Advances in Insect Physiology Volume 35 This page intentionally left blank Advances in Insect Physiology edited by S. J. Simpson School of Biological Sciences, The University of Sydney, Sydney, Australia Volume 35 Amsterdam Boston Heidelberg London New York Oxford Paris San Diego San Francisco Singapore Sydney Tokyo ACADEMIC Academic Press is an imprint of Elsevier PRESS Academic Press is an imprint of Elsevier 32 Jamestown Road, London NW1 7BY, UK Radarweg 29, PO Box 211, 1000 AE Amsterdam, The Netherlands Linacre House, Jordan Hill, Oxford OX2 8DP, UK 30 Corporate Drive, Suite 400, Burlington, MA 01803, USA 525 B Street, Suite 1900, San Diego, CA 92101-4495, USA First edition 2008 Copyright r 2008 Elsevier Ltd. 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Because of rapid advances in the medical sciences, in particular, independent verification of diagnoses and drug dosages should be made ISBN: 978-0-12-374329-9 ISSN: 0065-2806 For information on all Academic Press publications visit our website at elsevierdirect.com Printed and bound in United Kingdom 080910111210987654321 Contents Contributors vii Insect Excretory Mechanisms 1 M. O’DONNELL Collective Decision-Making and Foraging Patterns in Ants and Honeybees 123 C. DETRAIN, J.-L. DENEUBOURG Index 175 This page intentionally left blank Contributors J.-L. Deneubourg Unit of Social Ecology, Universite´ Libre de Bruxelles, Campus de la Plaine, Brussels, Belgium C. Detrain Unit of Social Ecology, Universite´ Libre de Bruxelles, Campus de la Plaine, Brussels, Belgium M. O’Donnell Department of Biology, McMaster University, Hamilton, Ontario, L8S 4K1, Canada This page intentionally left blank Insect Excretory Mechanisms Michael O’Donnell Department of Biology, McMaster University, Hamilton, Ontario, L8S 4K1, Canada 1 Introduction 2 2 Design principles underlying the insect excretory system 3 3 Secretion of physiological ions by insect Malpighian tubules 8 3.1 Ion transport across Malpighian tubules composed of a single cell type 8 3.2 Ion transport across Malpighian tubules composed of principal cells and stellate cells 19 3.3 Aquaporins and osmotic permeability of Malpighian tubules 27 4 Secretion and reabsorption by downstream segments of the Malpighian tubule and the hindgut 28 4.1 Reabsorption by the Malpighian tubules 28 4.2 The insect hindgut 30 5 Nitrogenous waste excretion 33 5.1 Uric acid 33 5.2 Ammonia transport in insects 39 5.3 Free amino acids 43 6 Transport and excretion of divalent ions and bicarbonate 46 6.1 Calcium 46 6.2 Magnesium 49 6.3 Sulfate 50 6.4 Bicarbonate 53 7 Excretion and sequestration of toxic metals 57 7.1 Sites and mechanisms of cadmium accumulation and transport 57 7.2 Regulated storage of zinc and copper in Drosophila 60 7.3 Detoxification and excretion of iron and heme 61 8 Transport of organic cations and organic anions 64 8.1 Transport of type I organic cations 65 8.2 Transport of type II organic cations by P-glycoprotein-like mechanisms 72 8.3 Transport of type I organic anions 84 8.4 Transport of type II organic anions by multidrug resistance-associated proteins 94 8.5 Interaction of excretory mechanisms with phases I and II detoxification mechanisms 98 9 Future directions 101 9.1 The impact of genome sequencing projects 101 9.2 Chemical ecology and insect physiology 101 ADVANCES IN INSECT PHYSIOLOGY VOL. 35 Copyright r 2008 by Elsevier Ltd ISBN 978-0-12-374329-9 All rights of reproduction in any form reserved DOI: 10.1016/S0065-2806(08)00001-5 2 MICHAEL O’DONNELL 9.3 Ion channels and insect excretory mechanisms 102 9.4 Diuretic and antidiuretic agents as candidates for development of novel insecticides 103 Acknowledgements 104 References 104 1 Introduction Excretion refers to the processes which remove from the metabolic pool substances which interfere with metabolism. In this chapter I will consider three separate aspects of excretion, as first proposed by Maddrell (1971): (1) removal of molecules which are undesirable or perhaps even poisonous at all except very low concentrations; (2) excretion of molecules which are not toxic but merely useless, and which would become obstructive if allowed to accumulate and (3) excretion of molecules which are useful or essential but are present to excess. This would include excretion of water and physiological ions in some circumstances. In writing this chapter I have attempted to link recent advances in our understanding of the physiology, biochemistry, genetics, molecular biology and chemical ecology of insect excretory mechanisms to the fundamental principles of design established more than 30 years ago. For example, the primary ATP-dependent transporter in insect epithelia was referred to in the literature until the early 1990s as the ‘electrogenic alkali cation pump’. This pump is now known to reflect the integrated actions of two separate transporters, an electrogenic vacuolar-type H+-ATPase and an exchanger of Na+ or K+ and H+ (Maddrell and O’Donnell, 1992; Wieczorek, 1992; Rheault et al., 2007). Similarly, the high osmotic permeability of insect epithelial cells noted in early studies (O’Donnell et al., 1982) is now seen to be based on aquaporins (Echevarria et al., 2001; Kaufmann et al., 2005). A third example is the multialkaloid transporter responsible for elimina- tion of alkaloids such as nicotine, morphine and atropine by insect excretory organs (Maddrell and Gardiner, 1976). Recent studies suggest that this transporter is a P-glycoprotein (P-gp)-like transporter (Gaertner et al., 1998; Leader and O’Donnell, 2005) produced by expression of multidrug resistance (MDR) genes (Tapadia and Lakhotia, 2005). A recurrent theme of this review is that studies of insect excretory mechanisms frequently provide illustrations of the Krogh principle: ‘‘For a large number of problems there will be some animal of choice or a few such animals on which it can be most conveniently studied.’’ In many instances, these examples of the Krogh principle are a consequence of unusual diets, such as blood, or life in extreme environments, as is the case for the tenebrionid beetles of the Namibian desert or mosquito larvae found in saline lakes containing very high levels of magnesium and sulfate. INSECT EXCRETORY MECHANISMS 3 Adaptations to extreme environments, coupled with the large number of unusual food sources exploited by insects and their extraordinary diversity, provides a fertile ground for research into excretory mechanisms. Several reviews in the last decade have analyzed literature relevant to this work. Comprehensive studies of insect diuretic and antidiuretic hormones are provided by Gade et al. (1997) and Coast et al. (2002). A briefer analysis of recent work on endocrine control of salt balance in insects has been written by Coast (2007), and Orchard (2006) has reviewed the orchestration of diuresis and other physiological events in the hemipteran Rhodnius by the amine serotonin. Much of what we know about the functioning of the insect hindgut is due to the extensive work of Phillips and co-workers (Phillips et al., 1996). The dominant role of the vacuolar-type H+-ATPase in driving solute transport across plasma membranes of insect epithelial cells has been reviewed frequently (e.g. Wieczorek et al., 2000; Beyenbach and Wieczorek, 2006). The mechanism and regulation of secretory transport in Malpighian tubules of the yellow fever mosquito Aedes aegypti has been reviewed by Beyenbach (2003). The application of genetic, molecular biological and physiological tools has lead to tremendous advances in our understanding of the mechanisms and control of solute and water transport by the Malpighian tubules of the fruit fly Drosophila melanogaster. This area has been reviewed frequently, primarily by Julian Dow and Shireen Davies (Dow and Davies, 2003, 2006; Davies and Day, 2006). 2 Design principles underlying the insect excretory system The insect excretory system is comprised of the Malpighian tubules and the gut, especially the hindgut (Fig. 1). Each Malpighian tubule consists of a single-layer of squamous epithelial cells which form a blind-ended tube. Tubules range from 2 to 70 mm in length, 2–250 in number and up to 100 mm in diameter (Phillips, 1981). Transport of ions (primarily K+,Na+ and ClÀ) and osmotically obliged water into the tubule lumen produces a near isosmotic secreted fluid. Fluid secretion is accompanied by passive diffusion of small solutes into the lumen, as well as selective secretion of solutes, including toxins. Some KCl and water may be reabsorbed down- stream in a proximal segment of the Malpighian tubule or the anterior hindgut. The bulk of water, ion and metabolite reabsorption occurs downstream in the posterior hindgut, in particular the rectum, resulting in strongly hyperosmotic or hypoosmotic excreta. In many terrestrial species of insect, the hindgut can recover virtually all the water from the gut contents and fluid secreted into the gut by the Malpighian tubules. So effective are these water recovery systems that in the mealworm Tenebrio (Ramsay, 1971) and in the firebrat Thermobia (Noble-Nesbitt, 1970), for 4 MICHAEL O’DONNELL FIG.