University of eyes and vision were ably summarized by Balss Southern California, Los Angeles, California 90007; Raymond (1938) in his review of the group. B. Manning, Department of Invertebrate Zoology, National Mu- seum of Natural History, Smithsonian Institution, Washington, In the past few years a great deal of research DC 20560. has been conducted on the optics and neuro- 1 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY physiology of compound eyes, especially on those daylight hours. This is at odds with current of insects. The analyses and models of optomotor knowledge of the behavior of Gonodactylus, all responses in the eye of the fly and other insects other species of which studied so far have been have yielded much information on integrative observed to be active diurnally (R.B.M., personal neural control (Barros-Pita and Maldonado, observations; M.L. Reaka, personal communica- 1970; Poggio and Reichardt, 1973; Mimura, tion). 1975; Northrop, 1975; Dvorak, Bishop, and Eck- Milne and Milne (1961) reported on scanning ert, 1975; Laughlin, 1975, 1976; Horridge and movements in the eyes of stomatopods, and Duelli, 1979). Studies on crustacean eyes have noted (p. 425) that species of Gonodactylus and included histological investigations (Waterman, Pseudosquilla appeared to use their eyes "inde- 1975; Nassel, 1975, 1976; Stowe, 1977; Hor- pendently more often than together . . . ." They ridge, 1978). Electrophysiological studies by concluded that a monocular stereoscopic effect Wiersma, Hou, and Martini (1977) revealed the in the eyes of members of these genera was more receptive fields and movement fibers in the optic significant than in the eyes of Squilla. nerve of several . Trevifio and Larimer (1969), by recording Our knowledge of the optics of the ommati- electroretinograms in the American species dium of the compound eye (Horridge, Mimura, Squilla empusa Say, 1818, found a maximum of and Hardie, 1976; Horridge, 1977a,b, 1978; responses at about 520 um. Schiff (1963), with Horridge and Duelli, 1979) and the theoretical single fiber recording in second order fibers in treatment of this (Snyder, 1975, 1979) has been the eye of Squilla mantis, found a slightly shifted based mainly on insect eyes. Literature reviews green maximum around 535 um and another are given in The Compound Eye and Vision of maximum of response for ultraviolet light. Using Insects, edited by Horridge (1975), Photoreceptor techniques of microspectrophotometry and fluo- Optics, edited by Snyder and Menzel (1975), rometry on isolated rhabdoms, T.W. Cronin Handbook of Sensory Physiology, edited by Autrum (1985) concluded that vision in Squilla empusa (1979, 1981a,b), and in a review in the Biology of was monochromatic. The shift towards the green Crustacea by Shaw and Stowe (1982). Land, Bur- in electrophysiological whole-eye experiments ton, and Meyer-Rochow (1979) and Land (1981) probably can be explained by the green light have studied the eyes of euphausiids and amphi- reflected by the green crystalline pigment on the pods from different habitats. retinal surface. Recently there has been a marked increase in The investigation by Schiff (1963) preceded a research on the eyes and vision of stomatopods, variety of studies on the eyes and optical systems most based on the common Mediterranean spe- of Squilla mantis: electron microscopy of the ret- cies Squilla mantis. Schaller (1953) studied optical ina (Schiff and Gervasio, 1969); observations on responses of S. mantis to different levels of illu- the visual code (Schiff and Schonenberger, mination and demonstrated that responses were 1971); scattering of light in the rhabdom (Schiff, inhibited at higher light intensities. He suggested 1974); analysis of electrophysiological responses that prey capture was dependent upon a combi- (Schiff, 1976); and monocular range finding nation of stimuli—chemical, tactile, and optical. (Schiff and Abbott, 1981; Schiff, Abbott, and In 1954, Bolwig reported on studies of a species Manning, 1985). During the same time period, oi Gonodactylus from the Indian Ocean. He con- other investigations were adding to our knowl- cluded that the animals responded negatively to edge of the eyes of Squilla mantis. Schonenberger daytime levels of illumination, and that this, in (1977) reported on the fine structure of the combination with a positive response to contact retina and Vivroux and Schonenberger (1981) with objects on the bottom, kept these animals studied light and dark adaptations of the eye. "trapped" under objects and in burrows through The eyes of other species also have been stud- NUMBER 440

ied in recent investigations. Horridge (1977a,b, is not restricted to the systematics of stomato- 1978) provided observations on the eyes of a pods. Fincham (1980) pointed out that optical Gonodactylus and Odontodactylus scyllarus and de- mechanisms largely had been ignored in the clas- picted their distinctive middle bands and pseu- sification of many malacostracan groups, but that dopupils. He pointed out that in these species in mysids, euphausiids, and decapods both ap- each eye included a range finder and noted position and superposition optics had developed; (1978:47): "The functions of the three parts of apposition optics were the most common in the the eye are not yet understood . . . ." Shaw and . Nilsson (1983) suggested that Stowe (1982, fig. 4), in their review of vision in there were evolutionary links between apposition crustaceans, figured the pseudopupils of O. scyl- and superposition optics in the Crustacea. larus and the optical axes in 5. mantis. Elsewhere (Manning, Schiff, and Abbott, Investigations also have been carried out on 1984a,b) we have pointed out that in stomato- the eyes of a common Japanese squillid, Orato- pods, eye structure appears to be distinctive in squilla oratoria (de Haan, 1844). Yanase, Okuno, each of the four recognized superfamilies (Man- and Fujimoto (1972) reported that in this species ning, 1980). In most stomatopods, the cornea is the cornea is divided into two parts, dorsal and divided into two parts by a band of specialized ventral, separated by a band of larger facets, two ommatidia, the middle band. This band is absent cells wide. Ochi and Yamaguchi (1976) examined in members of a relict, deep-sea superfamily, the various fibers in the optic nerve of O. oratoria. Bathysquilloidea. In Squilloidea the middle band Many investigators have reported that in sto- is composed of two rows of rectangular ommati- matopods the cornea is divided into two parts, dia. In the Gonodactyloidea, the middle band is separated by a band of distinctive cells. We refer six facets wide, and these facets are rectangular to this dividing band as the middle band (Man- and are the largest facets found on the cornea. ning, Schiff, and Abbott, 1984b). As early as The middle band in Lysiosquilloidea also is six 1891, Parker pointed out that the middle band facets wide; in members of this group, the facets in Gonodactylus was six cells wide; Balss (1938) of the middle band are not markedly larger than repeated these observations in his summary of those on the adjacent surface of the cornea, and the eyes of stomatopods. This configuration also they are hexagonal to spherical rather than rec- was observed in Odontodactylus by Horridge tangular. (1977a,b, 1978), Schiff and Abbott (1981), and It is remarkable that four distinct types of eyes figured in Shaw and Stowe (1982) and Land have developed in such a relatively small group (1984). That the middle band in Squilla mantis is of organisms. As we have already pointed out comprised of a band only two cells wide has been (Manning, Schiff, and Abbott, 1984b), each of recorded by many investigators, including De- these kinds of eyes must have differentiated at a moll (1909), Hanstrom (1934), Schaller (1953), very early stage in the evolutionary history of the Schiff (1963), Schiff and Gervasio (1969), Schiff stomatopods. Further, three of these superfami- and Sch6nenberger (1971), Schiff (1976), and lies contain species that live in bright as well as Schonenberger (1977). This condition was re- dim habitats, and in spite of this the distinct corded in another squillid, Oratosquilla oratoria, structure of the eye has been maintained. by Yanase, Okumo, and Fujimoto (1972). Other lines of research also have added to our Only recently has shape and structure of the understanding of the importance of eyes of sto- cornea been related to the higher classification matopods. Stomatopods are visual predators of stomatopods, although eye shape has been (Caldwell and Dingle, 1975), all of which live in known to be important at the specific and generic burrows (Reaka, 1980; Reaka and Manning, levels (see Serene (1962) for examples of diver- 1981). Gonodactyloids in particular are brightly sity of eye shape in stomatopods). This oversight colored, especially members of Gonodactylus. SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

Members of that genus have a colored spot on in each eye around the eye division, which prob- the inner, distal surface of the merus of the ably could provide them with the necessary in- raptorial claw (Hazlett, 1979); the color of the formation on distance and movement to allow spot is species-specific. Further, these animals are them to catch their prey. extremely aggressive, and, in intra- and interspe- The eyes of Squilla have long first, second, cific encounters, the meral spots are displayed. and third order nerve fibers, which simplify po- According to Dingle (1969), large amounts of sitioning an electrode at a desired level. The information are transmitted by visual signals. retinular cells are large and there are several Thus, it appears that eye structure may be types of large or giant fibers in each ganglion. important in the development of color, color We are particularly interested in the range-find- recognition, and behavior patterns of stomato- ing device and the possible transmission pathways pods, and that all of these, including eye struc- involved with the strike, and hypothesize that the ture, can be related to the classification of these giant integrating fibers are involved in transmis- organisms. sion of information relating to the strike. Our investigations so far have been limited to ACKNOWLEDGMENTS.—Much of this work was a few representatives of each superfamily (see list carried out with the support of Consiglio Nazion- in Manning, Schiff, and Abbott, 1984a). We ale di Ricerche (CNR)/National Science Foun- hope that the eyes of as many species as possible dation (NSF) grants 77.01544.63, 78.02741.63, will be studied. In addition to our work on eye and 80.02404.02, and NATO grant 1363 to H. structure, cited above, we have completed ac- Schiff. The Smithsonian Institution, through its counts of pseudopupils (Abbott, Manning, and Office of Fellowships and Grants, supported a Schiff, 1984), range-finding (Schiff, Abbott, and visit to Washington, D.C., by H. Schiff in 1983 Manning, 1985), and ommatidia (Schiff, Man- to further this study. Part of the writing and ning, and Abbott, in prep.). The unique eye of editing was done at the Smithsonian Marine Sta- Crenatosquilla oculinova (Glassell, 1942) also has tion at Fort Pierce; this paper is contribution been described (Schiff and Manning, 1984). number 147 from the Smithsonian Marine Sta- Here we describe some structural aspects of tion. Some of this work was carried out at the the eye of Squilla mantis from the Mediterra- Naples Zoological Station; support of the staff nean, based on observations largely made by one there, including the furnishing of specimens, is of us (H.S.). This species lives in burrows on level gratefully acknowledged. V. Braitenberg pro- bottoms at depths to 100 meters or more (Man- vided us with Figure 1. Mr. L. Burzio, Universita ning, 1977; Lewinsohn and Manning, 1980), in degli Studi di Torino, gave us excellent technical a generally dimly lit environment. photographic assistance, and the Istituto di An- As we show below, the eye of Squilla mantis tropologia of that institution supplied technical differs from typical compound eyes in several assistance and working space. respects. The cylindrical cornea is double, di- We are grateful to Page Hiller-Adams, Uni- vided into two halves by rows of specialized om- versity of California, Santa Barbara, Thomas W. matidia, the middle band. The cornea has small Cronin, University of Maryland, Baltimore acceptance angles and fields, but wide openings County, Horton H. Hobbs, Jr., Smithsonian In- of facets and cones, probably an adaptation to stitution, and to an anonymous reviewer, for relatively low levels of light in its habitat. The their critical reviews of the manuscript. cone slims to a diameter of 10 /im at its proximal and distal ends but, together with the corneagen- ous cells, transmits an image corrected for spher- Techniques ical aberration introduced by the corneal facets. Specimens of Squilla mantis were obtained One of the most interesting aspects of stomato- through the Naples Zoological Station. The eyes pod eyes is that they have collars of range-finders were excised rapidly from freshly killed animals NUMBER 440 and fixed as whole eyes, cut in half or into In general, any method in which preparations quarters, or pierced. Techniques used for this are stained before sectioning does not give satis- research included the following: (a) observations factory results, and this is true for all methods of live preparations stained with methylene blue, used on stomatopod eyes by us. On the contrary, (b) sections treated with standard stains such as in vitro methylene blue staining and Bodian or hematoxylin, Azan, Bodian, Golgi-Colonnier, any other staining of sectioned material give and other Golgi variations, (c) various modifica- good results (see Schiff, 1976; Strausfeld and tions of unstained sections using fluorescence Nassel, 1981). For Bodian staining, preparations techniques, and (d) semithin sections unstained were fixed in Carnoy and stained with a 2% or stained with Toluidine blue for phase contrast silver-albumose solution to which 1.5% copper- observations. Some preparations were observed mesh was added, then reduced with hydroqui- with an electron microscope. Most of these tech- none, and stained again in a 1% gold chloride niques are standard procedures described in any solution. Other than prolonging the time periods text book on histology. for fixation, staining, and washing, to about Strausfeld (1976) described the Golgi staining twice, and often more than twice, the normal method and its variations as well as Bodian stain- duration used for insects, the method followed ing for insect nervous systems, and provided was a standard Bodian staining (Strausfeld, references to the original literature on these 1976). techniques. Our variations of the Golgi methods Methylene blue in sea water stains very well if primarily were concerned with prefixation and the overlying tissue is gradually removed under the lengths of time the tissues were kept in dif- the stereomicroscope as staining of fibers pro- ferent solutions. Prefixations for the Golgi-Co- ceeds. This method is especially useful for follow- lonnier method included gradual substitution of ing long stretches of fibers through a live eye. sea water by buffered water followed by buffered Because of the unusual difficulties encoun- glutaraldelhyde, buffered water and sucrose, glu- tered in staining stomatopod eyes, the results taraldehyde-sea water, buffered glutaraldehyde, described below represent the distillation of re- and injection of Karnovski solution and 2% po- sults obtained by using many different techniques tassium dichromate. After the prefixation, the on several hundred eyes and sections. For ex- preparations were transferred to normal Golgi- ample, retinular cell axons have been followed Colonnier solutions. In general the usual proce- through to the lamina in several cases in live, dures were then followed, except that all impreg- methylene blue stained eyes and in some Golgi nation times had to be prolonged, requiring sections. The details of the subretinal pattern of more extensive washing. Some eyes were fixed fibers and the distribution of a fiber bundle at and stained by the Golgi-Kopsch method. None the lamina surface into the cartridge were ob- of the Golgi methods gave particularly satisfac- served mainly in Bodian- and Toluidine-stained tory results with Squilla eyes. sections. The crossing of the monopolar fibers Although the eyes of Squilla, being large and has been seen in in vitro methylene blue stained having large ommatidia as well as widely sepa- eyes as well as in many of the semithin sections. rated ganglia, are well suited for this type of Optical axes were measured using pseudopupil research, they also present at least one disadvan- observations; anatomical axes were measured tage. When using Golgi methods, nerve termi- from sectioned live eyes as well as from histolog- nals, axon bunches, and collaterals grouped in ical sections. Techniques for using pseudopupil certain regions stain well, but a completely observations as indicators of the optical axes of stained neuron is rare. This is unlike the tradi- ommatidia are described extensively by Horridge tional response of neurons to the Golgi method (1978) and Stavenga (1979). In photographs of and is probably due to the abundance of connec- cut living eyes and of histological sections, axes tive tissue around the nerves and ganglia. were drawn between the middle of the corneal 6 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY facets (with respect to the distal cone extension) re retinular cell and the proximal tip of the ommatidium. Angles re retina were measured between these anatomical axes rf receptive field and the basement membrane and compared with sv synaptic vesicle the pseudopupil location and the direction of the t tangential fibers optical axes of ommatidia belonging to the pseu- T fibers from the three tangential systems dopupil. Pseudopupils define the optical axes. (T1,T2,T3) Anatomical axes were determined from eyes sec- ta tangential plane and direction tioned in half from living whole-mount prepara- te terminals of second order fibers in me- tions. The same preparations after fixation and dulla externa subsequently prepared sections of whole-mounts V ventral showed no changes in skewing angles. No signif- ve vertical plane and direction icant differences were observed between optical x, y, z horizontal and vertical directions and anatomical axes of the ommatidia, the dif- xy sagittal plane ferences being less than the measuring errors. XZ horizontal plane Studies of the axes excluded the tips of the eye. yz frontal plane Corneal surfaces need not be marked in stoma- 1° first order fibers, axons from retinular topod eyes. Because of the unique shape of the cells double corneas, the positions of the pseudopu- 2° second order fibers, mainly axons from pils, with respect to their constituent ommatidia, lamina monopolars are always well defined. 3° third order fibers, between medulla ex- ABBREVIATIONS.—The following abbrevia- terna and medulla interna tions are used in the figures: Results am amacrine cells b bundles of nerve fibers GENERAL DESCRIPTION OF THE CORNEA bl blood vessels FIGURES 1, 2 c crystalline cone ca cartridges in lamina The cornea in Squilla mantis is bilobed and cap blood capillaries cylindrical (see Manning, Schiff, and Abbott, cc corneagenous cells 1984b, for more information on cornea shape CO cornea and structure in stomatopods), five to eight mil- col collaterals of the monopolar axons limeters long and two to three millimeters in d dorsal diameter, depending upon the size of the . f front The eye is of the apposition type, with about g ground 4000 ommatidia arranged in 70-80 rows, as ho horizontal direction and plane shown in Figure 1. The hexagonal corneal len- 1 left slets are arranged in rows in three directions: la lamina one row, the xz plane, is horizontal, and the rn monopolar other two rows are situated at angles of about me medulla externa 60° to the horizontal rows. The orientation of mi medulla interna (lobula) planes within the eye is shown in Figure 2a. The nv neurosecretary vesicles planes defined by arrows are horizontal (xz), o ommatidia sagittal (xy), and frontal. During optical atten- on optic nerve tion, the living animal holds the eyes with their r right long axes tilted backwards and with their upper ra rhabdom edges or sides approaching each other (Figure NUMBER 440

2b); much of the cornea is directed at a space in a row of ommatidia, consisting of the most front of and slightly above the animal. skewed ones on the surface of the eye, which The cornea is divided into an upper, dorsal have small, pentagonal corneal facets. half and a lower, ventral half by a groove (see The pseudopupils, ommatidia that look Figure 1), the middle band, which is made up of straight into the eye of the observer, comprise two rows of ommatidia. The ommatidia of the two, broad, elongate, elliptical areas, as shown in middle band are the largest ommatidia of the black in the lower part of Figure 2, together with eye. These large ommatidia are parallel to one a horizontal bar formed by the two rows of the another and are separated from the neighboring middle band; the position of the pseudopupils horizontal rows of ommatidia by wedge-shaped changes with viewing angle. The ommatidia at sinuses, delimited by the ommatidia of the mid- the sides of the eyes have very small or non- dle band, the basement membrane, and the first existent crystalline cones that form two symmet- row of skewed ommatidia parallel to the middle rical false pseudopupils at the upper side of the band. The diameter of the corneal facets of ommatidia in the middle band is 130 fim, whereas the diameter of the corneal facets of the adjacent horizontal row is 100 fim, with cone diameters of 72 /zm. Ommatidial diameters decrease from the middle towards the sides of the eye. Flanking the two rows of ommatidia in the middle band is

FIGURE 2.—Upper: definition of planes for the eye of Squilla (xy = sagittal, xz = horizontal, yz = frontal: la = lamina, re = retina). Lower: position of eyes during optical attention relative to each other (left) and to the ground (g; right); FIGURE 1.—The eye of a mantis shrimp, Squilla mantis; two pseudopupils are marked in black. The pair of circles in the dimensions, x and y, are defined (photograph courtesy of V. lower center show dorsal and ventral false pseudopupils (d Braitenberg). = dorsal, f = front, I = left, r = right, v = ventral). 8 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

cornea and another smaller false pseudopupil on in Figure 3a. The cone resembles a vase with a the bottom side of the cornea. Unlike true pseu- narrow neck extended to touch the corneal len- dopupils, the false pseudopupils do not change slet, with two transparent cells forming a wedge- position on the eye as the direction of observation shaped collar surrounding the neck. changes, because they reflect the absence of At the distal tip the cone slims to a 10 fim cones in those areas. strand, which is attached to the middle of the corneal facet. Around this strand the corneagen- SHAPE OF CONE AND RHABDOM ous cells form a transparent, wedge-shaped col- FIGURES 3, 4 lar. At the proximal tip the cone tapers to its The average dimensions of the optical equip- smallest diameter (7-8 /im) and then widens (to ment of a light-adapted ommatidium are shown about 15 /tm) to form a small, concave cup that

FIGURE 3.—The ommatidium: a, the average dimension in micrometers of the cornea-cone aperture and the rhabdom acceptance angle. Two values are given for the lengths of the cone (co) and rhabdom (ra), the first representing the dark-adapted state, the second the light- adapted state, b, cones and cornea in a Golgi-stained thick section showing the distal restriction of the cones (co) and the corneagenous cells (cc) surrounding the slim part of the crystalline cone (c). Notice also the thick corneal facets. Inset shows, in cross-section, the subdivision of the cones into four parts, c, ommatidia in a Bodian-stained section, d, corneal facets of the middle band in surface view. Cone extensions and corneagenous cells are shown in focus on the right. Inset: tangential section through middle facets and adjacent pentagonal facets, e, distal part of the cone./, proximal part of the cone. The layers of small niicrovilli (arrows) are darker than the remaining rhabdom (re = retinular cell). NUMBER 440

FIGURE 4.—The proximal cone and distal rhabdom tip (arrows indicate microvilli): a, diagram to show the shape of the cone tip and the transition between the cone (c) and the niicrovilli of the rhabdom (ra); b, oblique section through an ommatidium at the cone-rhabdom junction, as seen with the electron microscope (re = retinular cell); c, diagram showing several distinctive features of the eye of Squilla: the pattern of distribution of small microvilli; the radial arrangement of microvilli in the distal rhabdom; the gradual bulging out to a square rhabdom; and the gradual formation of layers of perpendicular microvilli. 10 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY fits onto the convex distal part of the rhabdom TABLE 1.—The angles (in degrees) between the optical (Figures 3a,b,c, 4a). The rhabdoms are 15 ^m axes of the skewed ommatidia and the basement membrane. across, square, with about 150 alternating per- pendicular bands of microvilli (diameter 1000 A) belonging to the seven retinular cells. Each band Ommatidium Dorsal part Ventral part number of eye of eye has an average thickness of two micrometers. 1 74±1.0 66±2.6 Corneal facets have a small central depression 2 77±0.4 7l±1.0 on their surface (arrows on left side in Figure 3d) 3 81 ±0.8 75±0.9 indicating the area of the distal attachment of 4 84±1.4 79±2.2 the cone. The distal 10 /xm of the cone passes 5 86±1.5 83±1.9 between the wedge of corneagenous cells and is 6 86+1.6 86±1.1 attached to the middle of the corneal facet. 7 89±1.8 87±1.2 8 92±2.0 87±1.3 Immediately below the crystalline cone is a 9 94 87±1.7 thin layer of small microvilli, about two-thirds of 10 95 89 the diameter of the other microvilli. These and 11 95 91 the first few micrometers of the dominant micro- 12 97 - villi are radially arranged into a star-shaped rhab- dom. At this level only four retinular cells send The optical axes of all horizontal neighbors of microvilli into the rhabdom; at a deeper level, ommatidia are divergent, but in the sagittal (xy) the rhabdom assumes its square shape, and three plane the optical axes show a peculiar pattern of other cells also have extensions into it. Gradually, skewing: the ommatidia of the two middle rows as the rhabdom takes its square shape, the layers have optical axes perpendicular to the basement of perpendicular microvilli form (Figures 3, 4) membrance and cornea; those of the ommatidia by penetration of the microvilli, between their of the next eight to 12 rows on each side are perpendicular neighbors, towards the retinular skewed towards the middle of the eye, as shown cells on the opposite side of the ommatidium. in Figure 5, and so the optical axes of these Preliminary results with the electron microscope ommatidia cross each other and those of the seem to indicate the existence of an eighth cell middle rows at different distances from the eye. distal to the other retinular cells, similar to the The ventral ommatidia thus look upward and eighth cell in several other crustaceans (Meyer- the dorsal ones look downward. The skewing Rochow, 1975; Waterman and Pooley, 1980), diminishes from the middle to the sides, where but we find only seven nerve fibers passing the ommatidia are again perpendicular to the cor- basement membrane. Intracellular recordings in neal surface. The angles between the optical axes the retinular cells with glass micropipettes of the skewed ommatidia and the basement mem- showed typical crustacean generator potentials in response to whole field illumination (H.S., branes are shown in Table 1 and in Figure 5. At unpublished data). The first, dynamic, phase is the sides of the eye all optical axes are divergent comparatively small. vertically as well as horizontally. When potential prey passes the visual field of OPTICAL AXES the eye, the number of ommatidia seeing it in- creases up to the middle in front of the eye. In FIGURES 5, 6 the middle, the visual fields of many ommatidia In the present studies, optical axes of omma- overlap strongly. Whereas one half of the eye is tidia are equated to anatomically derived longi- stimulated by a moving object in sequences of tudinal axes because we found no evidence of ommatidia from the middle towards the sides, significant deviations between histologically de- the other half is stimulated in a mirror sequence, rived axes and those derived from pseudopupils. from the sides towards the middle. NUMBER 440 11

b 12

FIGURE 5.—Stereovision, distribution of optical axes from ommatidia in a sagittal section: a, three ommatidia and a piece of the lamina are figured to show the dimensions with respect to (1) the crossing points (solid circles) of the optical axes of each corresponding pair of ommatidia and (2) the optical axes of the middle ommatidia (open circles). The two thicker lines are the optical axes of the two rows of large ommatidia in the middle band. 1, 2, 3 ... 12 are the optical axes of the first 12 horizontal rows of ommatidia in the dorsal part of the eye, counting from the middle band; 1', 2'. . . 11' are the optical axes of ommatidia in the ventral part of the eye. The angle d between 1 and 1', the field of stereoscopic vision, is 40°. b, optical axes on a different scale. The three thicker lines indicate not only the optical axes of the two middle rows of ommatidia but also the limits of the 15-20 rows of ommatidia with optical axes perpendicular to the corneal surface between the skewed ommatidia and the ommatidia of the sides of the eye. The horizontal lines on the top of the drawing show the extensions of the visual fields in a vertical plane for each half of the eye, neglecting the ommatidia of the sides.

ACCEPTANCE ANGLES AND LIGHT TRANSMISSION angle reflects only the amount of oblique rays, derived from the small visual field, that will be We calculated two angles from our observa- funneled into the rhabdom. Any light within the tions, the cornea-cone aperture and rhabdom solid angle of the aperture is funneled into the acceptance angle. The cornea-cone aperture is ommatidium and focused at the level of the distal the angle extended beyond the eye by the cornea- rhabdom tip, but only that part of the transmit- cone assembly, and it is calculated from the di- ted image that falls on the rhabdom surface can mensions of the corneal facet and the cone. This enter the rhabdom and be absorbed. The geo- 12 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY metrically calculated cornea-cone aperture is, on about 20°. This agrees with the value calculated average, 20°, confirming our experimental re- from the dimensions observed in sections and sults. means that the complex assemblage of cells sur- The acceptance angle determines the size of rounding the narrow distal neck of the cone the visual field of the ommatidium and can be combine to give an undistorted image. However, calculated, in approximation, from the following the rhabdom tip (15 jum) is much smaller than formula (Horridge and Duelli, 1979): the image of the large square, so the acceptance (A0')2 = (X/D)2+(d/f)2, angle of the ommatidium is much less than the aperture of 20°. Horridge and Duelli (1979) where have shown that the acceptance angle of an om- X = wavelength of light matidium in a compound eye depends upon two D = facet diameter characteristics, one derived from limitations set d = diameter of the distal rhabdom tip by the Airy diffraction disc, the other an anatom- f = distance of distal rhabdom tip from pos- ical limit set by the rhabdom diameter and by terior nodal point the position of the posterior node of the refrac- d/f = the angular subtense of the rhabdom tip tion system. In Squilla, with a facet diameter (D) extended through the posterior nodal of 100 nm, the component of diffraction (X/D) is point into the outside world negligible. Thus the theoretical acceptance angle X/D = the diffraction component must be the anatomical angle of d/f radians, where d, the diameter of the rhabdom tip, is 15 As defined by Snyder (1977), the acceptance nm, and f is the distance of the nodal point from angle defines the theoretical angular width of the that tip. Light entering an ommatidium can be angular sensitivity curve at its 50% sensitivity described as if it were passing through a single contour. refracting surface and forming its image at the The fields for the cornea and cones also were tip of the rhabdom. studied using surface slices of the eye cut to Let the refractive index of the medium be n contain both of these structures. Viewed through 0 and that of the cornea and cone be n . The a stereoscopic microscope, the images of an illu- 3 posterior nodal point is that point in the image minated object formed by such a slice were nearly space through which light rays can pass through identical for practically all of the ommatidia in the system without refraction. Let the posterior the slice, and shifted only slightly between more nodal point be at a distance r from the corneal distant ommatidia (Figure 6). For an object three surface. Then by simple laws of refraction, centimeters from the eye surface, the field viewed through each cornea-cone unit covers (n3/v)-(n0/u) = (n3-n0)/r, slightly more than one square centimeter, yield- where u = distance of an object from the refract- ing again an angle of 20° for the cornea-cone ing surface and v = distance of distal rhabdom aperture. The image seen is inverted, rotated tip from refracting surface. 180°, and diminished in size. For an object at infinity, u = », and These observations on the slices show that the (n /v) = (n -n )/r. cornea and cone assembly forms an effective lens. 3 3 0 The 1 cm square viewed at 3 cm from the cornea The distance of the nodal point N from the surface produced an image at the rhabdom tip. rhabdom tip is (v—r), and Because the tip is about 360 /*m from the poste- v-r = (n(,/n3)-v. rior nodal point, the size of the image produced will be 120 j/m. That the complete square is seen If we designate (v—r) as f, then, according to with minimal distortion through the slice dem- Horridge and Duelli (1979), onstrates that the aperture angle for the cone is f = (n(,/n3)-v. NUMBER 440 13

a b 1 2

FiGURE 6.—Diagrams of cornea-cone units and their respective images: a, (1) section of eye containing cornea-cone, (2) image presented at approximately 3 cm from the cornea. The image seen through the cornea-cone units is the same everywhere in the section, b, (1) cornea cone unit, (2) images seen at different levels, (3) images seen by units on the far sides, c, image in one cone, where the four parts are of slightly different lengths. Each quarter of the cone transmits a quarter of the image.

Horridge and Duelli (1979) point out that this the rhabdom by gradients of the refractive in- ratio is independent of surface curvature. dices but by refraction in the wedge-shaped col- For terrestrial insects, n0 = 1.0 for air, and the lars and total reflection in the cones. If we assume ratio is independent of the combination of that the cone material of stomatopods is similar curved surfaces. In the cases of the locust and to that in insects, with n3 = 1.5, and with a the praying mantis, Horridge, Duniec, and Mar- distance from distal cornea to rhabdom of 400± celja (1981), state that the posterior nodal points 38 fim, then are at one third of the distance from the corneal f/400 /xm = 1.34/1.5, and f = 357 /im. surface to the rhabdom tip. This implies that the refractive index of the cone n is 1.5. The anatomical acceptance angle of the rhab- 3 dom is defined by the angle subtended by the For the eye of a stomatopod in sea water, n0 = 1.34. The refractive indices of the cones and rhabdom at the posterior nodal point. The rhab- corneagenous cells of Squilla show no gradients dom diameter in Squilla is 15 jim, and so the for the contents, but the membranes delimiting anatomical acceptance angle 6, the angle sub- these structures and the extracellular fluids have tended by the rhabdom at the posterior nodal refractive indices that are different from those point, is of the contents. Light is not funnelled towards $ = d/f = 15/357 = 0.042 radians or 2.4°. 14 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

This measurement of d is from the light- the possible nervous substrate for measurements adapted state of the eye. For the mechanical of range-finding and angular velocity, whereas changes during dark, adaptation, see Schiff their report was concerned more with the gen- (1974). eral and detailed histology of this ganglion. Thus for the eye of Squilla in sea water, the GENERAL ORGANIZATION.—The ensemble of calculated acceptance angle is the same as or the ganglia in the eye of Squilla is shown in slightly greater than that found in the terrestrial Figure 7. The lamina of Squilla mantis is a sheath- locust and praying mantis. The change resulting like structure enveloping the second order fibers. from the higher refracting index of sea water Like the lamina of other stomatopods, it consists and the resultant need for increased cone length, of two parts, one upper or dorsal, one lower, or because of an increase in focal length, is compen- ventral. The two parts are connected in the sated for by a larger rhabdom. Whereas the middle by tangential fibers. The lamina contains visual field for each ommatidium remains very seven layers: small in Squilla, the very large facet and cone 1. A connective tissue sheath that envelops the diameters increase greatly the area over which lamina as in other Crustacea (Nassel, 1975, 1976; light from the small visual field is accepted, thus Stowe, Ribi, and Sandeman, 1977). This connec- increasing sensitivity. tive tissue is filled with white pigment droplets, Light from a point source is transmitted only especially in its distal part. The white pigment through the dioptric apparatus and exits at the also is present in the retina and among the first proximal cone tip. Not much stray light has been order fibers. The blood capillaries run on top of observed between the cones except in extreme, the distal part of the connective tissue sheath. unnaturally bright conditions. Whereas the cor- 2. A layer of cell somata, mainly monopolar neal facets exhibit a strong spherical aberration cells. and thus distortion of the image is seen, this 3. Another thin layer of connective tissue with distortion has not been observed in the cones. If flattened cells. the cornea is placed in polarized light, the middle 4. A distal tangential fiber layer that also con- and margins of each facet light up between ana- tains first order fibers running over the lamina lyzer and polarizer. A slight birefringence has surface. been observed throughout the cornea-cone as- 5. Approximately 4000 cartridges lying under sembly. and between the distal tangential fibers, ar- ranged in the same geometrically and spatially THE LAMINA ordered array as are the ommatidia in the retina. In sections through the surface of the lamina, FIGURES 7-9 the cartridges are of an elliptical shape, with their longer axes in the y direction (Figure 9b). While this paper was in the early stages of 6. A thick layer of proximal tangentials that preparation, an article by Strausfeld and Nassel contains the monopolar collaterals. Proximal and (1981) was published describing the histology of distal tangentials join in the middle of the eye, the lamina. As cited therein, their observations connecting the two lamina halves (Figure 7). resulted from a collaborative investigation be- 7. The connective tissue sheath that encloses tween N.J. Strausfeld and one of us (H.S.). We the lamina proximally. The second order fibers will review here some of the results already de- exit in bundles of three fibers. scribed by those authors. Because the sections we RETINA-LAMINA PROJECTION.—Our results report on were prepared in collaboration with differ slightly from the results described by Strausfeld, our results largely coincide with his. Strausfeld and Nassel (1981). The retina-lamina Some differences in interpretation result from projections (Figure 8) are difficult to observe in the fact that here we are concerned mainly with fixed sections, because the first order fibers are NUMBER 440 15

FIGURE 7.—Bodian-stained sagittal section through the eye of Squilla mantis (la = lamina, me = medulla externa, mi = medulla interna, on = optic nerve, re = retina). 16 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

fibers from one ommatidium, two from each a neighboring ommatidium in the row behind, and one fiber from an ommatidium, horizontally far- ther away (probably the third row behind), join into one bundle. Many bundles forming under the basement membrane remain together as sin- gle bundles up to the lamina. As many as five of these seven-fiber bundles may be enclosed to- gether by connective tissue. No crossing of fibers between neighboring bundles has been observed. Therefore, it seems unlikely that the axons from each ommatidium go to a single cartridge, as described for Leptograpsus by Stowe (1977). Bundles of first order fibers arrive and split up at the lamina surface. Each cartridge contains six first order endings, clearly grouped into two compartments. In many preparations a fiber bun- dle arriving at the lamina can be seen comprising three fibers to two horizontally neighboring car- tridges and one extending for longer distances over the lamina surface. In live, excised eyes stained with methylene blue, the retina-lamina projection can be observed directly. The first order fibers stain a deeper blue and are thinner FIGURE 8.—Retina-lamina projection of the first order fibers and varicose, thereby being easily distinguished (1 °): a, sets of onimatidia (o), which send axons into each from all other fibers. The first order fibers to- bundle of fibers and their entrance into the lamina cartridges gether with the distal tangential fibers form a (ca) (ho = horizontal, ve = vertical, T 1, T 2, and T 3 = tangential fibers, M 1-M 4 = monopolar axons). The dia- roughly hexagonal network just proximal to the gram on the right shows the occasional twisting of a first monopolar somata. order fiber bundle just before it enters the cartridge, b, the RECEPTOR TERMINALS IN THE CARTRIDGES bundles of first order fibers, deriving their axons from three (Figures 9, 10).—The cartridges are surrounded plus one onimatidia, form under the basement membrane, by loosely assembled glial cells. They are divided f, arrangement of neural elements in the lamina (am = amacrine cells, col = collaterals of the monopolar axons). into two halves (Figure 9a), with each half con- taining three receptor axon terminals ending at considerably longer than in most other arthro- three different depths within the cartridge. Each pod eyes and are rarely completely preserved in ending comprises many little branches, forming sections. Therefore we have also included obser- a pointed, brush-like terminal (Figure 9a,c). The vations made on eyes in vitro, unstained or receptor axon terminals are filled with synaptic stained with vital methylene blue. vesicles (Figure 9b), with a significant proportion As in the decapod Crustacea Pacifastacus (see of terminal surfaces covered by synapses; occa- Nassel, 1976) and Pandalus (see Nassel, 1975), sional tight junctions also are in evidence. Spines the retinular cell axons (2±0.53 jim in diameter) from monopolar dendrites penetrate the recep- join into bundles of seven fibers after emerging tor terminal branches, as described in Pandalus from the basement membrane. These seven first by Nassel (1975). Strausfeld and Nassel (1981) order fibers, or receptor axons, derive from four labelled the monopolars M 1 to M 6. Our labell- onimatidia (Figure 8a): in a vertical section two ing may be different, as indicated below. NUMBER 440 17

FIGURE 9.—Lamina cartridges: a, Bodian-stained sagittal section through the lamina, demon- strating the cartridges (ca); M 3 is a monopolar axon. b, EM photograph of part of a cartridge. Arrows indicate synapses from a first order fiber (1°) filled with synaptic vesicles (sv) to a second order fiber (2°). c, tangential section from Bodian preparation through the peripheral lamina surface showing the elliptical shape of the cartridges, the tangential fiber network, and neurosecretory vesicles (nv). Only some of the terminals of the retinular cell axons are in focus, as others end at different depths. 18 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY iP^r 1° -. 1° #m3 more diffusely. The M 3 monopolar cell (M 6 in Strausfeld and Nassel, 1981) has a very short branch distal to the cartridge, with few dendrites. The axon extends along the periphery, outside the cartridge, and then runs with one of the M 1 or M 2 axons (Figure 8c). At their exit from the cartridge, the M 1 and M 2 axons turn away from each other. Each fiber joins one of the axons from the neighboring cartridge, and the bundle is completed by the M 3 axon from one of the two participating cartridges (Figure 8c). The ax- ons squeeze through the branches from the tan- gential fibers, their diameter changing continu- ously because they are so tightly packed in be- tween the tangential fiber branches. Shortly before joining into one bundle of three fibers, the axons from M 1 and M 2 send off two to four long collaterals, which run together with the proximal, tangential fibers. The M 1 and M 2 axons thicken considerably and abruptly, proxi- mal to the collaterals, and acquire an average diameter of 3±0.5 /im. The bundles then exit from the lamina and run towards the medulla externa where they terminate. M 3 and M 4 ax- ons (Figure 1 Oc,d) are curved, with dendrites in the curved part. The fibers from the two hori- zontal middle rows of ommatidia next to the 100 *r 2 middle band end in two horizontal rows of car- tridges in the same (ventral) half of the lamina. FIGURE 10.—The monopolar: a, the four types of monopo- lar axons, M 1-M 4 (1° = first order fibers), b, Bodian- The second order fibers from these special car- stained section through the lamina with several monopolars tridges can be seen running along the outer shown by arrows (ca = lamina cartridge), c, three retinular surface around the medulla. We have not been cell axons are projected into the lamina cartridges under able to establish whether they bypass the medulla their respective ommatidia. Star shows the location of the axons from the middle ommatidia. d, enlargement of one of externa or enter at the proximalmost part of the the monopolars (M 4) shown in c. medulla. TANGENTIAL CONNECTIONS (Figures 11- 13).—In addition to the monopolar collaterals, The dendritic branches of M 1 and M 2 are four other elements with tangential connections inside and throughout the cartridges (Figure have been found. Three systems of tangential 10a,b). The M 1 cell lies close to the cartridge, fibers, T 1, T 2, and T 3, are seen frequently with the M 2 cell more distal and slightly shifted (T 1 corresponds to the small field T cells, T 3 horizontally. The M 1 dendrites start distal to to Tan 1, and T 2 to the "third type of tangential the receptor terminals, right after entering the ending" in Strausfeld and Nassel, 1981). T 1 has cartridge, whereas the M 2 dendrites start only small fields and T 2 and T 3 have wide fields at the level of the most proximal receptor brush. enclosed by their dendrites or terminals. Small The M 2 dendrites extend in a horizontally flat- field amacrine cells (see Figure 8c) have been tened array. The M 1 dendrites are distributed observed occasionally. NUMBER 440 19

la

/ b

FIGURE 11.—T 2 fibers: a, sagittal Golgi section showing a large T 2 fiber. These fibers branch out in an elliptical profile in the lamina, in a column-like array in the medulla (c) and possess small tree-like endings under the cartridges. Arrows indicate the beginnings of small branches, b, drawing of the same fiber shown in a, at a different depth of focus. c, the T 2 fiber branching in the medulla externa. d, tree- like endings of T 2 fibers. FIGURE 12.—T 3 fibers:a , sagittal section, b and c, tangential sections of the lamina (la) surface in a Golgi preparation show the vertical and horizontal branches of the T 3 fiber The T 1 system consists of numerous, small running over the distal lamina surface, d, branches from the (1.1 ±0.5 /tm) T-shaped fibers. One of these T 1 T 3 fiber (3°) are sent into the proximal medulla externa fibers traverses the lamina between each two (me; arrows) (mi = medulla interna). vertical neighboring cartridges, then divides into two fibers running in the y direction, each of larger fibers, 10 nm in diameter, which branch which sends terminals downward into the car- in the proximal tangential fiber layer. They ex- tridges. Thus they connect two neighboring car- tend over a large region of the lamina (Figure tridges and each cartridge gets terminals from 1 \a,b) and arborize extensively. The T 2 system two T 1 fibers (Figure 136). In addition to their connects many cartridges, with an elliptical dis- vertical branches, two roughly horizontally run- tribution approximately the shape and exten- ning short branches start at the T intersection. sions of the pseudopupils. In the medulla the T 2 The T 2 system consists of fewer but much fibers have large arborizations extending tangen- 20 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

pating in the hexagonal network on the distal lamina surface. They are easily distinguished from the thin, deeply blue staining, varicose first order fibers, because they are smooth, light blue, larger fibers. The T 3 fibers run from the lamina to the proximal border of the medulla, between the medulla externa and the medulla interna. On their way they send off several branches toward the medulla externa. They could be followed to the proximal border of the medulla, where a group of about 10 to 15 very large cells, 75-200 fim, are located. In eyes vitally stained with meth- ylene-blue we see two to three fibers with diam- eters of 25-66 nm emerging from these cells, which were called the "onion bodies" in the older literature (Hanstrom, 1934). Some of the tangential fibers contain large vesicles, probably neurosecretory in function. Smaller nerve fibers filled with neurosecretory vesicles are found in all cartridges in between the receptor terminals and the monopolar dendrites (Figure 9b). BLOOD SUPPLY OF THE LAMINA (Figure 14).— The blood sinuses and capillaries that supply each ommatidium and each cartridge are shown in FIGURE 13.—The three T systems of tangential fibers: a, schematic drawing showing the four cartridges connected Figure 14. Blood vessels proximal to the base- with each T 1 fiber, the two main vertical branches of the ment membrane, six in each half of the eye, T 2 fiber, and the rows of cartridges connected to the provide the blood supply for the retina. Loops horizontal branches of the T 3 fibers, which in turn branch of capillaries run vertically over the distal lamina off from a large, vertical T 3 trunk (2°, second order fibers). surface. These send off little loops that accom- b, diagrams of the distribution of the three T fiber types relative to the cartridges (ca): T 1 branches to 4 cartridges, pany each single cartridge (Figure 14c). the elliptical spread of T 2, and T 3 presumably collecting information from many horizontal rows of cartridges in the THE MEDULLA EXTERNA lamina. FIGURES 15-17 tially as well as in depth (Figure 1 \c). The medulla has alternating layers of fibers in The T 3 system (Figure 12) contains only a three perpendicular planes. Long second order few fibers but they are large. They run vertically fibers connect the lamina with the medulla ex- over the distal surface of the lamina, and between terna through a chiasma in the xz or horizontal the rows of cartridges they send off smaller, plane. The monopolar axons run through the horizontal fibers that extend over a distance of medulla externa and terminate in the interior of several to many cartridges. From the horizontal the medulla (Figure 15). Transmedullary neu- fibers little terminals extend into the underlying rons with their cell bodies on the peripheral cartridges. In live preparations stained with surface join the second order fibers on their way methylene blue, the T 3 fibers are seen partici- through the medulla. 21

FIGURE 14.—The circulatory system of the retina (re) and lamina (la) (closed loops of vessels and capillaries are char- acteristic of the system): a, schematic drawing of the blood vessels (bl). Inset: each ommatidium (o) receives a capillary loop, b, a large artery (bl) enters the region of the lamina (la), where it sends off the vessels running around the lamina. Arrow indicates a vessel going to the retina, c, capillaries (cap) branching off the vessels pass through the lamina (la) and form long loops on the distal lamina surface. Each FIGURE 15.—Fibers in the medulla interna: a, Bodian- cartridge (ca) is supplied with a small capillary loop. The stained sagittal section through the medulla externa showing arrows indicate a small region inside each loop, which, with the layers of fibers comprising the x,y,z directions. Termi- Azan, stains a distinct color similar to the neurosecretory nals of second order Fibers (te) lie between the two proxi- cells. malmost vertically running fiber layers. The third order fibers (3°) exit in the central part of the medulla externa. b, second order fiber terminals in the medulla externa. The most impressive feature of the medulla is a system of giant fibers and cells. In the middle systems are exactly parallel and very near to each of the medulla two large fibers, 25-30 (urn in other. The main branches then produce many diameter, send three main branches off in a smaller branches all parallel with one another sagittal plane, similar to an espalier (Figures 16, and at about right angles to the main branches. 17). The main branches and trunks of the two Nearly all further ramifications take place in a 22 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

FIGURE 16.—The giant fiber tree in the medulla externa: a, two reconstructions from sagittal, horizontal, and frontal serial sections, based on Golgi- and Bodian-stained preparations and fluorescence techniques. There are two parallel trees, as seen in b and c. Each of the three main branches in the sagittal plane sends off many parallel smaller branches, which branch again dichotomously, forming cup-like shells of fibers; only some of the branching is shown. Arrows and stars denote the two types of terminals (te). b, a large part of the two giant fiber trees in a particularly thick Golgi-stained section; the remaining parts of the tree are not in the same plane of the section. The figure also shows the boundaries of the medulla externa. dichotomous or T-like fashion. Many parallel fi- parallel branches running proximally from small, bers participate at each branching level and so horizontal fibers. Another type of terminal cup-like shells of parallel fibers exist throughout curves around the medulla in the z direction and the medulla. The most peripheral cup-like shell has small, peripherally directed bushes at each of belongs to the largest, most proximal branch, the its ends. intermediate shell to the intermediate branch, Large fibers are found between the optic nerve and the innermost cup is formed by the distal- and the medulla externa, where they enter. most branch (Figure 16a). The terminals are tiny These fibers run outside the ganglia, sending 23

THE MEDULLA INTERNA

FIGURE 18 Between the medulla externa and the medulla interna, couples of relatively large fibers (Figures I2d, 18a) are found with a regular spacing and collaterals. Fibers coming from the medulla ex- terna run in horizontally flattened bundles to the medulla interna. All over the surface of the me- dulla interna, large fiber couples with a very regular, geometric distribution repeat the pat- tern found in the connecting fibers. The rows of couples are set at an angle with regard to the large fibers in the medulla externa, distributed in this way by the second chiasma. One row of these fiber couples at about the middle of the medulla interna contains fibers larger than all the others. Therefore, the bilateral symmetry of an upper and a lower half of a ganglion is contin- ued in the medulla interna. In sections in the xy plane we find instead extensive, large arborizations extending throughout most of the medulla interna (Figure 18c).

HIGHER ORDER GANGLIA The medulla terminalis and other higher or- der ganglia have not yet been studied. FIGURE 16 (continued).—c, sagittal section (xy plane) through about the middle of the medulla externa, seen in In the optic nerve all of the fibers fire sponta- ultraviolet light. The giant trees are seen as shadows of neously, but only a few respond to whole eye smaller fibers of the medulla on the fluorescent background. stimulation. In the fibers that do respond, the d, fluorescent horizontal section (xz plane) in ultraviolet same five categories are found as in the third light, e, a diagrammatic drawing of the medulla to show the order fibers, although higher intensities of illu- distribution of layers in the sagittal plane (giant fiber trees mination are needed (for a more extensive de- are only indicated) and the extension of the giant trees in the horizontal (xz) plane. scription of the responses in second- and third- order fibers in the optic nerve see Schiff, 1976). branches to the medulla interna and the medulla Ochi and Yamaguchi (1976) describe the re- terminalis on their way. Two systems probably sponses of fibers in the optic nerve of Oratosquilla are present: one comprising the large fibers as a function of intensity and duration of illumi- forming parallel trees inside and throughout the nation and the receptive fields of these fibers. medulla externa, and another comprising a few large fibers running over the medulla surface in SUMMARY the y direction, similar to the contralateral fibers FIGURE 19 described for other , for example, the fly (Strausfeld, 1976), possibly responsible for Our results on the fiber distribution and pro- the delayed responses, mentioned below. jection pattern between retina and optic nerve, 24 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY a

FIGURE 17.—The medulla interna: a,b,c, serial, thick sections of the medulla externa, each containing part of the giant fiber system. Note the small terminal branches coming off their mother fiber (arrows) at right angles at regular intervals. The other type of terminal is best seen in c (star). (b,c, are photomontages from two (b) focusing depths (outlined areas) and from three (c) focusing depths.) d, extensively branched fiber in the medulla interna (mi; same section as shown in b) presumably connected to the giant fiber system in the medulla externa (3°, third order fiber).

with particular emphasis on giant fibers that we (Figure 19a), half of the fibers from behind come associate with emergency reactions and integra- to enter the medulla in front, and vice versa. tive signal transmission, are summarized in Fig- The second chiasma arranges the fibers in the ure 19. The inclination of lines in the retina flat, sheet-like bundles exiting from the medulla represents the skewing pattern in a column. The externa in such a way that dorsal bundles run to distribution of cartridges in the lamina corre- the part of the medulla interna that would be in sponds to the distribution of ommatidia. The front of the page and ventral bundles run to the chiasniata change the projection patterns be- medulla interna behind the page. tween the lamina and the medulla externa and Parallel to this system is the one with giant between the medulla externa and the medulla fibers, T 2 and T 3, in the lamina (T 1 probably interna. is involved in lateral inhibition), and the trees in With the interference of the first chiasma, the medulla externa and interna. The large fiber which is in a plane perpendicular to the page trees in the medulla externa may sum inputs NUMBER 440 25

from the dorsal and ventral halves of the eye as well as horizontal sequences of inputs. The ex- tension of the large branches of the giant fiber system in the medulla interna is at right angles to that in the medulla externa.

Discussion The results described herein were obtained from research carried out over several years and comprising investigations in several different dis- ciplines, particularly optics and neuroanatomy. We have studied the eye of Squilla mantis through a variety of approaches and intentionally have combined these observations here in one report. Our main purpose was to try to correlate the data derived from different lines of research. It now appears that certain principles of optics can be related to some of the results from neu- roanatomical studies, and these, in turn, can be related to results obtained from electrophysio- logical recording. Investigations of the optics yielded three sets of results: microoptics of the single ommatidium, the calculation of the acceptance angle and the cone aperture, and the distribution pattern of skewing of optical axes and the resultant inter- ommatidial angles. The proximal and distal cone extensions and the layer of small, radially arranged microvilli between the cone and the rhabdom are different from other ommatidia. The combi- nation of the distal cone extension with the wedges of corneagenous cells combines to cor- rect spherical aberration and funnels light into the cone and rhabdom. A perfect image is trans- mitted, but only that part of the light admitted that falls within the rhabdom acceptance angle will be admitted to the rhabdom. This light de- FIGURE 18.—The medulla interna: a, large fibers coming from the medulla externa send off branches in the y direc- rives from central rays passing through the distal tion in the most peripheral part of the medulla interna. and proximal cone extensions, which fit exactly These branches in turn produce smaller branches in the x the acceptance angle, and oblique rays from the direction, b, Bodian-stained section through the medulla visual field, which are bent into the central part interna; one of the couples of larger fibers enlarged in inset of the cone by the corneagenous cell wedges. (3°, third order fiber), c, part of the probable integrating tree in the medulla interna that expands mainly in the xy or The small microvilli and concave-convex cone- horizontal plane. A large branch extends in the z direction, rhabdom junction can be interpreted in two sending several branches horizontally (x) with small vertical ways, either as an ultraviolet light filter (similar fibers (y). 26 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

FIGURE 19.—The first three ganglia in the eye of Squilla: a, schematic diagram showing the distribution and orientation of fibers (1 °-4°, T 2, T 3), chiasmas, and integrating giant systems (la = lamina, me = medulla externa, mi = medulla interna, re = retina), b, projection pattern in the first three ganglia and the orientation and extension of the integrating fibers in the ganglia; T 2 integrates groups of cartridges in the x and y directions (small box in lamina); T 3 integrates many horizontal lines of cartridges. The a,b,c . . . (vertical, y) and 1,2,3 . . . (horizontal, z) are the projection patterns from one ganglion to the next. Connecting fibersar e omitted. This direct projection runs in parallel with the integrative large fiber matrix. arrangements in other arthropods have been de- pigment by ultraviolet light. It seems more likely scribed by Niissel, 1976; Goldsmith, 1978; Men- to us that these structures function as a thin zel and Blakers, 1975) or as a polarization filter lenslet, bending rays so that they enter the rhab- (Waterman, 1975). Ultraviolet and polarized dom as parallel rays, with obvious advantages for light essentially do not exist in the environment light absorption. Lenslet-like structures and of Squilla mantis. No differences in responses curved cone-rhabdom junctures have been ob- were found for different planes of polarization served occasionally in other arthropods and have (Schiff, 1963). Responses to ultraviolet light are been described and interpreted in different ways clearly different from those to visible light by Meyer-Rochow (1975), Trujillo-Cenoz and (Schiff, 1963), but rather than indicating the Melamed (1971), and Wilson (the latter cited in presence of an ultraviolet filter, the results fit a Laughlin, 1975). mechanism in insects as described by Hamdorf The large cornea-cone aperture, also admit- and Schwemer (1975), of degeneration of pho- ting oblique rays from the small visual field, and topigment by visible light and regeneration of the curved lenslet/cone-rhabdom junction to- NUMBER 440 27 gether show adaptation of an apposition eye to a sets of ommatidia or lamina cartridges, two other dim environment. By increasing the amount of mechanisms of distance and movement measure- light reaching the rhabdom and by increasing ments are possible: (1) by comparing the summed the length of the light path within the rhabdom, input from one half of the eye with that of the there is an increase in the amount of light ab- other half, somewhat like stereo images, or (2) sorbed. by evaluating distance by the shapes of the curves We believe that this adaptation is carried much representing the amount of overlap of visual farther by the pattern of skewing of ommatidia, fields of ommatidia in each column. Both inter- which results in strongly overlapping visual pretations require integrating fibers. Two types fields. We suggest that the skewed ommatidia of extensively branched large fibers, T 2 and constitute a monocular range-finding device in T 3, which could be integrating fibers, have been the Stomatopoda. For each vertical column of found in the lamina. T 2 fibers have dendritic ommatidia, the visual fields of the two halves of extensions that correspond with the shape of the the eye overlap for about 40° in front of the pseudopupil within one half of the eye; that is, middle ommatidia. Horizontally, along the rows, they may be collecting inputs from an elliptical the visual fields of single ommatidia and of the ensemble of ommatidia with parallel optical axes columns of ommatidia are separated from each within each of a few columns. The T 2 fibers other, but, for most ommatidia, visual fields over- feed directly into the medulla externa. The T 3 lap, vertically, along a column of ommatidia. In fiber, assuming that it is an integrating, feed- a vertical column, visual fields of all ommatidia forward fiber, collects information from rows of with parallel optical axes overlap with each other lamina cartridges and funnels it into one vertical and with the fields of the skewed ommatidia from fiber, which ends in or passes the proximal part the other half of the eye in a fixed pattern. We of the medulla externa. Although the T 2 fibers conclude from this that the ommatidia work to- might be interpreted as stereodividers, with dif- gether as cooperative sets, not as single units, if ferentiation in the medulla externa between in- integrating fibers can be found in the nervous puts of T 2 fibers from the two halves of the eye, system. The pattern of skewing of optical axes the T 3 fibers could constitute a mechanism for provides a monocular range-finding mechanism, integrating inputs over a row-column matrix. unique among arthropod eyes, in one of the Moreover, with integration in the T 3 fibers, it following ways: (1) crossing points of optical axes is possible to include a measurement of angular belonging to ommatidia from the two halves of velocity, if the discharge pattern of the spikes the eye lie at different distances from the corneal observed by us is a function of the intervals surface; (2) either the integration of the intersec- between the inputs. tions of axes of corresponding ommatidia or We found two types of large fibers in the intersections of axes of every ommatidium in one medulla externa, medulla-trees and tangential half of the eye, with a sequence of axes derived fibers on the medulla surface. Strausfeld (1976) from ommatidia of the other half of the eye, found fibers similar to the surface fibers in the could be involved in making a distance determi- fly and showed them to be contralateral fibers. nation. The condition for using intersections of We interpret the fibers found in Squilla in the optical axes is that the geometric position of each same way, suggest that they are responsible for ommatidium is transmitted throughout all optic delayed responses found in electrophysiological ganglia and that ommatidia work as single units. recording (Schiff, 1976), and tentatively assign Furthermore, for both intersection hypotheses, them a function in binocular vision, which would a large number of tangential fibers would be extend range-finding to longer distances required at the level of the lamina, a condition (Schaller, 1953; Burkhardt, Darnhofer-Demar, not found by us in histological studies. and Fischer, 1973). Instead, assuming that there are cooperative In the large medulla trees expanding through- 28 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY out the medulla externa, inputs from the two alert phase, in which the relevant slow muscles halves of the eye, possibly already integrated, in the claw are isometrically charged, and the come together and fuse. We correlate the large actual strike itself, with contraction of the small, spikes in undelayed responses of third order fi- fast muscles of the release mechanism. We be- bers (Schiff, 1976) with the medulla trees and lieve that muscle charging and alertness may be monocular range-finding. These large spikes are determined by the input from the "attention" found as brief bursts in response to changes of ommatidia on the dorsal side of the cornea and light and reflect the speed of light change. We that the actual strike is governed by an integra- therefore propose that these fibers, in which for tive mechanism, interpreting measurements of the first time inputs from the two halves of the distance and movement transmitted over the eye flow together, might be involved in trans- giant fibers. mitting information about distance and angular Other sensory modalities are certainly in- velocities of objects in the visual space of the eye, volved in the catching of prey. The optical alert either by the differentiation of the T 2 inputs movements of the eye are accompanied by for instantaneous shape recognition or for cor- searching movements of the antennules, which relating this information with other inputs arriv- almost certainly contain chemoreceptors. A few ing over the non-integrating monopolar axons. drops of juice added to an aquarium will The described correlation of our data is appli- send an animal into a frenzy of searching. With- cable mainly to one area of information trans- out chemical stimulation, optical attention may mission: the high-speed emergency channels for be turned off (see Schaller, 1953). Stomatopods prey capture, or for defense, by the rapid strike also have delicate, flat, leaf-like antennal scales of the claw, and instantaneous interspecies rec- fringed with setae. Through the transparent cu- ognition. ticle a dendrite can be seen extending into every Ochi and Yamaguchi (1976) described the vis- seta, with a cell at its base and a fiber extending ual fields of fibers in the optic nerve of Oratos- towards the central nervous system. This could quilla. Most fields are large, covering the whole well be a detector for pressure changes caused eye, or one half of the eye, or a strip around the by a moving object in the vicinity. middle band of ommatidia. All fields are sym- Schaller (1953) observed that Squilla mantis metrical with respect to the middle ommatidia. rarely strikes without vibrational stimuli. He de- Their results coincide well with our results and scribed an experiment in which 5. mantis, after our interpretations of extensive integration. The not striking at a sphere, struck at introduced air fields described by those authors fit the exten- bubbles. That result can now be interpreted in sions of either the T 2 or T 3 fibers, except for light of our present knowledge. The experiment the fields of ommatidia at the dorsal and ventral suggests that not only vibrational simuli are es- sides of the eye, which are concerned with optical sential for prey catching, but also that optical attention (Demoll, 1909; Schiff, 1963). information is stored or memorized and is re- Two optical phases are involved in catching trieved by adding mechanoreceptor inputs (see prey, an optical attention phase and a phase also Schiff, Abbott, and Manning, 1985). Mem- concerned with measurement of distance, speed, ory of visual inputs in single fibers has been and size. According to Burrows and Hoyle studied in other crustaceans by Wiersma, Hou, (1972), there are also two phases of muscle prep- and Martini (1974). aration associated with the strike. There is an Literature Cited

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