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Studies on the dispersal behaviour of apterous pea aphids acyrthosiphon pisum (Harris) Roitberg, Bernard D. 1978

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STUDIES ON THE DISPERSAL BEHAVIOUR OF APTEROUS PEA APHIDS Acyrthosiphon pi sum (Harris) by BERNARD DAVID ROITBERG B.Sc , Simon Fraser Univers i ty, 1976 A THESIS SUBMITTED IN PARTIAL FULFILLMENT OF THE REQUIREMENTS FOR THE DEGREE OF MASTER OF SCIENCE in THE FACULTY OF GRADUATE STUDIES DEPARTMENT OF PLANT SCIENCE We accept th is thesis as conforming to the required standard THE UNIVERSITY OF BRITISH COLUMBIA December, 1977. Bernard David Roitberg, 1977. In presenting th i s thes is in pa r t i a l fu l f i lment of the requirements for an advanced degree at the Un ivers i ty of B r i t i s h Columbia, I agree that the L ibrary sha l l make it f ree ly ava i l ab le for reference and study. I fur ther agree that permission for extensive copying of th is thesis for scho lar ly purposes may be granted by the Head of my Department or by his representat ives. It is understood that copying or pub l i ca t ion of this thes is for f inanc ia l gain sha l l not be allowed without my written permission. Department of ''P Ic » V £ t_ , c <^ The Univers i ty of B r i t i s h Columbia 2075 Wesbrook Place Vancouver, Canada V6T 1W5 Date i i ABSTRACT The dispersal behaviour of apterous pea aphids, Acyrthosipon pi sum (Harris) was studied in the laboratory and f i e l d . In the laboratory, aphids exhibited two types of behaviour while on the ground, a f te r drop-ping from plants in response to predators. Most aphids showed a high frequency of turning and tended to return to the plant they l e f t , while a smaller proportion walked in stra ight l ines and did not return to the plant they l e f t . Adults and older nymphs had the highest proportion of indiv iduals which showed the second type of behaviour and adults showed the greatest tendency to disperse to plants more distant than the nearest avai lable plants. Young instar aphids were less successful at locat ing a host than older nymphs and adults. Aphids were placed on the central bean seedlings within p lo t s , inside large f i e l d cages. Adult cocc ine l l i d s were released into two of the cages while the other cage remained predator-free. Aphids in the cages with predators frequently moved between plants, while aphids in the predator-free cage did not. Adult aphids colonized more plants and had a lower morta l i ty while on the ground than a l l other ins tar s . Aphids did not show a preferred dispersal d i rect ion and the distance dispersed by aphid nymphs was proportional to the density of aphids on the plant they l e f t . The importance of emigrating apterae in the exp lo i tat ion of new resources and the regulation of aphid populations i s discussed. Bean plants infected with an aphid transmitted virus were trans-planted into the central pos it ion of bean plots in the f i e l d cages. i i i Aphids were placed on the central infected plants and adult cocc ine l l i d s were released into two of the three cages for three days. Aphids f r e -quently moved to other plants from the centre infected plant in the two cages with predators but not in the predator-free cage. When plants were examined two weeks l a t e r , s i g n i f i c an t l y more plants were infected with virus in the cages.with predators than in the predator-free cage. New virus infect ions were correlated with plants that were v i s i t ed or colonized by aphids from the central infected plant. The influence of predators in the spread of aphid transmitted diseases is discussed. In laboratory experiments, pea aphids from Vancouver were presented with alarm pheromone from i r r i t a t e d conspecif ics. Adult and fourth in s tar aphids responded to the pheromone by e i ther dropping, running or backing up. Instars one, two and three responded to the pheromone only when a vibratory stimulus accompanied i t . A high proportion of a l l instars responded to the double stimulus by dropping. When adult aphids from Vancouver and Kami oops were presented with alarm pheromone, the Kamloops adults exhibited a more conservative reaction to alarm pheromone. Kami oops adults also were more conservative about leaving the i r plant when confronted by a c occ i ne l l i d predator. A hypothesis i s presented, which accounts for the differences in escape reactions between instars and biotypes. The hypothesis takes into consideration predation r i s k , escape behaviour repertoire and survival on the ground. Pea aphid adults res isted heat paralys is longer than f i r s t instars when subjected to high temperature treatments. A l l aphids succumbed to paralys is sooner at 42°C than at 37.5°C, but there appeared to be no i v difference in aphid survival in dry compared to moist conditions at high temperatures. Kami oops aphids were not more res i s tant to high temperatures. ACKNOWLEDGEMENTS Many people have contributed to the work contained in th i s thesis and I appreciate the i r help. My supervisor, Dr. Judy Myers, has provided a great deal of assistance f i n a n c i a l l y , i n t e l l e c t u a l l y , and phys ica l ly throughout th i s project. Dr. Bryan Frazer has been a constant source of ideas and help. Mr. Dave Ro l lo , Dr. Bob E l l i o t t , and Dr. Mitch Trimble a l l read e a r l i e r drafts of papers contained herein, and provided useful suggestions. Dr. Ron Forbes and Dr. Richard Hamilton of Agr icu l ture Canada helped me by suggesting ideas pertaining to aphid s t y le t s and for providing a su itable plant v i ru s , respect ive ly. Ms. Rosemarie Iyer, Ms. Carol Hubbard, and Ms. Maggie Chang gave much needed assistance in both the laboratory and f i e l d . Mr. Don Pearce and his crew maintained excel lent f i e l d conditions at the Vancouver study s i t e , as did the crew at Agr iculture Canada, Kami oops. Many other people have contributed as wel l and I thank a l l of them, pa r t i c u l a r l y my committee, Drs. Myers, Wellington, Frazer and Runeckles for t he i r help. vi TABLE OF CONTENTS Page APPROVAL i ABSTRACT i i ACKNOWLEDGEMENTS v TABLE OF CONTENTS vi LIST OF TABLES v i i LIST OF FIGURES v i i i INTRODUCTION 1 CHAPTER I DISPERSAL DYNAMICS 5 CHAPTER II THE SPREAD OF A PLANT VIRUS 34 CHAPTER III ADAPTATION OF ALARM PHEROMONE RESPONSES 43 CHAPTER IV ESCAPE REACTIONS AND POSSIBLE EFFECTS OF HIGH TEMPERATURE ON DISPERSAL SUCCESS 58 CONCLUSIONS 67 REFERENCES 72 v i i LIST OF TABLES Page Table 1. Behaviour of each instar of the pea aphid a f ter dropping from a plant in the laboratory 11 Table 2. Comparison of pea aphids showing running and searching behaviour 12 Table 3. Aphid movements in re la t ion to the locat ion of cocc ine l l i d s . 18 Table 4. Direct and ind i rect pea aphid morta l i t ie s from cocc ine l l id -aph id interact ions 22 Table 5. Comparison of success of three age classes of the pea aphid in f inding new host plants, a f ter leaving t he i r host . 23 Table 6. Spread of Bean Yellow Mosaic virus by pea aphids in predator-containing and predator-free cages 41 Table 7. The repeatab i l i t y of pea aphid responses when exposed to alarm pheromone on consecutive days 52 Table 8. Paralys is times of f i r s t instar and adult pea aphids from Vancouver and Kami oops at 2 temperatures and 2 humidity treatments 68 vi i i LIST OF FIGURES Page Figure 1. A conceptual model of a predator-pea aphid interact ion . . . 4 Figure 2. Comparison of search and run behaviour paths by adult pea aphids (drawn to sca le) . The points indicate the posit ion of the aphid at f i ve second in te rva l s . P = host plant. S = posit ion of aphid a f te r i t drops from the plant 10 Figure 3. The re lat ionsh ip between the distance a young nymph dispersed and the density of aphids on the plant from which the aphid l e f t . The number beside each point indicates the sample s ize 19 Figure 4. The re lat ionsh ip between the distance an old nymph dispersed and the density of aphids on the plant from which the aphid l e f t 20 Figure 5. The re lat ionsh ip between fecundity and dispersal in pea aphids. The number beside each point indicates the sample s i ze . ND = non-dispersers; C = aphids in predator-free cage. 21 Figure 6. The frequency d i s t r ibut ions of dispersal distance in three age classes of the pea aphid in the laboratory and f i e l d . 1 = Adults; 2 = Old nymphs; 3 = Young nymphs . . 24 Figure 7. The spread of BYMV by pea aphids in cages with and without c occ i ne l l i d predators 42 Figure 8. Responses of d i f fe rent age classes of the pea aphid to a vibratory stimulus. The number beside each point indicates the number of aphids tested 49 Figure 9. Types of responses to pheromone stimulus by pea aphids. Second and th i rd instar aphids respond s im i l a r l y to f i r s t instar aphids 50 i x Page Figure 10. Types of responses to a pheromone-vioratory stimulus by pea aphids. Second and th i rd instar insects respond s im i l a r l y to f i r s t ins tar insects 51 Figure 11. Comparative responses of Vancouver and Kami oops aphids to pheromone and pheromone-vibratory st imul i 53 Figure 12. Responses of adult Kamloops and Vancouver pea aphids in a d i rect confrontation with an adult c occ i ne l l i d 69 1 INTRODUCTION The pea aphid Acrythosiphon pi sum (Harris) i s preyed upon by a large number of natural enemies. These include Syrphids (Diptera), Chrysopids (Neuroptera), Anthocorids (Hemiptera), Cocc inel l ids (Coleoptera), Hymenop-teran paras ites, and many other more general predators. The pea aphid has evolved a repertoire of escape behaviours to prevent capture. The aphid may kick at natural enemies which are s imi la r in s ize (Evans, 1976), but in the presence of larger predators, they e i ther run from the predator or drop from the plant (Dixon, 1958). The dropping behaviour is the major topic of th i s thes i s . The fact that pea aphids read i ly drop from the i r plant suggests that they are able to e i ther return to the i r o r ig ina l host plant or locate a new plant. Host f inding behaviour has been extensively studied in alate aphids (Kring, 1972) but r e l a t i v e l y l i t t l e research has been conducted on the apterous morphs. Ferrar (1969) has demonstrated that Myzus persicae (Sulzer) do not u t i l i z e o l factory cues when searching for a plant and Niku (1973) reported that A. pi sum responds to ve r t i ca l objects when on the ground af ter dropping from a plant. The actions of natural enemies may enhance the spread of pea aphids throughout a crop. In the laboratory, the presence of predators (Niku, 1972) and parasites (Tamaki et al_., 1970) was correlated with the spread of apterous pea aphids. Blanchard (1934) reported that sp r ingta i l harrowing can reduce pea aphid spread and Cooke (1970) showed that r i l l i r r i g a t i o n reduces the spread of pea aphids more e f f ec t i ve l y than spr ink ler i r r i g a t i o n . 2 Both r i l l i r r i g a t i o n and harrowing reduced the movement of apterous aphids between rows, suggesting that cu l tura l practices may reduce aphid outbreaks. Niku (1975) has shown that within a group of pea aphids, some apterae run in a st ra ight l i ne after dropping to the ground while others turn f r e -quently, and respond pos i t i ve l y to v e r t i c l e s t r ipes . He suggested that those moving in a stra ight l i ne are act ive dispersers while those showing high turning rates are non-dispersers. This thesis i s composed of four separate studies, a l l dealing with dispersal in apterous pea aphids. The overal l aim of the thesis i s to elucidate the factors involved in the dispersal of apterous pea aphids, and the response of aphids to changes in these factors. In the f i r s t section of the thes i s , I examine the behaviour of indiv idual aphids while of f the i r plants, and make predictions about how pea aphids w i l l respond to predators in the f i e l d , and how environmental factors can modify dispersal behaviour. Since aphids are the most important vectors of plant viruses (Eastop, 1977), the role of predators as an agent increasing the dispersal of infect ious aphids and therefore the spread of plant disease i s of major importance. In chapter II, I examine the influence of adult cocc ine l l i d s on the spread of a plant virus by apterous pea aphids in the f i e l d . Dispersal i s an a c t i v i t y which can benefit the ent i re population, because i t allows for exp lo i tat ion of new plant resources and can re l ieve population pressure on the colonized food plant. But i t can have i t s costs through the mortal i ty of dispersers and reduction of time and energy for other a c t i v i t i e s . When costs exceed benefits in any a c t i v i t y , we should expect the a c t i v i t y to be modified or eliminated through natural se lect ion. Pea aphids ex i s t in both the hot dry i n t e r i o r of B r i t i s h 3 Columbia and the milder coastal zone. Because of the hot, dry weather in the i n t e r i o r region, conditions on the ground should be more d e t r i -mental to aphid dispersers than would be the case on the coast. I show that conditions in the i n te r i o r can resu l t in higher mortal i ty of dispersing apterae than on the coast. In the f i na l two chapters of th i s thesis I te s t the hypothesis that aphids that l i v e in s i tuat ions where r i sks of morta l i ty when leaving plants is high, should be more reluctant to leave the i r plants than aphids that l i v e in s i tuat ions where dispersal success is high, v i z . , the pea aphids in the i n t e r i o r compared to those on the coast. By examining the dispersal behaviour of pea aphids under d i f f e ren t environmental s i tuat ions , I hope to gain some ins ight as to how aphids exp lo i t t he i r food plants. Figure 1 shows a pea aphid behavioural model, upon which much of the work contained herein is based. 4 Fig. 1. A conceptual model of a predator-pea aphid i n te rac t ion . 4a predator, H I aphi iphia on plant misled predatorl - <s t ° P > run d r op f x escape 1 captured ( s t o p ) ( s t o p ) ca ptured KniE> kick rx I escape ca ptured < s t ° P > < s t ° P > run speed t i me a nal e no - c \ ie > s t a ^ > ^ S - ^ 5 t o p ^ ) 5 Chapter I DISPERSAL DYNAMICS 6 Introduction Apterous pea aphids, Acyrthosiphon pi sum (Harr i s ) , read i l y drop from plants when disturbed by natural enemies (Dixon, 1958). Pea aphid clones have indiv iduals which immediately search for a plant a f te r dropping, as well as indiv iduals which leave the area before searching for a host (Niku, 1975). In laboratory exercises, when natural enemies were present, pea aphids read i ly dispersed from a colonized host to non-colonized plants (Tamaki et_ al_., 1970; Niku, 1972). Therefore, the presence of predators can have a strong influence on the dispersal dynamics of pea aphids. Dispersal movements of pea aphids were quant i f ied under laboratory and f i e l d conditions both in the presence and absence of predators. The aim was to ident i f y the factors inf luencing the movement of pea aphids among plants in f i e l d populations and to assess the cost of dispersal of d i f fe rent ins tar s . Materials and Methods A colony of pea aphids was started from many ind iv idua l s co l lected from a l f a l f a on the Univers ity of B r i t i s h Columbia campus, Vancouver. Aphids were reared on broad bean V i c i a faba cv Exhib i t ion Long Pod, under a l i g h t regime of 16L:8D at 20°C t 1.5°C using the method of Harrison and Barlow (1972) to provide groups of aphids of known age. Maternal age was kept constant and a l l tests were conducted between 1100 and 1400 hr. F i r s t , second, th i rd and fourth instar nymphs as well as three day adults 7 were tested. The number of aphids on a plant varied between 4 and 8. When a group of aphids reached test ing age, the host plant on which they were feeding, was placed in the centre of a 0.9 x O . 9 m cardboard arena divided into 8,100 numbered 1 cm square blocks. The gr id also con-tained 48 v e r t i c a l l y positioned green p la s t i c straws in a 7 x 7 matrix with the host plant occupying the central pos i t ion. Each straw was 14 cm from i t s nearest neighbour. Pea aphids or ient to v e r t i c a l s t r ipes when searching for a host plant (Niku, 1974). Preliminary tests showed that straws were treated as i f they were potential hosts by the pea aphids. An adult c o c c i ne l l i d Coccinel la c a l i f o r n i c a Mannerheim which was starved for 24 hours, was released onto the central bean plant and allowed to search for aphids, un t i l an aphid dropped from the plant. I recorded whether the c o c c i n e l l i d contacted the aphid before i t dropped and the height from which i t dropped. Pea aphids go through a period of thanotosis (death feigning) a f ter dropping from a plant (Niku, 1975). The duration of th is behaviour was recorded. Once the aphid began moving, I recorded i t s pos it ion on the arena gr id at f i ve second i n te r va l s , un t i l the aphid e i ther returned to the or ig ina l p lant, sett led on a straw, or ceased moving for more than three minutes. The grid data were analyzed with a computer program which graphical ly displayed the dispersal path and computed the rate of movement, to ta l distance moved, and the distance from the host at the end of the t r i a l . Searching aphids exh ib i t rapid antennal move-ments and high turning rates compared to those showing running behaviour, which run in s t ra ight l ines and hold the i r antennae r i g i d over the i r back. By observing these behavioural t r a i t s and examining the dispersal paths, i t was possible to separate the two behaviour types (F ig. 2). 8 Results and Discussion S t a t i s t i c a l s ign i f icance was tested with the Dixon and Massey (1969) proportions test unless otherwise indicated. Data are presented as means, percents or proportions ± one standard error. A l l instars exhibited thanotosis af ter dropping, which increased in average duration with age although not s i g n i f i c an t l y so in a l l cases. F i r s t instars e i ther moved almost immediately a f ter h i t t i n g the surface or did not move for over three minutes and were therefore d i squa l i f i ed from the tests . Neither height of f a l l or-physical contact by cocc ine l l i d s had any e f fect on the length of the thanotosis period. This d i f f e r s from Niku's (1975) observation that the duration of thanotosis i s negatively correlated with the height of f a l l . Niku purposely varied the height of f a l l between 10 and 100 cm whereas my differences of between 10 and 25 cm were due to chance. Character ist ics of running and searching behaviour are given in Table 2. Searching aphids show a higher turning rate than runners, and also move at a slower rate. The aphid movement rates I observed are s imi la r to those shown by Phelan et_ al_. (1976) for aphids dropping after alarm pheromone st imulat ion. Whether an aphid shows running or searching behaviour, i n f l u -ences which host i t sett les upon. Searching aphids more frequently returned to the or ig ina l plant than aphids exhib i t ing running behaviour (Table 2). Adult pea aphids '. ran more often (Table 1) and returned to the or ig ina l host plant less often (p < 0.05) than a l l other instars (Fig. 6). Adults moved onto straws more distant than the nearest straw 9 more often than a l l other instars (Table 1). Generally, aphids e i ther searched or ran although in a few cases, mostly in the adults, aphids showed both behaviours separated by rest ing periods of 5 seconds to a minute. Most adults which were searching, found new host plants (94%) but f i r s t and second instars were less successful with only 55% of f i r s t and 78% of second instars f inding new hosts while searching. When the f i r s t two instars f e l l within 3 cm of a host, they walked d i r e c t l y to i t , but beyond that distance they usually showed a high frequency of small turns in the i r search paths. From these resu lts i t appears that older instars are more capable of locat ing host plants at greater distances than young i nstars. The results from the gr id studies allowed me to make some predictions regarding the aphid-predator interact ions in the f i e l d : (1) The presence of ac t i ve l y searching cocc ine l l i d s should resu l t in the dispersal of some indiv iduals of a l l instar classes to new host plants. (2) Adults, which more frequently adopt running behaviour, should disperse more widely in f i e l d plots and should be found beyond the nearest ava i lab le plants more frequently than the other instars . (3) Because the younger instars are less successful in locat ing plants they are expected to suffer higher morta l i ty . 1 0 Fig. 2. Comparison of search and run behaviour paths by adult pea aphids (drawn to sca le) . The points indicate the posit ion of the aphid at f i ve second in te rva l s . P = Host plant. S = Posit ion of aphid after i t drops from plant. 10a Search Run 11 Table 1. Behaviour of each ins tar of the pea aphid a f te r dropping from a plant in the laboratory. Thanotosis Proportion Duration Running Instar N (sec. ± SE) + SE ". Proportion'.' Proportion rof ' successful of successful host.f inders host f inders '-going"""beyond going to a nearest host new host ± SE + SE Adult 46 13.31 ± 2.15 .23 ± .07 .54 ± .07 .26 ± .06 4 ' th 40 12.58 + 2.53 .15 + .06 .33 + .07 .13 + .05 3 ' rd 22 6.20 ± 2.04 .05 ± .05 .32 ± .10 .14 ± .07 2'nd 28 2.80 + 0.90 .03 + .03 .29 + .09 0 T s t 12 0.46 + 0.16 .08 ± .08 .33 + .14 .08 + .08 12 Table 2. Comparison of pea aphids showing running and searching behaviour. Distance (c # aphids that # aphids that from o r i g -return to went to hosts inal host Behaviour Speed Turns/ the i r o r i g - beyond the that aphid Type N cm/sec 5 sec inal host nearest host sett led Running 11 .67 ± .03 .18 ± .06 0 8 31.3 ± 4.8 Searching 35 .27 ± .01* .75 + .04* 2] * * 3** 5.8 + 1.8* * S i gn i f i can t l y d i f fe rent (p < 0.05) using Dixon and Massey's proportion tes t . * * S i gn i f i can t l y d i f fe rent (p < 0.01) Chi Square. 13 F ie ld Studies Materials and Methods F ie ld experiments were conducted in cages measuring 3 x 3 x 1.85 m high, modified from the design of Woodford (1973) and Farrar (1963). The walls were nylon screen mesh s ize 7 threads/cm. . The cage environment was s imi la r to that outside, although day temperatures were 1° to 2°C cooler and night temperatures were 1° to 2°C warmer ins ide. Solar inso-l a t i on was reduced by the screen but did not v i s i b l y a f fect plant growth. Each cage contained 4 plots each 0.85 x 0,85 m in s i ze , with approxi-mately 0.65 m of bare s o i l between plots and 0.3 m between plots and cage wal l s . The distance between plots was such that aphids ra re ly moved between p lo t s , although cocc ine l l i d s could f ree ly do so. Within each plot , I transplanted a 7 x 7 array of broad bean seedlings. Each plant was 14 cm from i t s nearest neighbour. The cages were kept weed free. Pea aphids were co l lected from a l f a l f a on the Univers ity of B r i t i s h Columbia campus, and placed on broad beans in a screen house for three days to accl imatize them. After four days the aphids were separated into age classes. Because of the d i f f i c u l t i e s of rap id ly ident i fy ing instars in the f i e l d , we considered only three age classes: young nymphs of f i r s t and second in s ta r s ; old nymphs cons ist ing of t h i rd and fourth i n s ta r s , and apterous adults. I placed 15 aphids (5 from each c lass) on the centre plant in each D p lot . A p l a s t i c r ing coated with Fluon (a p l a s t i c coating too smooth for aphids to walk on) was placed around the centre plant for one day to ensure 14 that the aphids sett led on the i r host. At the end of twenty-four hours, the r ing was removed and twenty-five male coccinel 1 ids , C_. c a l i f o r n i c a , were released into the two experimental cages while the control cage remained predator f ree. Aphids and beetles were counted on every plant in each plot at 900, 1100, 1300, 1500 and 1700 hr (PDT) each day with the aid of dental mirrors (Tamaki e_t a]_., 1970). In addit ion, casual observations were made on the a c t i v i t y of beetles between counts, and I recorded whether they were ac t i ve l y moving about and whether beetles entered any p lots . Aphid movements were calculated from the changes in occupation pat-terns on plants within a plot from one observation to the next. With the density of aphids and cocc ine l l i d s that were used, the counts and estimates were accurate over the f i ve days of each experiment. From laboratory observations i t was estimated that 70% of the aphids dropped from a plant when a predator entered an aggregation of between 5 and 15 aphids. Therefore, i f a beetle interacted with an aggregation of ten aphids, I would assume that seven dropped and three remained. If the o r i g ina l plant now held two aphids and I found three on other p lants, I would estimate that one was k i l l e d on the plant and f i ve died on the ground. The return of aphids was estimated in three ways: (1) by d i rec t observation of a beetle-aphid group in te rac t ion ; (2) by the return of an aphid which was missing during one census and showed up on the next; (3) by the presence of more aphids than I would have estimated i f 70% l e f t the plant. In a l l cases i t was obvious i f a beetle had interacted with a group of aphids because the remaining and returning aphids were scattered over the plant instead of aggregated. 15 When poss ible, I calculated the fecundity of dispersing aphids on the day of dispersal and on the fol lowing three days. Fecundity was measured as the number of offspr ing per day-degree, above a threshold of 4°C (Campbell e_t al_., 1974). Temperatures f luctuated during the day and aphid b i r th rate increases with temperature. The fecundity of some aphids was measured over s ix hours and others over eight hours. The use of the physiological time scale allowed a l l measurements to be rendered to the same base. Results Aphids frequently moved between plants in the experimental cages, but rare ly in the predator free cages. The few movements observed in the control cages were found to be associated with the presence of c o cc i ne l l i d larvae that had managed to enter the cage. In a l l other cases, aphids in the predator free cage were t i g h t l y packed, ind icat ing an undisturbed state (Phelan et_ aj_., 1976). Aphids were rare ly found clumped in cages when predators were present and never for the duration of a t r i a l . The re lat ionsh ip of c occ i ne l l i d pos it ion and aphid movement is shown in Table 3. For a l l three age classes of aphids, cocc ine l l i d s were found in the v i c i n i t y of the aphid infested plant, when aphid movements were recorded. Direction of aphid dispersal The d i rect ion of aphid movement was calcualted by measuring the angle 16 between the plant the aphid l e f t and the new host. The path taken was considered to be a stra ight l i n e . The angular measurements were pooled into s ixteen, 22.5 degree arcs. The data were analyzed using the method of Batschelet (1965) to determine i f the aphids had a preferred d i rect ion of movement. R refers to the tendency for movement to occur in one d i r ec t i on . R equals 1 when a l l movement i s in one d i r e c t i o n , whereas R equals 0 when dispersal i s equal in a l l d i rect ions . In th i s study, R was between 0.074 and 0.2 for a l l ins tars . ) Aphid'density and dispersal distance Dispersal distances were calculated and compared with the density of aphids on the plant from which the aphids l e f t . Aphid density was pos i -t i v e l y correlated with the dispersal distance in the immature aphids (Figs. 3 and 4). The re lat ionsh ip was not s i gn i f i can t for the adults. Effects of dispersal on fecundity The fecundity of aphids was s i g n i f i c an t l y (p < 0.05) lower on the day a f ter dispersal than at a l l other times (Fig. 5). Fedundity was s l i g h t l y lower on the day of d i sper sa l , measured af ter the aphid reached a new plant, than on the second and th i rd day a f ter dispersal but the difference was not s i gn i f i can t at the 5% l e v e l . The fecundity of aphids in the control cage was the same as non-dispersing aphids in the exper i -mental cages. Morta l i ty factors Of the aphids that l e f t the i r plants, s i g n i f i c an t l y more (p < 0.05) 17 young nymphs were never found in l a te r counts (Table 4). Of the aphids which remained on plants during a cocc i ne l l i d encounter, young nymphs had higher morta l i t ie s than adults (p < 0.001) or older nymphs (p < 0.05). S im i l a r l y , the morta l i ty of old nymphs a f ter encounters with predators was twice that of adults (N.S.). D i s t r ibut ion of dispersers The distances moved by aphids of the three age groups d i f fe red s i g -n i f i c a n t l y (p < 0.001 Chi Square) (Fig. 6). Almost twice as many adults and old nymphs went to new plants a f te r leaving t he i r o r i g ina l host, as did young nymphs (Table 5). Almost three times as many adults and twice as many old nymphs moved beyond the nearest ava i lable plant than was the case for the younger nymphs (Table 5). Discussion Niku (1972) released Syrphus coro l lae (Fab.) larvae into small green-house plots in which the centre plants were colonized by pea aphids. Four days l a t e r , aphids were found throughout the p lot s , while the spread of aphids in the predator-free plots was minimal. Tamaki ejt al_. (1970) obtained s imi la r results by releasing Aphidius smithi Sharma and Subba Rao into pea aphid colonies. These studies suggest that natural enemies are important in the dispersal of apterous pea aphids and the present experiments have confirmed t h i s . Laboratory experiments can rare ly dupl icate nature; however, these Table 3. Aphid movements in re la t ion to the locat ion of coccinel1 ids . Proportion of aphid movements + SE Coccinel1 id Posit ion Adults Old nymphs Young nymphs On host plant .39 ± .06 .28 + .06 .36 + .04 On adjacent plant .29 ± 0.6 .22 ± .06 .39 ± .04 In plot .21 ± .05 .29 ± .07 .16 + .03 None act ive .11 + .04 .17 ± .05 .10 + .03 Total number observed 62 46 132 1 9 Fig. 3. The re lat ionsh ip between the distance a young nymph dispersed and the density of aphids on the plant from which the aphid l e f t . The number beside each point indicates the-sample: s i ze . 19a 20 Fig. 4. The relationship between the distance an old nymph dispersed and the density of aphids on the plant from which the aphid left. 20a D i s t ance d i s p e r s e d in cm 21 Fig. 5. The relationship between fecundity and dispersal in pea aphids. The number beside each point indicates the sample size. ND = non-dispersers; C = aphids in predator-free cage. Table 4. Direct and ind i rect pea aphid morta l i t ie s from c o c c i n e l l i d -aphid interact ions. K i l l ed on plant Died on ground Age Class + SE + SE Adult 100 .09 + :03 C06 ± .02 Old nymphs 49 .16 + .05 .14 + .05 Young nymphs 315 .18 + .02* .31 + .03** * S i gn i f i cant l y d i f fe rent from adults and old nymphs (p < 0.05) * * S i gn i f i can t l y d i f fe rent from adults (p < 0.001) and old nymphs (p < 0.05) Table 5. Comparison of success of three age classes of the pea aphid in f inding new host plants, a f ter leaving t he i r host. Age class Proportion returning to host + SE Proportion f inding new plant ± SE Proportion f inding new plant beyond nearest plant ± SE Adults 91 Old nymphs 41 Young nymphs 257 .27 ± .05 .22 + .06 .28 + .03 .67 ± .05 .61 + .08 .34 + .03* .31 + .05 .22 + .06 .11 + .02** * S i gn i f i can t l y d i f fe rent from adults and old nymphs (p < 0.001) * * S i gn i f i can t l y d i f ferent from adults (p < 0.001) and old nymphs (p < 0.05). 24 Fig. 6. The frequency d i s t r ibut ions of dispersal distance in three age classes of the pea aphid in the laboratory and f i e l d . 1 = Adults; 2 = Old nymphs; 3 = Young nymphs. 25 studies point out important aspects of a behavioural process. I found two behaviour types, runners and searchers, in the laboratory studies. Niku (1975) made s imi la r observations on a d i f fe rent biotype of the pea aphid. An important feature of these differences in behaviour i s that one type allows the aphid to return to the plant from which i t dropped. The behaviour of the other type reduces the probab i l i ty of i t s returning to the o r i g ina l plant. More aphids returned to the i r o r ig ina l host plants in the laboratory studies than in the f i e l d . This i s probably due to differences in te r ra in between the two studies. In the laboratory, a l l instars eas i l y moved in the paper arena. Natural te r ra in is never as f l a t as that in the labora-tory, and from the aphid 's perspective, i t i s a rough p la in strewn with very large masses. I often observed an aphid to change course a f te r encountering d i f f i c u l t y moving over the ground. This was espec ia l ly true for the younger instars when the ground was dry and so i l pa r t i c le s loose. It appears that, even though the laboratory experiments allowed for an estimation of the proportions of aphids that are motivated to return to a plant, physical ef fects can modify the actual numbers that do so. The proportion of aphids which were unsuccessful in f ind ing plants while on the ground, was highest in the young instars . Since the cages excluded predators which are normally present on the ground, I assume that those aphids died before f inding a host plant. In the laboratory, many young instars did not move after dropping to the ground, and a high propor-t ion of those that d i d , did not f ind a plant in the time a l l o t t e d . Aphids which spend more time on the ground are exposed longer to the detrimental conditions found there. On warm sunny days, cocc ine l l i d s are most act ive 26 (Frazer and G i l be r t , 1976). Temperatures were measured within the bean plant fo l iage and on the ground with a Yellow Springs Instruments ther-mister. When the average temperature within the fo l iage was 18°C - 1.0°C, the ground temperatures were 25.4°C - 2.1°C. Although aphids can wi th -stand temperatures as high as 41°C for twenty-five minutes (Harrison and Barlow, 1973), experiments in chapter IV show that they are unable to walk a f te r a short time when exposed to high temperatures (6.2 minutes for adults N=90 and 2,8 minutes fo r f i r s t instars N=80, both at 42°C). That means that survival on the ground is dependent upon the length of time the aphid can continue to walk in search of a new plant. Young i n -stars are in double jeopardy i f they leave a plant because they are less successful at f inding new plants and are more susceptible to the high ground temperatures than adults. I suggest, therefore, that young instars should require a stronger stimulus to e l i c i t drop behaviour, compared to older instars . F i r s t , second and th i rd instar pea aphids only respond to alarm pheromone when i t i s accompanied by a v ibratory stimulus, while adults and fourth instars respond to alarm pheromone alone (chapter I I I ) . If r i sks are higher for young in s ta r s , and the data indicate they are, one would expect young instars to return to the i r host plant as quickly as possible. This does occur, because thanotosis duration is shortest in the younger instars and only two of fo r ty young instars exhibited running behaviour in the laboratory. Young nymphs rare ly dispersed beyond the nearest host. Young instars are also under greater pressure from predation while on the i r host plant. The proportion of aphids that were estimated to have been taken by predators was s i g n i f i c an t l y higher fo r young instars than 27 adults. Frazer and G i lbert (1976) reported s imi la r d i f f e r e n t i a l pre-dation morta l i t ie s between pea aphid instars on a l f a l f a . Pea aphid fecundity is less the day after d i sper sa l , which may be due to two causes. F i r s t , the aphid is unable to feed but continues to use energy reserves while on the ground. Fecundity is not affected on the day of d i sper sa l , probably because the embryos to be born" that day are already formed (Ulchanco, 1921; 1924). However, the i n a b i l i t y to feed and the energy used for dispersal may af fect the development rate of the embryos to be born the fo l lowing day. Randolph et_ al_. (1975) showed that as much as 91% of the energy required for the production of young comes from the food an aphid ingests. Roff (1977) found that a reduction in fecundity related to the energy costs of dispersal in Drosophila, and Burns (1971) showed that f l i g h t in the vetch aphid Megoura v i c i a Buckton, reduces the number of young produced. High ground temperatures may also harm developing embryos when the aphid is dispersing (Muride, 1969a). Thus far I have focused on the process of dispersal in the apterous pea aphid. The costs and benefits of that process w i l l n o w be examined, not only for the pea aphid, but as i t may re la te to other species of aphids. Van Valen (1971) and L id icker (1962) have discussed the importance of emigration in population regulation and the co lon izat ion of new r e -sources. In populations composed of s o l i t a r y ind iv idua l s , the advantages of emigrating (new resources, higher chance of f ind ing a mate, e t c . ) , must be weighed >against the costs (greater potential morta l i ty , lower fecundity) for that i nd i v idua l . When a family group occupies a s ingle resource un i t , the costs and benefits of dispersal can be analyzed from the group's standpoint as well as the i nd i v i dua l ' s (Myers and Campbell, 28 1976). If we view aphid clones as one " i nd i v i dua l " made up of many parts (cf Jansen, 1977), then the r i sk s can be spread between the tota l number of aphids of that " i n d i v i d u a l " . Emigration of some of the aphids re l ieves population pressure on those which remain on the known resource: while possibly extending the clone to new resources. Overall f i tness of the clone w i l l be maximized by a balance of the number of aphids which emigrate, to those that stay. In th i s way, there is competition between clones to most e f fec t i ve l y balance the i r proportions of d i f fe rent behaviour types to su i t d i f fe rent environments. When the host plant is dec l in ing , two tac t i c s might be employed. F i r s t , aphids may immigrate to new plants by developing winged forms. A second ploy is to reduce competition on the plant through a reduction in s ize and fedundity of the adultswhich remain (Murdie, 1969b). When plant qua l i ty is good and i s expected to remain so, then select ion should favour high numbers of apterous non-dispersers, since these produce more young than alates (MacKay and Wellington, 1975) and they avoid the r i s k of dispersal morta l i ty. Predator influenced dispersal of apterous aphids is an extension of the pr inc ip les discussed above, but with one major advantage over alate d i spersa l . The production of alates in response to decl in ing resource qual i ty has a lag time of up to one generation. Apterous dispersers eliminate th i s lag. Niku (1975) suggests that running behaviour increases in frequency in aphids dropping from plants, as plant qua l i ty decreases. Way (1973) noted that migratory urge in apterae may increase with i n -creasing crowding. Both of these suggestions are consistent with the argument I have developed for aphid emigration in general. 29 The presence of a predator in the v i c i n i t y of an aphid decreases the survival value of i t s staying on the plant and therefore makes d i s -persal a more favourable option. Selection pressure from predators w i l l reduce the probabi l i ty of overcrowding of aphids on a plant. There-fore, i f aphids have evolved with predation as a regulating force e i ther by dispersing the population or through predator induced morta l i t y , then those aphids are l i k e l y to lack mechanisms to prevent overcrowding in an environment without predators. For example, the a l f a l f a aphid Therioaphis maculata (Buckt.), l i k e the pea aphid, readi ly leaves the host plant when disturbed. In the absence of predators, th i s species continues to mult iply at high rates un t i l the host plant collapses (Messenger and Force, 1963). Not a l l species of aphids read i ly drop from host plants when d i s -turbed and so we should expect to f ind, differences in l i f e s t y l e s between the two i f both can avoid depleting the i r food resources. We can view the production of a late emigrators and readi ly dispersive apterae as i n t r i n s i c mechanisms which allow populations to lower the i r numbers below carrying capacity. Ext r ins ic factors such as predator or other physical disturbance can also be important in emigration, much more so in some species than others. In many species of aphids, apterae seldom leave a plant. The cabbage aphid Brevicoryne brassicae (L.) i s a sedentary aphid and i s found t i g h t l y packed on plants. Apterae rare ly leave the i r plants and when they do i t i s across plant bridges (Hughes, 1963). We suggest that B_. brassicae should be very sens i t ive to plant conditions which stimulate alate pro-duction. In f ac t , young aggregates of B_. brassicae contain alates 30 (Way and Cammell, 1971), but they do not necessari ly emigrate (Way, 1973). In contrast, the pea aphid, at least the Vancouver biotype, does not produce alates at low dens i t ies . A test for the hypothesis that aphids which are ret icent to leave the host plant as apterates should have a lower threshold for alate production, comes from observations on the Kami oops biotype pea aphids. Summer weather in Kami oops is hotter than in Vancouver. Higher morta l i ty on the ground associated with hotter ground temperatures may have lead to the observed reduced dispersal by apterae of the Kami oops biotype in comparison to the Vancouver biotype (chapter I I I ) . The Kami oops biotype produces alates in the laboratory even at low densit ies while the Vancouver biotype does not. Sutherland (1969) has shown that d i f fe rent strains of the pea aphid can have d i f f e r -ent s e n s i t i v i t i e s to st imul i that promote alate production. The black bean aphid Aphis fabae Scopol i , i s often found in dense aggregations and i t does not drop in response to predators, although apterae w i l l leave the i r plants when food qual i ty is poor. A. fabae clones contain alates which vary quant i tat i ve ly . Some alates f l y long distances, others colonize nearby plants and s t i l l others do not emigrate at a l l . The proportion of alates showing the migratory urge i s affected by crowding (Shaw, 1970). This i s s imi la r to my observations on the distance dispersed by apterous pea aphids, in that crowded nymphs disperse farther (Figs. 3 and 4). Wolfenbarger et_ al_. (1975) made s imi la r obser-vations on Myzus persicae (Sulz.) under highly a r t i f i c i a l condit ions. It i s curious that adult pea aphids did not show a re lat ionsh ip between distance dispersed and aphid density. The reason may be related to the manner in which the d i f fe rent instars are aggregated on a plant. Young 31 instars are t i g h t l y aggregated, and adults, espec ia l ly those that have been disturbed, may be in loosely aggregated groups or i so lated on a plant. My data considered only aphid density per plant and not the degree of packing of that group of aphids on the plant. Because of the way in which they are aggregated on plants, tota l population numbers are l i k e l y to be more r e a l i s t i c estimates of the s ize of the group the aphid l e f t , for ayyoung in s ta r , than an adult. Future experiments on th i s phenomena should centre on aggregate s ize (cf Way, 1968). Aphids whose apterae readi ly disperse from the i r plants, probably are d i s t r ibuted d i f f e r en t l y in the f i e l d than species that rare ly disperse as apterae.- The pea aphid^.for example, should be more evenly^dispersed around a central colonizat ion point than the black bean or cabbage aphid. Way (1968) showed that even at low tota l population dens i t ies , A. fabae can be d i s t r ibuted so that most of the aphids are crowded beyond an optimal level on a few plants, while many of the avai lable plants are not colonized. The pea aphid on a l f a l f a i s much more evenly d i s t r ibuted in the f i e l d and group sizes tend to be small. The a c t i v i t i e s of predators can e f fect the d i s t r i bu t i on of aphids within a f i e l d in two ways. In species whose apterae do not disperse, predators could keep populations s u f f i c i e n t l y low that alates are rarely produced. The d i s t r i bu t i on of clones in the f i e l d would remain nearly constant. In contrast, species whose apterae readi ly leave the plant could be spread throughout a f i e l d without alates being produced. If predators are adapted to search for groups of prey, a more uniformly dispersed aphid population would be perceived as a lower density population. There-fore, predator a c t i v i t y could spread the aphids to the extent that the predator would leave even though the number of aphids in the area was s t i l l 32 r e l a t i v e l y high (cf Murdoch and Oaten, 1975). Population studies rarely take into account, movements within a system because of the d i f f i c u l t i e s involved in measuring them (cf G i lbert et_ al_., 1977). The large s t a f f required to fol low aphid movements and the d i f f i c u l t i e s in marking aphids (Petterson, 1969), make large scale studies of aphid movements impract ica l . Because of these d i f f i c u l t i e s , ecologists often ignore movement even though i t i s known to be an impor-tant process in many species of insects , e.g. cherry bug (Fu j i sak i , 1975), cinnabar moth (Myers and Campbell, 1976), cabbage but te r f l y (Jones, 1976). The present studies provide information on between plant movements of pea aphids when food plants are discrete and separated by short d i s -tances (14 cm). Future studies should evaluate th i s process when plant and other environmental character i s t i c s are var ied. It may be possible to gain further ins ight into how aphids exp lo i t food plants under d i f f e r -ent circumstances by comparing a var iety of aphid species and of d i f f e r -ent biotypes within a species: those that readi ly disperse as apterae as well as those, whose apterae rare ly leave plants in response to predators. E a r l i e r I alluded to the importance select ion might play in adjusting the rat io of runners and searchers in pea aphid clones under d i f fe rent circum-stances. Pea aphids which colonize plants that ex i s t as large continuous mats should be more prone to drop from plants and show running behaviour, than aphd.ds which l i v e on discrete plants separated by long distances since the i r apterae would largely be unsuccessful in f inding new plants. Myers and Campbell (1976) found an association between plant spacing and the ten-dency of c innibar moth larvae to drop from plants when disturbed. It may be possible to compare the apterae of readi ly dispersing species and 33 species whose apterae do not read i ly disperse, in terms of MacArthur and Wilson's (1967) r and K model. For example, the pea aphid read i ly disperses, has a r e l a t i v e l y high fecundity (Frazer, 1972), and i t s popu-lat ions on a plant are often brought below carrying capacity by external forces ( i . e . predator induced dispersal from clones). The cabbage aphid is a sedentary species, has a r e l a t i v e l y low fecundity (Way, 1968) and maintains i t s population below carrying capacity through i n t r a spec i f i c mechanisms. Chapter II THE SPREAD OF A PLANT VIRUS 35 Introduction Aphids are the most important vectors of plant virus diseases. Of the 620 known plant v iruses, 164 are aphid transmitted (Eastop, 1977). Control of virus spread by the use of chemical aphicides has met with mixed success (cf Adams et_ al_., 1976). Ref lect ive s o i l mulches reduce the a b i l i t y of virus carrying aphids to locate host plants (Smith and Webb, 1969), and non-toxic chemicals can be used to reduce transmission success (Bradley et_ al_., 1966). Natural enemies may eventually control aphid numbers, but do not necessari ly lower virus incidence (Gry l l s , 1972). Aphid predators are not always successful in capturing the i r prey (Dixon, 1958), and the i r searching behaviour dislodges prey from the host plant. This interact ion disperses aphids to new host plants (Tamaki et a l . 1970; Niku, 1972) which can have serious implications for the spread of virus disease. Frazer (1977) suggested that the spread of A l f a l f a Mosaic virus by pea aphids may be increased by the presence of the i r c o cc i ne l l i d predators. In th i s chapter, I examine the influence of adult cocc ine l l i d s on the spread of a s t ra in of Bean Yellow Mosaic virus (BYMV) by the pea aphid Acyrthosiphon pi sum (Harris) to broad beans. Materials and Methods The BYMV i so la te was obtained from Dr. R. Hamilton, Agr iculture Canada Vancouver. The virus had been maintained by mechanical transmissions to broad bean V i c i a faba cv Exhibit ion Long Pod in the greenhouse for 1 year. 36 BYMV i s transmitted in a non-persistent manner ( i . e . read i ly picked up on and los t from the mouthparts of the vector) by pea aphids. Obvious symptoms of ch lorot ic mott l ing, often with leaf margins r o l l ed down, show in broad beans ten days a f te r inoculat ion when grown in the greenhouse. Fifteen bean seedlings were mechanically inoculated and af ter ten days, eight plants showing de f i n i te symptoms were transplanted to the central posit ion of a 7 x 7 array of healthy bean seedlings in 0.85 x 0.85 meter p lots. Each plant was 14 cm from i t s c losest neighbour. A l l experiments were conducted in the large f i e l d cages 3 x 3 x 1.85 meters with walls of nylon screen, 7 threads/cm used e a r l i e r . Conditions in the cage were s imi la r to those.outside, although a i r temperatures in the cage were generally 1° to 2°C cooler during the day and 1° to 2°C warmer at night. Three plots were planted in each of the two experimental cages and two plots in the control cage. Pea aphids were col lected from a l f a l f a growing near the f i e l d cages on the Univers ity of B r i t i s h Columbia campus, Vancouver. The aphids were placed on bean plants in a screen house to accl imatize them. In order to rapid ly i dent i f y indiv iduals in the f i e l d , we separated the aphids into three major classes: (1) apterous adults (2) t h i rd and fourth instars (3) f i r s t and second instars Fifteen apterous aphids, f i ve from each c l a s s , were placed on each of the central plants in each plot and allowed to se t t l e for twenty-four hours. Twenty adult coccinel1 ids , Coccinel la c a l i f o r n i c a Mannerheim were released into each of the experimental cages. Beetle and aphid censuses 37 were 900, 1100, 1300, 1500 and 1700 hr. (PDT) each day. I was able to ascertain numbers and posit ions of a l l of the aphids without disturbing them by using dental mirrors (Tamaki et_ al_., 1970). Through frequent censuses, the ident i ty of indiv idual aphids in each plot was known. Three days a f ter the release of the cocc i ne l l i d s , the central plant i n each of the experimental plots harboured few or no aphids. The exper i -ment was terminated after three days and a l l of the aphids from a l l plants in each of the eight plots were removed. The cages were kept closed for twelve days and then the plants were examined for virus symptoms. Twenty-five f i e l d co l lected aphids were placed ind i v idua l l y onto bean plants for 1 day. None of these plants showed any signs of virus i n fec -t ion after fourteen days, so i t was assumed that a l l infected plants in the experiment were produced by aphids having acquired the virus from the diseased central plant. Results Aphids in the cages with cocc ine l l i d s frequently moved between plants but only 4 of the 64 aphids in the two control plots l e f t t he i r host plant. The aphids on the control plants were in dense colonies while those in the experimental plots were far less aggregated. At the end of three days, the aphid populations were larger in the control plots than the experimental plots (Table 6). In 89.5% ± SE 7.0 cases of observed aphid movements, act ive cocc ine l l i d s were present in that p lo t . In the experimental p lo t s , an average of 11.33 (range 9 to 15) new 38 plants were colonized by aphids from the central plant compared to an average of only 2 (range 1 to 3) in the control p lot (Table 6). Because the virus was non-persistent, only movements of aphids from the infected plant to new plants were considered as potential inoculat ions. In a c tua l i t y , an average of 16.66 (range 10 to 24) plants per p lot were v i s i t ed by aphids in the cages with cocc ine l l i d s compared to a mean of 2 (range 1 to 3) in the control cage. New virus infect ions were s i g n i f i c an t l y higher (p< 0.001) in the experimental p lots. Figure 7 shows the d i s t r i bu t i on of infected plants in each of the eight p lots. The in fect ion front was calculated by measuring the most distant infected plant from the central plant. S ixty cm was the maximum distance the in fect ion could spread in any p lo t , and this was reached in four of the s ix experimental plots (Table 6). The average distance was 55.40 cm t 3.10 in the experimental plots and only 14 cm in both of the control p lots . A l l except f i ve of the newly infected plants were known to have received aphidsfrom the central plant. Adjacent plants to the f i ve excep-tions had received colonizers from the central plant. It i s highly l i k e l y those aphids v i s i t ed one of those f i ve plants before s e t t l i n g on the adjacent plant. Discussion Apterous pea aphids frequently drop from the plant and move to new hosts when disturbed by predators (Niku, 1972). Ferrar (1969) has suggested 39 that apterous aphids may be important in the spread of plant v iruses. Considerable controversy exists as to whether apterous or alate aphids are the more important f i e l d vectors of plant virus diseases (Broadbent, 1965; Ribbands, 1965). Watson and Healy (1953) showed that Myzus  persicae (Sulz.) apterae can be important vectors when in fect ion sources are randomly d i s t r ibuted within a crop. Ribbands (1962) reported heavy cocc i ne l l i d predation of apterates coincident with the spread of beet yellows. In another study on groundnuts, Booker (1962) noted the corres-pondence between heavy predation on aphid populations and the short time that an aphid population persisted on any one plant. As in the present study, plant disease was more c losely related to the number of plants infested by aphids rather than to tota l aphid numbers. Where timing of virus inoculation i s c ruc ia l to the existence of high virus incidence, the a c t i v i t y of aphid predators may actua l ly enhance the probab i l i ty of vector spread. We might envision the fol lowing scen-a r i o : a number of infect ious alates a l i gh t in d i f fe rent sections of an agroecosystem, creating a number of point source in fect ions , Barley yellow dwarf virus is only economically damaging for a short part of the early growing season (Doodson and Saunders, 1970). The aphid populations bui ld up, but not to such extremes that alates are produced. In the presence of predators, the apterous aphids disperse, creating patches of infected plants as opposed to point source in fect ions . A short delay of an i n f l ux of predators un t i l a f te r the infect ious period has passed might s t i l l allow for reduction of aphid numbers without a f fect ing the virus spread. In th i s study, the virus spread ca 4 times as far in the plots with cocc ine l l i d s compared to the contro ls . This i s probably a conservative 40 estimate because: (1) In four of the s ix experimental plots the virus spread the maximum distance possible with the experimental design. I do not know how far the virus may have spread over the three days given unlimited space. (2) I used a non-persistent virus so that transmission success w i l l be small a f ter the f i r s t plant i s v i s i t ed (Kennedy et aj_., 1962). A pers istent virus could be carr ied on with further dispersal movements. (3) The experiment covered only three days. Over a longer period, symptoms could develop in newly inoculated plants, and aphids from these could further inoculate non-infected plants. These experiments have shown that the importance of predators in reducing aphid populations may be overridden by the i r e f fect on the spread of virus by dislodged aphids. Even though populations were lower in the experimental cages than in the con t ro l , v irus incidence was higher. Therefore, the abundance and degree of a c t i v i t y of aphid predators i s an important aspect of the epidemiology of aphid-borne plant viruses. 41 Table 6. Spread of Bean Yellow Mosaic virus by pea aphids in predator-containing and predator-free cages. Total plants Total no. aphids colonized by No. of infected Infection in plot a f ter 3 aphids from plants a f ter 12 spread Plot days infected plant days (cm) 1 12 11 7 60 2 9 11 9 60 3 10 12 12 50 4 9 12 10 60 5 15 15 8 60 6 16 9 4 42 Control 1 47 3 1 14 2 27 1 1 14 42 Fig. 7. The spread of BYMV by pea aphids in cages with and without cocc i ne l l i d predators. 42a Plots with Predators o infection source • new infection • • • o • • • o • • o • • • • Control Chapter III ADAPTATION OF ALARM PHEROMONE RESPONSES OF THE PEA APHID 44 Introduction When attacked by natural enemies, many aphids release a corn ic le secret ion. Although th i s secretion may be employed in a defensive manner (Edwards, 1966), an act ive alarm pheromone often present in the secretion warns other nearby aphids of imminent danger. Alarm pheromones are present in many species of aphids (Kislow and Edwards, 1972; Nault ejt al_., 1973; Wientjens et al_., 1973; Nault and Bowers, 1974; Bowers et_ a l . , 1977). Aphids respond to the pheromone by leaving the area of phero-mone reception. This escape response is considered to be an adaptation for avoiding predators (Nault, 1973). The survival value of th i s w i l l vary, however, depending upon the circumstances. For example, an indiv idual which leaves the host plant reduces the probab i l i ty of being captured by a predator on that plant, but now must face the advers i t ies of being on the ground. I used the pea aphid Acyrthosiphon pi sum (Harris) to test the hypo-thesis that the response of aphids to alarm pheromone has been adjusted by the i r a g i l i t y in avoiding predators on the plant and by the probab i l i ty of the i r successful ly f inding another host plant a f ter leaving the or i g ina l plant. This suggests two hypotheses: f i r s t , var ia t ion in mobi l i ty and host plant f inding a b i l i t y among instars (see chapter 1) leads to the predict ion that young instars should be more conservative than adults in responding to alarm pheromone. Second, aphids l i v i n g in hot, dry climates are exposed to more severe stress on the ground than those l i v i n g in more salubrious surroundings. I p red ict , therefore, that aphids from the hot, dry i n t e r i o r of B r i t i s h Columbia should respond more 45 conservatively to alarm pheromone than those from Coastal B r i t i s h Columbia, because the r i sks of leaving the plant are higher in the hot, dry region. Materials and Methods Age Class Responses A colony of pea aphids was started from many indiv iduals co l lected from a l f a l f a on the Univers ity of B r i t i s h Columbia campus, Vancouver. Aphids were reared on broad bean V i c i a faba cv Exhibit ion Long Pod, under a l i gh t regime of 16L:8D at 20°C i 1.5°C. The aphids were reared using the methods of Harrison and Barlow (1972) to provide groups of apterous aphids of known age. The groups I used, ranged in s ize from three to eleven indiv iduals with one or two groups per plant. Maternal age was kept constant and a l l tests were conducted between 1100 hr and 1400 hr. Cornicle secretions generally indicate pheromone release. In over 73% of the times that aphids released corn ic le secretions, there was response by aphids ind icat ing presence of b i o l o g i c a l l y act ive levels of alarm pheromone. This i s consistent with the estimate for adult pea aphids by Nault ejt a]_. (1973). Cornicle secretions w i l l be ca l led alarm pheromone throughout th i s paper since i t i s th i s act ive component which is of interest here. One of three st imul i were presented to each of the groups of aphids: (1) Pheromone - A fourth ins tar aphid was removed from the main colony and brought within 0.5 to 1.0 cm of the group being tested. The aphid 's thorax was gently squeezed with microforceps to cause the release of alarm pherome. 46 (2) Vibratory stimulus - The plant was gently prodded with micro-forceps near the group being tested. This was done to simulate the presence of a natural enemy. This stimulus did not d i f f e r in i t s e f fect from that of a struggl ing aphid (Dixon and Stewart, 1975). (3) Pheromone-vibratory stimulus - This i s the presentation of the two st imul i described above, applied simultaneously. The aphids were allowed three seconds to respond in each tes t . A group was tested only once, with one of the three s t imu l i . The responses recorded were: (1) Run - The aphid removes i t s s t y l e t from the plant and runs from the area where i t was feeding. (2) Drop - The aphid drops from the plant. (3) Back up - The aphid removes i t s s t y l e t from the plant and, in so doing, moves i t s body backwards and then remains r i g i d . (4) No v i s i b l e response. Another group of adult aphids were tested to determine i f the behavioural response to alarm pheromone was constant for an indiv idual or i f i t var ied. Environmental and rearing conditions were the same as in the previous te s t . Adults were exposed to alarm pheromone from a squeezed aphid. Those that dropped in response were placed on a new plant with two others that res-ponded s im i l a r l y . The aphids were again exposed to alarm pheromone twenty-four hours l a te r and the i r responses recorded. Aphids that did not drop on the f i r s t day were also exposed to alarm pheromone on the fol lowing day. 47 Behaviour of Kami oops aphids Pea aphids were col lected from a l f a l f a in the i n te r i o r region of B r i t i s h Columbia, near Kamloops. The aphids were brought to Vancouver and reared under the same conditions as the Vancouver pea aphids. Fourth instar Kamloops aphids were exposed to alarm pheromone and adult Kamloops aphids were exposed to alarm pheromone or pheromone-vibratory s t imu l i . Methods employed were the same as in the age class experiments, Results A l l s ign i f icance tests employed e i ther the Chi-square test or Dixon and Massey's (1969) proportions te s t . Results of tests are followed with * or * * respect ively to indicate which test was used. Less than 20% of any instar showed a v i s i b l e response to the v ib ra -tory stimulus alone (Fig. 8). Older instars tended to respond more f r e -quently. A greater proportion of fourth instar and adult aphids (p < 0.01**) responded to the pheromone than the younger ins tars . Figure 9 shows the proportion of each type of response with back up behaviour being the most prevalent response by the oldest ins tars . The proportions of the d i f fe rent responses by instars two and three (not shown) was s imi la r to instar one. At least 78% of a l l instars responded to the pheromone-vibratory stimulus. More than 80% of the responses were the dropping type in the f i r s t four instars (Figure 10). The dropping behaviour demonstrated by some indiv iduals was repeatable. 48 Individuals which l e f t the plant in response to pheromone on day one, dropped more frequently on day two (p < 0.01**) (Table 7). Day one non-droppers responded s i g n i f i c an t l y less on day two (p < 0.05**) than did the tota l group of the f i r s t day. Data of day one were not s i g n i f i -cantly d i f fe rent from the data col lected for adults in the age class experiments. Fourth- ins tar nymphs and adult aphids from Kamloops responded less than the i r counterparts from Vancouver (p < 0.05*) (Figure 11). Aphids from the hotter, d r i e r i n t e r i o r region showed a lower frequency of back up behaviour and were more reluctant to leave the host plant when stimulated by pheromone alone. However, both groups reacted s im i l a r l y when exposed to the pheromone-vibratory stimulus. Discussion If an animal i s to survive when the environment i s frequently changing, i t must be able to a l t e r i t s behaviour and/or physiological state. The pea aphid displays p l a s t i c i t y in the response to alarm phero-mone between instars and biotypes. Adult and fourth ins tar pea aphids are about three times larger than f i r s t instar pea aphids. Adults c o l -lected from the f i e l d were 3.175 mm in length (SE=0.025, N=l05) from antennal tubercle to anal plate while f i r s t instar aphids were only 1.041 mm long (SE=0.014, N=94). Related to s ize differences are the r i sks of predation associated with each in s ta r . For example, a l l stages of the p i rate bug Anthocoris 49 Fig. 8. Responses of different age classes of the pea aphid to a vibratory stimulus. The number beside each point indicates the number of aphids tested. 49a .3 Ol H 0) c -6 c o a 48 C o o a o 48 53 48 J2-3. 4. Instar Adult 50 Fig. 9. Types of responses to pheromone stimulus by pea aphids. Second and th i rd instar aphids respond s im i l a r l y to f i r s t instar aphids. { € i i i i i J ! I I L J I I 1 L x O Z Q. 3 U D CO O-O CN O CN CN •3 "S + 6uipuodsej UOIIJOCIOJJ 51 Fig. 10. Types of responses to a pheromone-vibratory stimulus by pea aphids. Second and th i rd instar aphids respond s im i l a r l y to f i r s t instar aphids. Instar 1 N = 64 Instar 4 N r 5 5 + Run Jump Back up No Rx Type of response to stimulus Adult N = 50 52 Table 7. The repeatab i l i ty of pea aphid responses when exposed to alarm pheromone on consecutive days. Type of Response Proportion Proportion Proportion Day Group N Run ± SE Drop ± SE Back up ± SE 1 A l l aphids 71 .07 i .03 .18 ± .05* .44 ± .06 2 F i r s t day droppers 18 .05 ± .05 .28 ± .11** .33 ± .11 2 F i r s t day non-droppers 45 0 .07 + .04 .22 + .06 * S i gn i f i can t l y d i f fe rent from day 1 non-droppers (p 0.05) * * S i g n i f i c an t l y d i f fe rent from day 1 non-droppers (p 0.01) 53 Fig. I t . Comparative responses of Vancouver and Kami oops aphids to pheromone and pheromone-vibratory s t imu l i . ra /y Kamloops E3 N - 51 / / Vancouver L_J N" 46 __»lnstar 4 Pheromone I Kamloops N- 41 Vancouver N* 41 r 71 I Adult Pheromone only 1*1 Kamloops N* 35 Vancouver N* 50 lult Pheromone-Vibratory No R> 54 nemorum (L.) (Heteroptera: Anthocoridae) are more e f f i c i e n t at capturing f i r s t instar than fourth instar pea aphids (Evans, 1976). In the labor-atory, Frazer and G i lbert (1976) found that when a cocc i ne l l i d was present on an aphid infested, the probabi l i ty of a f i r s t instar pea aphid being captured and eaten was 3.5 times greater than for an adult. In the f i e l d , they found that most of the aphids captured by the beetles were the younger ins tars . These observations are to be expected i f one examines the probable success of each escape option ava i lable to the d i f fe rent instars . When predator:aphid s ize ra t io i s large, the probabi l i ty of avoiding capture by running is low (Evans, 1976). F i r s t and second instars are generally unsuccessful at escaping predators whereas the older instars may be successful, espec ia l ly i f the predator i s small (e.g. young cocc i ne l l i d larvae). Back up behaviour requires the removal of the s t y le t from the feeding s i t e . The s t y l e t lengths of e a r l i e r instars of aphids are d isproport ion-ately large. For example, f i r s t instar green peach aphid Myzus persicae (Sulzer) nymphs possess s ty le t s only s l i g h t l y smaller than the adults (Forbes, 1969). Presumably, the f i r s t instar needs a disproport ionately longer s t y le t in order to reach the same feeding s i tes as the adults. Sty let removal may be more awkward and energet ica l ly cost ly to the younger ins tar s , which appear to have d i f f i c u l t y doing t h i s . For a once only response, th i s expenditure may appear i n s i gn i f i c an t , however, with numerous exposures to alarm pheromone, constant removal of the s t y le t may be d e t r i -mental to the young instars . The younger instars are reluctant to move about on the plant compared to the fourth instars and adults. Unprovoked 55 movements in the former tend to occur only around moulting time when the s ty lets must be removed. Dropping behaviour ensures the success of escaping predation on the plant but th i s response may be cos t l y . Aphid survival on the ground in warm weather can be very low. Greenbugs, Schizaphis graminum (Rondani), pushed off the i r host plants on a hot sunny day were unable to survive high ground temperatures for more than four seconds (Ruth et a]_., 1975). Frazer and G i lber t (1976) reported that young instars of A. pisum have a more d i f f i c u l t time f ind ing a host plant when knocked o f f a plant. Young instars suffer a s i g n i f i c an t l y higher mortal i ty (p < 0.01) on the ground than adults (see chapter 1), in dispersal experiments in f i e l d cages. The mortal i ty rates are probably even higher in the f i e l d , since the cages shade the ground, thereby reducing ground temperatures and potential dessication rates. When exposed to alarm pheromone only, the younger instars may drop or stay. Other options such as running do not s i g n i f i c an t l y reduce the probab i l i ty of capture and can enta i l even greater r i sks once of f the plant. Pheromone alone signals a disturbed aphid nearby, but the signal i s not de f i n i t e enough to warrant drast ic act ion. Nearby t a c t i l e stimulus accompanying the pheromone probably does indicate more imminent danger, requir ing an immediate response. Aphid predators show a much higher turning frequency once an aphid has been contacted (Dixon, 1959). In th i s s i t ua t i on , the probab i l i ty of mortal i ty from predation may be higher than the probab i l i t y of death on the ground. The dual stimulus of pheromone and v ibrat ion caused over 90% of the f i r s t instar aphids to leave the plant. The older instars improve the i r chances of survival with a larger 56 repetoire of escape responses. Dropping has the highest potential cost and i s the least u t i l i z e d . Pheromone-vibratory st imulation e l i c i t s a high probabi l i ty of,dropping and th i s complies with the argument presented for the smaller ins tars : when a l l indicat ions are that a predator is near, i t i s time to leave. But, other avoidance behaviours are also successful fo r these instars and they occur with a r e l a t i v e l y high frequency. Aphids in Kami oops are exposed to a harsher environment than those in Vancouver. In a survey of maximum monthly temperatures in the summer months for the years of 1968 to 1974, the Kamloops region average maxima were 37.8°C ± 3.6°C compared to Vancouver's average maxima of 25.4°C ± 2.5°C. These differences are even greater at ground level where temperatures are much higher than ambient a i r temperatures. For example, I recorded ground temperatures of 40°C and 33°C when a i r temperatures were 31°C and 28°C respect ively. In the summer of 1977, I ran aphid dispersal tests in f i e l d cages in Kamloops, s imi la r to those conducted in Vancouver in 1976. On-ground mor-t a l i t y was much higher for the Kamloops adults and f i r s t instars than i t was for the i r Vancouver counterparts (p < 0.001*). The Kamloops adults tend to act more l i k e the young nymphs in Vancouver with regard to dropping. Selection would favour those indiv iduals that u t i l i z e non-dropping escape options because of the harsh on-ground environ-ment in Kamloops. Other physiological and behavioural differences are known to occur between d i f fe rent biotypes of the pea aphid. Frazer (1972) has shown difference in population dynamics between the Vancouver and Kamloops biotypes. The Kamloops adult pea aphid i s more reluctant to drop in a d i rec t confrontation with a c o c c i ne l l i d than the Vancouver type (see 57 chapter 4). Some indiv iduals show a repeatable tendency to drop in response to alarm pheromone. The offspr ing of one female consists of droppers and non-droppers, so i t appears that the t r a i t i s not charac te r i s t i c of the whole clone. This mixed strategy i s s imi la r to the production of both alates and apterae by one female which allows her offspr ing to better exp lo i t avai lable resources (McKay, 1974). Those offspr ing which drop from the host plant may possibly f ind new resources. Those that stay and are not captured by predators, ensure the survival of the group of a known resource. Way and Cammell (1971) have reasoned s im i l a r l y for aphid popu-lat ions in which d i f f e r e n t i a l reproductive e f f o r t under varying circumstances ensures the maximum number of indiv iduals of the group w i l l reach adulthood. Chapter IV ESCAPE REACTIONS AND POSSIBLE EFFECTS OF HIGH TEMPERATURE ON DISPERSAL SUCCESS 59 Introduction The pea aphid Acyrthosiphon pi sum (Harris) drops from a plant when disturbed by natural enemies (Klingauf, 1967) and the micro-environment on the ground is often very d i f fe rent from that on the plant. Conditions on the ground may be. hot and dry or wet and muddy. An aphid that leaves a plant must be able to move on the ground for long enough to f ind a host plant i f i t i s to survive. In B r i t i s h Columbia, pea aphids occur in many areas where a l f a l f a i s grown. Two such areas are Vancouver and Kamloops. Aphids l i v i n g in these two areas are considered to be two d i f fe rent biotypes and differences between the two have been shown for population dynamics (Frazer, 1972) and behaviour (chapter I I I ) . In Kamloops, ground temperatures and evaporation rates at ground level are much higher than those in Vancouver, and th i s would be a greater stress on dispersing apterae in Kamloops than in Vancouver. Aphids in Kamloops could cope with th i s problem in two ways: (1) through reduced tendency to drop in response to predator a c t i v i t y , (2) through greater physiological resistance to heat and des iccat ion. Pea aphids release alarm pheromone when disturbed by natural enemies (Nault ejt al_., 1973). Alarm pheromone can e l i c i t e i ther run, drop, or back up escape responses from aphids which are near the aphid that releases the pheromone. Kamloops aphids of a l l instars and Vancouver aphids in the f i r s t three instars do not readi ly drop when exposed to alarm pheromone, whereas adult Vancouver aphids do. Higher morta l i t ie s on the ground in the former groups was suggested as the force select ing against dropping 60 in response to reception of an alarm pheromone. Relative responses to alarm pheromone provide an ind i rect measure of wi l l ingness to disperse. In th is chapter I examine the predator-escape responses of adult aphids from Vancouver and Kamloops, to test the hypothesis that Kamloops aphids are conservative about leaving the host plant. This i s done by observing the behaviour of the two biotypes when d i r e c t l y confronted by a predator. Secondly, I test the physiological tolerance of the two aphid b io-types to heat and des iccat ion. If aphids from hotter regions are more res i s tant to heat and des iccat ion, then the conditions that they face on the ground might not be perceived as more s t r e s s f u l . Harrison and Barlow (1973) showed that f i r s t instar pea aphids can survive temperatures of 41°C at near 100% re l a t i ve humidity for up to 25.5 minutes. Harrison and Barlow's (1973) data cannot be used to test the hypothesis of temperature effects on pea aphid dispersal success because they did not indicate what effects the high temperatures had on behaviour. Ruth et_ al_. (1975) showed that greenbugs, Schizaphis graminum (Rondani), ceased moving within four seconds of dropping to the ground on a sunny day when ground temperatures ranged from 45°C to 54°C. We also do not know what effects high evaporation rates might have on aphid surv ival at high temperatures. On hot, sunny days, evaporation rates at ground level would be much higher than in the closed tubes used by Harrison and Barlow (1973). 61 Materials and Methods A colony of pea aphids was started from many indiv iduals co l lected from a l f a l f a on the Univers ity of B r i t i s h Columbia campus, Vancouver, in the mi ld , moist coastal region of B r i t i s h Columbia. A second colony was co l lected from a l f a l f a at the Agr iculture Canada Research Stat ion, Kamloops which is s ituated in the hot, dry i n t e r i o r region of the province. The two colonies were reared separately on broad bean V i c i a faba cv Exhib it ion Long Pod, under a l i g h t regime of 16L:8D at 20°C * 1.5. The aphids were reared using the method of Harrison and Barlow (1972) to provide three-day-old adult aphids for the escape-reaction experiments and one-day-old f i r s t instars and three-day-old adults fo r the temperature treatment tes t s . A l l tests were conducted between 1100 and 1400 hr. The colonies were 8 generations old when the experiments began. Escape Response Experiments One adult c occ i ne l l i d Coccinel la c a l i f o r n i c a Mannerheim (starved for twenty-four hours) was released onto a plant holding a group of three-day-old adult aphids. The beetle was allowed to search un t i l i t confronted and e l i c i t e d a reaction from an aphid. Three aphid reactions were recorded: (1) run - the aphid removes i t s s t y l e t from the plant and runs to another part of the plant; (2) drop - the aphid drops from the plant; (3) back up - the aphid removes i t s s t y l e t from the plant and, in so doing, moves i t s body backwards and then remains r i g i d . If the aphid ran or dropped within one second of exh ib i t ing a back 62 up react ion, then the reaction was not recorded as the back up type. Only results from d i rec t confrontations were recorded. Reactions of aphids that were approached from the back or side were not recorded. In a l l , 61 Kamloops adults and 62 Vancouver adult aphids were tested. High Temperature Experiments Ground temperatures were measured with a Yellow Springs Instruments thermistor surface probe in f i e l d plots containing bean seedlings separ-ated by 14 cm. Measurements were taken at 0900, 1100, 1300, 1500 and 1700 hr (PDT) over 2 five-day periods in Kamloops and 6 f ive-day periods in Vancouver. At the same time, evaporation was measured using a 1 mm bore glass c ap i l l a r y tube described by Wellington (1949) over a three-minute period. The locomotory response and or ientat ion of insects can be affected by high temperatures (Barlow and Kerr, 1969; Wellington, 1960). Adult aphids were placed in the centre of an arena with a 25 x 25 cm cardboard f l oo r and 5 cm p l a s t i c walls which were coated with Fluon (a smooth p l a s t i c coating which aphids are unable to walk on) to prevent the aphids from escaping. The arena contained four bean plants which were evenly spaced 10 cm from the middle of the f l oo r . The arena was kept in a Hot-pack temperature-controlled growth chamber at 40°C. Aphids were released into the centre of the arena and allowed to search for plants. Of the 20 aphids tested ( in groups of 5), 14 were able to f ind plants before exh ib i t ing signs of heat stupor. This showed that aphids are able to locate plants un t i l they are paralyzed by the heat. 63 Temperature Chamber Experiments Aphids were removed from the i r plants and immediately placed into open glass Petr i dishes whose walls were coated with Fluon . The dishes were placed into a sealed p l a s t i c box (33 x 22 x 7.75 cm high) which was kept in an incubator for test ing at two temperatures, 42°C and 37.5°C. Twenty-four hours before a group of aphids was tested, 50 gm of dehydrated s i l i c a gel was placed into the incubator and 30 gm into the p l a s t i c box. The fol lowing morning, three hours before the experiment began, the s i l i c a was renewed. In a further set of treatments, s imi la r procedures were used but water was used instead of s i l i c a , to provide a moist atmosphere. Aphids were tested in groups of f i v e , two groups at one time. The p l a s t i c box had a c lear cover that allowed me to observe the aphids without disturbing them. Observations were made every 5 minutes at 37.5°C and every 2 minutes at 42°C. A rep l i cate was terminated when a l l aphids exhibited signs of paralys is ( i . e . heat stupor); aphids that remained motionless a f te r having f a l l en on the i r backs or sides with the i r legs curled inwards were considered paralyzed. Aphids in th i s condition usually remained that way un t i l death. On a few occasions, an aphid would recover temporarily. I did not record such an aphid as having been paralyzed un t i l the condition was permanent. Each of the four aphid groups, adult and f i r s t instar Kamloops and Vancouver aphids, were tested with the fol lowing four treatments: (1) 42°C + s i l i c a (3) 37.5°C + s i l i c a (2) 42°C + water (4) 37.5°C + water Control aphids were kept at room temperature and humidity in the 64 same manner as the heat-treated aphids. Probit analysis (Busvine, 1971) was applied to the data to ca lcu-la te the PT c n (the time at which 50% of the aphids were paralyzed) and ou the 95% confidence l im i t s for PT 5 Q . A non-parametric test (Mann Witney U Test) was used to compare group mean paralys is times because the experimental design was such that paralys is times were not independent within any one group tested. Results and Discussion Kamloops adult aphids exhibited back up behaviour more frequently (p > 0.001) than Vancouver adult aphids (Figure 12). Back up behaviour i s a response to predators which allows an aphid to prepare i t s e l f fo r immediate dropping, should i t become necessary. However, the aphid does not commit i t s e l f to leaving the p lant, and i f the threat of predation diminishes, the aphid can re insert i t s s t y l e t and continue feeding. Coc-c i n e l l i d s do not usually recognize the presence of an aphid un t i l they contact i t (Dixon, 1959). Therefore, an aphid which faces high morta l i ty r i sks on the ground, should wait un t i l the l a s t possible moment before dropping because an approaching predator may not contact i t . An aphid should only drop in response to the approach of a predator i f i t i s able to cope with the environment on the ground of i f the potential morta l i ty on the ground i s less than i f the aphid were to remain on the plant. Adult aphids in Kamloops suffer higher morta l i ty on the ground than the adult pea aphids in Vancouver (.33 ±.0 8 compared to .06 * .02) (p > 0.01). 65 Therefore, the probab i l i ty of capture by an approaching predator should exceed .33 before a Kamloops adult aphid drops, whereas the probab i l i ty of capture need not be very high before an adult pea aphid in Vancouver should drop to improve i t s chances of su rv i va l . Whereas dropping behaviour eliminates the p o s s i b i l i t y of the aphid being captured while on the plant, an aphid may occasionally be captured while exh ib i t ing back up behaviour. However, the potential mortal i ty during back up behaviour i s much lower than that on the ground in Kamloops and so the Kamloops aphid's best strategy i s to exh ib i t back up behaviour as a preliminary step for dropping and then only drop when necessary. Ground temperatures in Vancouver were not as high as those measured in Kamloops. The highest ground temperature recorded in Vancouver was 33°C and the mean temperature was 25.4°C (SE 2.1, N = 35). By contrast, I recorded temperatures exceeding 40°C on f i ve d i f fe rent occasions on three d i f fe rent days during July 1977 at Kamloops; the highest temperature recorded was 44°C and the mean temperature was 31.3°C (SE 1.6, N = 30). Evaporation rates at ground level were s i g n i f i c an t l y higher (p > 0.001) at Kamloops (2.9 mm/min SE 0.2, M = 30) than at Vancouver (2.0 mm/min SE 0.2, N = 35). Adults and f i r s t instar aphids from Kamloops and Vancouver exhibited signs of paralys is far sooner (p > 0.001) at 42°C than at 37.5°C (Table 8). F i r s t instar aphids always succumbed to heat paralys is sooner than the adults. In the 42°C treatments, aphids res isted paralys is longer in the moist treatments but the differences were not s i gn i f i can t at the 5% l e v e l . At 37.5°C, Kamloops adults became paralyzed sooner (p > 0.02) in the dry atmosphere than in moist condit ions. None of the other three 66 classes of aphids tested became paralyzed sooner in the dry atmosphere. In f a c t , Vancouver adults res i sted paralys is longer (p > 0.04) in the dry than the moist treatment at 37.5°C. I am unable to explain th i s unex-pected re su l t , although there i s some evaporative cool ing of the aphids in the dry atmosphere for a short time. There was no c lear pattern of a greater inherent resistance to heat paralys is by Kamloops aphids compared with Vancouver aphids. Kamloops adults res i sted paralys is longer (p > 0.003) than Vancouver adults at 37.5°C but at 42°C the biotypes are not s i g n i f i c an t l y d i f f e ren t , I suspect that the treatment temperatures are so high that physiological resistance at these extreme temperatures cannot be selected for without high costs to other physiological or enzymatic functions which normally occur at lower temperatures. Since Kamloops adult aphids do not appear to be any more res i s tant to high temperatures, I conclude that the high ground temperatures observed in Kamloops would be s t ress fu l to the i r dispersing apterae. F ie ld conditions in the dispersal experiments were s imi la r for both b io -types, except for temperature and evaporation rates. Therefore, high ground temperatures should be considered as a factor in the higher mor-t a l i t y rates of Kamloops aphids since paralys is times are r e l a t i v e l y short at high temperatures. Kamloops aphids appear to have adjusted the i r escape behaviour in order to cope with higher r i sks on the ground rather than to adjust phys io log ica l l y . F i r s t instars are not only more susceptible to high temperatures but they also tend to be exposed longer on the ground because they have d i f f i c u l t y locating plants and walking over the te r ra in in the f i e l d (chapter I ) . F i r s t instars appear to have made a s imi la r behavioural 67 adjustment as the Kamloops adult aphids. However, f i r s t instar aphids and Kamloops adult aphids w i l l drop from the plant when the dropping st imul i i s strong enough, e.g. contact with a c o c c i n e l l i d . There i s consistent with the argument developed e a r l i e r for dropping response in high r i s k s i tuat ions for Kamloops adult aphids. I consider paralys is times a more r e a l i s t i c indicator of potential mortal i ty for aphids on the ground than lethal times at a given temperature. A paralyzed aphid w i l l probably die while ly ing exposed on the ground unless microenvironmental conditions change r a d i c a l l y , and even then i t i s not known how quickly an aphid can recover from heat stupor. Therefore, paralys is can be viewed as an ind icat ion of imminent death (Darby and Kapp, 1933). CONCLUSIONS These studies provide the f i r s t d e f i n i t i v e evidence that natural enemies are an important factor in the dispersal of apterous pea aphids in the f i e l d . This i s espec ia l ly important from an agr i cu l tu ra l point of view, since the actions of predators may increase the spread of plant diseases by inducing infect ious aphids to disperse to virus free plants. Pea aphids show a p l a s t i c i t y in behaviour not only between popu-lat ions but also within indiv idual clones. This means that the clone as an " i nd i v i dua l " can react to a var iety of s i tuat ions by containing a number of behavioura l ly-d i f ferent aphids, some of which w i l l react 68 Table 8. Paralys is times of f i r s t instar and adult pea aphids from Vancouver and Kamloops at 2 temperatures and 2 humidity treatments. Temp. N MOIST PT™ (95% confidence b U l im i t s ) N DRY PT K n (95% confiden b U l im i t s ) ADULTS Van. 42 60 7.2 (6.4, 8.1) 85 6.2 (5.4, 7.1) Kam. 42 60 7.0 (6.0, 8.2) 75 6.6 (5.6, 7.7) Van. 37.5 60 29.0 (25.2, 33.4) 60 29.0 (24.4, 34.4) Kam. 37.5 60 34.5 (30.3, 39.3) 40 29.5 (25.0, 34.8) FIRST INSTARS Van. 42 90 4.2 (3.8, 4.7) 80 2.8 (1.9, 4.2) Kam. 42 100 4.9 (4.5, 5.3) 60 3.0 (2.0, 4.6) Van. 37.5 60 14.0 (11,2, 17.5) 70 15.0 (17.8, 12.6) Kam. 37.5 90 16.5 (14.2, 19.1) 70 15.0 (18.2, 12.4) Paralys is times are in minutes. 69 Figure 12. Responses of adult Kamloops and Vancouver pea aphids in a d i rect confrontation with an adult c o c c i n e l l i d . .5 o 2 Kamloops p 3 Vancouver I—1 Run Drop Back up 70 optimally to a given s i tua t ion . If we imagine two clones of aphids l i v i n g in two cons istent ly d i f fe rent environments, we can expect natural se lect ion to act upon the clones to promote greater numbers of those indiv iduals whose behaviour best su i ts the environment they are i n . Dixon (1971) stated that i t would be surpr is ing i f d i f fe rent morphs of the bird cherry-oat aphid Rhopalosiphum padi L. exhibited s imi la r repro-ductive strategies since they are exposed to d i f fe rent environments. The same can be said for the same morphs of the pea aphid l i v i n g in d i f f e ren t environments. If aphid clones are able to a l t e r the propor-t ion of behavioural and physiological types contained w i th in , to best su i t environmental s i tuat ions , they may be able to track the i r environ-ment. However, i t i s important that they maintain enough var iat ion within the clone so that a l l responses are ava i lab le for a given s i tuat ion. Janzen (1977) stated that we know almost nothing of aphid population dynamics because what we view as an ent i re f i e l d population of aphids, may in r e a l i t y be a few indiv idual clones spread wide and th in over a large area. I support th i s concensus and suggest that i t i s very d i f -f i c u l t to determine f i tness values of a pa r t i cu la r behavioural of physio-log ica l reaction in the f i e l d because the real value can only be measured by the number of genes an " i n d i v i dua l " contributes to the gene pool and indiv iduals are d i f f i c u l t to recognize in the f i e l d . These very impor-tant problems should not discourage further: research into population processes and the effects of natural enemies on aphids, but instead should provide d i rect ion for future inqu i r ie s . The past decade has seen a resurgence in the use of natural enemies for the control of insect pests (cf Debach, 1974). Although there have been some dramatic successes in b io log ica l con t ro l , I feel that introduction of natural enemies to control pests must be done in a cautious and wel1-developed manner. The results of the virus spread experiments described in th i s thesis point to the fact that the actions of predators may not always be economically benef ic ia l in the f i n a l analys is . 72 BIBLIOGRAPHY Adams, R., L i l l y , J . and Gent i le, A. 1976. Evaluation of some insect ic ides in cont ro l l i ng and reducing flower losses for virus diseases in g ladiola plantings. J . Econ. Ent. 69_: 171-2. Barlow, C.A. and Kerr, W.D. 1969. 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