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University of Cincinnati UNIVERSITY OF CINCINNATI Date:___________________ I, _________________________________________________________, hereby submit this work as part of the requirements for the degree of: in: It is entitled: This work and its defense approved by: Chair: _______________________________ _______________________________ _______________________________ _______________________________ _______________________________ Structural and Functional Organization of The Visual System of The Larvae of The Sunburst Diving Beetle, Thermonectus marmoratus A Thesis submitted to the Division of Research and Advanced Studies of the University of Cincinnati in partial fulfillment of the requirements for the degree of MASTER OF SCIENCE in the Department of Biological Sciences of the College of Arts and Sciences 2005 by Karunyakanth Mandapaka M.Sc; Pondicherry University, 2002 Committee Chair: Dr. Elke K. Buschbeck Abstract: The visual system of the aquatic and predatory diving beetle larvae, Thermonectus marmoratus consists of 12 stemmata and two eye patches. Chapter one presents evidence that: (1) these stemmata are unique with features like multiple retinas in each stemma and some ‘perpendicular to the axis of light’ photoreceptors and (2) each eye monitors a unique visual field. Chapter two presents evidence that: (1) the visual fields of the large tubular eyes one and two are extremely narrow, while those of the other eyes are wide; (2) optic nerve from each stemma projects majorly to a unique neuropil; (3) each optic lobe has six distinct neuropils and (4) giant neurons are richer in the neuropils three though six than in one and two. From these studies I suggest that eyes one and two are the principal hunting eyes and that the other eyes are important in detecting the prey. 2 Acknowledgements: I am thankful to Dr. Elke Buschbeck for being a wonderful advisor. Her guidance, kind concern, and ever inspiring enthusiasm have been of enormous help, at every step. Her intention to help has been a resource that I could always be assured of. My research would not have been possible without her support. I am thankful to my Research Advisory Committee members, Dr. Edwin Griff, Dr. John Layne and Dr. Dennis Grogan for their guidance, kind concern, suggestions, discussions, and encouragement. Their help has been valuable and essential for the successful completion of my research. I am thankful to the Cincinnati Zoo Insectarium for kindly providing the adult Sunburst Diving beetles. I am thankful to Randy Morgan, the Invertebrate Conservation Program Manager, Cincinnati Zoo, for his help in rearing the adults and larvae in the lab conditions and much advice. I am also thankful to Dr. Dan-Eric Nilsson of the Lund University for his helpful advice. I am thankful to Heather Hoy, Srdjan Maksimovic, and Kelly Hagen of the Buschbeck lab for their technical, moral and intellectual support; and for their amicability. I am thankful to all the faculty members of the department for excellently teaching the courses and for guiding me to do well with the TA responsibilities. I am thankful to Dr. Carl Huether and Dr. Dennis Grogan for their moral support and encouragement on times that I most needed. I am thankful to all the fellow graduate students of the department for being very friendly and interactive; for sharing ideas and study materials and for all the fun we had together. I am thankful to Dr. Guy Cameron, the head of the department and Dr. Brian Kinkle, and Dr. Charlotte Paquin, directors of the graduate affairs for their support and kind concern. I am thankful to all the staff members in the Biological Sciences department for all their help and support with my academic and TA responsibilities. I am thankful to Dr. Elke Buschbeck, the department of Biological Sciences and the University of Cincinnati for the financial support and for providing me with an opportunity to learn. I am also thankful to NSF for the grant awarded to Dr. Elke Buschbeck, IBN- 0423963, from which I was funded. 3 4 Contents: List of Tables and Figures …………………………………………………………6 General Introduction………………………………………………………………..8 Chapter One: “Twenty eight retinas but only twelve eyes; an anatomical analysis of the larval visual system of Thermonectus marmoratus (Dytiscidae)” Abstract…………………………………………………………………………………13 Introduction…………………………………………………………………………….14 Materials and Methods…………………………………………………………………17 Results……………………………………………………………………………….....20 Discussion……………………………………………………………………………...39 References……………………………………………………………………………..46 Chapter Two: “Measurement of the visual fields for eyes four, five and six, anatomical description of the optic lobes and the functional organization of the visual system in T. marmoratus larvae” Introduction………………………………………………………………………………51 Materials and Methods…………………………………………………………………...53 Results……………………………………………………………………………………58 Discussion………………………………………………………………………………..73 General Discussion………………………………………………………………………77 References………………………………………………………………………………..81 5 List of Tables and Figures Table 1 Acceptance angles of eyes one, two and three- measured by Dr. Buschbeck…59 Table 2 Average BFDs; and focal lengths of the eyes four, five and six……………….63 Table 3 Acceptance angles of eyes four, five and six in different sectional planes……..63 Figure 1 First instar T. marmoratus larva external features……………………………....9 Figure 2 Anatomical features of the large tubular eyes one and two……………………21 Figure 3 Three dimensional reconstructions of eyes one and two viewed from medial (left) and dorsal (right)…………………………………………………………………...23 Figure 4 Detailed anatomical features of the crystalline cone and the lateral retina in eye one………………………………………………………………………………………..25 Figure 5 Anatomical features of the horizontal and vertical retinas in eye one…………28 Figure 6 Organization of the rhabdoms of the vertical retina of eye one……………….30 Figure 7 Anatomical features of the eyes three and four………………………………..32 Figure 8 Anatomical features of the eyes five and six; and the eye patch………………36 Figure 9 An illustration of the procedure of measurement of optical parameters………56 Figure 10 An illustration depicting various optical parameters measured……………...58 Figure 11 Acceptance angles of eyes four, five and six in different sectional planes…..60 Figure 12 An overview of the visual fields of the stemmata in sagittal plane…………..61 Figure 13 An overview the visual fields of the stemmata in the horizontal plane………62 Figure 14 External and anatomical features of the optic lobes………………………….65 Figure 15 Three dimensional reconstructions of the optic lobe…………………………66 6 Figure 16 Fluorescent stained neuronal projections from eyes one, three, five and six onto the respective optic neuropils………………………………………………………68 Figure 17 Fluorescent stained projections of nerve terminals in the neuropils two and four, from backfill studies of eye four…………………………………………………...70 Figure 18 Detailed anatomical features of the optic neuropils and fluorescent stained neuronal projections onto to the optic lobe neuropils from eyes two and four…………..71 7 General Introduction: Though visual systems in the adult holometabolous insects have been extensively studied, those in larvae still remain poorly investigated. Many holometabolous insect larvae have single lens eyes, generally referred to as stemmata, which vary to a large degree in their number, location, size and functional capability (Gilbert, 1994); among their wide range of species. For example, they can be highly reduced, as they are in the maggot larvae of higher flies (Paulus, 1989) or they can be sophisticated image forming lens eyes with extended cup-shaped retinas such as in the largest stemmata of the tiger beetle larvae (Toh and Mizutani, 1987). This variation makes the studies of the holometabolous insect larval visual systems interesting. In the current study, “Structural And Functional Organization of The Visual System of The Larvae of The Sunburst Diving Beetle, Thermonectus marmoratus”, I investigate an interesting visual system of the larvae in the Sunburst diving beetle (also referred to as the Spotted water beetle), T. marmoratus. There are three larval instars in T. marmoratus and all of them are almost exclusively aquatic. Larvae are aggressive predators, feeding on soft bodied insects and other larvae. They have six stemmata (single lens eyes in many holometabolous insect larvae) and an eye patch on either side. They also have two optic lobes for processing visual inputs. 8 Figure 1 First instar T. marmoratus larva external features (A) A first instar T.marmoratus larva, about 1cm in length. (B) Fronto-dorsal view of the larva showing E1 and E2 on both sides; the eye patch (EP) and the pincer shaped mandibles (M). (C) Right lateral view of the right larval head showing the disposition of E1-6. 9 The objectives of this study are to investigate the structural organization of specific components of the visual system (stemmata, optic lobes and neuronal connections between them) and to derive hypothesis about the mode of function of the visual system. This study is divided into two chapters. In chapter one, “Twenty eight retinas but only twelve eyes; an anatomical analysis of the larval visual system of the diving beetle, Thermonectus marmoratus (Dytiscidae)”, I describe the structural details of each of the six stemmata and the eye patch on one side of the larva. My preliminary anatomical studies on all the three larval instars showed no major differences in the visual systems among the three larval instars. So, in chapter one all the studies
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