Solar-Powered Sea Slugs

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© Jupiterimages Corp. Matching Draw a line to match each word on the right with the group of words on the left that relate to it. © Learning A–Z.com presented by Science a-z a division of Learning A-Z creature, pet, plant critter, wild Solar-Powered Sea Slugs hot, bright, animal By Ron Fridell ray, daytime One animal is unlike any supply. It’s part plant and deadly, hunt, sea other known animal on part animal. You could call it enemy, prey Earth. It’s a species of sea a planimal! slug called Elysia chlorotica. eat, energy, sunlight This creature lives in ocean This creature looks like a diet, hungry waters along the eastern green leaf swimming in United States. What makes the sea. Its favorite meal is stem, leaf, swim it so special? Like an animal, green sea plants called algae. green, flower it eats food. But like a plant, Sounds yummy, right? But E. it also makes its own food chlorotica only needs to eat wave, salt, predator one meal of algae at fish, algae the very beginning of its life. So how does float, dive, defend it get the energy it water, wade needs to survive after protect, guard, food it stops eating? help, watch © iStockphoto.com/ Rebecca Lowe © Nick Curtis and Ray Martinez Elysia chlorotica © Jupiterimages Corp. See Solar Sea Slugs on page 2 © Learning A–Z All rights reserved. 4 www.sciencea-z.com 1 Solar Sea Slugs Continued from page 1 Write About This! What would it be like if you could make your own food inside © iStockphoto.com/Leo Blanchette your body instead of eating? Don’t bother How would your life be different? © iStockphoto.com/Zurijeta looking for What would be the pros and planimal in cons? Use your answers to help a dictionary. It’s not an official word . you write a story, essay, or poem yet. But scientists think about your new life as a planimal. they will find more animal species that behave like © 2008 Proceedings of the National © 2008 Proceedings Academy of Sciences Publication plants in some ways. E. chlorotica takes in some If they do, then maybe pointy protection of the algae’s genes while someday you will find planimal in a dictionary. it eats. Genes are the parts Sea slugs don’t have shells, and their bodies are soft. of cells that tell the body So how do they defend themselves? Many sea slugs have how to make what it needs. color patterns to blend in with their habitat. Some sea slugs This sea slug takes in the also have poisonous stingers. Ouch! They’re not born with genes that tell algae how Some plants them, though. These sea slugs eat creatures that have stingers, to perform a process called look like such as stinging jellyfish and anemones. But they don’t digest animals, and some photosynthesis. This process the stingers. The stingers stick out © Jupiterimages Corp. is how plants, algae, and animals resemble plants. through the sea slugs’ skin. These Are these organisms sharp features help the sea slugs other living things make food plants or animals? from sunlight. © iStockphoto.com/Cathy Keifer/Keiichi Hiki protect themselves from predators. After just one meal, this sea slug can use sunlight to make its own food. It never Inc. Researchers, Photo has to eat again! With the © Eye of Science/ algae’s genes in its cells, A slug’s mouth is just a tiny hole. E. chlorotica could be called When the slug opens it up, rows of teeth scrape food into tiny bits. a “solar-powered” animal. animals! both They’re © Learning A–Z All rights reserved. 2 3 www.sciencea-z.com.

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The Identification of Functional, Sequestered, Symbiotic Chloroplasts

University of South Florida Scholar Commons Graduate Theses and Dissertations Graduate School 2006 The identification of functional, sequestered, symbiotic chloroplasts in Elysia clarki: A crucial step in the study of horizontally transferred, nuclear algal genes Nicholas E. Curtis University of South Florida Follow this and additional works at: http://scholarcommons.usf.edu/etd Part of the American Studies Commons Scholar Commons Citation Curtis, Nicholas E., "The identification of functional, sequestered, symbiotic chloroplasts in Elysia clarki: A crucial step in the study of horizontally transferred, nuclear algal genes" (2006). Graduate Theses and Dissertations. http://scholarcommons.usf.edu/etd/2496 This Dissertation is brought to you for free and open access by the Graduate School at Scholar Commons. It has been accepted for inclusion in Graduate Theses and Dissertations by an authorized administrator of Scholar Commons. For more information, please contact [email protected]. The Identification of Functional, Sequestered, Symbiotic Chloroplasts in Elysia clarki: A Crucial Step in the Study of Horizontally Transferred, Nuclear Algal Genes by Nicholas E. Curtis A thesis submitted in partial fulfillment of the requirements for the degree of Doctor of Philosophy Department of Biology College of Arts and Sciences University of South Florida Major Professor: Sidney K. Pierce, Jr., Ph.D. Clinton J. Dawes, Ph.D. Kathleen M. Scott, Ph.D. Brian T. Livingston, Ph.D. Date of Approval: June 15, 2006 Keywords: Bryopsidales, kleptoplasty, sacoglossan, rbcL, chloroplast symbiosis Penicillus, Halimeda, Bryopsis, Derbesia © Copyright 2006, Nicholas E. Curtis Note to Reader The original of this document contains color that is necessary for understanding the data. The original dissertation is on file with the USF library in Tampa, Florida.
Chloroplast Incorporation and Long-Term Photosynthetic Performance Through the Life Cycle in Laboratory Cultures of Elysia Timid

Chloroplast incorporation and long-term photosynthetic performance through the life cycle in laboratory cultures of Elysia timida (Sacoglossa, Heterobranchia) Schmitt et al. Schmitt et al. Frontiers in Zoology 2014, 11:5 http://www.frontiersinzoology.com/content/11/1/5 Schmitt et al. Frontiers in Zoology 2014, 11:5 http://www.frontiersinzoology.com/content/11/1/5 RESEARCH Open Access Chloroplast incorporation and long-term photosynthetic performance through the life cycle in laboratory cultures of Elysia timida (Sacoglossa, Heterobranchia) Valerie Schmitt1,2, Katharina Händeler2, Susanne Gunkel2, Marie-Line Escande3, Diedrik Menzel4, Sven B Gould2, William F Martin2 and Heike Wägele1* Abstract Introduction: The Mediterranean sacoglossan Elysia timida is one of the few sea slug species with the ability to sequester chloroplasts from its food algae and to subsequently store them in a functional state in the digestive gland cells for more than a month, during which time the plastids retain high photosynthetic activity (= long-term retention). Adult E. timida have been described to feed on the unicellular alga Acetabularia acetabulum in their natural environment. The suitability of E. timida as a laboratory model culture system including its food source was studied. Results: In contrast to the literature reporting that juvenile E. timida feed on Cladophora dalmatica first, and later on switch to the adult diet A. acetabulum, the juveniles in this study fed directly on A. acetabulum (young, non-calcified stalks); they did not feed on the various Cladophora spp. (collected from the sea or laboratory culture) offered. This could possibly hint to cryptic speciation with no clear morphological differences, but incipient ecological differentiation.
Chloroplast Genes Are Expressed During Intracellular Symbiotic

Proc. Natl. Acad. Sci. USA Vol. 93, pp. 12333-12338, October 1996 Cell Biology Chloroplast genes are expressed during intracellular symbiotic association of Vaucheria litorea plastids with the sea slug Elysia chlorotica (photosystem II reaction center/photosynthesis/chromophytic alga/ascoglossan mollusc/gene expression) CESAR V. MUJER*t, DAVID L. ANDREWS*t, JAMES R. MANHART§, SIDNEY K. PIERCES, AND MARY E. RUMPHO*II Departments of *Horticultural Sciences and §Biology, Texas A & M University, College Station, TX 77843; and IDepartment of Zoology, University of Maryland, College Park, MD 20742 Communicated by Martin Gibbs, Brandeis University, Waltham, MA, August 16, 1996 (received for review January 26, 1996) ABSTRACT The marine slug Elysia chlorotica (Gould) lowing metamorphosis from the veliger stage when juvenile forms an intracellular symbiosis with photosynthetically ac- sea slugs begin to feed on V litorea cells (1, 2). Once ingested, tive chloroplasts from the chromophytic alga Vaucheria litorea the chloroplasts are phagocytically incorporated into the cy- (C. Agardh). This symbiotic association was characterized toplasm of one of two morphologically distinct, epithelial cells over a period of 8 months during which E. chlorotica was (3) and maintain their photosynthetic function (1, 3). The deprived of V. litorea but provided with light and CO2. The fine plastids are frequently found in direct contact with the host structure of the symbiotic chloroplasts remained intact in E. cytoplasm as revealed by ultrastructural studies (3). In nature, chlorotica even after 8 months of starvation as revealed by the adult animal feeds on algae only sporadically, obtaining electron microscopy. Southern blot analysis of total DNA metabolic energy from the photosynthetic activity of the from E.
The Making of a Photosynthetic Animal

303 The Journal of Experimental Biology 214, 303-311 © 2011. Published by The Company of Biologists Ltd doi:10.1242/jeb.046540 The making of a photosynthetic animal Mary E. Rumpho1,*, Karen N. Pelletreau1, Ahmed Moustafa2 and Debashish Bhattacharya3 1Department of Molecular and Biomedical Sciences, 5735 Hitchner Hall, University of Maine, Orono, ME 04469, USA, 2Department of Biology and Graduate Program in Biotechnology, American University in Cairo, New Cairo 11835, Egypt and 3Department of Ecology, Evolution and Natural Resources, Institute of Marine and Coastal Sciences, Rutgers University, New Brunswick, NJ 08901, USA *Author for correspondence ([email protected]) Accepted 6 August 2010 Summary Symbiotic animals containing green photobionts challenge the common perception that only plants are capable of capturing the sun’s rays and converting them into biological energy through photoautotrophic CO2 fixation (photosynthesis). ‘Solar-powered’ sacoglossan molluscs, or sea slugs, have taken this type of symbiotic association one step further by solely harboring the photosynthetic organelle, the plastid (chloroplast). One such sea slug, Elysia chlorotica, lives as a ‘plant’ when provided with only light and air as a result of acquiring plastids during feeding on its algal prey Vaucheria litorea. The captured plastids (kleptoplasts) are retained intracellularly in cells lining the digestive diverticula of the sea slug, a phenomenon sometimes referred to as kleptoplasty. Photosynthesis by the plastids provides E. chlorotica with energy and fixed carbon for its entire lifespan of ~10months. The plastids are not transmitted vertically (i.e. are absent in eggs) and do not undergo division in the sea slug. However, de novo protein synthesis continues, including plastid- and nuclear-encoded plastid-targeted proteins, despite the apparent absence of algal nuclei.
Endosymbiotic Chloroplasts in Molluscan Cells Contain Proteins Synthesized After Plastid Capture

The Journal of Experimental Biology 199, 2323–2330 (1996) 2323 Printed in Great Britain © The Company of Biologists Limited 1996 JEB0480 ENDOSYMBIOTIC CHLOROPLASTS IN MOLLUSCAN CELLS CONTAIN PROTEINS SYNTHESIZED AFTER PLASTID CAPTURE SIDNEY K. PIERCE1,*, RACHEL W. BIRON1,† AND MARY E. RUMPHO2 1Department of Zoology, University of Maryland, College Park, MD 20742, USA and 2Department of Horticultural Sciences, Texas A & M University, College Station, TX 77843, USA Accepted 11 July 1996 Summary Endosymbiotic chloroplasts within the cells of the and subsequently translocated into the chloroplasts. Thus, ascoglossan slug Elysia chlorotica synthesize a variety of the plastids not only synthesize proteins during this long- proteins including the large subunit of ribulose-1,5- lived association, but the host cell seems to play a role in bisphosphate-carboxylase oxygenase (RuBisCO) and the plastid protein turnover. photosystem II protein D1. In addition, the effects of protein synthesis inhibitors suggest that some chloroplast- Key words: endosymbiosis, chloroplast, slug, Elysia chlorotica, associated proteins are synthesized in the animal cytosol protein synthesis. Introduction Most plant–animal symbioses are cellular associations, with selectively take up and retain the algal chloroplasts (West, either entire algal cells residing between animal cells 1979). The long-term survival of the chloroplasts within the (Muscatine et al. 1975; Trench, 1979; Pardy et al. 1983) or a animal cells suggests that these plastids possess an extremely complete plant cell existing within a vacuole produced by the high degree of genetic and biochemical autonomy, or that the animal cell (Muscatine et al. 1975; Anderson, 1983). However, host cells of E. chlorotica play a signiﬁcant role in promoting in the marine ascoglossan slug Elysia chlorotica, a single the survival of the chloroplasts, or perhaps both.
Elysia Chlorotica</Em>

University of South Florida Scholar Commons Graduate Theses and Dissertations Graduate School 2-24-2015 A Functional Chlorophyll Biosynthesis Pathway Identified in the Kleptoplastic Sea Slug, Elysia chlorotica Julie A. Schwartz University of South Florida, [email protected] Follow this and additional works at: https://scholarcommons.usf.edu/etd Part of the Biology Commons, and the Molecular Biology Commons Scholar Commons Citation Schwartz, Julie A., "A Functional Chlorophyll Biosynthesis Pathway Identified in the Kleptoplastic Sea Slug, Elysia chlorotica" (2015). Graduate Theses and Dissertations. https://scholarcommons.usf.edu/etd/5576 This Thesis is brought to you for free and open access by the Graduate School at Scholar Commons. It has been accepted for inclusion in Graduate Theses and Dissertations by an authorized administrator of Scholar Commons. For more information, please contact [email protected]. A Functional Chlorophyll Biosynthesis Pathway Identified in the Kleptoplastic Sea Slug, Elysia chlorotica by Julie A. Schwartz A thesis submitted in partial fulfillment of the requirements for the degree of Master of Science in Biology Department of Integrative Biology College of Arts and Sciences University of South Florida Major Professor Kathleen Scott, Ph.D. Christina Richards, Ph.D. James Garey, Ph.D. Date of Approval: February 24, 2015 Keywords: Horizontal gene transfer, kleptoplasty, plastid endosymbiosis, Vaucheria litorea Copyright © 2015, Julie A. Schwartz Dedication I am dedicating this thesis to my husband, Fran, and my sons, Joel and Matthew. Without their endless love, support and encouragement I would never have continued this life- changing endeavor to the finish. When I decided to pursue my graduate degree, little did I realize that my entire family would have to experience the rollercoaster ride of ups and downs as well as successes and defeats and I am eternally grateful that they always stayed by my side to help me attain my goal.
GISELA JOÃO RIBEIRO LEMOS DIONÍSIO Effects of Climate Change

Universidade de Aveiro Departamento de Biologia 2016 GISELA JOÃO Effects of climate change on the physiology and RIBEIRO LEMOS photobiology of photosynthetic sea slugs DIONÍSIO Os efeitos das alterações climáticas na fisiologia e fotobiologia das lesmas do mar fotossintéticas Universidade de Aveiro Departamento de Biologia 2016 GISELA JOÃO RIBEIRO Effects of climate change on the physiology and LEMOS DIONÍSIO photobiology of photosynthetic sea slugs Os efeitos das alterações climáticas na fisiologia e fotobiologia das lesmas do mar fotossintéticas Tese apresentada à Universidade de Aveiro para cumprimento dos requisitos necessários à obtenção do grau de Doutor em Biologia, realizada sob a orientação científica do Doutor Ricardo Calado, Investigador Principal do Departamento de Biologia da Universidade de Aveiro, do Doutor Rui Rosa, Investigador Principal do Laboratório Marítimo da Guia da Faculdade de Ciências da Universidade de Lisboa e do Professor Doutor João Serôdio, Professor Auxiliar com Agregação do Departamento de Biologia da Universidade de Aveiro. Gisela Dionísio was supported by a PhD scholarship (SFRH/BD/73205/2010) funded by Fundação para a Ciência e Tecnologia Portugal (QREN-POPH – Type 4.1 – Advanced Training, subsidized by the European Social Fund and national funds MCE) Prediction is very difficult, especially about the future. Niels Bohr o júri presidente Doutor Artur Manuel Soares da Silva Professor Catedrático do Departamento de Química da Universidade de Lisboa vogais Doutor Henrique Manuel Roque Nogueira Cabral Professor
First Record of Two Mangrove Leaf Slugs, Elysia Leucolegnote and E

Northern Territory Naturalist (2016) 27: 97–101 Short Note First record of two mangrove leaf slugs, Elysia leucolegnote and E. bangtawaensis (Sacoglossa: Plakobranchidae), in mangrove forests in the Northern Territory Adam J. Bourke1, Carmen Walker1 and Richard C. Willan2 1 EcoScience NT, 29 Ostermann St, Coconut Grove, Darwin, NT 0810, Australia Email: [email protected] 2 Museum and Art Gallery of the Northern Territory, GPO Box 4646, Darwin, NT 0810, Australia Abstract Here we report for the first time on the occurrence of the distinctive and highly ephemeral sap-sucking sea slugs Elysia leucolegnote and E. bangtawaensis from mangrove forests from Darwin Harbour, Northern Territory, Australia. Individuals of both species apparently attain smaller body size than their counterparts elsewhere in Australia and the Indo-Pacific region, with maximum extended crawling lengths recorded between 17–22 mm. It appears the northern Australian (i.e. Northern Territory and northern Queensland) populations of E. bangtawaensis differ consistently from their counterparts elsewhere in the world in aspects of (parapodial and rhinophoral) colouration. The ability to retain functioning chloroplasts sequestered from algal host(s) is widespread in the group of sea slugs known as sap-sucking slugs (order Sacoglossa). Numerous species in the genus Elysia (family Plakobranchidae, the largest family numerically in the Sacoglossa) are known for their ability to sequester live chloroplasts within their extensively branched digestive diverticula, imparting a bright green colour (e.g. Trench et al. 1973; Rumpho et al. 2008; Jesus et al. 2010). Some of them match their host food precisely (Burn 1998). The genus Elysia is species-rich, with some 95 named species (Bouchet & Gofas 2015) and at least that number again undescribed (RCW pers.
A Photosynthetic Animal: a Sacoglossan Sea Slug That Steals Chloroplasts

© 2021 The Japan Mendel Society Cytologia 86(2): 103–107 Cytologia Focus: A Photosynthetic Animal: A Sacoglossan Sea Slug that Steals Chloroplasts Ryota Aoki1 and Sachihiro Matsunaga2* 1 Department of Applied Biological Science, Faculty of Science and Technology, Tokyo University of Science, 2641 Yamazaki, Noda, Chiba 278–8510, Japan 2 Laboratory of Integrated Biology, Department of Integrated Biosciences, Graduate School of Frontier Sciences, 5–1–5 Kashiwanoha, Kashiwa, Chiba 277–8561, Japan Received April 8, 2021; accepted April 15, 2021 Summary Sacoglossan sea slugs are able to steal chloroplasts from their algal prey and acquire photosynthetic capacity (termed kleptoplasty). These ‘stolen’ plastids provide sea slugs with a long-term supply of organic car- bon and energy. This augmented nutrient supply brings many benefits in terms of survival, body planning, repro- ductive traits, and body regeneration. However, the mechanisms of maintenance of chloroplasts and photosynthe- sis in sea slugs are poorly understood. Here, we introduce this mysterious phenomenon, including recent research findings, and consider its feasibility for synthetic biology, e.g., construction of artificial photosynthetic animal cells. Keywords Kleptoplasty, Sacoglossan sea slug, Photosynthesis, Alga, Synthetic biology. Research on algae has rapidly diversified into various photosynthesise using these ‘stolen’ plastids and assimi- fields, including cell biology (Mine et al. 2018, Takano late photosynthate for periods ranging from a few days et al. 2018, Miyamura et al. 2019, Kuroiwa et al. 2020, to several months. A particular puzzle is that the sea Yoshida et al. 2020), molecular biology (Uchida et al. slugs are able to maintain photosynthetic activity despite 2018, Ota et al.
The Potential of Indonesian Heterobranchs Found Around Bunaken Island for the Production of Bioactive Compounds

marine drugs Review The Potential of Indonesian Heterobranchs Found around Bunaken Island for the Production of Bioactive Compounds Katja M. Fisch 1,2, Cora Hertzer 2, Nils Böhringer 1,2, Zerlina G. Wuisan 1,2, Dorothee Schillo 3, Robert Bara 4, Fontje Kaligis 4, Heike Wägele 3, Gabriele M. König 2,5,* and Till F. Schäberle 1,2,5,* 1 Institute for Insect Biotechnology, Justus-Liebig-University Giessen, 35392 Giessen, Germany; [email protected] (K.M.F.); [email protected] (N.B.); [email protected] (Z.G.W.) 2 Institute for Pharmaceutical Biology, Rheinische Friedrich-Wilhelms-University Bonn, 53115 Bonn, Germany; [email protected] 3 Centre of Molecular Biodiversity, Zoological Research Museum Alexander Koenig, 53113 Bonn, Germany; [email protected] (D.S.); [email protected] (H.W.) 4 Faculty of Fisheries and Marine Science, Sam Ratulangi University, Manado 95115, Indonesia; [email protected] (R.B.); [email protected] (F.K.) 5 German Center for Infection Research, Partner Site Bonn-Cologne, 53115 Bonn, Germany * Correspondence: [email protected] (G.M.K.); [email protected] (T.F.S.); Fax: +49-228-73-3250 (G.M.K.); +49-641-99-37149 (T.F.S.) Received: 14 July 2017; Accepted: 28 November 2017; Published: 7 December 2017 Abstract: The species diversity of marine heterobranch sea slugs found on ﬁeld trips around Bunaken Island (North Sulawesi, Indonesia) and adjacent islands of the Bunaken National Marine Park forms the basis of this review. In a survey performed in 2015, 80 species from 23 families were collected, including 17 new species.
A Sea Slug's Guide to Plastid Symbiosis

Acta Societatis Botanicorum Poloniae INVITED REVIEW Acta Soc Bot Pol 83(4):415–421 DOI: 10.5586/asbp.2014.042 Received: 2014-10-29 Accepted: 2014-11-26 Published electronically: 2014-12-31 A sea slug’s guide to plastid symbiosis Jan de Vries1, Cessa Rauch1, Gregor Christa1,2, Sven B. Gould1* 1 Institute for Molecular Evolution, Heinrich Heine-University, Düsseldorf 40225, Germany 2 CESAM, University of Aveiro, 3810-193 Aveiro, Portugal Abstract Some 140 years ago sea slugs that contained chlorophyll-pigmented granules similar to those of plants were described. While we now understand that these “green granules” are plastids the slugs sequester from siphonaceous algae upon which they feed, surprisingly little is really known about the molecular details that underlie this one of a kind animal-plastid symbiosis. Kleptoplasts are stored in the cytosol of epithelial cells that form the slug’s digestive tubules, and one would guess that the stolen organelles are acquired for their ability to fix carbon, but studies have never really been able to prove that. We also do not know how the organelles are distinguished from the remaining food particles the slugs incorporate with their meal and that include algal mitochondria and nuclei. We know that the ability to store kleptoplasts long-term has evolved only a few times independently among hundreds of sacoglossan species, but we have no idea on what basis. Here we take a closer look at the history of sacoglossan research and discuss recent developments. We argue that, in order to understand what makes this symbiosis work, we will need to focus on the animal’s physiology just as much as we need to commence a detailed analysis of the plastids’ photobiology.
Elysia Chlorotica (Photosystem II Reaction Center/Photosynthesis/Chromophytic Alga/ Ascoglossan Mollusc/Gene Expression)

Proc. Natl. Acad. Sei. USA Vol. 93, pp. 12333-12338, October 1996 Cell Biology Chloroplast genes are expressed during intracellular symbiotic association ofVaucheria litorea plastids with the sea slug Elysia chlorotica (photosystem II reaction center/photosynthesis/chromophytic alga/ ascoglossan mollusc/gene expression) C esar V. MujER*t, D a v id L. A n d r ew s **, Jam es R. M an h a r t §, Sid ney K. P ierce ^, a n d M ary E. R u m ph o*H Departments of * Horticultural Sciences and ^Biology, Texas A & M University, College Station, TX 77843; and ^Department of Zoology, University of Maryland, College Park, MD 20742 Communicated by Martin Gibbs, Brandeis University, Waltham, MA, August 16, 1996 (received for review January 26, 1996) ABSTRACT The marine slug Elysia chlorotica (Gould) lowing metamorphosis from the veliger stage when juvenile forms an intracellular symbiosis with photosynthetically ac sea slugs begin to feed on V litorea cells (1, 2). Once ingested, tive chloroplasts from the chromophytic algaVaucheria litorea the chloroplasts are phagocytically incorporated into the cy (C. Agardh). This symbiotic association was characterized toplasm of one of two morphologically distinct, epithelial cells over a period of 8 months during whichE. chlorotica was (3) and maintain their photosynthetic function (1, 3). The deprived ofV. litorea but provided with light and CO2. The fine plastids are frequently found in direct contact with the host structure of the symbiotic chloroplasts remained intact Ein. cytoplasm as revealed by ultrastructural studies (3). In nature, chlorotica even after 8 months of starvation as revealed by the adult animal feeds on algae only sporadically, obtaining electron microscopy.