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POPULATION DYNAMICS of the SYCAMORE APHID (Drepanosiphum Platanoidis Schrank)

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POPULATION DYNAMICS of the SYCAMORE APHID (Drepanosiphum Platanoidis Schrank) POPULATION DYNAMICS OF THE SYCAMORE APHID (Drepanosiphum platanoidis Schrank) by Frances Antoinette Wade, B.Sc. (Hons.), M.Sc. A thesis submitted for the degree of Doctor of Philosophy of the University of London, and the Diploma of Imperial College of Science, Technology and Medicine. Department of Biology, Imperial College at Silwood Park, Ascot, Berkshire, SL5 7PY, U.K. August 1999 1 THESIS ABSTRACT Populations of the sycamore aphid Drepanosiphum platanoidis Schrank (Homoptera: Aphididae) have been shown to undergo regular two-year cycles. It is thought this phenomenon is caused by an inverse seasonal relationship in abundance operating between spring and autumn of each year. It has been hypothesised that the underlying mechanism of this process is due to a plant factor, intra-specific competition between aphids, or a combination of the two. This thesis examines the population dynamics and the life-history characteristics of D. platanoidis, with an emphasis on elucidating the factors involved in driving the dynamics of the aphid population, especially the role of bottom-up forces. Manipulating host plant quality with different levels of aphids in the early part of the year, showed that there was a contrast in aphid performance (e.g. duration of nymphal development, reproductive duration and output) between the first (spring) and the third (autumn) aphid generations. This indicated that aphid infestation history had the capacity to modify host plant nutritional quality through the year. However, generalist predators were not key regulators of aphid abundance during the year, while the specialist parasitoids showed a tightly bound relationship to its prey. The effect of a fungal endophyte infecting the host plant generally showed a neutral effect on post-aestivation aphid dynamics and the degree of parasitism in autumn. However, density of oviparae was suppressed on endophyte infected plant material. This, together with premature leaf fall of endophyte leaves, has the capacity to curtail the autumn aphid population, which may result in low aphid density in the following spring. In autumn, third generation aphids gave rise to a female-biased sex ratio. Oviparae were always laid first in the progeny sequence followed, after a brief reproductive pause, by males. Nymphal development time was longer in oviparae than in males, and was accelerated on good host plant quality. Improved nutritional status of the host induced the production of a greater proportion of males, reduced development time of sexual morphs, and increased their survival. In addition, the potential fecundity of oviparae was a function of maternal body weight and host quality. 2 Oviparae mainly laid their eggs in clusters on the rough bark surfaces of tree trunks and branches, away from the more exposed smooth surfaces of twigs and terminal buds. Fierce intra-specific competition among oviparae for optimal overwintering sites was seen at high density. Egg mortality was a function of time in hibernation, with the greatest mortality rates occurring in mid to late winter. March temperature was shown to be important in determining the time of egg hatch and bud burst. The preceding autumnal and spring aphid densities were positively related. These findings suggest that while host plant food quality was a key factor in determining aphid abundance, density-independent seasonal and meterological variables were the over-riding components driving the population dynamics of D. platanoidis. 3 DECLARATION The work described in this thesis is entirely my own, except for the inputs from the following people in the chapter below: Chapter 5 - Aspects of overwintering in the sycamore aphid. Dr. Simon Leather permitted the use of field data on sycamore aphid eggs collected during the winters of 1982 to 1991 at Bush N.R.S., Edinburgh, Scotland. He also allowed data on the number of sycamore aphid eggs, time of fundatrix appearance and bud burst recorded during the winters of 1992 to 1997 at Silwood Park, Berkshire, England to be used. In addition, Mr. James Culverhouse provided computerised data on the aerial March temperatures at Silwood Park during 1993 to 1998. However, all the data handling and analyses were performed by me. Signed C-I2 A A c's-c'L-12- Frances Antoinette Wade (Student) Confirmed Dr. Simon Leather (Supervisor) Prof. Charles Godfray (Supervisor) 4 To A.M.D.G., my Parents, the late Professor Kinmonth and staff of St. Thomas'. "It is not the critic who counts; not the man who points out how the strongman stumbles, or uhere the doer ofdeeds could actually haw done better. The credit belongs to the man who is actual& in the arena, whose face is marred by dust and sweat and blow uho strives valiantly; who errs and comes short again and again; Because there is not on&about error and shortcomings; but who does actually strive to do the dee4 ub knows great enthusiasm, the great devotion, who spends himself in a worthy cause; who at best knows in the end high achie-cement and who, at the uvrst, if he fails, at least he fails while daring greatly. So that his place shall never be with those cold and timid souls who know neither victory nor defeat." - Taken from "For him read her" by Theodore Roose-celt. 5 ACKNOWLEDGEMENTS I would like to thank my two supervisors, Dr. Simon R. Leather and Prof. H.C.J. Godfray, for their technical support and rapid feedback during this project, and to the Natural Environment Research Council (N.E.R.C.) for funding this studentship (Grant No. GT4/95/1 80/T). My gratitude is expressed to the `Aphid/Drosphila Research Group' for informal discussions, and especially Christine Muller, Lex Kraaijeveld and Donald Quicke for stimulating feedback. Recognition should be made towards Mike Cammell, Mick Crawley and particularly Jim Hardie for their inspiration and help. The comments from Nigel Barlow of AgResearch New Zealand were also greatly appreciated. Thanks also go to Frank van Veen, Darren Greene, Mark Fellows and Milton Mendota for their snippets of advice and moreover their entertaining company over the last three years. My sincere appreciation is owed to Dominik Wodarz whose patient help with manuscript reading and special friendship has been invaluable. To Nicholas Jarraud for his constant support and tea break chats throughout this Ph.D. — it shall never be forgotten. To Patricia Walker, Kingsley Shadish and Mike Haynes for their friendship, kindness and constructive advice. To Aunty Pauline and Aunty Anne in reception for their stalwart encouragement and sense of humour. To Carole Collins and Anne-Marie Sarney for always being willing to help quickly with administrative duties and in any other way they can. To Peter Muller, Sim Adamson and Martin Couchman for their computer support and technical advice. Not forgetting Martin Parsons for his constant stream of witticisms while I was student warden at Silwood Park, and Sharon Ives also in the accommodation office offering great cheer. Last, but by no means least, special thanks to go to my parents who have given me constant support and love throughout this project. 6 CONTENTS Abstract 2 Declaration 4 Acknowledgements 6 Contents 7 List of Figures 9 List of Plates 13 List of Tables 14 Chapter 1: General Introduction Introduction 15 Dynamics of phytophagous forest insect populations 15 Theory of population regulation 17 Dynamic behaviour of phytophagous forest insect populations 19 Factors affecting population dynamics of phytophagous forest insects 20 The study organism 27 Overall aims of the thesis 28 Thesis outline 28 Chapter 2: Population dynamics and life history responses of Drepanosiphurn platanoidis (Schrank), on saplings with different initial aphid densities Abstract 30 Introduction 31 Methods & Materials 34 Results 39 Discussion 51 Conclusion 59 Chapter 3: Does endophytic fungal infection affect the dynamics of the sycamore-aphid-parasitoid interaction? Abstract 60 Introduction 61 Natural history 64 Methods & Materials 65 Results 70 Discussion 79 Conclusion 85 7 Chapter 4: Reproductive sequencing and the sex ratio of the sycamore aphid Abstract 87 Introduction 88 Methods & Materials 92 Results 97 Discussion 111 Conclusion 118 Chapter 5: Aspects of overwintering in the sycamore aphid Abstract 119 Introduction 120 Methods & Materials 124 Results 129 Discussion 148 Conclusion 154 Chapter 6: General Discussion 156 References 164 Appendix: Preliminary pesticide screening 183 8 LIST OF FIGURES Fig. 2-1. The effects of season on the natural aphid population trends of Drepanosiphum platanoidis between autumn 1996 and spring 1997 40 Fig. 2-2. Correlation between the spring and the autumn aphid populations 40 Fig. 2-3. The effect of four aphid load treatments on cumulative aphid densities in spring and autumn 1997 41 Fig. 2-4. The effect of four aphid density treatments in spring 1997 on the 1997autumnal populations of Drepanosiphum platanoidis 42 Fig. 2-5 i: The numerical response of anthocorids to spring aphid densities 44 Fig. 2-5 ii: The numerical response of anthocorids to autumnal aphid densities 44 Fig. 2-5 iii: The numerical response of coccinellids to spring aphid densities 44 Fig. 2-5 iv. The numerical response of coccinellids to autumnal aphid densities 44 Fig. 2-5 v: The numerical response of arachnids to spring aphid densities 45 Fig. 5 vi: The numerical response of arachnids to autumn aphid densities 45 Fig. 2-5 vii: The numerical response of syrphid larvae to spring aphid densities 45 Fig. 2-5 viii: The numerical response of syrphid larvae to autumn aphid densities 45 Fig. 2-5 ix: The numerical response of total primary parasitoids to spring aphid densities 45 Fig. 2-5 x: The numerical response of total primary parasitoids to autumn aphid densities 45 Fig. 2-6 i: Mean duration of the first, second and third instar nymphal development times for generations two and three of Drepanosiphum platanoidis in relation to aphid density treatment 47 Fig.
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