Variability among individuals and populations: implications for arthropod physiology John S. Terblanche Dissertation presented for the Degree of Doctor of Zoology at the University of Stellenbosch Promoter: Professor Steven L. Chown April 2006 Stellenbosch University http://scholar.sun.ac.za Declaration I, the undersigned, hereby declare that the work presented in this dissertation is my own original work and that I have not previously in its entirety or in part submitted it at any university or institution for a degree. Signature……………............ Date…………………………. ii Stellenbosch University http://scholar.sun.ac.za Abstract Within arthropods, inter-individual and inter-population variation is generally poorly explored for physiological parameters. Such physiological variability is important, as it can provide insight into the capacity for evolutionary adaptation and how animals may cope with anthropogenic climate change. Insect vectors of human and animal diseases, such as tsetse flies (Diptera, Glossinidae) which carry trypanosomes, are of particular interest. Predictions of tsetse fly (Glossina spp.) range expansion, possibly paralleled by increased disease occurrence, have been made under future climate scenarios. Moreover, since there are generally strong relationships between abiotic variables (e.g. temperature and moisture availability), population dynamics, distribution and abundance, determining the physiological mechanisms influencing such relationships has utility for predictive modelling of spatial and temporal changes in tsetse fly distributions. I investigated physiological variation among individuals and populations, focusing mainly on Glossina spp. but using other arthropods to address certain issues. Specifically, I show the following: i) metabolic rate is repeatable (intra-class correlation coefficient) within individuals, and may be influenced by several factors such as age, gender, body mass and pregnancy; ii) while metabolic rate is repeatable within individuals, it remains unaltered with acclimation to laboratory conditions from field collection; iii) within a population, metabolic rate-temperature relationships are surprisingly invariant among physiological states such as age, gender, feeding status, pregnancy and temperature acclimation; iv) the magnitude of the effect of temperature acclimation differs among traits, in that upper thermal tolerances respond less than lower thermal tolerances, while metabolic rate responds to heat but not to cold. Water loss rate is relatively unresponsive to either treatment; v) plasticity can account for most inter-population variation in physiological traits related to climatic stress resistance (e.g. thermotolerances and desiccation rates) in the natural environment; vi) adult physiological performance responds differently to developmental and adult acclimation, such that marked trait- specific variation occurs, and combinations of both developmental and adult plasticity can result in further alteration of adult performance. These results have implications for the evolution of stress resistance to abiotic factors in these and other arthropods. I conclude by discussing the potential physiological patterns linking population dynamics and abiotic factors, with particular reference to tsetse flies. iii Stellenbosch University http://scholar.sun.ac.za Opsomming Binne arthropoda, is tussen-individu en tussen-bevolking variasie in die algemeen sleg bestudeer vir fisiologiese parameters. Hierdie fisiologiese variasie is belangrik want dit kan insig gee in die mate van evolusionêre aanpassing en hoe diere antropogenies klimaatsverandering kan hanteer. Dit is veral belangrik in die geval van insekte wat mens- en diersiektes kan dra, soos tsetse vlieë (Diptera, Glossinidae) wat trypanosome oordra. In die geval van tsetse vlieë (Glossina spp.) is voorspellings vir verhoogde verspreiding, en gevolglik verhoogde siekte voorkoms, gemaak onder toekomstige voorkoms klimaat senario’s. Verder, aangesien daar in die algemeen sterk verwantskappe tussen abiotiese parameters (bv. temperatuur en water beskikbaarheid), bevolkingsdynamika, verspreiding en voorkoms is, is die bepaling van die fisiologiese meganisme, wat ‘n invloed het op hierdie verwantskappe, nuttig vir die voorspelling van tsetse oor spasie en tyd. Hier, met hoofsaaklik die gebruik van Glossina spp., maar ook ander arthropoda wanneer dit nodig is, word navorsing wat fisiologiese variasie tussen individue en bevolkings aanspreel voorgelê. Spesifiek, word dit gewys dat i) metaboliese tempo is herhaalbaar (intra-klas korrelasie koeffisient) binne individue, alhowel metaboliese tempo kan beinvloed word deur faktore soos ouderdom, geslag, liggaamsmassa en swangerskap, ii) terwyl metaboliese tempo binne individue herhaalbaar is, verander dit nie met akklimasie na laboratorium toestande vanaf versameling in die veld, iii) binne ‘n bevolking metaboliese tempo-temperatuur verwantskappe is verbasend eenders tussen fisiologiese toestande soos ouderdom, geslag, voeding staat, swangerskap en temperatuur akklimasie, iv) die grootte van die effek van temperatuur akklimasie verskil tussen eienskappe, en die boonste termiese limiete reageer minder as laer termiese limiete, terwyl metaboliese tempo reageer op hitte maar nie koue nie, en waterverlies tempo is relatief terughoudend tot enige temperatuur toestand, v) buigbaarheid kan die meeste van inter-bevolkingsvariasie in fisiologiese eienskappe van klimaatstres weerstandsvermoë (termiese toleransie en uitdrogingstempo) in die natuurlike omgewing verklaar, vi) volwasse fisiologiese prestasie reageer verskillend op ontwikkelende en volwasse akklimasie, soveel dat eienskap-spesifieke variasie kan voorkom, en ‘n kombinasie van beide ontwikkelende en volwasse buigbaarheid ‘n verskillende volwasse prestasie tot gevolg kan hê. Hierdie resultate het implikasies vir die evolusie van weerstandsvermoë tot abiotiese faktore in hierdie en ander arthropoda. Hierdie tesis word afgesluit met ‘n bespreeking van die moontlikke fisiologiese patrone wat bevolkingsdinamika en abiotiese faktore kan verbind, met ‘n fokus op tsetse vlieë. iv Stellenbosch University http://scholar.sun.ac.za Acknowledgements I am sincerely grateful to Steven Chown for his constructive supervision. Steven, thank you for correcting my thinking when erroneous, encouraging me when my ideas were unclear or vague, and most importantly, the space to exercise my mind both philosophically and academically. I am also indebted to Steven for providing financial support and several important opportunities for me to travel, grow and develop as a scientist. I am indebted to Jaco Klok for driving my arthropod physiological education, without which this project would never have started. I sincerely appreciate the time and effort discussing the work, and aiding in the transition from vertebrate to invertebrate physiology. Furthermore, Jaco’s experimental wisdom and patience with teaching and formulating new ideas, has helped me progress through difficult times, both in the field and in the laboratory. ‘Laat hy val waar hy wil!’ I am thankful to the SPACE Group for discussion and comments on the work presented in this thesis, in particular Brent Sinclair, Elrike Marais and Jacques Deere. Both Elrike and Jacques held several discussions of phenotypic plasticity and repeatability which enabled me to develop some important ideas in this thesis. I am thankful for the professional and skilled laboratory assistance of Henry Davids, Larissa Heyns and Erika Nortje at several stages in this project. I owe a huge debt of thanks to Brent Sinclair, Steven Chown, Jaco Klok and Sue Jackson for facilitating or providing the opportunity to participate in trips to Antarctica, Marion Island, Europe and East Africa. Spectacular places, good memories! To my friends, Marc Rütschlin, Clinton Martinengo, Maarten Turkstra, Carl Kritzinger and Ben Harper for patiently listening to my problems, providing motivation, and simply being there. I am eternally indebted to my family, Charlene and Benjamin Herr for their unwavering support, love, wisdom and assistance in any project that I have chosen to undertake. v Stellenbosch University http://scholar.sun.ac.za Finally, this work would not be possible without the support and love provided by Susana Clusella Trullas. Thank you for discussion and insight throughout the course of this work. Your interest in natural history, wildlife, conservation, rock climbing, as well as your honesty and intellect, provide me with great happiness and inspiration. vi Stellenbosch University http://scholar.sun.ac.za Table of Contents Title page i Declaration ii Abstract iii Opsomming iv Acknowledgements v Table of Contents vii Chapter 1. General Introduction 1 Physiological Variability and Adaptation 6 Physiological Plasticity and Phenotypic Flexibility 7 Thesis Goals 10 Tsetse Flies as a Model Organism for Understanding Vectors of Disease in a World of Changing Climate 13 Tsetse Biology 16 Desiccation and Water Balance in Tsetse 19 Critical Thermal Limits in Tsetse 20 Metabolic Rate in Tsetse 23 Summary 24 References 25 Chapter 2. Metabolic rate variation in Glossina pallidipes (Diptera: Glossinidae): gender, ageing and repeatability 40 Introduction 41 Materials and methods 43 Results 46 Discussion 48 Acknowledgements 55 References 56 vii Stellenbosch University http://scholar.sun.ac.za Chapter 3. Metabolic rate in the whip-spider, Damon annulatipes (Arachnida: Amblypygi) 62 Introduction 63 Materials and methods 65 Results 69 Discussion 73 Acknowledgements