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Feeding on Milkweeds (Asclepias Species) in Central California

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Feeding on Milkweeds (Asclepias Species) in Central California ASPECTS OF THE CHEMICAL ECOLOGY OF LYGAEID BUGS (ONCOPELTUS FASCIATUS AND LYGAEUS KALMII KALMII) FEEDING ON MILKWEEDS (ASCLEPIAS SPECIES) IN CENTRAL CALIFORNIA by MURRAY BRUCE ISMAN B.Sc, University of British Columbia, 1975 A THESIS SUBMITTED IN PARTIAL FULFILLMENT OF THE REQUIREMENTS FOR THE DEGREE OF MASTER OF SCIENCE, in THE FACULTY OF GRADUATE STUDIES (Department of Zoology) We accept this thesis as conforming to the required standard THE UNIVERSITY OF BRITISH'COLUMBIA April, 1977 (c) Murray Bruce Isman, 1977 In presenting this thesis in partial fulfilment of the requirements for an advanced degree at the University of British Columbia, I agree that the Library shall make it freely available for reference and study. I further agree that permission for extensive copying of this thesis for scholarly purposes may be granted by the Head of my Department or by his representatives. It is understood that copying or publication of this thesis for financial gain shall not be allowed without my written permission. Department of ZOOLOGY The University of British Columbia 2075 Wesbrook Place Vancouver, Canada V6T 1WS Frontispiece. Adult Oncopeltus fasciatus and Lygaeus kalmii kalmii (center) on a dehiscent pod of Asclepias fascicularis in Napa County, California. (iii) (iv) ABSTRACT A plant-insect allomonal system was investigated, involving seed bugs (Lygaeidae) on milkweeds (Asclepias spp.). The ability of the insects to sequester secondary compounds from host plants was studied in detail in central California. A colorimetric assay was used to quanitify the amount of cardenolides (cardiac glycosides) in the lygaeid bugs Oncopeltus fasciatus and Lygaeus kalmii kalmii and nine species of milkweed host plants. The cardenolide content of individual adult insects, deter• mined in microgram equivalents of digitoxin, varied from zero to over 300 pg per insect. Sources of variation of cardenolide content in the insects included interspecific and intraspecific differences in the cardenolide content of the host plant species, and also differences in the content of plant organs on which insects were feeding. When reared in the laboratory on a diet of milkweed seeds, the uptake of cardenolides by the bugs was proportional to the cardenolide content of the seeds. However, field collected lygaeids contained fewer cardenolides than were available in the plants on which they were feeding. This suggests that several ecological parameters, such as different reproductive phenologies and morphologies of the different host species, may interfere with the bugs' acquisition of cardenolides. fj. fasciatus and L. k. kalmii differ in their feeding require• ments, host plant utilization, and ability to sequester cardenolides from their hosts. However, the larval growth and development of (v) CJ. fasciatus and L_. k_. kalmii in the laboratory on seeds of different milkweed species did not vary with plant species or cardenolide content of the seeds. Therefore, seeds of all plant species were equally suitable as food sources for the bugs. The colonization pattern of CJ. fasciatus on species of Asclepias in north central California suggests.that this species does not maximize its opportunities to sequester large quantities of cardenolides from potential hosts. Over 50 per cent of field collected lygaeids in this study contained less than 50 yg of cardenolide. The ecological sig• nificance of cardenolide sequestration by lygaeids as a defensive strategy may depend on several modes of pharmacological activity in potential vertebrate predators, not simply emetic potential. Alternately, the presence of volatile secretions from the scent glands and histamine-like compounds in the dorso-lateral space fluid of (). fasciatus and I. k_. kalmii could be more important than sequestered cardenolides as anti-predator strategies. The data suggest that the effectiveness of cardenolide seques• tration as a chemical defense strategy may vary over the geographical range of these insect species, and may vary in the course of a season at a particular location. Therefore, cardenolide sequestration does not appear to be a crucial aspect in the feeding and population ecology of these lygaeid species at least in central California. (vi) TABLE OF CONTENTS Page Title Page i Frontispiece iii Abstract iv Table of Contents vi List of Tables vii List of Figures ix Acknowledgements xi I INTRODUCTION 1 II MATERIALS AND METHODS A. Field Study of Milkweeds and Lygaeids 6 B. Extraction of Cardenolides from Plant Material 9 C. Colorimetric Assay of Cardenolides 11 D. Extraction of Cardenolides from Lygaeids 12 E. Laboratory Rearing of Lygaeids 15 III RESULTS A. Milkweed Flora and Lygaeid Fauna 20 B. Cardenolide Content of Plant Material 25 C. Cardenolide Content of Field Collected Lygaeids 32 D. Cardenolide Content of Laboratory-Reared Lygaeids 47 E. Larval Growth and Development of Lygaeids on 47 Different Species of Milkweed in the Laboratory IV Discussion 73 References 97 (vii) LIST OF TABLES Table Page I Occurrence of CL fasciatus and L^. k. kalmii on different 12 SDecies of Asclepias in two areas of California, summer 1976 II Gross cardenolide content of seed of Asclepias species 27 from California III Gross cardenolide content of plant samples of Asclepias 29 from California IV Gross cardenolide content of CJ_. fasciatus and L^. k_. 36 kalmii collected on Asclepias in central California in 1976 V Temporal variation in gross cardenolide content of field 44 collected CL fasciatus from central California VI Gross cardenolide content of (3. fasciatus and L. k. 48 kalmii reared in the laboratory at 25°C on milkweed seed VII Gross cardenolide content of CJ. fasciatus reared in the 51 the laboratory at 21oC on milkweed seed VIII Duration of larval development and teneral adult wet 57 weight of 0_. fasciatus reared in the laboratory at 25°C on the seeds of different species of Asclepias and Helianthus IX Duration of larval development and teneral adult wet 58 weight of I. k. kalmii reared in the laboratory at 25°C on the seeds of different species of Asclepias and Helianthus X Influence of sequestered cardenolides on larval 59 development of 0_. fasciatus reared in the laboratory at 21°C on the seeds of different species of Asclepias XI Adult body weight of CJ. fasciatus reared in the laboratory 65 at 21°C on the seeds of different species of Asclepias XII Pronotal width of adult CJ. fasciatus reared in the 69 laboratory at 21°C on the seeds of different species of Asclepias Comparison of female to male ratios for teneral wet weight and cardenolide content of 0_. fasciatus reared on different seed diets Correlations between mean cardenolide content and means of body weight, body size and larval duration in fj. fasciatus reared in the laboratory at 21°C on the seeds of different species of Asclepias (ix) LIST OF FIGURES Page Frontispiece Adult Oncopeltus fasciatus and Lygaeus kalmii 111 kalmii (center) on a dehiscent pod of Asclepias fasicularis in Napa County Cal i form'a Figure 1 Structures of some cardenolides 3 2 Map of California showing localities where 7 milkweed plants were examined and plant material collected Fruiting season in native Californian Asclepias 24 species, and the population trend of fJ. fasciatus at one milkweed stand 4 Gross cardenolide content of seed of Asclepias 31 species from California 5 Gross cardenolide content of plant samples of 34 Asclepias from California 6 Gross cardenolide content of field collected 38 CJ. fasciatus 7 Gross cardenolide content of field collected 40 L. k_. kalmi i 8 Comparison of gross cardenolide contents of 42 field collected 0. fasciatus and L. k. kalmii 9 Gross cardenolide content of field collected 46 lygaeids: distribution of classes based on cardenolide content 10 Relationship between cardenolide concentration 50 in the diet (milkweed seeds) and the cardenolide content of adult (J. fasciatus and L_. k_. kalmii 11 Relationship between cardenolide concentration 53 in the diet (milkweed seeds) and the cardenolide content of adult male and female fJ. fasciatus reared at 21°C Relationship between duration of larval development and teneral wet weight of 0. fasciatus and _L. J<. kalmii reared in the laboratory at 25°C on seeds of different species of Asclepias and He!ianthus Weight gain in fJ. fasciatus and L k. kalmii during larval development, reared in the laboratory at 25°C on the seeds of A. fascicularis Relationship between gross cardenolide content and duration of larval development of fJ. fasciatus reared in the laboratory at 21°C on the seeds of different species of Asclepias Relationship between gross cardenolide content and adult body weight of Cj. fasciatus reared in the laboratory at 21°C on the seeds of different species of Asclepias (xi) ACKNOWLEDGEMENTS I would like to express my sincerest thanks to Prof. G.G.E. Scudder, who, as my research supervisor, provided invaluable encouragement, criticism, and guidance throughout the course of this study. His time consuming assistance in the preparation of manuscripts derived from this thesis for publication is most appreciated. Although not officially recognized as a co-supervisor, Dr. S.S. Duffey generously provided working space and supplies during a five month stay in his laboratory in the Department of Entomology, University of California at Davis. His combination of patience and pressure helped me to overcome my inertia in dealing with the phytochemical techniques required to do this study. I would also like to express my thanks to Dr. C. Juddson and the Department of Entomology for allowing me the use of the spectrophotometer. Ken E. Evans receives special thanks for sending several packages of milkweed seeds, which established the foundation for this study. I also thank Ken for permission to reproduce his photograph which appears as the frontispiece of this thesis. I will remember Ken not only for providing plant material and some insects, but also for our stimulating discussions in regard to our respective studies of lygaeids. Finally, Ken's enthusiasm on our joint collecting trips made the field work a pleasure.
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