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Some Aspects of the Sequestration of Cardenolides in the Large Milkweed Bug, Oncopeltus Fasciatus (Dallas) (Hemiptera: Lygaeidae)

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Some Aspects of the Sequestration of Cardenolides in the Large Milkweed Bug, Oncopeltus Fasciatus (Dallas) (Hemiptera: Lygaeidae) SOME ASPECTS OF THE SEQUESTRATION OF CARDENOLIDES IN THE LARGE MILKWEED BUG, ONCOPELTUS FASCIATUS (DALLAS) (HEMIPTERA: LYGAEIDAE) by LYNN MARIE VASINGTON MOORE B.Sc. (Magna Cum Laude) UNIVERSITY OF CONNECTICUT, 1975 M.Sc. UNIVERSITY OF MASSACHUSETTS, 1978 A THESIS SUBMITTED IN PARTIAL FULFILLMENT OF THE REQUIREMENTS FOR THE DEGREE OF DOCTOR OF PHILOSOPHY in THE FACULTY OF GRADUATE STUDIES DEPARTMENT OF ZOOLOGY We accept this thesis as conforming to the-f5e.auired standard April, 1985 (c) Lynn Marie Vasington Moore, 1985 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 or her representatives. It is understood that copying or publication of this thesis for financial gain shall not be allowed without my written permission. Department of The University of British Columbia 1956 Main Mall Vancouver, Canada V6T 1Y3 OE-6 (3/81) ii ABSTRACT Specific aspects of the selective sequestration, excretion and tolerance of cardenolides in the large milkweed bug, Oncopeltus fasciatus have been studied using spectrophotometry assays, thin-layer chromatography, tracer studies, in vivo tolerance assays, and enzyme inhibition techniques. The cardenolide content of the dorsolateral space, gut, wings and fat body of Oncopeltus fasciatus was examined. The results indicate that the majority of cardenolides sequestered in the insect are concentrated in the dorsolateral space, which confirms the basic pattern of quantitative distribution of cardenolides in fJ. fasciatus determined in earlier work. Large amounts of cardenolides were not found in the gut, wings and fat body. The female fat body contained 4-5% of the total cardenolide content of the insect. The cardenolide content of male fat body, and gut and wings of both sexes was below the detection limit of the cardenolide assay. Thin-layer chromatography was used to determine the cardenolide array of various tissues and secretions of fJ. fasciatus reared on seeds of a single species of milkweed (A. speciosa) and adult extracts and dorsolateral space fluid of 0. fasciatus reared on seeds of two species of milkweed with different cardenolide arrays (A. speciosa and A. syriaca)• The results indicate that cardenolides are not sequestered in the insect simply on the basis of polarity and that metabolism and differential excretion of cardenolides are involved in the sequestration of cardenolides in fJ. fasciatus.. The similarities in the cardenolide profiles of 0. fasciatus reared on different food sources, and tissues of fj. fasciatus reared on a single food source indicates that there is regulation of the cardenolide array in 0. fasciatus. An in vitro preparation of Malpighian i 1* i tubules was used to investigate the excretion of the polar cardenolide, ouabain, in 0. fasciatus. Both segments of the tubules were found to metabolize ouabain. The distal Segment (Segment II) secreted primary urine and ouabain. Secretion of ouabain by Segment II was not observed to occur against a concentration gradient and increased with increasing fluid secretion. The proximal segment (Segment I) reabsorbed fluid and ouabain but not metabolites of ouabain. Ouabain was reabsorbed against a strong concentration gradient (23-fold), was independent of fluid reabsorption, and increased with increasing fluid secretion by Segment II. In rapidly secreting Malpighian tubules (a situation of high cardenolide secretion by Segment II), the presence of Segment I reduced the excretion of ouabain by 84 - 93%, mainly by reducing ouabain concentration. It appears excretory loss of cardenolides can be reduced in 0. fasciatus and thus may be a factor in the sequestration of cardenolides in this insect. 0. fasciatus tolerated 1954x and 7288x, respectively, the LD50 ouabain dose of Schistocerca gregaria and Periplaneta americana when ouabain was injected into the hemocoel of these insects. The maximum ouabain dose that could be injected into 0_. fasciatus (200 nmoles) resulted in no mortality; this dose is higher than the lethal ouabain doses recorded for vertebrates and invertebrates. The ouabain concentration resulting in 50% inhibition (I50) of Na,K-ATPase activity was determined in lyophilates of nervous tissue of 0. fasciatus and brain and recta of j>. gregaria and were 2.0 x 4 6 6 lO" , 2.0 x 10" , and 1.0 x 10~ M, respectively. The I50 value for ouabain inhibition of Na,K-ATPase activity in the nervous tissue of 0_. fasciatus is higher than the I50 values for nervous tissue in most other insects as well as many other invertebrate and vertebrate iv tissues. Thus, the presence of ouabain resistant Na,K-ATPases appears to be a factor in the tolerance and sequestration of plant cardenolides in 0. fasciatus. V Table of Contents Page Abstract . ii Table of Contents v List of Tables viii List of Figures x Acknowledgements xii CHAPTER 1: GENERAL INTRODUCTION 1 Toxic plant compounds in plants and insects 1 Cardenolide chemistry and toxicity 2 Cardenolides and the Asclepiadaceae (milkweeds) 5 Ouabain and digitoxin 6 Cardenolide sequestration in insects 10 Oncopeltus fasciatus 11 Cardenolide sequestration in Oncopeltus fasciatus 13 CHAPTER 2: SELECTIVE SEQUESTRATION OF MILKWEED (ASCLEPIAS sp.) CARDENOLIDES IN ONCOPELTUS FASCIATUS 17 Summary 17 Introduction 18 Material and Methods 20 1) Insects 20 2) Collection of samples 20 3) Extraction of cardenolides 21 4) Cardenolide determinations 22 a) Total cardenolide concentrations 22 b) Determinations of cardenolide profiles with thin-layer chromatography (TLC) 23 vi Page Results 25 1) Total cardenolide content of the fat body, wings, gut and dorsolateral space fluid of fj. fasciatus reared on A. speciosa 25 2) Cardenolide profiles of 0 fasciatus reared on A speciosa and A. syriaca seeds 28 3) Cardenolide profiles of adult extracts, tissues and dorsolateral space fluid of 0. fasciatus reared on A. speciosa seeds 38 4) Geographic differences in the cardenolide profile of A. syriaca seeds 41 Discussion 43 CHAPTER 3: EXCRETION OF OUABAIN BY MALPIGHIAN TUBULES OF ONCOPELTUS FASCIATUS 50 Summary 50 Introduction 51 Material and Methods 52 1) Insects 52 2) Salines 53 3) In vitro Malpighian tubule preparation 53 4) Chromatography 55 Results 59 1) Characteristics of ouabain transport by Segment II 59 a) Secretion of ouabain by Segment II 59 b) Metabolism of ouabain by Segment II 65 2) Ouabain Reabsorption in Segment 1 65 vii Page a) Direct analysis 65 b) Set droplets 72 3) Modification of Segment II secretion by Segment 1 76 Discussion 79 CHAPTER 4: OUABAIN RESISTANT NA.K ATPASES AND CARDENOLIDE TOLERANCE IH THE LARGE MILKWEED BUG, ONCOPELTUS FASCIATUS 84 Summary 84 Introduction 85 Material and Methods 86 1) Insects 86 2) Ouabain injections 87 3) Na++K+ -dependent ATPase activity and ouabain sensitivity 88 Results 90 1) Sensitivity of insects to injections of ouabain into the hemocoel 90 2) Activity and ouabain sensitivity of Na++K+ -dependent ATPases in tissue lyophilates of 0. fasciatus and S^. gregaria 92 Discussion 99 CHAPTER 5: GENERAL DISCUSSION 108 Literature cited 113 viii List of Tables Page Table 2.1 Total cardenolide content of adult an 5th instar Oncopeltus fasciatus samples 26 Table 2.2 Rn, values of cardenolides and non-cardenolides detected in extracts of 0. fasciatus and its food sources, A. speciosa or A. syriaca 32 Table 2.3 The variability in cardenolide profiles of 0_. fasciatus and A..speciosa..'. 40 Table 2.4 Distribution of cardenolides in Oncopeltus fasciatus expressed as % of the adult total 44 • Table 3.1 Chromatographic systems used for the separation of cardenolides and their metabolites 57 Table 3.2 Ionic composition (mM) of whole-tubule secretions, reabsorbed fluid and bathing saline 73 Table 4.1 Survival of _0. fasciatus injected with 10 - 200 nmoles ouabain 91 Table 4.2 Post-injection recovery times of 0_. fasciatus 93 Table 4.3 Ouabain tolerance of CJ. fasciatus, _S. gregaria and P_. americana 96 Table 4.4 Total, Mg2+ and Na,K-ATPase activity of tissue lyophilates of 0_. fasciatus and S^. gregaria 98 Table 4.5 Inhibition of Na,K-ATPase activity by ouabain in nervous tissue of 0. fasciatus and brain and rectum of S. gregaria 102 ix Page Table 4.6 Effects of ouabain on tissue processes and survival in insect and millipede species 103 Table 4.7 Toxicity values for ouabain in invertebrates and vertebrates 105 X List of Figures Page Figure 1.1 General structure of cardenolides 4 Figure 1.2 General structures of the three groups of Asclepias cardenolides 7 Figure 1.3 The chemical structures of ouabain and digitoxin.... 9 Figure 2.1 Cardenolide profiles of A. speciosa and A. syriaca seeds and adult extracts and dorsolateral space fluid of fJ. fasciatus reared on each seed 30 Figure 2.2 Cardenolide profiles of 0. fasciatus adults, tissues and secretions and A. speciosa seeds 35 Figure 2.3 Cardenolide profiles of A. syriaca seeds from four geographic locations 42 Figure 3.1 In vitro preparation of rj. fasciatus Malpighian tubules 54 Figure 3.2 The effect of varying external ouabain concentration on urine-to-plasma (U/P) ratios 60 Figure 3.3 Effect of varying external ouabain concentration on fluid secretion rate 61 Figure 3.4 Effect of fluid secretion rate on the rate of ouabain secretion by Segment II alone 63 Figure 3.5 Effect of fluid secretion rate on ouabain concentration in fluid secreted by Segment II alone 64 Figure 3.6 Distribution of radioactivity in typical chromatograms of experimental and control fluids 66 xi Page Figure 3.7 Amount of fluid, ouabain, metabolised ouabain, and ouabain concentration in Segment II secretion, reabsorption droplets and whole-tubule secretion... 68 Figure 3.8 Amount of fluid secreted by whole tubule in 2 h in relation to ouabain reabsorption by Segment I during same time period 71 Figure 3.9 Change in fluid volume, radioactive label, and radioactive label concentration in four set droplets and whole-tubule secretion over 2 h 74 Figure 3.10 Rate of ouabain secretion with time 77 Figure 3.11 Ouabain concentration in secreted fluid with time.
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