Post-Embryonic Growth and Fine-Structural Organization of Arthropod Photoreceptors. a Study Involving Selected Species of Insect

POST-EMBRYONIC GROWTH ESSI AND FINE-STRUCTURAL KESKINEN ORGANIZATION OF Faculty of Science, Department of Biology, ARTHROPOD University of Oulu PHOTORECEPTORS A study involving selected species of insects and crustaceans

OULU 2004

ESSI KESKINEN

POST-EMBRYONIC GROWTH AND FINE-STRUCTURAL ORGANIZATION OF ARTHROPOD PHOTORECEPTORS A study involving selected species of insects and crustaceans

Academic Dissertation to be presented with the assent of the Faculty of Science, University of Oulu, for public discussion in Kuusamonsali (Auditorium YB210), Linnanmaa, on December 4th, 2004, at 12 noon.

Supervised by Professor V. Benno Meyer-Rochow Professor Kari Koivula

Reviewed by Professor Silvana Allodi Docent Magnus Lindström

ISBN 951-42-7559-4 (nid.) ISBN 951-42-7560-8 (PDF) http://herkules.oulu.fi/isbn9514275608/ ISSN 0355-3191 http://herkules.oulu.fi/issn03553191/

OULU UNIVERSITY PRESS OULU 2004 Keskinen, Essi, Post-embryonic growth and fine-structural organization of arthropod photoreceptors A study involving selected species of insects and crustaceans Faculty of Science, Department of Biology, University of Oulu, P.O.Box 3000, FIN-90014 University of Oulu, Finland 2004 Oulu, Finland

Abstract Arthropod photoreceptors are versatile sense organs. Any investigation of these organs has to consider that their structure and functional limitations at the moment of fixation depend on many factors: species, sex, developmental and nutritional state of the animal, time of day and ambient light. The microscopic image of an arthropod photoreceptor is always a sample frozen in time and space. Quite often publications on arthropod photoreceptors only provide the name of the species studied, but nothing beyond that. At least the developmental status of the study animals ought to be noted, possibly even the sex and body size. Forty publications on insect and 54 on crustacean photoreceptors were checked for the information that was given about the investigated animals: Out of these papers 40% provide only information on the name of the studied species and nothing else. The aim of this thesis, thus, was to investigate, to what extent the developmental state and the sex of the animal as well as the ambient light conditions affect the structure of the eye of a given species. Five species of arthropods were chosen: (a) the semi-terrestrial isopod Ligia exotica and two aquatic Branchiuran fishlice, Argulus foliaceus and A. coregoni, to represent the Crustacea, and (b) the stick insect Carausius morosus and the spittle bug Philaenus spumarius, both terrestrial, to represent the Insecta. The addition of new ommatidia was studied in a paper on L. exotica, which also dealt with the site of newly added ommatidia. It was found that all of these species had two sessile, large compound eyes firmly positioned on their heads (but fishlouse compound eyes were bathed in haemocoelic liquid). In all species, the compound eye was found to be of the apposition type. The gross structural organization of the ommatidia stayed approximately the same during the whole post- embryonic development. Lateral ocelli of the A. coregoni nauplius eye changed from elongated to spherical between the metanauplius and the 8th stage pre-adult. The sex of the specimens was not found to affect the structure of the eye. In all species, it turned out that the larger the animal and hence the eye, the better its sensitivity. The addition of new ommatidia in the L. exotica compound eye was concluded to take place in the anterior and ventral marginal areas of the eye.

Keywords: Compound eye, crustaceans, insects, nauplius eye, post-embryonic development

To my family

Acknowledgements

When I first came to Oulu as a first year biology student, graduating seemed one of those projects that will go on forever and never see the end. Yet, here I am, eight years later, writing the acknowledgements to my Ph.D. thesis. The past four years that I have worked with arthropod eyes have taught me a lot. Even though there were never many other peo- ple in the same project, it still always felt that I had a team around me – supervisors, laboratory personnel, university staff, friends and family. First of all, I want to thank my ever-so patient supervisor, Prof. V. Benno Meyer- Rochow. He showed me how insects and crustaceans see the world: in little pieces that need to be put together in order to form a bigger picture. Prof. Meyer-Rochow should be acknowledged as the best supervisor one can have. I am very grateful to the reviewers Dr. Silvana Allodi and Dr. Magnus Lindström for their very valuable comments. I owe my gratitude to the small Department of Electron Microscopy in Tohoku Univer- sity in Japan. Prof. Taka Hariyama taught me everything I needed to know about transmission and scanning electron microscopes, microtomes and making samples. In only six months, he helped me put together enough material for two scientific publications. I also want to thank his wonderful students Kawauchi-kun and Takaku-san, for all the help in the lab and conversations outside the lab. Without the help of laboratory personnel at the Department of Pathology of Oulu Uni- versity, I would have been in trouble. Technician Anna-Liisa Oikarinen not only processed my specimens but also helped me through tough days when the specimen blocks grouped against me, the knives were scratched and nothing seemed to work. I also want to thank Sirpa Kellokumpu and Raija Sormunen for all their help. I want to aknowledge the help of the Institute of Electron Optics of Oulu University. Tehnical officers Jouko Paaso, Päivi Huhtala and Elvi Hiltula helped me with the microscopes and processed my samples. I also want to thank Prof. Kari Koivula and Sisko Veijola at the Biology Department of the University of Oulu, for all the pieces of information they have given me along the way. If I didn’t know where else to turn to, they always either gave me the answer or at least pointed me to the right direction. I thank the technician Seija Leskelä at the Department of Dentistry, University of Oulu, for her help with editing the pictures. I am also very thankful for M.Sc. Laura K. Säilä for her skillful drawings. I wish to express my deepest gratitude to all my friends who always believed in me and helped me to have a normal life as well, and my family, who never doubted that I wouldn’t finish this project. With two professors as parents, it sometimes felt like I would be just finishing my basic education and not the highest degree one can earn. During my studies, it was only a good thing that Ph.D. studies were taken for granted in my family: my parents never thought that anything would be too hard for me, or that I couldn’t do something. Last but definitely not least, I owe my gratitude to my dear husband Mikko, who has addressed me as ”Doctor Keskinen” already for the past year. He never doubts that I couldn’t do everything, and all of it at the same time, to a point that he sometimes makes it sound like I’m some sort of a superhero. Thank you for standing by me. This research was financially supported by the Jenny and Antti Wihuri Fund, Oulu University, the Oulu University Fund, the Oskar Öflund Fund, Alfred Kordelin Fund and the Finnish Konkordia Fund.

Oulu, November 2004 Essi Keskinen List of tables

Table 1 Specimen information given in 40 randomly chosen publications of insect compound eye structure. ”+” = information available...... 30 Table 2 Specimen information given in 40 randomly chosen publications of crustacean compound eye structure. ”+” = information available...... 31 Table 3 Specimen information given in 14 publications of crustacean nauplius eye structure. ”+” = information available...... 32 Table 4 Measures that were taken in the original papers (I–VI)...... 36

List of figures

Fig. 1. Arthropod compound eyes and ocellus, including the features that determine the anatomical resolution...... 18 Fig. 2. A semi-schematic drawing of a basic type of one arthropod apposition ommatidium...... 20 Fig. 3. The eye and the optic lobe in an arthropod head...... 21

List of original papers

The present thesis is based on the following papers, which are referred to in the text by their Roman numerals: I Meyer-Rochow VB, Au D & Keskinen E (2001) Photoreception in fishlice (Branchiura): The eyes of Argulus foliaceus Linné, 1758 and A. coregoni Thorell, 1865. Acta Parasitologica 46: 321–331. II Keskinen E, Takaku Y, Meyer-Rochow VB & Hariyama T (2002) Postembryonic eye growth in the seashore isopod Ligia exotica (Crustacea, Isopoda). Biol Bull 202: 223–231. III Keskinen E, Takaku Y, Meyer-Rochow VB & Hariyama T (2002) Microanatomical characteristics of marginal ommatidia in three different size-classes of the semi-terrestrial isopod Ligia exotica (Crustacea; Isopoda). Biocell 26: 441–450. IV Meyer-Rochow VB & Keskinen E (2003) Post-embryonic photoreceptor development and dark/light adaptation in the stick insect Carausius morosus (Phasmida, Phasmatidae). Applied Entomology & Zoology 38: 281–291. V Keskinen E & Meyer-Rochow VB (2004) Post-embryonic photoreceptor development and dark/light adaptation in the spittle bug Philaenus spumarius (L.) (Homop- tera, Cercopidae). Arthropod Structure & Development, in press. VI Keskinen E & Meyer-Rochow VB (2004) Post-embryonic photoreceptor development in a fishlouse Argulus coregoni Thorell, 1865 (Crustacea: Branchiura). Acta Parasitologica, in press.

Contents

Abstract Acknowledgements List of tables List of figures List of original papers Contents 1 Introduction ...... 17 1.1 Arthropod photoreceptors ...... 17 1.1.1 Insect ocelli ...... 17 1.1.2 Crustacean nauplius eyes ...... 19 1.1.3 Extraocular photoreceptors ...... 19 1.1.4 Compound eye ...... 20 1.1.4.1 Apposition eye ...... 21 1.1.4.2 Superposition eye ...... 23 1.2 Photoreceptor flexibility ...... 24 1.2.1 Post-embryonic development ...... 24 1.2.2 Light/dark adaptation ...... 25 1.2.3 Sex ...... 27 1.3 Light-induced photoreceptor damage ...... 27 1.4 Aims of this study ...... 28 2 Materials and methods ...... 33 2.1 Study species ...... 33 2.2 Collecting sites, treatment and measuring ...... 35 2.3 Statistical methods ...... 36 2.4 Fixation procedures ...... 37 2.4.1 Samples for light microscopy (LM) ...... 37 2.4.2 Samples for transmission electron microscopy (TEM) ...... 37 2.4.3 Samples for scanning electron microscopy (SEM) ...... 37 3 Results ...... 39 3.1 Morphological observations ...... 39 3.2 Anatomical features of the compound eyes ...... 40 3.2.1 General organization ...... 40 3.2.2 Light/dark adaptational changes ...... 41 3.3 Anatomical features of the nauplius eye ...... 42 3.4 Accretion of new ommatidia in L. exotica ...... 42 4 Discussion ...... 44 4.1 Sex ...... 45 4.2 Development ...... 46 4.3 Light/dark adaptation ...... 49 5 Conclusions ...... 51 References 1 Introduction

1.1 Arthropod photoreceptors

During the course of evolution, arthropods (only insects and crustaceans, and no chelicer- ates or myriapoda, will be considered in this thesis) have developed at least three different types of photoreceptive organs for sensing light: (1) compound eyes, (2) ocelli and nauplius eyes, and (3) extraocular or extraretinal photoreceptors. Several excellent reviews on the structure and function of compound and other arthropod eyes have been published over the years. I will list only a few comprehensive examples: Handbooks by Carterette and Friedman (eds) (1978), Autrum (ed) (1981), Kerkut and Gilbert (eds) (1985), Eguchi and Tominaga (eds) (1999), reviews, for example, by Cronin (1986), Land (1980, 1981, 1988, 1997), Gaten (1998), Meyer-Rochow (2001). Insect and crustacean taxa diverged about 500 million years ago from a common ancestor, which itself may already have had good vision (Osorio et al. 1997). In spite of considerable similarities with regard to the existing eyes of all species of the animal king- dom, the origin of the eye is still obscure. Thought not to be monophyletic by some (Fer- nald 2000), others, citing new molecular genetic evidence, strongly support the monophyletic origin (Gehring & Ikeo 1999). The latest view on the arthropod eye is that the crustacean and the insect compound eyes, because of identical embryological scenarios, may have a monophyletic origin (Paulus 1979, 2000, Melzer et al. 1997, 2000, Nilsson & Osorio 1997, Osorio et al. 1997, Harzsch & Walossek 2001). This led to the establish- ment of a taxon “Tetraconata”, including both crustacea and insecta (Dohle 2001).

1.1.1 Insect ocelli

Ocelli are simple insect photoreceptive organs, often with poor spatial resolution (Fig. 1. d), which are present individually or in clusters of separate ocelli and hail back to at least the trilobites. Insect ocelli can be divided into two distinct groups: (1) larval eyes of exopterygote insects, where the ocelli are the only eyes that the larvae possess, and (2) 18 the dorsal ocelli of most winged adult insects (Land 1985). The three dorsal ocelli of the adult insect are typically situated on the dorsal side of the head and are thought to make quick flying maneuvers possible by observing the horizon without letting any details become distractive (the adult dorsal ocelli are permanently out of focus, a fact that has puzzled scientist for decades: Land 1985, Mizunami 1999). The stemmata (also known as larval or lateral ocelli) can be divided into two functional types: (a) the ommatidium type, which is similar to one ommatidium of a compound eye and is thought to be “highly specialized for color vision” in butterflies (Ichikawa 1999), and (b) the lens-eye type lateral ocelli, which resemble the dorsal ocelli with a cup-shaped retina with many rhabdoms, covered by a biconvex corneal lens (Meyer-Rochow 1974, Land 1985, Ichikawa 1999). This latter type of ocellus seems to be specialized for detecting movement, but its resolution is usually poorer than that of a compound eye (Ichikawa 1999).

Fig. 1. Arthropod compound eyes and ocellus, including the features that determine the anatomical resolution. a) Apposition type compound eye without the clear zone between the dioptric apparatus and the rhabdoms. C = center of curvature, D = facet diameter, R = radius of a compound eye, ∆φ interommatidial angle or the angular separation of visual axes. b) Dipteran neural superposition eye. Signals from adjacent rhabdomeres are recombined to form a single image in the lamina. c) Optical superposition eye with a clear zone. C(N) = center of curvature ∆φ and nodal point, drr = distance from one rhabdom center to the next, = angular separation of visual axes, f = focal length. d) Ocellus or a simple eye (for abbreviations, see Fig. 1, c). Red- rawn from Land, 1985. e–f) Optical superposition eyes. e) Reflecting (mirror) superposition eye, where the facets are always perfect squares at the surface. f) Refracting superposition optics with a refractive index. Redrawn from Nilsson (1990). 19 1.1.2 Crustacean nauplius eyes

Many crustaceans possess a well-developed dorsal nauplius eye, either throughout their whole life or only as larvae (Elofsson, 1963, 1965, 1966a, compares the light microscopic structure of the nauplius eye of 238 crustacean species from most major groups). Many of the lower crustaceans often have a 3-part nauplius eye during the larval stage, but the eye later metamorphoses into three separate ocelli in the adults (Takenaka et al. 1993). The basic nauplius eye structure is a single median eye on the dorsal side of the animal, where three ocelli are situated in cups, formed by a varying number of pigment and tapetal cells (cf, fine-structural papers by Fahrenbach 1964, Dudley 1969, Elofsson 1969, Wolken & Florida 1969, Ong 1970, Andersson 1979, Andersson & Nilsson 1979, Takenaka et al. 1993, Meyer-Rochow 1999a, Martin et al. 2000). The rhabdoms formed by the microvilli are situated in the photoreceptor cells in each of the three cups and do not normally form the central columns known from compound eye ommatidia. In Branchiura, Branchiopoda, Cladocera, Euphausiacea, Stomatopoda and in many decapod crustaceans, the nauplius eye persists concomitantly with the compound eye while other species of crustaceans either have a nauplius or a compound eye (Waterman 1961). Nauplius eye structure has been much investigated over the years, but mostly with light microscopic techniques (see a comprehensive list of the earliest papers in Dudley 1969), and its optics are still not well understood (an exception is a paper by Wolken & Florida 1969, which deals with the nauplius eye of Copilia that resembles one ommatidium in a compound eye). Why a crustacean with powerful compound eyes would need a much smaller extra medial nauplius eye is still an unanswered question.

1.1.3 Extraocular photoreceptors

As the term suggests, extraocular, or extraretinal, photoreceptors are photoreceptive organs, membranes or tissues that can be found outside the crustacean and insect compound eyes and ocelli (Arikawa 1999a). These photoreceptors, which may be present in endocrine glands and/or nervous tissues, most probably have something to do with set- ting the circadian clock (Sandeman et al. 1990). When extraocular photoreceptors are situated in the brain, they are called ‘intracerebral ocelli’ (Sandeman et al. 1990, Felisberti et al. 1997, Hariyama 2000). Some of the most thoroughly studied extraocular photoreceptors in insects are the butterfly genital photoreceptors that are needed to achieve suc- cessful copulation (Arikawa & Miyako-Shimazaki 1996, Arikawa et al. 1997, Arikawa 1999a). Another example of a well-known extraocular photoreceptor is the tail or caudal photoreceptor that has been found in the abdominal ganglion of some decapods (reviewed in Wilkens 1988, Pei et al. 1996). In the horseshoe crab, Limulus polyphemus, the ventral photoreceptor organ in the telson is connected to the circadian clock in the animal’s brain so that illuminating only the telson will produce phase-shifts in the circadian activity rhythm of the animal (Renninger et al. 1997). 20 1.1.4 Compound eye

The typical arthropod compound eye involves two principal components: (1) the dioptric structures, consisting of cornea and cone cells, and (2) the retinal elements, consisting of photoreceptive cells (the so-called retinula cells) and their specialized microvillar borders (the so-called rhabdoms) (Fig. 2). Additional cells like corneagenous cells, primary and secondary screening pigment cells, basal lamina cells, interommatidial cells, and glial cells, surrounding the axons of the retinula cells, may be present. The homologies of these cells between different species, and in particular between crustaceans and insects, have not yet satisfactorily been explained (Harzsch et al. 1970). The embryological and morphological relationships of the cell types to each other are also still a matter of intense research (Müller et al. 2003). Compound eyes are represented by two different fundamental constructions (Fig. 1): (1) the apposition eye, where the dioptric apparatus and the retina are in contact with each other, and (2) the superposition eye with a clear zone between the cone and the retina (“a region devoid of pigment at least under dark-adapted conditions”: Meyer-Rochow 1999b).

Fig. 2. A semi-schematic drawing of a basic type of one arthropod apposition ommatidium. a) Longitudinal section. b) Cross-section of the rhabdom and the surrounding retinula cells from the central level of the ommatidium. a) The lens and the cone together form the dioptric apparatus. Proximal to that and without a separating clear zone is the rhabdom, composed of the rhabdomeres of the 7–9 retinula cells (eight in this species). The whole structure from the cornea to the basement membrane is surrounded by pigment cells. Left side of both figures a and b is as seen in a light-adapted (LA) specimen. Right side (DA) features dark-adaptation. In a light-adapted specimen, the pigment granules are aggregated to surround the cone and the rhabdom and the rhabdom is thinner and shorter. In dark-adapted conditions the rhabdom is more voluminous and the pigment granules are in dispersed positions in the cell cytoplasm. Abbreviations: bm, basement membrane; c, cone cell; cc, crystalline cone; cor, cornea; n, nucleus; ppc, primary pigment cell; rh, rhabdom; spc, secondary pigment cell. 21 1.1.4.1 Apposition eye

Apposition compound eyes can still be further divided into (a) the basic apposition eyes and (b) the special Dipteran neural superposition eyes (Fig. 1 a and b, 2). While the image in an apposition eye is formed in the retina, in a neural superposition eye it is formed in the lamina (Land 1985) (Fig. 3). The characteristic of all apposition eyes is that each rhabdom has its own dioptric apparatus. The rhabdom, which is made up of photoreceptive membrane material, acts as a light guide: each lens forms a separate, inverted image at the distal tip of the rhabdom, but the final image is erect (Land 1988). Apposition eyes are widely distributed in diurnal insects and crustaceans (Land 1985). New ommatidia are added to the compound eyes from the edges of the eye as the arthropods molt (Elofsson 1969, III). These marginal ommatidia are frequently different from the ventrally or medially placed ones. Other irregularities in the otherwise regular faceted lattice can be found in the foveal areas. A fovea or an acute zone is defined as a limited area of a compound eye with a higher resolution than in the surrounding areas (see, for example, Sherk 1977, 1978a, b, c, Horridge 1978, Land 1985, 1997, Cronin 1986). This is achieved by wider facets and/or smaller interommatidial angles (Horridge 1978, Land 1985, 1997). Foveas can be found in both crustaceans and insects (Cronin 1986, Land 1997). An acute zone can be directed anywhere where the animal needs better vision: in species that need binocular vision to estimate the distance to their prey, the fovea is often situated so that it looks directly forward, permitting binocular focusing (for example mantids, Maldonado et al. 1974).

Fig. 3. The eye and the optic lobe in an arthropod head. Signals from the compound eye are pas- sed through the three ganglia (lamina, medulla and lobula) and two chiasms before reaching the brain. Redrawn from Osorio et al. 1997. 22

Species, which detect their prey or mate against the sky, have developed specialized dorsal rim areas of large ommatidia, which are quite regularly sensitive to polarization and which may also be sensitive to short-wavelength light (Kolb 1986, Labhart & Nilsson 1995, Hämmerle & Kolb 1996, Ukhanov et al. 1996, Land 1997, Sakamoto et al. 1998, Arikawa 1999b, Labhart & Meyer 1999, Blum & Labhart 2000, Dacke et al. 2002, Homberg & Paech 2002). Ommatidia in regions other than the dorsal rim area may possess other or similar specialized functions such as color, UV or polarized light reception (Tokarski & Hafner 1984, Cronin et al. 1994, Schiff 1996, Bennett et al. 1997, Giger & Srinivasan 1997, Lehrer 1998, Giurfa et al. 1999, Qiu et al. 2002). Many insects set the rhythm of their internal clock by photic information from special regions of the compound eye (Shiga & Numata 1996, Morita & Numata 1997, Tomioka & Yukizane 1997, Shiga et al. 1999). In crustaceans, the cornea (functioning more as a protective cover than a lens) is formed by two ‘corneagenous cells’, which are originally unpigmented, while in insects, the cornea is formed by ‘primary pigment cells’ (cf, review by Meyer-Rochow 1999b) (Fig. 2). Because the cornea is only a specialized, transparent part of the chitinous exosk- eleton, it is shed at every molt (Trujillo-Cenós 1985, Meyer-Rochow 1999b). The cone is the major refractive element and consists of four unpigmented cone cells, which, when looked at with an electron microscope, seem to contribute to the cone either equally (see for example IV, V), or unequally: two can be accessory with the other two cone cells actually making up the whole cone (see for example Hariyama et al. 1986). Many nocturnal arthropods have a solid crystalline cone consisting of four cells, which contain highly refractive transparent substance. Eyes of this sort are called (a) the eucone eyes, which are characterized by cones with a dense core (the classification of cone-types goes back to Grenacher 1879, but is cited in, for example, Trujillo-Cenós 1985, Meyer-Rochow 1999b). Another type of cone is (b) the pseudocone, which is ‘a gelatinous substance contained within a two-cell, cup-like container’ (Trujillo-Cenós 1985). This type of dioptric aid can be found, for example, in higher Dipterans (Trujillo-Cenós 1985). A third type of cone, termed (c) the acone, is present in diurnally active arthropods (Trujillo-Cenós 1985, Meyer-Rochow 1999b). Acone eyes do not have either a solid core or a pseudocone gela- tin construction (Trujillo-Cenós 1985, Meyer-Rochow 1999b). In an apposition eye, the cone and the rest of the ommatidium are peripherally surrounded by an assortment of pigment cells (Fig. 2). Hallberg and Elofsson (1989) list six different types of pigment cells in the crustacean eye, while in insects at least three kinds of pigment cells are commonly acknowledged: (1) the primary pigment cells that surround the cone, (2) the elongated, secondary pigment cells that surround the whole ommatidium at its full length, and (3) the basal pigment cells at the base of the rhabdom and often partially below the basement membrane as well (Trujillo-Cenós 1985, Meyer- Rochow 1999b). Pigment granules within the pigment cells absorb oblique rays of light and protect the photoreceptor against light-induced damage (Meyer-Rochow 1999b, 2001). Photoreception takes place in the retina, or, to be more precise, in the visual membranes of the photoreceptor through the interaction of photons with the photopigment (Fig. 2). The retina is composed of individual (mostly) identical photoreceptive units [but see III (and above) about special regions in the compound eye], the ommatidia, which contain the rhabdoms with their photoreceptive membranes. Together, five (Donner 1971, 23

Rosenberg & Langer 1995) or seven to nine retinula cells make up the rhabdom, which is formed by clusters of centrally aligned microvilli (the rhabdomeres), in which most of the photopigment is located (Trujillo-Cenós 1985, Meyer-Rochow 1999b, Suzuki 1999). Pho- tons, that are absorbed by the microvillar photopigments, via a cascade of short-lived biochemical events, cause graded depolarizations of the photoreceptive membrane as a con- sequence of the phototransduction process (Suzuki 1999). The depolarizations spread in the receptor axons to the lamina (the next neuropile from the retina, Fig. 3) (Horridge 1978). Spectrally different photopigments for different colors are situated in different retinula cells (rhabdomeres) in one ommatidium, and form the basis of color vision in arthropods (Trujillo-Cenós 1985, Cronin et al. 1994, Bartsch 1995, Bennett et al. 1997, Giger & Srnivasan 1997, Arikawa 1999b, Giurfa et al. 1999, Qiu et al. 2002). Retinula cells as well as the pigment cells contain the usual assemblage of cell organelles: nucleus, membranes, mitochondria, cisternae, vesicles and various other organelles in addition to pigment granules. The rhabdom is said to be of the ‘fused’ or the ‘closed’ type, if the rhabdomeres are fused to form a single rod (Fig. 2). Rhabdoms can also be ‘open’, if the rhabdomeres leave an empty membrane-free central core in the center (see for example Fig. 3 in Hariyama et al. 1986) or ‘semifused’ (for example, Lin et al. 1992). A special case of an open apposition eye rhabdom is the Dipteran neural superposition eye, where the axons from each rhabdomere in one ommatidium do not form a common image together, as in the basic apposition type eye, but instead are rearranged between the retina and the lamina in a way that the seven axons from seven adjacent ommatidia from seven rhabdomeres looking at the same point in space, are collected together in one cartridge in the lamina (Kirschfeld 1967, cited in Land 1985) (Fig. 1. b). From the lamina onwards (Fig. 3), a neural superposition eye functions like a typical apposition eye. The advantage in neural superposition is that, when the information from the adjacent ommatidia is collected together, the sensitivity of the eye increases, and movement perception is also said to be enhanced (Land 1985).

1.1.4.2 Superposition eye

The superposition eye differs from the apposition eye in that the dioptric elements and the photoreceptive structures are separated by a clear zone (Fig. 1 c). The clear zone lacks pigments, at least during dark-adaptation, and the only structures found in the clear zone are the proximal cone cell roots or the distal retinula cell extensions, both of which possibly can act as light guides (Meyer-Rochow 1999b). The optical superposition eye forms a single, deep-lying, erect image by superimposing light that enters through many facets (Land 1985, 1988). Optical superposition is most commonly found in the eyes of nocturnal arthropods, notably Decapods amongst the crustaceans and Coleoptera and moths in the insects. In a superposition eye, light can be affected by the cones in two different ways: by (1) refraction, where the cone has a refractive index, that changes the course of the light, and (2) reflection, where a beam of light is reflected to the rhabdom with the help of biologi- cal mirrors on the walls of a square-shaped (when transversely cut) cone (see for example 24

Cronin 1986, Land 1980, 1988, Gaten 1998) (Fig. 1 e–f). Although refracting optical superposition has been found in various insect and crustacean species (Land 1997), reflecting superposition optics have only been confirmed for Decapod crustaceans and male mayflies (Cronin 1986, Nilsson 1990, Gaten 1998).

1.2 Photoreceptor flexibility

An arthropod photoreceptor (and in particular the compound eye) is by no means an unchangeable, stiff organ. On the contrary, its structure is affected, for example, by the level of ambient light, the time of day, the temperature, and the sex, age and nutritional state of the animal and even certain carapace characteristics (Wasserman & Cheng 1996). A sample fixed for microscopic studies can only reveal information about the eye’s structure according to the specific condition under which the animal’s eye was fixed. In compound eye research, structure represents function frozen in time and space.

1.2.1 Post-embryonic development

Very few arthropods hatch from an egg as a full grown adult. Usually there are larval stages, and the larvae are, with very few exceptions (eg, the tsetse fly), much smaller in body size than the adults. The photoreceptors, too, are smaller, or of a completely different type from those of the adult. Insects, which are of the hemi- or holometabolous type, with a partial or a complete metamorphosis, respectively, may possess only compound eyes or ocelli in their larval life, but usually ocelli and compound eyes together as adults. Crustaceans, with a different type of metamorphosis than that of the insects, often have a nauplius eye during the larval phase and a compound eye or both when adult. This means, that with each molt (ecdysis) an arthropod photoreceptor has to undergo some change to better serve the newly molted animal (Maldonado et al. 1974, Kral 1998). In the case of praying mantises, for example, the forelegs, which the mantis uses for catching prey, increase in length with each ecdysis. The compound eye structure, too, has to change and adjust to match the enlarged brain and the new dimensions of the body (Maldonado et al. 1974, Kral 1998). Quite often, the larvae and the adults occupy completely different habitats, as, for example, with dragonflies, in which the larvae live in water and the adults fly in the air, or flesh flies, whose larvae live inside their food source, eg, meat, and the adults fly about in search of sugary food. When a larva turns into an adult and changes its habitat, its eye has to accommodate itself to this change. The same kind of compound eye design may not function satisfactorily in both water and air. In crustaceans, larvae and adults quite often share the same environment, water, but sometimes the larvae may be reared under the female’s abdomen and so be prevented from seeing much and at the same time be protected from light-induced damage. Another change that influences the eye of a growing animal is that the larger the eyes and the facets, the easier they can be damaged by light as more light (especially the 25 energy-rich UV-rays) can enter the photoreceptors. This problem can be overcome by protecting the eye better either by a more efficient light adaptation system or by the animal becoming more and more nocturnal – and thus light-avoiding – as it grows (Meyer- Rochow 1975). When considering post-embryonic development, dragonfly compound eyes are probably one of the best-studied photoreceptive organs in insects (if not the very best), (Prit- chard 1966, Lerum 1968, Sherk 1977, 1978a,b,c, Sakamoto et al. 1998). Unfortunately, most of these studies only describe how the surface of the compound eye changes (morphological changes), where the new ommatidia are added etc., and not what happens to the inner structure of the compound eye. In several studies, Such (1969, 1975, 1978) deals with the embryonic growth of the eye in a stick insect and Friedrich and coauthors (1996) with the flour beetle’s eye embryology, while Lerum (1968) and Rafi and Burtt (1974) occupy themselves with the postembryonic development in the dragonflies and Ortho- ptera (respectively). Warrant and coauthors (1990) studied dung beetle photoreceptor maturation as a function of age following adult ecdysis. The eye of the fruit fly, Droso- phila melanogaster has, of course, also attracted a great deal of attention [for example, a thorough handbook of D. melanogaster development with a detailed chapter on the development of the compound eye, edited by Bate & Arias (1993) exists]. A massive and voluminous treatise by Bernard, from as early as 1937, deals with the postembryonic changes involving the compound eyes’ structural changes in as many as 47 insect and crustacean species. Unfortunately, (for me) this rare light-microscopic study is written in French, but luckily the illustrations are very detailed. By examining the figures and the tables, it is easy to see that great developmental changes take place in the eyes of many of the species before the adult state is reached and that the individual ommatidia gain both in length and width during the process. Another good review con- cerns the development of the structure and especially the neural connections in the fly compound eye (Trujillo-Cenós 1985). Crustaceans, on the other hand, have yielded a greater sample of postembryonic studies concerning structural changes of the photoreceptors (for example, Bernard 1937, Pea- body 1939, Elofsson 1966b, Dudley 1969, Meyer-Rochow 1975, Hafner et al. 1982a, Fin- cham 1984, 1988, Tokarski & Hafner 1984, Nilsson et al. 1986, Eguchi et al. 1989, Meyer-Rochow et al. 1990, Takenaka et al. 1993, Hafner & Tokarski 2001, Zupo & Butt- ino 2001). All of these studies have proven that the size of the photoreceptor cells increases with the increase in the number of ommatidia as the animal grows, and in some cases, the compound eye changes from the apposition to the superposition type (Meyer- Rochow 1975, Fincham 1984, Nilsson et al. 1986, Douglas & Forward 1989, Gaten & Herring 1995, for a review, see Harzsch 2001). This means, that even though the morphological changes in a crustacean body may not be as fundamental as in a metamorphosing insect, the structure of the eye is no less affected during molts.

1.2.2 Light/dark adaptation

In addition to the long-term changes that take place in an eye in the course of the animal’s growth, a wide variety of short-term adaptations to differing light conditions may 26 take place in insect and crustacean eyes every day. These structural changes aim to protect the eye against light-induced damage in bright light, and increase the eye’s sensitivity at the cost of acuity in dimly lit environments (Fig. 2). Light adaptational changes may take minutes or may be slow and occupy hours. The slower changes are quite often induced by the animal’s inner circadian clock and depend less on the ambient light level, as, for example, in Ligia exotica (Hariyama et al. 1986, 2001, Hariyama & Tsukahara 1992, see also the reviews on circadian rhythms by Aréchiga 1993 and Green 1998, and the studies on insect circadian clocks by Giebultowicz 1999 and crustacean clocks by Aréchiga et al. 1993). In the fishlice, on the other hand, at least some of the changes are exogenously regulated (I) and can take place in a matter of seconds (changes in ambient light intensity: a cloud covering up the sun, the animal entering a shady place etc.). The only arthropods that are apparently not affected by fluctuations of the ambient light environment are those living in the deep sea, caves, underground or burrowed in a substrate (Meyer-Rochow 1999b, Meyer-Rochow & Nilsson 1999). A number of excellent reviews have been published on the functional and anatomical consequences of the arthropod eye’s ability to adapt to dark and light environments: cf, Autrum 1981, Meyer-Rochow 1999b, 2001, to mention just three of the more comprehensive ones. A recent book by Land and Nilsson (2001) covers all invertebrate as well as vertebrate eyes. All the authors who have studied the light/dark adaptational changes in an arthropod photoreceptor agree that a number of basic common adjustments occur in both crustaceans and insects (Fig. 2). In bright light, the pigment granules are aggregated around the rhabdom and the cone to shield the photoreceptive membranes from too intense a light. In superposition eyes, the pigment granules are often translocated into the clear zone to cut off the oblique rays. In the light adapted condition, a superposition eye may almost function like an apposition type of eye (for example, Nicol & Yan 1982, Nilsson 1983). In darkness, the pigment granules move peripherally in the retinula cell as well as the pigment cells to let the photoreceptive membranes catch as many of the arriving photons as possible. For the same reason, the palisades around the rhabdom often widen. In darkness, the rhabdom frequently increases in both diameter and length, thereby increasing the volume of the photoreceptive membrane. There may also be changes in the sizes or the shapes of the cones (Meyer-Rochow 1974, Meyer-Rochow & Waldvogel 1979, Nilsson & Odselius 1981, Vivroux & Schönenberger 1981), some cellular organelles, or even in the cuticle thickness and shape (Meyer-Rochow & Waldvogel 1979, Tsutsumi et al. 1981, Toh & Waterman 1982, Doughtie & Rao 1984, Frixione & Porter 1986, Gokan et al. 1987, Martin et al. 2000). Some of the structures may be controlled endogenously, while others are affected by ambient light (see above). The screening pigments present in the retinula cells of the compound eyes in Argulus foliaceus and A. coregoni (I) and in Ligia exotica (Hariyama et al. 1986) were found to be under a circadian control, but the small screening pigments between the two adjacent crystalline cones in Argulus foliaceus and A. coregoni, which exhibited migrations according to ambient light condition and not the time of day, were not (I). On the other hand, even in continuous darkness (but fixed at noon), the rhabdomeric microvilli in L. exotica were arranged as if in a normal dark- adapted night animal (Hariyama et al. 1986, 2001). Ambient light or time of day (circadian clock) are still not the only factors that may trigger the photoreceptor’s structural adaptations. For example, high temperature may 27 sometimes mimic environmental light so that the photoreceptor turns from dark-adapted to a light-adapted condition even in complete darkness (Meyer-Rochow & Tiang 1979, 1982, Nordström & Warrant 2000). In the moth Ephestia kuehniella, light-induced adaptation took place in the temperature range from +5°C to +37°C, but in temperatures colder or warmer than this, the screening pigments were always in the dispersed, i.e., dark- adapted, position (Weyrauther 1988). Unusual amounts of nitrogen and carbon dioxide have also been shown to affect the light-mediated changes in the photoreceptors (Banis- ter & White 1987).

1.2.3 Sex

In many species of arthropods, the compound eyes are different in the two sexes (Bêle- hrádek & Huxley 1930, Bernard 1937, Segerstråle 1937, Horridge & McLean 1978, Hor- ridge et al. 1982, Gupta et al. 2000, and some additional older papers in German by authors mentioned in Gupta et al. 2000). The difference can be related to the size of the eye, as, for example, in Gammarus chevreuxi (Bêlehrádek & Huxley 1930) and in various species in Bernard’s study (1937), or the morphology, as in a baetid mayfly Cloeon sp., where the lateral compound eyes are different in the males and the females (Gupta et al. 2000). Sexual dimorphism in arthropods arises from the different visual needs of the two sexes: for example, while the mayfly female wants to find oviposition sites on the water, the male needs to find only a female and track her down against the sky (Gupta et al. 2000). Sexual dimorphism seems to be more common among the insects than in the crustaceans, and quite often differences between male and female photoreceptors can simply be explained by a difference in size between the two sexes.

1.3 Light-induced photoreceptor damage

An arthropod photoreceptor may be damaged in a variety of ways. The eye can be harmed by physical injury (hitting or scraping the eye somehow, getting attacked by a predator, incomplete molting, disease or a fungal attack etc.) or radiation (ionic, photic, thermal). I will briefly consider photoreceptor damage due to photic radiation (light). These matters, especially concerning the crustacean eye, have recently been reviewed by Meyer-Rochow (1994, 2001). Photoreceptor damage may sometimes be difficult to distinguish from normal, light/ dark adaptational phenomena. After all, it may be hard to draw the line between a still harmless but extremely brightly lit environment and the amount or quality of light that is already causing damage. If an animal with dark adapted eyes would be left uncovered to witness a sunrise, its eyes would have time to adjust to the changing light environment and to translocate pigment granules into the light adapted positions, but in the case in which the specimen could not cope well with direct, intense or long-term sunlight, its eyes would slowly cross from light-adaptation to light-induced damage. 28

In most cases, and most notably, the damage manifests itself ultrastructurally by dis- rupting membranes in the retinula cells (Horridge et al. 1981, Eguchi & Meyer-Rochow 1983, Nilsson & Lindström 1983, Shelton et al. 1985, Chamberlain et al. 1986, Rosen- berg & Langer 1995, Kashiwagi et al. 1997, Wakakuwa et al. 1997, Meyer-Rochow 2001, Meyer-Rochow et al. 2002), but many other injuries may be found in addition to that (Gaten 1988). The most serious part of the membrane damage, in the short run, is the dis- ruption (swelling, dislocation and break-up) of the photoreceptive membranes, the microvilli. This will quickly impair the photoreceptor’s performance, since fewer photopigment molecules can be held in the damaged membranes and ion-leakages occur. Dis- ruption of photoreceptive membranes may just as well be induced by sudden temperature elevation. This is the case in the compound eye of the crayfish Procambarus clarkii when cold (+4°C) and dark-adapted animals are suddenly exposed to bright light and a high water temperature (+25°C): light alone does not cause as much damage to the photic membranes as the light with the abnormally high temperature together (Kashiwagi et al. 1997). Light-induced damage can be avoided through behavioral reactions (hiding or shelter- ing from harmful amounts of light, being active at night) as well as by changing the eye to a light-adapted position and/or through changes in the membranes’ lipid composition, but the latter changes require time, often weeks and sometimes months (Kashiwagi et al. 1997, Meyer-Rochow et al. 1999).

1.4 Aims of this study

As can be seen from chapter 1.2., an arthropod photoreceptor is a very versatile structure that not only changes daily in concert with the environmental brightness and temperature, but is also different depending on sex and developmental status of the animal. This is why, when studying an arthropod photoreceptor, age/developmental state, sex and time of day, as well as the laboratory conditions, all have to be carefully considered. In many arthropod species, most pronouncedly in insects, the adult represents only a very short-time state of the whole life history of the species: the most extreme examples are the stone- and the mayflies, which in Finland may spend years as aquatic larvae and only hours or days as flying adults. Especially in these kinds of cases, it should be carefully considered whether a larval or an adult eye is used in the investigation. At the least, all possible information about the studied species should be given in a report on eye structure. A review and a study by Meyer-Rochow and Reid 1996, states that the age of a crustacean under investigation can be an issue when studying the photoreceptor structure. In their paper, Meyer-Rochow and Reid list 50 randomly chosen publications on crustacean photoreceptors, and what information, if any, in addition to the species was given with regard to the specimen. The two authors also show that the microvillar diameters (at least in Petrolisthes elongatus) depend on the age (size) of the crabs. This shows, that the information given in publications is often inadequate, or only applicable to the eyes of a small portion of the whole population of a species and its life history. Expanding from Meyer-Rochow and Reid’s paper, I randomly chose 40 insect (Table 1) and 40 crustacean (Table 2) compound eye fine structural publications and 14 crusta- 29 cean nauplius eye structural papers (Table 3), and inspected their “Materials and methods” sections. Surprisingly, only little more than half of the total number of authors (56/94) give any information beyond the name of the species studied, even though it is known, that the arthropod photoreceptor organization may depend on a variety of factors. Sixteen insect (40 %) and 13 crustacean (32.5 %) compound eye studies out of the 80 investigated and 9 out of 14 (64 %) nauplius eye investigations did not give any information about the studied animals other than the name of the species. About half of the publications in both arthropod categories mention the developmental state of the studied animals (larva, adult, mature). Sex was mentioned more often in insect studies (in 37.5 % of the papers) than in the crustacean studies (only 4 papers or 10 % of the compound eye papers and 3 out of the 14 or 21 % of the nauplius eye papers). This may be a conse- quence of the more wide-spread sexual dimorphism in insects. None of the studied insect species were weighed or measured, while as many as 15 crustacean species got their body/carapace length/width measured, and one got weighed. This difference is most probably due to the fact that while the insects go through successive metamorphoses, which can usually be quite easily distinguished from each other and correlated with the age/ developmental state of the animal, many of the crustaceans keep molting for the rest of their adult lives and successive developmental stages resemble each other in everything but size. The insect papers, on the other hand, mention the age of the studied animals more often (6/40) than the crustacean investigations (4/54). The insect studies scanned for these details were from the years 1966–2002 and the crustacean studies covered the period from 1939–2003. The publication year did not indicate the number of the given details about the species: the 16 insect papers with no information other than the name of the studied species were published between 1983–1998 and the comparable crustacean papers between 1963–2000. Some of the earliest as well as the latest papers give some of the details in question. 30

Table 1. Specimen information given in 40 randomly chosen publications of insect compound eye structure. ”+” = information available.

Authors in alphabetical order Specimen details Larva Adult Mature Age Size Weight Sex Bandai and coauthors (1992) – + – + – – + Brammer (1970) – + – + – – – Buschbeck and coauthors (1999)––––––+ Buschbeck and coauthors (2003) – + – + – – + Dacke and coauthors (2002)–+––––+ Eguchi and Meyer-Rochow (1983) ––––––– Friedrich and coauthors (1996) + – – + – – – Gokan (1998) ––––––– Gokan and coauthors (1987)––––––+ Gokan and Masuda (1998) ––––––+ Gokan and Meyer-Rochow (1984)––––––– Gokan and Meyer-Rochow (1990)––––––– Grünevald and Wunderer (1996) ––––––– Homberg and Paech (2002)–+––––+ Kolb (1986) ––––––– Kral and coauthors (1990) ––––––+ Land and coauthors (1997)––––––– Land and coauthors (1999)––––––– Lin and coauthors (1992) ––––––+ McIntyre and Caveney (1998)––––––– Meyer-Rochow (1974) –+––––– Meyer-Rochow (1978a) ––+–––– Meyer-Rochow and Gokan (1987)––––––+ Meyer-Rochow and Gokan (1988a)––––––– Meyer-Rochow and Gokan (1988b) ––––––– Meyer-Rochow and coauthors (2002) ––––––– Meyer-Rochow and Waldvogel (1979) + + ––––– Miskimen and Rodriguez (1981) – + – + – – – Nagashima (1990) – + ––––+ Nagashima and Meyer-Rochow (1995) – + ––––+ Nagashima and Senoh (1990)––––––– Pritchard (1966) + + ––––– Qiu and coauthors (2002) – + – + – – + Sakamoto and coauthors (1998) + + ––––– Smith and Butler (1991) ––––––– Stavenga and coauthors (1990) ––––––+ Wakakuwa and coauthors (1997) ––––––– Warrant and coauthors (1990)––––––– Weber and coauthors (1996)––––––– Yang and coauthors (1998) ––––––+ 31

Table 2. Specimen information given in 40 randomly chosen publications of crustacean compound eye structure. ”+” = information available.

Authors in alphabetical order Specimen details Larva Adult Mature Age Size Weight Sex Andersson (1979) – + – – – – + Ball (1977) – – – – – – – Bursey (1975) – – + – – – – Chamberlain and coauthors (1986) – – – – – – – Denys and coauthors (1983) – – – – – – – Diersch and coauthors (1999) – – – – – – – Doughtie and Rao (1984) – – – – + – – Edwards (1969) – – – – – – – Eguchi and coauthors (1989) – – – – + – + Elofsson and Odselius (1975) – + – – – – – Gaten (1990) – + – – – – – Gaten and coauthors (1992) – – – – – – – Gaten and coauthors (2002) – – – – + – – Hafner and coauthors (1982a) + – – + + – – Hafner and Tokarski (2001) – + – – – – – Hallberg (1982) – + – – – – – Hariyama and coauthors (1986) – + – – + – + Krebs (1972) – – – – – – – Lakin and coauthors (1997) – – – – – – – Marshall and coauthors (1991) – – – – – – – Meyer-Rochow (1975) + + – – – – – Meyer-Rochow (1978b) – – – – + – – Meyer-Rochow (1981) – – – – + – – Meyer-Rochow (1982) – – – – + – – Meyer-Rochow (1985) – + – – – – – Meyer-Rochow and coauthors (1990) – – – – + – + Meyer-Rochow and Juberthie-Jupeau (1983) – + – – + – – Meyer-Rochow and Juberthie-Jupeau (1987) – + – – + – – Meyer-Rochow and Tiang (1979) – – – – + – – Meyer-Rochow and Walsh (1977) – – – – – – – Meyer-Rochow and Walsh (1978) – – – – – – – Nemanic (1975) – + – – – – – Nicol and Yan (1982) – – – – + + – Nilsson (1978) – + – – – – – Nilsson et al (1986) + + – – – – – Odselius (1980) – – – – – – – Peabody (1939) + + – – + – – Rosenberg and Langer (1995) – + – – – – – Schiff and Handrickx (1997) – – – – – – – Tokarski and Hafner (1984) – – – – + – – 32

Table 3. Specimen information given in 14 publications of crustacean nauplius eye structure. ”+” = information available.

Authors in alphabetical order Specimen details Larva Adult Mature Age Size Weight Sex Andersson (1979) – + – – – – + Andersson and Nilsson (1979) – + – – – – + Dudley (1999) ++++––+ Elofsson (1963) – – – –––– Elofsson (1965) – – – –––– Elofsson (1966a) – – – –––– Elfsson (1966b) + + – + – – – Elofsson (1999) – – – –––– Fahrenbach (1964) ––––––– Martin and coauthors (2000)––––––– Meyer-Rochow (1999a) – – – –––– Ong (1970) – – – –––– Takenaka and coauthors (1993) + + – + – – – Wolken and Florida (1999) – – – ––––

The aim of this study, thus, was to investigate the influence of sex, developmental state and time of day (or ambient light level) on arthropod photoreceptors. Since structural understanding is the basis for an appreciation of function, I focused my study on structural changes only. Three sample species were selected to represent the crustaceans (Argu- lus foliaceus, A. coregoni, Ligia exotica) and two for the insects (Carausius morosus, Philaenus spumarius). 2 Materials and methods

2.1 Study species

a) The Crustacean species The fishlice Argulus foliaceus and A. coregoni (Crustacea, Branchiura) are aquatic ecto- parasites which attach themselves temporarily to fish, crustaceans and larger amphipods to suck the hosts’ blood. Many of the host species, for example carps and various species of salmonids, are commercially bread in fish farms where infections of fishlice may cause considerable financial losses (Hakalahti &Valtonen 2003). Argulus species can be found living in fresh, brackish and salt water bodies (Aagaard 1978, Økland 1985, Pasternak et al. 2000, Mikheev et al. 2001). The eggs overwinter and hatch in spring (Aagaard 1978, Pasternak et al. 2000, Mikheev et al. 2001) and the newly emerged metanauplius larvae have to find a host in the first two days (Mikheev et al. 1998). The fishlice detect their potential host using vision under sufficient illumination (Mikheev et al. 1998, Mikheev et al. 2001), although chemical and tactile senses may play an important role during a state of hunger and in the absence of light (Galarowicz & Cochran 1991, Mikheev et al. 1998, Mikheev et al. 2001). Argulus spp. were selected as crustacean study species because they are easily available from fish farms, they are commercially important, they represent the only fully aquatic species in this thesis and they possess nauplius eyes in addition to compound eyes (Madsen 1964, Shimura 1981, Rushton-Mellor & Boxhall 1994). Ligia exotica (Crustacea, Isopoda), the seaslater or the ‘funamushi’ in Japanese, is a semi-terrestrial crustacean, which inhabits rocky shores and beaches along the coast of Japan. These 0.3–4 cm long isopods are diurnal and bask on boulders in the sun, but seek to hide when they sense the slightest hint of danger. They have keen eyesight and are agile and alert, which makes catching them a difficult task. L. exotica is mainly terrestrial, but if, by accident, it happens to fall off a cliff or a boulder and land in water, it can sur- vive and feed for at least 14 days submersed (Taylor & Carefoot 1990). The larvae are reared in a marsupium under the female’s abdomen. The larvae have six pairs of legs, compared with the seven pairs of the young adults, which are ready to leave the marsupium. The adults increase in size and keep molting for the rest of their lives. 34

L. exotica was selected as a crustacean study species because of its availability and the large background information about its photoreception (Sharma 1982, Hariyama et al. 1986, 1993, 2001, Hariyama & Tsukahara 1992). These isopods are also easy to handle, their compound eyes are large and distinct, and vision is obviously very important to them (Taylor & Carefoot 1990). b) The insect species The stick insect Carausius morosus (Phasmida, Phasmatidae) is a common representa- tive of phasmids, which inhabits almost all terrestrial habitats on the globe with the exception of the most northern and southern regions. Stick insects are herbivores that feed on almost any green vegetation that is offered to them. C. morosus is a widely used laboratory species and a pet, probably due to its easy rearing and parthenogenetical mode of reproduction. Males are encountered extremely rarely (Clark 1976). Diurnal 1 cm larvae molt 5 to 6 times and finally reach the body length of about 8 cm as nocturnal adults (Godden 1973). C. morosus was selected as an insect study species because it is easy to rear in the laboratory and its compound eyes are large and easy to handle, it has been shown to use its vision (Jander & Volk-Heinrichs 1970, Frantsevich & Frantsevich 1996) and it possesses compound eyes from the first instar (Such 1969, 1975, 1978) to adulthood. It also resembles L. exotica in that the young, even though they are nymphs, look like the adult specimens, whereas the fishlice larvae do not resemble adults until after the 8th or the 9th molt (Rushton-Mellor & Boxshall 1994). The meadow spittle bug Philaenus spumarius (Homoptera, Cercopidae) is a wide- spread insect species which lives in most terrestrial habitats throughout the whole world (Zimmerman 1948, cited in Quartau & Borges 1997, Thompson & Halkka 1973, Archibald et al. 1979, Thompson 1984, Halkka & Halkka 1990, Quartau et al. 1992). The female spittle bug lays its eggs on a suitable plant or in a litter in autumn and the eggs hatch in the spring (Halkka et al. 1967). The nymphs feed on plant sap and produce a protecting bubble nest around them as a by-product. The nymphs spend the first few weeks of their lives inside the foamy spit bubble which they leave when they molt into adults (Halkka et al. 1967). The spittle bug was selected as the second insect study species because it is widely available at any forest or road edge throughout the whole of Finland, the nymphs are easy to handle and to take to the laboratory together with their host plants, and because the spittle bug’s lifestyle differs from that of the stick insect. While the spittle bug nymphs spend the first part of their lives in a completely different environment (spit bubble) compared to the adults (air), the stick insect young and adults share the same “leafy” environment. Also, while L. exotica and the stick insect only molt but do not metamorphose, the fishlice and the spittle bug larvae and adults differ from each other. These five arthropod species were thought to represent 1) a wide variety of ecological lifestyles (terrestrial, semi-terrestrial, aquatic), 2) post-embryonic metamorphic stages (fishlouse metanauplius-larvae and meadow spittle bug nymphs which differ from the adult body form and L. exotica and the stick insect, which already resemble small adults as young) and 3) environmental differences during post-embryonic development (spittle bug nymphs live in the spit bubble and the adults without it, while in the other species examined, the young and the adults share the same environment). 35 2.2 Collecting sites, treatment and measuring

Juvenile and adult fishlice and their eggs were obtained from fishfarms in Central Fin- land. Adult fishlice for investigation I (A. foliaceus and A. coregoni) were transported to Oulu University, Finland, in spacious containers together with their host fish at +4°C. The fishlice were kept at 12 : 12 light : dark environment and decapitated and immersed in the first fixative solution at noon (light-adapted) or at night (dark-adapted) within the first 30 hours after the arrival (I). Juvenile and adult A. coregoni for investigation VI were collected from the fish and decapitated and prefixed in situ at noon. A. coregoni eggs were kept in spacious containers at 12:12 light:dark environment until the metanauplius larvae started to hatch. The metanauplii were introduced into the first fixative solution at noon (light-adapted) or at midnight (dark-adapted) during the first 24 hours after their emergence (VI). All specimens were identified, measured with a ruler and sexed under a dissection microscope. The measurements that were taken are summarized in Table 4. L. exotica were collected by hand at low tide at noon in Shiogama (Miyagi Prefecture, Japan: II) and Yokohama (Japan: III), from where they were transported to the laboratory of Tohoku University in Sendai, Japan. Transportation took place in covered plastic containers, in which the temperature never exceeded +25°C. For approximately one week after capture and prior to the experiments, the animals were kept in spacious containers in a regular light environment (12 h light:12 h dark) at a constant temperature of +24°C. During this time they were fed commercially available dry pellets of insect food. At noon, after one week of regular day/night periodicity in the laboratory, the L. exotica were externally sexed, measured and weighed (II and III). They were then decapitated and their eyes were fixed for further studies. For the measurements taken, see Table 4. Young and adult stick insects were obtained from two different pet populations (IV). They were kept in spacious containers with seasonally available greenery in a constant 12:12 light:dark environment at approximately +20°C. Two days prior to fixation, one container was transported to the laboratory under constant (24 h) light and another under constant (24 h) darkness. In all three light treatments, the animals were decapitated and measured at noon (12.00) and at midnight (24.00) and their heads were fixed for further studies. Stick insects are all female (Clark 1976), so there was no need to sex the animals. Measurements that were taken are listed in Table 4. Spittle bug larvae and adults were collected during the month of July from forest edges in north Finland (V). Some were decapitated in situ at noon (12.00 light-adapted) or at midnight (24.00 dark-adapted) in temperatures between +15°–+25°C, measured and their heads were immersed in the pre-fixative solution. Some specimens were transported to the laboratories with their host plants and left for 24 hours at either constant light or darkness at approximately +20°C. Spittle bugs from both light treatments were decapitated at noon or at midnight, measured and their heads were kept in the pre-fixative solution. All P. spumarius nymphs and adults were later sexed under a dissection microscope (V). The measurements that were taken are summarized in Table 4. Measurements of the photoreceptor structures were either taken directly with a computer attached to the microscope (IV), photographed and measured by hand, or printed with the help of a computer program from microscopic samples and then measured by hand (I–VI). 36

Table 4. Measures that were taken in the original papers (I–VI). I and VI concern Argulus sp., II and III L. exotica, IV stick insect C. morosus and V meadow spittle bug P. spumarius. + = this measurement was taken in the original paper I–VI.

Measurements Original papers I II III IV V VI Body length + + + + + + Nauplius eye diameter + Compound eye diameter + + + + + Number of ommatidia + + + + + Facet diameter + + + Ommatidium diameter + + + + + Ommatidium area + Length of dioptric structure + Cornea thickness + + Cone length + + + + Cone width + + + Retina length ++++++ Rhabdom diameter + + + + Microvilli diameter + + + + + Visual angle + Interommatidial angle + + + + + Pigment percentage (for explanation, see III) + Pigment granule number + Pigment grain diameter + + + + Miscellaneous (mitochondria, nuclei, other cells etc.) + +

2.3 Statistical methods

The statistical methods that were employed were the Independent samples t-test (to test differences between two groups, III), R2 correlation coefficients for Pearson’s least- squares fit (to test how well the measurements fit the regression line, II, IV, V and VI) and ANCOVA (Analysis of Covariance), which tests, whether there are any differences between two groups which are both affected by a common factor, in this case the animal’s body size. The latter test removes the effect of a common factor (IV, V). All statistical analyses were performed with a computer statistical program SPSS. Used levels of significance were p<0.001 = highly significant ***, p<0.01 = significant ** and p<0.05 = barely significant *. 37 2.4 Fixation procedures

2.4.1 Samples for light microscopy (LM)

For LM, specimens were decapitated in the prefixative solution (2 % paraformaldehyde and 2 % glutaraldehyde in 0.1 M sodium cacodylate at pH 7.4: I, II, III and IV; 4 % paraformaldehyde and 1 % glutaraldehyde at pH 7.4: V, VI). The eyes were surgically removed from the head with a sharp razor blade and kept in ice-cold prefixative solution overnight. The surface of the intact eyes in II was then observed with LM (Nikon FX) by epi (=orthrodromic) illumination. Following the first fixative solution, the samples were rinsed three times for 10 minutes with phosphate buffer and fixed in ice-cold 2 % buff- ered OsO4 for 1 h (I) or 2 h (II–VI). After rinsing the samples for another three times for about 10 minutes (II–VI) or 15 minutes (I) in distilled water, they were dehydrated in a graded series of ethanol and finally immersed twice for 10 minutes in propylene oxide. The samples were embedded in 100 % Epon after passing through a graded series of Epon. The blocks were dried at +60°C in an oven for about 2 days. Semithin sections were cut with a glass knife on an ultramicrotome and stained for a few seconds up to a minute in an aqueous solution of 1 % toluidine blue. The samples were then observed under a light microscope.

2.4.2 Samples for transmission electron microscopy (TEM)

Embedded and dried blocks were cut with an ultramicrotome with a glass or a diamond knife and ‘silver’ sections were picked up on coated copper mesh grids (I, III, IV, V, VI). The samples were then stained in 2 % uranyl acetate, washed in distilled water, stained again in 0.4 % lead citrate and then washed again. After letting the grids dry, the sections were observed under a transmission electron microscope at 60 kV accelerating voltage and either photographed or measured directly with a computer attached to the microscope.

2.4.3 Samples for scanning electron microscopy (SEM)

L. exotica samples for SEM comprised surgically removed eyes immersed in 0.1 M phosphate buffer (pH 7.2), which were then fixed for 2 h in 2.5 % glutaraldehyde in 0.1 M sodium cacodylate (pH 7.2) (II). The preparations were then rinsed three times for 10 min in 0.1 M phosphate buffer and dehydrated in a graded series of ethanol. After immersing the preparations in isoamyl acetate, they were dried with a critical point drying apparatus, attached to a metal plate, and ion-coated with white-gold vapor (Eico ion coater IB- 3). The samples were then observed with a Hitatchi S-430 scanning electron microscope, operated at an accelerating voltage of 20 kV. To observe the longitudinal and inner orga- 38 nization of the compound eye, some of the preparations, after fixation, were frozen with liquid nitrogen, split longitudinally with a razor blade to reveal the interior architecture, and dried and ion-coated like the rest of the samples. C. morosus samples for SEM observations consisted of specimens that had died and which were left to dry in air, after which they were attached to a metal plate, ion-coated with gold-palladium and observed under a scanning electron microscope like the earlier- mentioned specimens (IV). Spittle bug SEM samples were selected from the pre-fixed samples, washed in distilled water, dehydrated in a graded series of ethanol and dried in a critical point dryer (V). The samples were attached to aluminium stubs, coated with gold-palladium and observed with the scanning electron microscope. Measurements were taken from printed images in all three studies involving SEM (II, IV, V, Table 4). 3 Results

3.1 Morphological observations

All terrestrial or semi-terrestrial study species were found to have sessile, faceted compound eyes positioned laterally on both sides of the head (II, III, IV, V). Fishlice compound eyes were positioned more dorsally and it was confirmed that they were surrounded by haemocoelic liquid (I, VI). The hexagonal ommatidial lattice in L. exotica, P. sp u- marius and adult C. morosus was found to be very regular with no specialized foveas or other areas of differentiated facets, except for the extreme marginal areas in L. exotica, where the ommatidia were found to be smaller and sometimes forming incomplete hexagons (II and III). The same was true in the nymphal spittle bugs (V). In the larger C. morosus, a horizontal pigmented stripe of dark brownish coloration ran across the eye in an antero-posterior direction (IV) while L. exotica and P. spumarius eyes were uniformly black or brown, respectively (II, III, V). The ommatidial lattice in immature stick insects was not as regular as in adults, but varied from almost circular facets to pentagons and hexagons (IV). Spittle bug nymph facets were always circular in outline even though the facets of the adult were more or less hexagonal (V). The C. morosus cornea was smooth (IV), while that of L. exotica had tiny 0.5 µm high corneal nipples (Hariyama et al. 1986), as did the adult spittle bug eye as well (V). Corneal nipples form an anti-reflection coating on the surface of, for example, moth and butterfly compound eyes (Land 1985). This coating may function as a camou- flage during the day, improve transmission, or suppress the reflections from the tapetum, if it is present, inside the eye (Miller 1979, cited in Land 1985). 3–10 µm long interommatidial hairs and holes were found in the adult spittle bug eyes (V). Nymphs that were ready to molt into adults had few short hairs on their eyes (V). Fishlice adults measured 10–12 mm (I, VI) and the newly hatched metanauplius larvae only 0.6 mm (VI). L. exotica’s body lengths varied from approximately 0.5 cm to 4 cm (II), while the stick insect specimens varied from 1.2 cm in the first instars to 8 cm as adults (IV) and the spittle bugs from 2–8 mm in total body length (V). In all species, the general shape of the compound eye stayed approximately the same during the whole post- embryonic growth period, with the antero-posterior and the dorso-ventral dimensions (II 40 and IV) or the diameter (V, VI) growing at a comparable pace. In both study species that only molt and grow larger but do not otherwise metamorphose (L. exotica and the stick insect), the body lengths increased about eight fold while the eye dimensions increased about three fold (II and IV). Also the total number of ommatidia increased about two fold in both L. exotica and the stick insect (II and IV). Facet diameters in L. exotica and the stick insect were about two times greater in the adults of both species when compared with those of the smaller instars (for exact measures, see II and IV). Spittle bugs, on the other hand, had larger eyes (dorso-ventral axis) as 7 or 8 mm adults than as a nymph of corresponding body length (V). The same held true for the spittle bug facets as well: all adults had larger facets than the nymphs even though their body lengths were the same (V). In the fishlouse A. coregoni the body length increased to about 20-fold while the compound eye diameter grew approximately 10-fold (VI). The A. coregoni nauplius eye grew about 4-fold in diameter from the metanauplius larva to an adult (VI). The nauplius eye of A. coregoni comprised two lateral ocelli and one anterior ocellus, which in the adult were all circular in outline (VI). In the metanauplius, the lateral ocelli were found to be considerably more elongated and protruding out of the central pigment cups. The elongated, lateral ocelli turned into the circular adult ocelli at some point between the metanauplius and the 8th larval stage at 3 mm body length (VI).

3.2 Anatomical features of the compound eyes

3.2.1 General organization

Ommatidia in the middle of the eye in all study species were found to be the largest in the whole eye and seemingly mature (I–VI), instead of the irregular, smaller and obviously not fully differentiated and, thus, immature ommatidia found around the edges of, for example, the compound eye in L. exotica (III). The marginal ommatidial facets in the insect study species’ larval compound eyes were sometimes incomplete as well (IV, V). Adult facets were complete hexagons even at the margins of the eye, but their ultrastructure was not investigated. In the compound eyes of the fishlice the marginal ommatidia were much smaller than the central, seemingly mature ommatidia (VI). The basic structure of an ommatidium described here refers to the mature, centrally-placed ommatidia in all species. All of the studied species had apposition type compound eyes equipped with a cornea (except the fishlice, which had a thin epithelial layer covering the eye, I, VI), a cone (made up of four pigment-free cone cells) beneath it, and a retina proximal to the cone (I– VI). While the cone in all other species consisted of four equally sized cone cells (I, IV, V, VI), the crystalline cone in L. exotica consisted of two equally large and two very much smaller cone cells (II). With the exception of L. exotica, the rhabdoms were of the closed type with a varying number of rhabdomeres, formed by seven (IV) or eight (I, V, VI) retinula cells. In L. exotica, the rhabdom was closed only at the very distal tip, and open for the rest of the length of the retina (II and III). The L. exotica rhabdom consisted of six 41 rhabdomeres made up of seven retinula cells (II and III). At the proximal end of the retina, an eighth retinula cell with a large rhabdomere joined the rhabdom (Hariyama et al. 1986). In all species, the cone was surrounded by two primary pigment cells and by an unknown number of secondary pigment cells shielding the ommatidium from its neigh- bors (I–VI). Pigment cells, as well as the retinula cells, in all species contained organelles such as mitochondria, rough and smooth endoplasmic reticula, vesicular material, pigment granules etc. The microvillar diameters varied between 45 nm (stick insect, IV) and 55 nm in L. exotica (II, III) and the fishlice (I, VI). In all species, the rhabdomeres consisted of microvilli aligned uniformly in centrifugal directions away from the rhabdom’s central axis (II, IV, V, but see III) or in two orthogonal directions perpendicular to the direction of the light entering the facet (I, VI). In all species, during post-embryonic development, the structure of the ommatidia stayed rather constant with the individual structures growing quite isometrically (II, IV, V, VI). Interommatidial angles stayed approximately the same during the whole post-embryonic growth of the ‘funamushi’ L. exotica, the stick insect and the spittle bug, but in A. coregoni the interommatidial angle decreased from ca. 42° in the metanauplius to 13° in the adult. The growth or the structure of the eye were not found to be influenced in any way by gender in fishlice (I, VI), L. exotica (II) or the spittle bug (V), while C. morosus individuals are anyhow almost always entirely female (Clark 1976). An effect of sex, therefore, could not be investigated in the eye of this species, although it can be said, that since almost all the individuals in a stick insect population are female, the structure of the eye in that population should not vary. Stick insect males are encountered so rarely (Clark 1976), that even if the eye would be different, it represents an almost insignificant percentage of the overall eye structure variation encountered in a given population.

3.2.2 Light/dark adaptational changes

Since L. exotica’s light/dark adaptational changes have previously been studied by Hariyama and coauthors and published in 1986, 1992 and 2001, there seemed no need to concentrate on that aspect in these experiments. In all five study species, the pigment granules gathered around the rhabdom at noon in the light (Hariyama et al. 1986, I, IV, V, VI) to shield the photoreceptive membranes. In L. exotica, however, time of day was found to be more important than ambient illumination (Hariyama et al. 1986, 2001, Hariyama & Tsukahara 1992), but the situation in the stick insect was different and the illumination was a stronger factor (IV). The shapes of the closed rhabdoms in the stick insect and the spittle bug stayed roughly the same throughout changes in lighting, but the cross sectional area grew larger at night (IV, V). The normally open rhabdom of L. exotica, on the other hand, lost its open structure and resembled more that of a closed type rhabdom at night (Hariyama et al. 1986, 2001); furthermore, the microvilli in the rhabdomeres lost their regular alignment (see also III about the microvilli regularity). A slight 10 % increase in the rhabdom length and a correspondingly even greater increase in rhabdom volume was noticed in the adult fishlice in the dark adapted conditions (I). 42

Some of the most obvious changes in the light/dark adaptation were affected by the post-embryonic growth of the stick insect (IV). While the rhabdom diameter increased in darkness approximately the same amount in larvae and adult stick insects, the thickness of the retinal layer grew significantly more in large and adult C. morosus compared with small individuals. This means, that the light/dark adaptational changes were more pronounced in larger individuals. The situation was the opposite regard to the pigment granules aggregating around the rhabdom during the day: the larger the specimen, the less pronounced was the change between the noon and the midnight specimens (IV). In the spittle bug, the developmental state did not affect the magnitude of the light-mediated changes to any great extent (V).

3.3 Anatomical features of the nauplius eye

The fishlouse A. coregoni nauplius eye fine structure changed surprisingly little during the growth from a metanauplius larva to adult (VI). The largest change was noticed in the shape of the two lateral ocelli: in the metanauplius larval eye, the two ocelli were elongated and protruded far out of the pigment cups while in the larger fishlice, the nauplius eyes, i.e., all three ocelli, were circular. In the metanauplius larvae, the photoreceptor cell nuclei were much more elongated and situated in the protruding distal end of the cups, but in the adult fishlice, the nuclei were round or slightly oval in shape and situated in the distal hemisphere of the cups. No aggregated forms of endoplasmic reticulum (ER) were found in the metanauplius eyes, but from the 8th stage to adult, large stacks of rER and phaosomes were present in the middle and distal parts of the photoreceptor cells. The Golgi apparatus was not seen in the metanauplius eye. All mitochondria in the 1st stage larvae were full of cisternae and none of the half-empty mitochondria that were found in the pre-adult and adult eyes were found in the metanauplius. Microvillar diameters were approximately 71 nm and did not change during the post-embryonic development of the fishlouse. Also, the rhabdom organization stayed about the same throughout the development of the nauplius eye: in a longitudinal section through the rhabdom hemisphere of the ocelli, the rhabdoms resembled thin sausages in an orderly row and in transverse sections, the rhabdoms formed a meshwork, in which all retinula cells were surrounded by approximately six other cells (VI).

3.4 Accretion of new ommatidia in L. exotica

While all the ommatidia in the middle parts of the compound eyes in L. exotica were found to be mature, of full length and size, and equipped with six regular rhabdomeres (II and III), ommatidia around all edges of the eye were found to be either smaller or to consist of very different numbers of rhabdomeres and other organelles (III). Ommatidia around the posterior and the dorsal marginal areas resembled those in the middle regions of the eye with the exception that they were significantly smaller. All the six rhabdomeres and seven retinula cells were present, with the normal assemblage of cell organelles 43 and pigment granules, but with variable retinal thickness instead of the long, mature retina in the middle of the eye. In the anterior and ventral marginal areas of the compound eye, the number of rhabdomeres per one ommatidium was found to vary between 0 and 6, with very irregularly aligned microvilli that did not point toward the center of the rhabdom as in the mature ommatidia. Pigment granules started to appear and to aggregate around the rhabdom as soon as any of the microvilli were present. Microvillar diameters were found to be constant in all parts of the small L. exotica eye, but to be significantly smaller in the central regions of the middle-sized and large animals (III). 4 Discussion

From the moment the arthropods first appeared on the face of the Earth, they seem to have occupied almost all imaginable environments on the planet. This has created an enormous challenge with regard to the light-sensing organs. Every environment has its specific photic conditions, and the species that occupy them must have adjusted their photoreceptors accordingly. In many arthropods variations in photoreceptor structure cor- relate well with the depth of the water they occupy (Elofsson & Hallberg 1977, Hiller- Adams & Case 1984, 1988, Schiff et al. 1986, Land 1989, Gaten et al. 1990, 1992, Shel- ton et al. 1992, Cronin et al. 1994, O’Neill et al. 1995, Nuckley et al. 1996, Frank 1999, Johnson et al. 2000) or the transparency (Lindström & Nilsson 1984, 1988, Dontsov et al. 1999). Fundamental differences have also been found in the photoreceptors of nocturnal and diurnal, closely related species of mosquitoes (Land et al. 1999) and ants (Menzi 1987). This topic has also been reviewed in a more general way by Eguchi (1986). Even the animals that live in the polar regions, the deep sea and the caves, where the sunlight is either completely absent or can be seen only sporadically, often possess and sometimes “have developed” highly specialized photoreceptors (recently reviewed by Meyer- Rochow & Nilsson 1999). For example, the amphipod Orchomene sp. cf, O. rossi that lives under the 400 m thick Ross Ice Shelf in Antarctica, may be able to make use of the few occasional photons that find their way through the snow, ice and 200 m of water (Meyer-Rochow 1981). Nordtug and Melø 1988, investigated the “diurnal variations in natural light conditions at summer time in arctic and subarctic areas”. In their report, they conclude that since the amount of light varies very little between the arctic summer night and day, the insects must have evolved to use different cues, i.e., Zeitgebers, to set their circadian clocks, and for example, may depend on changes in the spectral composition of the light instead of the change in light intensity accompanying the daily path of the sun. An absence or presence of light changes the photoreceptors in the long run [Eguchi & Ookoshi 1981, bred Drosophila in darkness for 600 generations; crayfish have been kept in darkness for 2–16 weeks (Eguchi & Waterman 1979), 11 weeks (Roach & Wiersma 1974) and one month (Hafner et al. 1982b)], and differences in the photic environment during a life-time of an individual have triggered the evolution of species, in which the photoreceptors of the young and the adults differ (photoreceptor structure in an individual). For example, a change from the apposition type compound eye to a superposition 45 type takes place in the western rock lobster Panulirus longipes and in mysids (Nilsson et al. 1986). These species’ young are planctonic and float around in the upper, brightly lit surface water, while the adults are feeding close to the bottom (Meyer-Rochow 1975). These kinds of changes in habitat selection during the course of an animal’s life have resulted in the young and the adults exhibiting differences in their photoreceptor structure and function. A very pronounced difference can be found in the holometabolous insects, where the larval forms frequently possess eyes (ocelli) that differ structurally and func- tionally from those of the adults (compound eyes). The changes that take place in the shortest time are the ones that are caused on a daily basis or by the seasonally changing environmental light conditions (Hariyama & Tsuka- hara 1988 concluded that the crayfish retinula cells have seasonal variation in their spectral sensitivity). Many of the arthropods have endogenously controlled adaptations to the daily fluctuations in light intensity (sunrise and sunset), but in addition to that, the photoreceptors are often capable of responding to even very quick changes in the lighting conditions. When considering all the factors that have affected the arthropod photoreceptors for generations, and the factors that affect them every day, it is not surprising, that so many variations of the organs to sense light have evolved, and that the arthropod photoreceptor displays such variability across different taxa and even developmental stages of individual species.

4.1 Sex

Many arthropod species have developed sexually dimorphic traits. Quite often the females form a subpopulation of smaller individuals of the whole population of the species (for example in Gammarus chevreuxi, Bêlehrádek & Huxley 1930, Petrolisthes elongatus, Meyer-Rochow et al. 1990, and L. exotica, II), but this does not have to mean that their photoreceptors would necessarily be different from the males’ eyes in relation to structure as well as function. In the case of L. exotica (II), no differences were found between the compound eyes of the two sexes during the entire post-embryonic development, except for sheer size, and in the P. elongatus and G. chevreuxi the trends in photoreceptor growth were identical, except that the female eyes ultimately remained smaller. In the insects, on the other hand, many species with sexually dimorphic photoreceptors can be found (see 1.2.3. Sex). Gupta and coauthors (2000) noticed, that the baetid mayfly Cloeon sp. has sexually strongly dimorphic compound eyes. The difference manifests itself at the molt from nymph to subimago. In this species, the two sexes have very different visual needs: the female needs to first select a mate out of a swarm of flying conspecifics and then find an oviposition site on the water surface; the male, on the other hand, has to find itself a female against a dimly lit evening sky. In the case of this species, a pair of identical compound eyes in males and females would have been inadequate to serve the different tasks, and both sexes developed exactly the kind of photoreceptors they needed. Gupta and coauthors (2000) even suggest that the mayfly female might choose the male with the largest dorsal eyes. In the case of L. exotica, both sexes live in the same environment, even in the same microhabitats, which has been proved repeatedly by capturing specimens within an area 46 of a few square meters and always catching an equal number of males and females (II, III). L. exotica females seem to have the same visual needs as the males: the females have to escape predators, find food and locate a mate. Therefore female individuals do not need different photoreceptors from those of the males. With the exception of the fact that the female L. exotica were found to be slightly smaller than the males, the photoreceptors in the two sexes were not found to differ from each other. The same is true in the fishlice as well: both male and female have to find a host in the water and their visual needs are, therefore, the same (I, VI). Fishlice copulate most often on the body surface of the fish and only occasionally somewhere else (Kollatsch 1959, cited in Pasternak et al. 2000). The two sexes, thus, might not have to look for a mate visually if the opposite sex can be found on the same host. Females lay their eggs on the bottom of the lake but they have to return to a host periodically to feed before they can lay all their eggs (Shafir & Van As 1986). In order to successfully perform this, female fishlice need just the same visual acuity as the males, which also have to be able to locate their hosts. In the spittle bug, in which the eyes of both sexes were found to be identical, the situation is similar (V). After leaving the spit bubble, both sexes feed on the same plants where they should have no problems locating possible partners to mate with. The females lay their eggs on the ground or on dead parts of the aquatic plants (Halkka et al. 1967). Find- ing these does not require any special features from their visual abilities and may rather involve olfaction or other forms of chemoreception. C. morosus, on the other hand, has never been recorded to breed in any other way than parthenogenetically, even though some males have occasionally been found in some populations (Clark 1976). To the best of my knowledge, a male stick insect compound eye morphology or anatomy has never been studied, so I can not say whether the structure differs from that of the female eye or not, but the fact is that the stick insect populations consist of only females for most of the time, and they all have identical eyes. In case a male stick insect compound eye structure was studied, it would most probably turn out quite much like the female photoreceptor since males would occupy the same environment as the females. A single male, which happens to hatch and mature in a population of only female conspecifics, will most definitely have no problems finding a mate, if sexual reproduction does exist in this species. Also, a male stick insect resembles the opposite sex morphologically to a point that they are quite difficult to distinguish (Clark 1976), so it seems that there would be no point for the rare males for their photoreception to be any different from that of the females’.

4.2 Development

The largest change that can be expected to happen in an arthropod photoreceptor, is the one that takes place during the most pronounced jump in development, i.e., metamorphosis of the species. Quite often in parallel with a metamorphosis, a change in the environment, which the animals occupy, also takes place. One of these fundamental metamorphoses is that of an aquatic nymph molting into an aerial adult or a subimago. This is because the photoreceptors, which are adapted to function in water, have problems focus- 47 ing in air due to the difference in the refractive index between the air and the water. In the baetid mayfly Cloeon sp., this step in the life history of the species separates the female and the male compound eyes from a more or less unisexual nymphal eye (Gupta et al. 2000). Molting to subimagos, both sexes exhibit a large reduction in facet diameter of the lateral eyes, but while in the male also the number of lateral ommatidia is decreased, in the female it increases. Sherk (1978c) concludes that the dragonfly larvae have to bear compromises in their compound eyes because the ommatidia, which are formed in their larval eyes, still have to function in the adult eye. According to Sherk (1978c), the ommatidia that mature during each larval phase are best suited for that particular developmental state, but are only compromises in the following instars. As the adult finally emerges from the water and turns to air, the larval ommatidia are pushed to the posterior edge of the compound eye and in some species some of the first larval instar ommatidia are even discarded as useless in the adult eye. Nothing quite this dramatic happens to either of the crustacean species in the present study: it is not known, how the L. exotica compound eye changes when the young leave the female’s marsupium, but after that, they spend the rest of their lives in the same environment as the rest of the adult individuals (II). These species’ photoreceptors do not need to adapt to a new environment or to sexual dimorphism during the post-embryonic development, and so the changes that take place in the eye are quite straight-forward. When in L. exotica the body length grows 8-fold, the number of its ommatidia increases about two-fold (II). A. coregoni body length increases 20-fold and the number of ommatidia in its compound eye increases about four-fold (VI). A record from the isopod Glyp- tonotus antarcticus shows, that when its carapace length increased 20-fold, the number of the ommatidia in the dorsal compound eye increased 6-fold while the number of the ommatidia in the ventral eye increased from 0 to about 25 (Meyer-Rochow 1982). This relatively greater increase of ommatidia in the ventral eye seemed a reflection of the prac- tice of mature, large animals to turn upside down when swimming. The nauplius eye of A. coregoni, on the other hand, went through a structural change between the metanauplius larvae and a 3 mm 8th stage pre-adult (VI). In the metanauplius, the lateral ocelli and the nuclei of the photoreceptor cells were greatly elongated. All three ocelli were circular in the 8th stage pre-adult larvae, but the photoreceptor nuclei were still elongated. It was not until in the first adult form (4 mm) that both the ocelli and the nuclei had required the shapes that the adults exhibit. Another relative change that was found to take place during the post-embryonic development of A. coregoni was that while the compound eye diameter grew from about 50 µm to 500 µm (10-fold increase), the nauplius eye ocelli grew only from approximately 25 µm to 100 µm (4-fold increase) (I, VI). Yet, both of the photoreceptors were larger in relation to body length in the metanauplius, considering that the A. coregoni body length grew 20-fold (VI). Unfortunately none of the other authors, who have studied the post- embryonic growth of the nauplius eye (Elofsson 1966b, Dudley 1969, Takenaka et al. 1993) mentioned the sizes of their study animals. The only comparison that could be made was that of Doropygus seclusus, in which the diameters of the nauplius eye ocelli grew only about 2–4 -fold (Dudley 1969), just like they did in the fishlouse nauplius eye (VI), and not as much as in the compound eyes of most species. The stick insect compound eye grew exactly the same amount as the L. exotica compound eye. C. morosus body length grew 8-fold while the number of its ommatidia 48 increased about 2-fold (IV). The spittle bug body length, on the other hand, grew from 2 mm to 8 mm while its compound eye’s dorsoventral axis grew from little less than 0.4 mm to about 0.6 mm (V). The difference between the three species, whose compound eye post-embryonic development was studied from one molt stage to another, was that in L. exotica and the stick insect, all parts of the eye grew rather isometrically (II, IV, respectively), while the spittle bug eye structure leaped from the last instar larvae to the adult stage (V). A significant difference between the last larval instar and the adult compound eye has also been reported in a number of dragonfly species (Lerum 1968, Sherk 1978b, Saka- moto et al. 1998) and the mayfly Cloeon sp. (Gupta et al. 2000). In these species, the aquatic larvae molt into avian adults and the photoreceptor changes accordingly. The spittle bug nymph, when molting into an adult, is ready to leave the semi-aquatic spit bubble that protected the eye from both mechanical and radial damage. This can be seen in the significant increase of the photoreceptor cuticular layer thickness in the spittle bug between the last nymphal instar and the adult (V). L. exotica, A. coregoni and C. morosus young and adults share the same environment and tasks for their photoreception, which can well be seen in the fact that their photoreceptors only grow but do not change their cellular organization or general shape during their post-embryonic development. In most of the crustacean species, the animals spend their whole lives in the same environment, namely water, so the post-embryonic changes are usually not as noticeable as in the insects between the successive developmental stages (see 1.2.3. Post-embryonic development). In all of the study species’ compound eyes, it was found that their eyes cope better with dim environments as they grow larger (I, II, IV, V, VI). This is due to a larger total area of the compound eye, larger facet or cone diameters, and an increase in the ommatidial numbers (Barlow 1952, Autrum 1981, Cronin 1986, Land 1985, 1997). A phenome- non, that occurs due to the growth in the stick insect, is that some of the light adaptational changes are much more pronounced in the adults than in the larvae: for example, the retinal layer is relatively thicker in light adapted adults than in light adapted larvae (IV). In the spittle bug, the light adaptational changes were just as strong in all developmental stages (V). Most authors agree that an increase in the compound eye size owes its enlargement to two facts: 1) addition of new ommatidia from the borders of the eye (III), and 2) increase in the size of old facets (II, IV, V, VI). Accretion of new ommatidia in L. exotica happens from the anterior and the ventral sides of the compound eye (III). In virtually all species studied, the new ommatidia are added at the molt (Lew 1934, cited in Lerum 1968, Sherk 1978a, c, Shelton et al. 1981, Cloarec 1984, Gupta et al. 2000), but Young (1969) argues that in the larval eye of the corixid Sigara arguta, which he has studied, new ommatidia are also added between molts. When the new ommatidia are starting to proliferate, it will still take a while before they function properly. Sakamoto and coauthors (1998) conclude that the dragonfly larvae have in the posterior corner of their eye the so-called ‘X-tissue’, which later forms the large facet region in an adult eye. In the last larval instar before the emergence as a flying adult, this tissue does not contain any photoreceptive membranes, and is thus useless for vision in the larvae. Something similar seems to hold true for L. exotica, where the most immature ommatidia only have a few microvilli put together and hardly anything else to 49 show that they will become mature, functioning ommatidia (III). It is, indeed, difficult to imagine a complicated structure like that of an ommatidium to be fully functional before all the necessary structures have matured and are in their proper places.

4.3 Light/dark adaptation

Basically, the light/dark adaptational phenomena are quite universal among most of the arthropods (see 1.2.2. Light/dark adaptation). Apart from light, the same kind of structural and functional changes may occur in the arthropod photoreceptors because of, for example, temperature (eg, Meyer-Rochow 1982, Meyer-Rochow & Tiang 1982, Kashi- wagi et al. 1997), cell poisoning with CO2 or anesthetization (Delmelle 1977, Henkes 1952 and Frixione et al. 1979, cited in Meyer-Rochow 1982, Banister & White 1987). In all of these cases, the objective is to protect the photoreceptive membranes from environmental stress, which could lead to damage and a reduction in performance. Long term dark adaptation during a life time or during a developmental state of an individual and its consequences have been studied by Roach and Wiersma (1974), Eguchi and Waterman (1979), Eguchi and Ookoshi (1981), Hafner and coauthors (1982b). In a very few species of arthropods, mainly in some Crustaceans, investigations have been made to find out, how light affected animals of the same species but of different size. Working with the crab Hemigrapsus sanguineus, Eguchi and coauthors (1989) concluded, that light/dark adaptation takes place in individuals of all sizes. Ziedins and Meyer-Rochow (1990) on the other hand, revealed that even though the characteristics of the electroretinogram (ERG) did not change with the age of the half-crab Petrolisthes elongatus, a two-fold shift in threshold sensitivity due to adaptation state was, however, observed. Peabody, who studied Idothea baltica and I. metallica in 1939, could show that the young taken out of the female’s brooding pouch did not exhibit any pigment migration even after a long period of darkness. In young I. baltica, the pigment remained inactive in the light-adapted position for several weeks after the young left the brooding pouch. On the other hand, glowworm larvae (Arachnocampa luminosa), which live in a crevice or a cave and possess stemmata, and the adults, which are flying forms with compound eyes, both exhibit light/dark adaptational changes in their photoreceptors (Meyer-Rochow & Waldvogel 1979). Arctiid moths exhibit light/dark adaptational changes in the adult ocelli as well (Grünewald & Wunderer 1996). In A. foliaceus, A. coregoni, L. exotica, C. morosus and P. spumarius, the light/dark adaptation followed the same paths with regard to pigment translocations (I, VI, Hariyama et al. 1986, IV, V, respectively), except that in the isopod, some of the changes were controlled endogenously, whereas in the stick insect, the ambient brightness seemed to be the stronger cue. The spittle bug (V) and the fishlice (I, VI) compound eye structures were partly controlled by light and partly by a circadian rhythm. As a stick insect grows, it turns from diurnal to nocturnal (IV). This can easily be veri- fied by looking into a stick insect container during the day, or observing animals in the field when the small larvae are actively eating but the larger nymphs and the adults lie passively and still on the ground. The situation is a bit different in L. exotica populations, where all the individuals, regardless of size, are apparently basking in the sun at noon. 50

The large eye of an adult L. exotica seems to be better adapted to see in a dim environment than the small eye of a young animal with its poorer sensitivity (II), and at least some individuals are still active at dark, as can be witnessed if one steps into an L exotica container laboratory in the dark and hears them crawling around. Their visual abilities are still impressive in twilight, which was demonstrated by T. Hariyama (pers. communica- tion), who noticed them fleeing at the sight of a glove hanging from a fishing rod above them at a beach at night. Taylor and Carefoot 1990, on the other hand, saw them either swimming in an arbitrary direction or sinking to the bottom if released into the water at night. The compound eyes of both A. coregoni and the spittle bug were found to be larger and their facets/ommatidia wider in the adults compared with those of the young (I, V, VI). This means that they should see better in dim light as they grow older. However, it has not been reported that either fishlice or spittle bugs would become more nocturnal as they grow older. In these cases, the growth of the compound eye may mostly be just a conse- quence of the increased body size. In all of the species, the younger animals had distinctly smaller eyes than the adults, and so the possibility of the light-induced damage to the eye is actually reduced (II, IV, V, VI). This risk is smaller in the small eyes, simply because of size: the larger the compound eye with more ommatidia and the larger the facet diameter, the greater the amount of potentially damaging radiation that can enter the eye. This is why the young of these species cope seemingly well with direct sunlight. The fishlice photoreceptors are at least partly protected from the damaging UV-light by the layer of water on top of them. 5 Conclusions

As has been shown in this thesis, the arthropod photoreceptor is truly an extremely versatile and variable structure. Therefore, when studying it with a microscope, it should be remembered that a certain sample only represents the specific conditions under which the animal was sacrificed. Sex and developmental state of the animal may affect the structure of the compound eye, as do ambient brightness level and time of day. All of these parameters should be considered when studying an arthropod photoreceptor. The species that were chosen in this study to represent the crustaceans (Argulus foliaceus, A. coregoni and Ligia exotica) and the insects (Carausius morosus and Philaenus spumarius), were all found to have an apposition type compound eye. Under the adult, mature hexagonal facet, an ommatidium in all species was found to consist of the dioptric apparatus (the cornea and the cone) and the photoreceptive layer. The latter consisted of 7 (C. morosus) or 8 (A. foliaceus, A. coregoni, L. exotica, P. spumarius) retinula cells, which all contributed microvilli to the central rhabdom. In L. exotica, the rhabdom was found to be of the open type, composed of 6 rhabdomeres, while in the other species, the rhabdom was of the closed type with a varying number of rhabdomeres (either 5 or 6 as in the fishlice, or 7 or 8 as in the insects). In all species, a different number of various kinds of pigment cells surrounded the ommatidium from the cornea to the basement membrane. In all of the studied species, the growth of the animal affected the size of the compound eye and its individual units, but not the structure itself. As the ommatidia grew longer, their diameters increased as well, but their shapes were not affected. In the spittle bug, the cornea grew thicker with the molt from the last nymphal instar to the adult, along with a change in the facet shape. In the fishlouse A. coregoni, the nauplius eye shape changed between the metanauplius and the 8th stage larvae. The post-embryonic development did not affect dark/light adaptation except that in C. morosus the change in retinal thickness was more pronounced in adults than in the larvae. The ambient bright light and daytime caused the rhabdom to shrink in both diameter and length and forced the pigment granules in the retinula cells to aggregate close to the photoreceptive membranes and around the proximal ends of the cones (light adaptation). The new ommatidia were found to be added to the L. exotica compound eye from the anterior and ventral marginal areas. The proliferation zone was at least five cell rows thick. A gradually maturing series of ommatidia, ranging from only a few microvilli to 52 fully grown 6 rhabdomeres, were observed in these marginal areas. Until all the structures in an ommatidium have matured, it is unlikely that it could perform its function as a photoreceptor properly. As can be seen from the above comments, an arthropod photoreceptor is constantly in a transitional state, and its structure depends on many different factors. This is why one has to be careful about the conditions and the circumstances when examining an arthropod eye to report on its anatomical organization and draw conclusions on its functional limitations. References

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