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

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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. OULUN YLIOPISTO, OULU 2004 Copyright © 2004 University of Oulu, 2004 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, labo- ratory 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 trans- mission 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 pro- cessed 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 micro- scopes 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-ter- restrial isopod Ligia exotica (Crustacea; Isopoda). Biocell 26: 441–450. IV Meyer-Rochow VB & Keskinen E (2003) Post-embryonic photoreceptor develop- ment 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 develop- ment 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 develop- ment 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 .
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