UBC Theses and Dissertations

UBC Theses Logo

UBC Theses and Dissertations

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

Your browser doesn't seem to have a PDF viewer, please download the PDF to view this item.

Item Metadata

Download

Media
831-UBC_1978_A6_7 R63.pdf [ 3.5MB ]
Metadata
JSON: 831-1.0094299.json
JSON-LD: 831-1.0094299-ld.json
RDF/XML (Pretty): 831-1.0094299-rdf.xml
RDF/JSON: 831-1.0094299-rdf.json
Turtle: 831-1.0094299-turtle.txt
N-Triples: 831-1.0094299-rdf-ntriples.txt
Original Record: 831-1.0094299-source.json
Full Text
831-1.0094299-fulltext.txt
Citation
831-1.0094299.ris

Full Text

STUDIES ON THE DISPERSAL BEHAVIOUR OF APTEROUS PEA APHIDS Acyrthosiphon pi sum (Harris)  by  BERNARD DAVID ROITBERG B.Sc,  Simon Fraser U n i v e r s i t y , 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 t h i s thesis as conforming to the required standard  THE UNIVERSITY OF BRITISH COLUMBIA December, 1977. Bernard David Roitberg, 1977.  In p r e s e n t i n g t h i s  thesis  in p a r t i a l  fulfilment of  the requirements f o r  an advanced degree at the U n i v e r s i t y of B r i t i s h Columbia, the I  Library shall  make i t  freely available  f u r t h e r agree t h a t p e r m i s s i o n  for  reference and  f o r e x t e n s i v e copying o f  this  that  study. thesis  s c h o l a r l y purposes may be granted by the Head of my Department or  by h i s of  for  I agree  this  representatives. thesis  It  is understood that copying or p u b l i c a t i o n  f o r f i n a n c i a l gain s h a l l  written permission.  Department of The  ''P Ic » V  University of B r i t i s h  2075 Wesbrook Place Vancouver, Canada V6T 1W5  Date  £ t_ ,  c <^  Columbia  not be allowed without my  ii  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 l a b o r a t o r y ,  aphids exhibited two types of behaviour while on the ground, a f t e r dropping from plants i n 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 s t r a i g h t l i n e s and did not return to the plant they l e f t .  Adults and older nymphs had the highest proportion  of i n d i v i d u a l s which showed the second type of behaviour and adults showed the greatest tendency to disperse to plants more d i s t a n t than the nearest a v a i l a b l e plants.  Young i n s t a r aphids were less successful at l o c a t i n g  a host than older nymphs and a d u l t s . Aphids were placed on the central bean seedlings w i t h i n p l o t s , inside  large f i e l d cages.  Adult c o c c i n e l l i d s were released i n t o two  of the cages while the other cage remained predator-free.  Aphids i n the  cages with predators frequently moved between p l a n t s , while aphids i n the predator-free cage did not.  Adult aphids colonized more plants and  had a lower m o r t a l i t y while on the ground than a l l other i n s t a r s .  Aphids  did not show a preferred dispersal d i r e c t i o n 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 i n the e x p l o i t a t i o n of  new resources and the regulation of aphid populations i s discussed. Bean plants infected with an aphid transmitted virus were t r a n s planted i n t o the central p o s i t i o n of bean plots i n the f i e l d cages.  i ii  Aphids were placed on the c e n t r a l infected plants and adult c o c c i n e l l i d s were released i n t o two of the three cages f o r 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 a n t l y more plants were infected with v i r u s in the cages.with predators than i n the predator-free cage.  New  v i r u s i n f e c t i o n s were c o r r e l a t e d with plants that were v i s i t e d or colonized by aphids from the central infected plant.  The influence of predators in  the spread of aphid transmitted diseases i s discussed. In laboratory experiments, pea aphids from Vancouver were presented with alarm pheromone from i r r i t a t e d c o n s p e c i f i c s .  Adult and fourth  i n s t a r aphids responded to the pheromone by e i t h e r dropping, running or backing up.  Instars one, two and three responded to the pheromone only  when a v i b r a t o r y stimulus accompanied i t .  A high proportion of a l l  i n s t a r s responded to the double stimulus by dropping.  When adult aphids  from Vancouver and Kami oops were presented with alarm pheromone, the Kamloops adults e x h i b i t e d a more conservative reaction to alarm pheromone. Kami oops adults also were more conservative about leaving t h e i r plant when confronted by a c o c c i n e l l i d predator. A hypothesis i s presented,  which accounts f o r the differences i n  escape reactions between i n s t a r s and biotypes.  The hypothesis takes  i n t o consideration predation r i s k , escape behaviour r e p e r t o i r e and s u r v i v a l on the ground. Pea aphid adults r e s i s t e d heat p a r a l y s i s longer than f i r s t when subjected to high temperature treatments.  instars  A l l aphids succumbed to  p a r a l y s i s sooner at 42°C than at 37.5°C, but there appeared to be no  iv  d i f f e r e n c e in aphid s u r v i v a l in dry compared to moist conditions at high temperatures. temperatures.  Kami oops aphids were not more r e s i s t a n t to high  ACKNOWLEDGEMENTS  Many people have contributed to the work contained i n t h i s and I appreciate t h e i r help.  thesis  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 p h y s i c a l l y throughout t h i s p r o j e c t . ideas and help.  Dr. Bryan Frazer has been a constant source of  Mr. Dave R o l l o , Dr. Bob E l l i o t t , and Dr. Mitch Trimble  a l l read e a r l i e r d r a f t s of papers contained h e r e i n , and provided useful suggestions.  Dr. Ron Forbes and Dr. Richard Hamilton of A g r i c u l t u r e  Canada helped me by suggesting ideas p e r t a i n i n g to aphid s t y l e t s and f o r providing a s u i t a b l e plant v i r u s , r e s p e c t i v e l y .  Ms. Rosemarie  Ms. Carol Hubbard, and Ms. Maggie Chang gave much needed assistance both the laboratory and f i e l d .  Iyer, in  Mr. Don Pearce and his crew maintained  e x c e l l e n t f i e l d conditions at the Vancouver study s i t e , as d i d the crew at A g r i c u l t u r e Canada, Kami oops.  Many other people have contributed as  well and I thank a l l of them, p a r t i c u l a r l y  my committee, Drs. Myers,  Wellington, Frazer and Runeckles f o r t h e i r help.  vi  TABLE OF CONTENTS  Page APPROVAL  i  ABSTRACT  ii  ACKNOWLEDGEMENTS  v  TABLE OF CONTENTS  vi  LIST OF TABLES  vii  LIST OF FIGURES  viii  INTRODUCTION  1  CHAPTER I  DISPERSAL DYNAMICS  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  5  58  CONCLUSIONS  67  REFERENCES  72  vii  LIST OF TABLES  Page Table 1. Behaviour of each i n s t a r of the pea aphid a f t e r dropping from a plant in the laboratory  11  Table 2. Comparison of pea aphids showing running and searching behaviour  12  Table 3. Aphid movements i n r e l a t i o n to the l o c a t i o n of c o c c i n e l l i d s .  18  Table 4. Direct and i n d i r e c t pea aphid m o r t a l i t i e s from coccinellid-aphid interactions  22  Table 5. Comparison of success of three age classes of the pea aphid in f i n d i n g new host p l a n t s , a f t e r leaving t h e 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 r e p e a t a b i l i t y of pea aphid responses when exposed to alarm pheromone on consecutive days  52  Table 8. P a r a l y s i s times of f i r s t i n s t a r 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 i n t e r a c t i o n . . .  Figure  2. Comparison of search and run behaviour paths by adult pea aphids (drawn to s c a l e ) .  The points i n d i c a t e the  p o s i t i o n of the aphid at f i v e second i n t e r v a l s . host plant.  P =  S = p o s i t i o n of aphid a f t e r i t drops from  the plant Figure  4  10  3. The r e l a t i o n s h i p 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 z e Figure  19  4. The r e l a t i o n s h i p between the distance an old nymph dispersed and the density of aphids on the plant from which the aphid l e f t  Figure  20  5. The r e l a t i o n s h i p between fecundity and dispersal in pea aphids.  The number beside each point i n d i c a t e s the  sample s i z e .  ND = non-dispersers; C = aphids in  predator-free cage. Figure  21  6. The frequency d i s t r i b u t i o n s of dispersal distance in three age classes of the pea aphid in the laboratory and f i e l d .  Figure  1 = A d u l t s ; 2 = Old nymphs; 3 = Young nymphs . . 24  7. The spread of BYMV by pea aphids in cages with and without c o c c i n e l l i d predators  Figure  8. Responses of d i f f e r e n t age classes of the pea aphid to a v i b r a t o r y stimulus.  The number beside each point  indicates the number of aphids tested Figure  42  49  9. Types of responses to pheromone stimulus by pea aphids. Second and t h i r d i n s t a r aphids respond s i m i l a r l y to f i r s t i n s t a r aphids  50  ix  Page Figure 10. Types of responses to a pheromone-vioratory stimulus by pea aphids.  Second and t h i r d i n s t a r insects respond  s i m i l a r l y to f i r s t i n s t a r insects  51  Figure 11. Comparative responses of Vancouver and Kami oops aphids to pheromone and pheromone-vibratory s t i m u l i  53  Figure 12. Responses of adult Kamloops and Vancouver pea aphids in a d i r e c t confrontation with an adult c o c c i n e 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), C o c c i n e l l i d s (Coleoptera), Hymenopteran p a r a s i t e s , and many other more general predators.  The pea aphid  has evolved a r e p e r t o i r e of escape behaviours to prevent capture.  The  aphid may kick at natural enemies which are s i m i l a r in s i z e (Evans, 1976), but in the presence of larger predators, they e i t h e r run from the predator or drop from the plant (Dixon, 1958).  The dropping behaviour i s the  major t o p i c of t h i s t h e s i s . The f a c t that pea aphids r e a d i l y drop from t h e i r plant suggests that they are able to e i t h e r return to t h e i r o r i g i n a l host plant or locate a new plant.  Host f i n d i n g behaviour has been extensively studied i n a l a t e 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 f a c t o r y cues when searching for a plant and Niku (1973) reported that A. pi sum responds to v e r t i c a l objects when on the ground a f t e r 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 s p r i n g t a i l harrowing  can reduce pea aphid spread and Cooke (1970) showed that r i l l  irrigation  reduces the spread of pea aphids more e f f e c t i v e l y than s p r i n k l e r 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 c u l t u r a l practices may reduce aphid outbreaks. Niku (1975) has shown that w i t h i n a group of pea aphids, some apterae run i n a s t r a i g h t l i n e a f t e r dropping to the ground while others turn f r e quently, and respond p o s i t i v e l y to v e r t i c l e s t r i p e s .  He suggested that  those moving in a s t r a i g h t l i n e are a c t i v e dispersers while those showing high turning rates are non-dispersers. This thesis i s composed of four separate s t u d i e s , a l l dealing with dispersal in apterous pea aphids.  The o v e r a l l aim of the thesis i s to  e l u c i d a t e the f a c t o r s involved in the dispersal of apterous pea aphids, and the response of aphids to changes in these f a c t o r s .  In the f i r s t section  of the t h e s i s , I examine the behaviour of i n d i v i d u a l aphids while o f f t h e i r p l a n t s , and make predictions about how pea aphids w i l l respond to predators i n the f i e l d , and how environmental f a c t o r s can modify d i s p e r s a l behaviour.  Since aphids are the most important vectors of plant viruses  (Eastop, 1977), the r o l e of predators as an agent increasing the dispersal of i n f e c t i o u s aphids and therefore the spread of plant disease i s of major importance.  In chapter II,  I examine the influence of adult c o c c i n e 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 e n t i r e population, because i t allows f o r e x p l o i t a t i o n of new plant resources and can r e l i e v e population pressure on the colonized food p l a n t .  But i t can have i t s  costs through the m o r t a l i t y of dispersers and reduction of time and energy f o r other a c t i v i t i e s .  When costs exceed benefits i n 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 selection.  Pea aphids e x 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 i n the i n t e r i o r can r e s u l t i n higher m o r t a l i t y of dispersing apterae than on the coast.  In the f i n a l two chapters of t h i s thesis  I  t e s t the hypothesis that aphids that l i v e i n s i t u a t i o n s where r i s k s of m o r t a l i t y when leaving plants i s high, should be more r e l u c t a n t to leave t h e i r plants than aphids that l i v e in s i t u a t i o n s where d i s p e r s a l success i s high, v i z . , the pea aphids i n 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 r e n t  environmental s i t u a t i o n s , I hope to gain some i n s i g h t as to how aphids e x p l o i t t h e i r food p l a n t s .  Figure 1 shows a pea aphid behavioural model,  upon which much of the work contained herein i s based.  4  F i g . 1.  A conceptual model of a predator-pea aphid i n t e r a c t i o n .  4a  predator,  H  I  misled  aphi iphia on plant  predatorl - <  ca ptured  fx  escape  ( s t o p )  t  °P  >  KniE>  kick r  d r op  run  s  x  I  1 captured  ca ptured  escape  ( s t o p )  <  s t  °P  >  run  no  st ^>^S-^5top^) a  <  s  t  °P>  speed t i me a nal e - c \  ie  >  5  Chapter I  DISPERSAL DYNAMICS  6  Introduction  Apterous pea aphids, Acyrthosiphon pi sum ( H a r r i s ) , r e a d i l y drop from plants when disturbed by natural enemies (Dixon, 1958).  Pea aphid clones  have i n d i v i d u a l s which immediately search f o r a plant a f t e r dropping, as well as i n d i v i d u a l s which leave the area before searching f o r a host (Niku, 1975).  In laboratory e x e r c i s e s , when natural enemies were present,  pea aphids r e a d i l y 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 q u a n t i f i e d under laboratory and f i e l d conditions both i n the presence and absence of predators.  The  aim was to i d e n t i f y the f a c t o r s i n f l u e n c i n g the movement of pea aphids among plants i n f i e l d populations and to assess the cost of d i s p e r s a l of different instars.  Materials and Methods  A colony of pea aphids was started from many i n d i v i d u a l s c o l l e c t e d from a l f a l f a on the U n i v e r s i t y of B r i t i s h Columbia campus, Vancouver. Aphids were reared on broad bean V i c i a faba cv E x h i b i t i o n 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 t e s t s were conducted between 1100 and 1400 hr. F i r s t , second, t h i r d and fourth i n s t a r nymphs as well as three day adults  7  were t e s t e d .  The number of aphids on a plant varied between 4 and 8.  When a group of aphids reached t e s t i n g age, the host plant on which they were feeding, was placed i n the centre of a 0.9 x O . 9 m cardboard arena divided i n t o 8,100 numbered 1 cm square blocks.  The g r i d also con-  tained 48 v e r t i c a l l y positioned green p l a s t i c straws i n a 7 x 7 matrix with the host plant occupying the central p o s i t i o n . from i t s nearest neighbour.  Each straw was 14 cm  Pea aphids o r i e n t to v e r t i c a l s t r i p e s when  searching for a host plant (Niku, 1974).  Preliminary t e s t s showed that  straws were treated as i f they were p o t e n t i a l hosts by the pea aphids. An adult c o c c i n e l l i d C o c c i n e l l a c a l i f o r n i c a Mannerheim which was starved f o r 24 hours, was released onto the c e n t r a l bean plant and allowed to search f o r aphids, u n t i l an aphid dropped from the p l a n t .  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 t e r dropping from a plant (Niku, 1975). of t h i s behaviour was recorded.  The duration  Once the aphid began moving, I recorded  i t s p o s i t i o n on the arena g r i d at f i v e second i n t e r v a l s , u n t i l the aphid e i t h e r returned to the o r i g i n a l p l a n t , s e t t l e d on a straw, or ceased moving f o r more than three minutes.  The grid data were analyzed with a  computer program which g r a p h i c a l l y displayed the d i s p e r s a l path and computed the rate of movement, t o t a l distance moved, and the distance from the host at the end of the t r i a l .  Searching aphids e x h i b i t rapid antennal move-  ments and high turning rates compared to those showing running behaviour, which run i n s t r a i g h t l i n e s and hold t h e i r antennae r i g i d over t h e i r back. By observing these behavioural t r a i t s and examining the d i s p e r s a l i t was possible to separate the two behaviour types  ( F i g . 2).  paths,  8  Results and Discussion  S t a t i s t i c a l s i g n i f i c a n c e was tested with the Dixon and Massey (1969) proportions t e s t unless otherwise i n d i c a t e d .  Data are presented as  means, percents or proportions ± one standard e r r o r . All  i n s t a r s exhibited thanotosis a f t e r dropping, which increased i n  average duration with age although not s i g n i f i c a n t l y so i n a l l cases. F i r s t i n s t a r s e i t h e r moved almost immediately a f t e r h i t t i n g the surface or did not move f o r over three minutes and were therefore d i s q u a l i f i e d from the t e s t s . Neither height of f a l l or-physical contact by c o c c i n e l l i d s had any e f f e c t 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 c o r r e l a t e d 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. C h a r a c t e r i s t i c s 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 r a t e .  The aphid movement rates I observed are s i m i l a r to those  shown by Phelan et_ al_. (1976) f o r aphids dropping a f t e r alarm pheromone stimulation.  Whether an aphid shows running or searching behaviour, i n f l u -  ences which host i t s e t t l e s upon.  Searching aphids more frequently  returned to the o r i g i n a l plant than aphids e x h i b i t i n g running behaviour (Table 2).  Adult pea aphids  '.  ran more often (Table 1) and returned  to the o r i g i n a l host plant less often (p < 0.05) than a l l other i n s t a r s (Fig.  6).  Adults moved onto straws more d i s t a n t than the nearest straw  9  more often than a l l other i n s t a r s (Table 1). Generally, aphids e i t h e r searched or ran although i n a few cases, mostly i n the a d u l t s , aphids showed both behaviours separated by r e s t i n g 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 i n s t a r s were less successful with only 55% of f i r s t and 78% of second i n s t a r s f i n d i n g new hosts while searching.  When the f i r s t  two i n s t a r s f e l l w i t h i n 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 i n t h e i r search paths.  From these r e s u l t s i t appears that older i n s t a r s  are more capable of l o c a t i n g host plants at greater distances than young i nstars. The r e s u l t s from the g r i d studies allowed me to make some predictions regarding the aphid-predator i n t e r a c t i o n s i n the f i e l d : (1) The presence of a c t i v e l y searching c o c c i n e l l i d s should r e s u l t i n the dispersal of some i n d i v i d u a l s of a l l i n s t a r classes to new host p l a n t s . (2) A d u l t s , which more frequently adopt running behaviour, should disperse more widely in f i e l d plots and should be found beyond the nearest a v a i l a b l e plants more frequently than the other i n s t a r s . (3) Because the younger i n s t a r s are less successful in l o c a t i n g plants they are expected to s u f f e r higher m o r t a l i t y .  1 0  F i g . 2.  Comparison of search and run behaviour paths by adult pea aphids (drawn to s c a l e ) .  The points i n d i c a t e the p o s i t i o n of  the aphid at f i v e second i n t e r v a l s .  P = Host plant.  P o s i t i o n of aphid a f t e r i t drops from plant.  S =  10a  Search  Run  11  Table 1.  Behaviour of each i n s t a r of the pea aphid a f t e r dropping from a plant in the laboratory.  Instar  N  Thanotosis Duration (sec. ± SE)  Proportion Running + SE  Proportion of successful host finders going to a new host ± SE  ". Proportion'.' r o f ' successful host.finders '-going"""beyond nearest host + 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  Tst  12  0.46 + 0.16  .08 ± .08  .33 + .14  0 .08 + .08  12  Table 2.  Comparison of pea aphids showing running and searching behaviour.  Behaviour Type  N  Speed cm/sec  Turns/ 5 sec  Running  11  .67 ± .03  .18 ± .06  Searching  35  .27 ± .01*  .75 + .04*  # aphids that return to their original host  0 2] * *  # aphids that went to hosts beyond the nearest host  8 3**  Distance (c from o r i g i n a l host that aphid settled  31.3 ± 4.8 5.8 + 1.8*  * S i g n i f i c a n t l y d i f f e r e n t (p < 0.05) using Dixon and Massey's proportion test. * * S i g n i f i c a n t l y d i f f e r e n t (p < 0.01) Chi Square.  13  F i e l d Studies  Materials and Methods  F i e l d 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  w a l l s were nylon screen mesh s i z e 7 threads/cm. . The cage environment was s i m i l a r to that o u t s i d e , although day temperatures were 1° to 2°C cooler and night temperatures were 1° to 2°C warmer i n s i d e .  Solar i n s o -  l a t i o n was reduced by the screen but did not v i s i b l y a f f e c t plant growth. Each cage contained 4 plots each 0.85 x 0,85 m in s i z e , with approximately 0.65 m of bare s o i l between plots and 0.3 m between plots and cage walls.  The distance between plots was such that aphids r a r e l y moved  between p l o t s , although c o c c i n e l l i d s could f r e e l y do so. Within each p l o t broad bean seedlings.  , I transplanted a 7 x 7 array of Each plant was 14 cm from i t s nearest neighbour.  The cages were kept weed f r e e . Pea aphids were c o l l e c t e d from a l f a l f a on the U n i v e r s i t y of B r i t i s h Columbia campus, and placed on broad beans in a screen house f o r three days to a c c l i m a t i z e them. classes.  A f t e r four days the aphids were separated i n t o age  Because of the d i f f i c u l t i e s of r a p i d l y i d e n t i f y i n g i n s t a r s in the  f i e l d , we considered only three age c l a s s e s : young nymphs of f i r s t and second i n s t a r s ; old nymphs c o n s i s t i n g of t h i r d and fourth i n s t a r s , and apterous adults. I placed 15 aphids (5 from each c l a s s ) on the centre plant i n each D  plot.  A p l a s t i c r i n g coated with Fluon  (a p l a s t i c coating too smooth f o r  aphids to walk on) was placed around the centre plant f o r one day to ensure  14  that the aphids s e t t l e d on t h e i r host.  At the end of twenty-four hours,  the r i n g was removed and twenty-five male coccinel 1 i d s , 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 r e e . Aphids and beetles were counted on every plant in each p l o t at 900, 1100, 1300, 1500 and 1700 hr (PDT) each day with the aid of dental mirrors (Tamaki e_t a]_., 1970).  In a d d i t i o n , casual observations were made on the  a c t i v i t y of beetles between counts, and I recorded whether they were a c t i v e l y moving about and whether beetles entered any p l o t s . Aphid movements were c a l c u l a t e d from the changes i n occupation patterns on plants w i t h i n a p l o t from one observation to the next.  With the  density of aphids and c o c c i n e l l i d s that were used, the counts and estimates were accurate over the f i v e 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 i n a l plant now held two aphids and I found three on other p l a n t s , I would estimate that one was k i l l e d on the plant and f i v e died on the ground. The return of aphids was estimated in three ways: (1) by d i r e c t observation of a beetle-aphid group i n t e r a c t i o n ; (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 p l a n t .  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 p o s s i b l e , I c a l c u l a t e d the fecundity of dispersing aphids on the day of dispersal and on the f o l l o w i n g three days.  Fecundity was  measured as the number of o f f s p r i n g per day-degree, above a threshold of 4°C (Campbell e_t al_., 1974).  Temperatures f l u c t u a t e d during the day and  aphid b i r t h rate increases with temperature.  The fecundity of some aphids  was measured over s i x 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 i n the experimental cages, but r a r e l y in the predator free cages.  The few movements observed i n the  control cages were found to be associated with the presence of c o c c i n e 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, i n d i c a t i n g an undisturbed state (Phelan et_ aj_., 1976).  Aphids were r a r e l y found clumped in cages  when predators were present and never for the duration of a t r i a l . The r e l a t i o n s h i p of c o c c i n e l l i d p o s i t i o n and aphid movement i s shown i n Table 3.  For a l l three age classes of aphids, c o c c i n e l l i d s were found  i n the v i c i n i t y of the aphid infested p l a n t , when aphid movements were recorded.  D i r e c t i o n of aphid dispersal The d i r e c t i o n of aphid movement was c a l c u a l t e d by measuring the angle  16  between the plant the aphid l e f t and the new host. considered to be a s t r a i g h t l i n e . into s i x t e e n , 22.5 degree a r c s .  The path taken was  The angular measurements were pooled The data were analyzed using the method  of Batschelet (1965) to determine i f the aphids had a preferred d i r e c t i o n of movement. direction.  R refers to the tendency f o r movement to occur in one R equals 1 when a l l movement i s i n one d i r e c t i o n , whereas R  equals 0 when dispersal i s equal i n a l l d i r e c t i o n s .  In t h i s study, R was  between 0.074 and 0.2 f o r a l l i n s t a r s .  ) Aphid'density and dispersal distance Dispersal distances were c a l c u l a t e d and compared with the density of aphids on the plant from which the aphids l e f t .  Aphid density was p o s i -  t i v e l y c o r r e l a t e d with the dispersal distance in the immature aphids 3 and 4).  (Figs.  The r e l a t i o n s h i p was not s i g n i f i c a n t f o r the a d u l t s .  Effects of dispersal on fecundity The fecundity of aphids was s i g n i f i c a n t l y (p < 0.05) lower on the day a f t e r d i s p e r s a l than at a l l other times ( F i g . 5).  Fedundity was  s l i g h t l y lower on the day of d i s p e r s a l , measured a f t e r the aphid reached a new p l a n t , than on the second and t h i r d day a f t e r dispersal but the d i f f e r e n c e was not s i g n i f i c a n 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 e x p e r i mental cages.  Mortality factors Of the aphids that l e f t t h e i r p l a n t s , s i g n i f i c a n t l y more (p < 0.05)  17  young nymphs were never found i n l a t e r counts (Table 4).  Of the aphids  which remained on plants during a c o c c i n e l l i d encounter, young nymphs had higher m o r t a l i t i e s than adults (p < 0.001) or older nymphs (p < 0.05). S i m i l a r l y , the m o r t a l i t y of old nymphs a f t e r encounters with predators was twice that of adults (N.S.).  D i s t r i b u t i o n of dispersers The distances moved by aphids of the three age groups d i f f e r e d s i g n i f i c a n t l y (p < 0.001 Chi Square) ( F i g . 6).  Almost twice as many adults  and old nymphs went to new plants a f t e r leaving t h e i r o r i g i n a l host, as did young nymphs (Table 5).  Almost three times as many adults and twice  as many old nymphs moved beyond the nearest a v a i l a b l e plant than was the case f o r the younger nymphs (Table 5).  Discussion  Niku (1972) released Syrphus c o r o l l a e (Fab.) larvae i n t o small greenhouse plots i n which the centre plants were colonized by pea aphids. Four days l a t e r , aphids were found throughout the p l o t s , while the spread of aphids in the predator-free plots was minimal.  Tamaki ejt al_. (1970)  obtained s i m i l a r r e s u l t s by releasing Aphidius smithi Sharma and Subba Rao into pea aphid c o l o n i e s .  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 r a r e l y d u p l i c a t e nature; however, these  Table 3.  Aphid movements i n r e l a t i o n to the l o c a t i o n of coccinel1 i d s .  Proportion of aphid movements + SE Coccinel1 i d Position  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 p l o t  .21 ± .05  .29 ± .07  .16 + .03  None a c t i v e  .11 + .04  .17 ± .05  .10 + .03  62  46  132  Total number observed  19  F i g . 3.  The r e l a t i o n s h i p between the distance a young nymph dispersed and the density of aphids on the plant from which the aphid left.  The number beside each point indicates the-sample: s i z e .  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  Distance  dispersed  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 i n d i r e c t pea aphid m o r t a l i t i e s from c o c c i n e l l i d aphid i n t e r a c t i o n s .  K i l l e d on plant + SE  Age Class  Adult Old nymphs Young nymphs  Died on ground + SE  100  .09 + :03  C06 ± .02  49  .16 + .05  .14 + .05  315  .18 + .02*  .31 + .03**  * S i g n i f i c a n t l y d i f f e r e n t from adults and old nymphs (p < 0.05) * * S i g n i f i c a n t l y d i f f e r e n t 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 i n d i n g new host p l a n t s , a f t e r leaving t h e i r host.  Proportion returning to host + SE  Age class  Proportion f i n d i n g new plant ± SE  Proportion f i n d i n g new plant beyond nearest plant ± SE  Adults  91  .27 ± .05  .67 ± .05  .31 + .05  Old nymphs  41  .22 + .06  .61 + .08  .22 + .06  257  .28 + .03  .34 + .03*  .11 + .02**  Young nymphs  * S i g n i f i c a n t l y d i f f e r e n t from adults and old nymphs (p < 0.001) * * S i g n i f i c a n t l y d i f f e r e n t from adults (p < 0.001) and old nymphs (p < 0.05).  24  F i g . 6.  The frequency d i s t r i b u t i o n s of dispersal distance in three age classes of the pea aphid in the laboratory and f i e l d . 2 = Old nymphs; 3 = Young nymphs.  1 = Adults;  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 i m i l a r observations on a d i f f e r e n t biotype of the pea aphid.  An important feature of these differences in behaviour  is  that one type allows the aphid to return to the plant from which i t dropped. The behaviour of the other type reduces the p r o b a b i l i t y of i t s returning to the o r i g i n a l plant. More aphids returned to t h e i r o r i g i n a l host plants in the laboratory studies than in the f i e l d . between the two studies. the paper arena.  This i s probably due to differences i n t e r r a i n In the laboratory, a l l i n s t a r s e a s i l y moved in  Natural t e r r a i n i s never as f l a t as that in the l a b o r a -  t o r y , and from the aphid's perspective, i t i s a rough p l a i n strewn with very large masses.  I often observed an aphid to change course a f t e r  encountering d i f f i c u l t y moving over the ground.  This was e s p e c i a l l y true  f o r the younger i n s t a r s when the ground was dry and s o i l p a r t i c l e s loose. It appears t h a t , even though the laboratory experiments allowed f o r an estimation of the proportions of aphids that are motivated to return to a p l a n t , physical e f f e c t s can modify the actual numbers that do so. The proportion of aphids which were unsuccessful while on the ground, was highest i n the young i n s t a r s .  in f i n d i n g plants Since the cages  excluded predators which are normally present on the ground, I assume that those aphids died before f i n d i n g a host plant.  In the laboratory, many  young i n s t a r s did not move a f t e r dropping to the ground, and a high proport i o n of those that d i d , did not f i n d 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, c o c c i n e l l i d s are most a c t i v e  26  (Frazer and G i l b e r t , 1976).  Temperatures were measured w i t h i n the bean  plant f o l i a g e and on the ground with a Yellow Springs Instruments mister.  ther-  When the average temperature w i t h i n the f o l i a g e was 18°C - 1.0°C,  the ground temperatures were 25.4°C - 2.1°C.  Although aphids can w i t h -  stand temperatures as high as 41°C f o r twenty-five minutes (Harrison and Barlow, 1973), experiments i n chapter IV show that they are unable to walk a f t e r a short time when exposed to high temperatures (6.2 minutes f o r adults N=90 and 2,8 minutes f o r f i r s t i n s t a r s N=80, both at 42°C). That means that s u r v i v a l on the ground i s dependent upon the length of time the aphid can continue to walk i n search of a new plant.  Young i n -  stars are i n double jeopardy i f they leave a plant because they are less successful at f i n d i n g new plants and are more susceptible to the high ground temperatures than a d u l t s .  I suggest, t h e r e f o r e , that young i n s t a r s  should require a stronger stimulus to e l i c i t drop behaviour, compared to older i n s t a r s .  F i r s t , second and t h i r d i n s t a r pea aphids only respond to  alarm pheromone when i t i s accompanied by a v i b r a t o r y stimulus, while adults and fourth i n s t a r s respond to alarm pheromone alone (chapter  III).  I f r i s k s are higher f o r young i n s t a r s , and the data i n d i c a t e they a r e , one would expect young i n s t a r s to return to t h e i r host plant as q u i c k l y as possible.  This does occur, because thanotosis duration i s shortest i n  the younger i n s t a r s and only two of f o r t y young i n s t a r s e x h i b i t e d running behaviour i n the laboratory.  Young nymphs r a r e l y dispersed beyond the  nearest host. Young i n s t a r s are also under greater pressure from predation while on t h e 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 a n t l y higher f o r young i n s t a r s than  27  adults.  Frazer and G i l b e r t (1976) reported s i m i l a r d i f f e r e n t i a l pre-  dation m o r t a l i t i e s between  pea aphid i n s t a r s on a l f a l f a .  Pea aphid fecundity i s less the day a f t e r d i s p e r s a l , which may be due to two causes.  F i r s t , the aphid i s unable to feed but continues to  use energy reserves while on the ground.  Fecundity i s not affected on  the day of d i s p e r s a l , probably because the embryos to be born" are already formed (Ulchanco, 1921; 1924).  that day  However, the i n a b i l i t y to  feed and the energy used f o r dispersal may a f f e c t the development rate of the embryos to be born the f o l l o w i n g day.  Randolph et_ al_. (1975) showed  that as much as 91% of the energy required f o r the production of young comes from the food an aphid ingests.  Roff (1977) found that a reduction  i n fecundity r e l a t e d to the energy costs of dispersal i n Drosophila, and Burns (1971) showed that f l i g h t i n 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 i s d i s p e r s i n g (Muride, 1969a). Thus f a r 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 f o r the pea aphid, but as i t may r e l a t e to other species of aphids.  Van Valen (1971) and L i d i c k e r (1962) have discussed the importance  of emigration in population regulation and the c o l o n i z a t i o n of new r e sources.  In populations composed of s o l i t a r y i n d i v i d u a l s , the advantages  of emigrating (new resources, higher chance of f i n d i n g a mate, e t c . ) , must be weighed >against the costs (greater p o t e n t i a l m o r t a l i t y , lower fecundity) for that i n d i v i d u a l .  When a family group occupies a s i n g l e  resource u n i t , the costs and benefits of dispersal can be analyzed from the group's standpoint as well as the i n d i v i d u a l ' s (Myers and Campbell,  28  1976).  If we view aphid clones as one " i n d i v i d u a l " made up of many  parts (cf Jansen, 1977), then the r i s k s can be spread between the t o t a l number of aphids of that " i n d i v i d u a l " .  Emigration of some of the aphids  r e l i e v e s population pressure on those which remain on the known resource: while possibly extending the clone to new resources.  Overall f i t n e s s  of the clone w i l l be maximized by a balance of the number of aphids which emigrate, to those that stay.  In t h i s way, there i s competition  between clones to most e f f e c t i v e l y balance t h e i r proportions of d i f f e r e n t behaviour types to s u i t d i f f e r e n t environments. When the host plant i s d e c l i n i n g , two t a c 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 i s to reduce competition on the plant through a reduction i n s i z e and fedundity of the adultswhich remain (Murdie, 1969b).  When plant  q u a l i t y i s good and i s expected to remain so, then s e l e c t i o n should favour high numbers of apterous non-dispersers, since these produce more young than a l a t e s (MacKay and Wellington, 1975) and they avoid the r i s k of d i s p e r s a l m o r t a l i t y . Predator influenced dispersal of apterous aphids i s an extension of the p r i n c i p l e s discussed above, but with one major advantage over a l a t e dispersal.  The production of alates in response to d e c l i n i n g resource  q u a l i t y has a lag time of up to one generation. eliminate t h i s l a g .  Apterous  dispersers  Niku (1975) suggests that running behaviour increases  i n frequency i n aphids dropping from p l a n t s , as plant q u a l i t y decreases. Way (1973) noted that migratory urge i n 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 i n 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 p r o b a b i l i t y of overcrowding of aphids on a plant.  There-  f o r e , i f aphids have evolved with predation as a regulating force e i t h e r by dispersing the population or through predator induced m o r t a l i t y , then those aphids are l i k e l y to lack mechanisms to prevent overcrowding i n 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, r e a d i l y leaves the host plant when disturbed.  In the absence of predators, t h i s  species  continues to m u l t i p l y at high rates u n t i l the host plant collapses (Messenger and Force, 1963). Not a l l species of aphids r e a d i l y drop from host plants when d i s turbed and so we should expect to f i n d , differences in l i f e s t y l e s between the two i f both can avoid depleting t h e i r food resources.  We can view  the production of a l a t e emigrators and r e a d i l y dispersive apterae as i n t r i n s i c mechanisms which allow populations to lower t h e i r numbers below carrying capacity.  E x t r i n s i c factors such as predator or other  physical disturbance can also be important i n emigration, much more so i n some species than others. In many species of aphids, apterae seldom leave a p l a n t .  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 r a r e l y leave t h e i r plants and when they do i t  i s across plant bridges (Hughes, 1963).  We suggest that B_. brassicae  should be very s e n s i t i v e to plant conditions which stimulate a l a t e production.  In f a c t , young aggregates of B_. brassicae contain alates  30  (Way and Cammell, 1971), but they do not necessarily emigrate (Way, 1973).  In c o n t r a s t , the pea aphid, at l e a s t the Vancouver biotype, does  not produce alates at low d e n s i t i e s .  A t e s t f o r the hypothesis  that  aphids which are r e t i c e n t to leave the host plant as apterates should have a lower threshold f o r alate production, comes from observations on the Kami oops biotype pea aphids. than in Vancouver.  Summer weather in Kami oops i s hotter  Higher m o r t a l i t y 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 d e n s i t i e s while the Vancouver biotype does not.  Sutherland  (1969) has shown that d i f f e r e n t s t r a i n s 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 s t i m u l i that promote a l a t e production. The black bean aphid Aphis fabae S c o p o l 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 t h e i r plants when food q u a l i t y i s poor. clones contain alates which vary q u a n t i t a t i v e l y .  A. fabae  Some alates f l y long  d i s t a n c e s , 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 a f f e c t e d  by crowding (Shaw, 1970).  This i s s i m i l a r to my observations on the  distance dispersed by apterous pea aphids, i n that crowded nymphs disperse f a r t h e r (Figs. 3 and 4).  Wolfenbarger et_ al_. (1975) made s i m i l a r obser-  vations on Myzus persicae (Sulz.) under highly a r t i f i c i a l  conditions.  It i s curious that adult pea aphids did not show a r e l a t i o n s h i p between distance dispersed and aphid density.  The reason may be r e l a t e d to the  manner in which the d i f f e r e n t i n s t a r s are aggregated on a plant.  Young  31  i n s t a r s are t i g h t l y aggregated, and a d u l t s , e s p e c i a l l y those that have been d i s t u r b e d , may be in loosely aggregated groups or i s o l a t e d on a plant.  My data considered only aphid density per plant and not the  degree of packing of that group of aphids on the p l a n t .  Because of the  way in which they are aggregated on p l a n t s , t o t a 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 i z e of the group the aphid l e f t , f o r ayyoung i n s t a r , than an a d u l t .  Future experiments on t h i s  phenomena should centre on aggregate s i z e (cf Way, 1968). Aphids whose apterae r e a d i l y disperse from t h e i r p l a n t s , probably are d i s t r i b u t e d d i f f e r e n t l y in the f i e l d than species that r a r e l y disperse as apterae.-  The pea aphid^.for example, should be more evenly^dispersed  around a central c o l o n i z a t i o n point than the black bean or cabbage aphid. Way (1968) showed that even at low t o t a l population d e n s i t i e s , A. fabae can be d i s t r i b u t e d so that most of the aphids are crowded beyond an optimal l e v e l on a few p l a n t s , while many of the a v a i l a b l e plants are not c o l o n i z e d . The pea aphid on a l f a l f a i s much more evenly d i s t r i b u t e d 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 f e c t the d i s t r i b u t i o n 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 r a r e l y produced.  The d i s t r i b u t i o n of clones i n the f i e l d would remain nearly  constant.  In c o n t r a s t , species whose apterae r e a d i l y leave the plant could  be spread throughout a f i e l d without alates being produced.  If predators  are adapted to search f o r groups of prey, a more uniformly dispersed aphid population would be perceived as a lower density population.  There-  f o r e , 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 r a r e l y take into account, movements w i t h i n a system because of the d i f f i c u l t i e s involved in measuring them (cf G i l b e r t et_ al_., 1977).  The large s t a f f required to follow 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 i m p r a c t i c a 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 important process in many species of i n s e c t s , e.g. cherry bug ( F u j i s a k i , 1975), cinnabar moth (Myers and Campbell, 1976), cabbage b u t t e r f l y (Jones, 1976). The present studies provide information on between plant movements of pea aphids when food plants are d i s c r e t e and separated by short d i s tances (14 cm).  Future studies should evaluate t h i s process when plant  and other environmental c h a r a c t e r i s t i c s are v a r i e d .  It may be possible  to gain f u r t h e r i n s i g h t into how aphids e x p l o i t food plants under d i f f e r ent circumstances by comparing a v a r i e t y of aphid species and of d i f f e r ent biotypes w i t h i n a species: those that r e a d i l y disperse as apterae as well as those, whose apterae r a r e l y leave plants in response to predators. E a r l i e r I alluded to the importance s e l e c t i o n might play in adjusting the r a t i o of runners and searchers in pea aphid clones under d i f f e r e n t circumstances.  Pea aphids which colonize plants that e x 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 d i s c r e t e plants separated by long distances since t h e i r apterae would l a r g e l y be unsuccessful  in f i n d i n g new p l a n t s .  Myers  and Campbell (1976) found an association between plant spacing and the t e n dency of c i n n i b a r moth larvae to drop from plants when disturbed.  I t may  be possible to compare the apterae of r e a d i l y dispersing species and  33  species whose apterae do not r e a d i l y disperse, in terms of MacArthur and Wilson's (1967) r and K model.  For example, the pea aphid r e a d i l y  disperses, has a r e l a t i v e l y high fecundity (Frazer, 1972), and i t s popul a t i o n s 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 c a r r y i n g capacity through i n t r a s p e c i f i c mechanisms.  Chapter  II  THE SPREAD OF A PLANT VIRUS  35  Introduction  Aphids are the most important vectors of plant v i r u s diseases.  Of  the 620 known plant v i r u s e s , 164 are aphid transmitted (Eastop, 1977). Control of v i r u s spread by the use of chemical aphicides has met with mixed success (cf Adams et_ al_., 1976).  R e f l e c t i v e s o i l mulches reduce the  a b i l i t y of virus c a r r y i n g 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 n e c e s s a r i l y lower v i r u s incidence ( G r y l l s , 1972). Aphid predators are not always successful in capturing t h e i r prey (Dixon, 1958), and t h e i r searching behaviour dislodges prey from the host plant.  This i n t e r a c t i o n disperses aphids to new host plants (Tamaki et a l .  1970; Niku, 1972) which can have serious i m p l i c a t i o n s f o r the spread of v i r u s 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 t h e i r c o c c i n e l l i d predators.  In t h i s chapter, I examine the influence of adult c o c c i n e l l i d s  on the spread of a s t r a i n of Bean Yellow Mosaic v i r u s (BYMV) by the pea aphid Acyrthosiphon pi sum (Harris) to broad beans.  Materials and Methods  The BYMV i s o l a t e was obtained from Dr. R. Hamilton, A g r i c u l t u r e Canada Vancouver.  The virus had been maintained by mechanical transmissions to  broad bean V i c i a faba cv E x h i b i t i o n Long Pod in the greenhouse f o r 1 year.  36  BYMV i s transmitted in a non-persistent manner ( i . e . r e a d i l y picked up on and l o s t from the mouthparts of the vector) by pea aphids.  Obvious symptoms  of c h l o r o t i c m o t t l i n g , often with l e a f margins r o l l e d down, show in broad beans ten days a f t e r i n o c u l a t i o n when grown i n the greenhouse. F i f t e e n bean seedlings were mechanically inoculated and a f t e r ten days, eight plants showing d e f i n i t e symptoms were transplanted to the central p o s i t i o n of a 7 x 7 array of healthy bean seedlings in 0.85 x 0.85 meter p l o t s .  Each plant was 14 cm from i t s c l o s e s t neighbour.  All  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 i m i l a 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 i n each of the two experimental cages and  two plots i n the control cage. Pea aphids were c o l l e c t e d from a l f a l f a growing near the f i e l d cages on the U n i v e r s i t y of B r i t i s h Columbia campus, Vancouver.  The aphids were  placed on bean plants in a screen house to a c c l i m a t i z e them.  In order to  r a p i d l y i d e n t i f y i n d i v i d u a l s in the f i e l d , we separated the aphids i n t o three major c l a s s e s : (1) apterous adults (2) t h i r d and fourth i n s t a r s (3) f i r s t and second i n s t a r s Fifteen apterous aphids, f i v e from each c l a s s , were placed on each of the central plants i n each p l o t and allowed to s e t t l e for twenty-four hours. Twenty adult coccinel1 i d s , C o c c i n e l l a 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  a s c e r t a i n numbers and positions of a l l of the aphids without d i s t u r b i n g them by using dental mirrors (Tamaki et_ al_., 1970).  Through frequent  censuses, the i d e n t i t y of i n d i v i d u a l aphids in each p l o t was known. Three days a f t e r the release of the c o c c i n e l l i d s , the central plant i n each of the experimental plots harboured few or no aphids.  The e x p e r i -  ment was terminated a f t e r 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 f o r  twelve days and then the plants were examined f o r v i r u s  symptoms.  Twenty-five f i e l d c o l l e c t e d aphids were placed i n d i v i d u a l l y onto bean plants for 1 day.  None of these plants showed any signs of v i r u s i n f e c -  t i o n a f t e r fourteen days, so i t was assumed that a l l infected plants in the experiment were produced by aphids having acquired the v i r u s from the diseased central plant.  Results  Aphids i n the cages with c o c c i n e 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 h e i r host plant. The aphids on the control plants were in dense colonies while those in the experimental plots were f a r 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,  a c t i v e c o c c i n e l l i d s were present i n that p l o t . In the experimental p l o 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 l o t (Table 6).  Because  the v i r u s was non-persistent, only movements of aphids from the infected plant to new plants were considered as p o t e n t i a l i n o c u l a t i o n s .  In a c t u a l i t y ,  an average of 16.66 (range 10 to 24) plants per p l o t were v i s i t e d by aphids i n the cages with c o c c i n e l l i d s compared to a mean of 2 (range 1 to 3) in the control cage.  New virus i n f e c t i o n s were s i g n i f i c a n t l y higher (p< 0.001)  in the experimental p l o t s .  Figure 7 shows the d i s t r i b u t i o n of infected  plants i n each of the eight p l o t s . The i n f e c t i o n f r o n t was c a l c u l a t e d by measuring the most d i s t a n t infected plant from the central plant.  S i x t y cm was the maximum distance  the i n f e c t i o n could spread in any p l o t , and t h i s was reached i n four of the s i x experimental plots (Table 6).  The average distance was 55.40 cm  t 3.10 in the experimental plots and only 14 cm i n both of the control plots. A l l except f i v e of the newly infected plants were known to have received aphidsfrom the central plant.  Adjacent plants to the f i v e excep-  tions had received c o l o n i z e r s from the central p l a n t .  It i s highly l i k e l y  those aphids v i s i t e d one of those f i v e 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 i r u s e s . Considerable controversy e x i s t s as to whether apterous or a l a t e aphids are the more important f i e l d vectors of plant virus diseases 1965; Ribbands, 1965).  (Broadbent,  Watson and Healy (1953) showed that Myzus  persicae (Sulz.) apterae can be important vectors when i n f e c t i o n sources are randomly d i s t r i b u t e d w i t h i n a crop.  Ribbands (1962) reported heavy  c o c c i n e l l i d predation of apterates coincident with the spread o f beet yellows.  In another study on groundnuts, Booker (1962) noted the c o r r e s -  pondence between heavy predation on aphid populations and the short time that an aphid population persisted on any one plant.  As i n the present  study, plant disease was more c l o s e l y r e l a t e d to the number of plants infested by aphids rather than to t o t a l aphid numbers. Where timing of virus i n o c u l a t i o n i s c r u c i a l to the existence of high v i r u s incidence, the a c t i v i t y of aphid predators may a c t u a l l y enhance the p r o b a b i l i t y of vector spread.  We might envision the f o l l o w i n g scen-  a r i o : a number of i n f e c t i o u s alates a l i g h t in d i f f e r e n t sections of an agroecosystem, creating a number of point source i n f e c t i o n s ,  Barley yellow  dwarf v i r u s i s only economically damaging f o r a short part of the e a r l y growing season (Doodson and Saunders, 1970).  The aphid populations b u i l d  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 i n f e c t i o n s .  A short delay of an i n f l u x  of predators u n t i l a f t e r the i n f e c t i o u s period has passed might s t i l l allow f o r reduction of aphid numbers without a f f e c t i n g the virus spread. In t h i s study, the v i r u s spread ca 4 times as f a r i n the plots with c o c c i n e l l i d s compared to the c o n t r o l s .  This i s probably a conservative  40  estimate because: (1) In four of the s i x experimental plots the v i r u s spread the maximum distance possible with the experimental design.  I do not know  how f a r the virus may have spread over the three days given unlimited space. (2) I used a non-persistent v i r u s so that transmission success w i l l be small a f t e r the f i r s t plant i s v i s i t e d (Kennedy et aj_., 1962).  A  p e r s i s t e n t v i r u s could be c a r r i e d on with f u r t h e r dispersal movements. (3) The experiment covered only three days.  Over a longer p e r i o d ,  symptoms could develop in newly inoculated p l a n t s , and aphids from these could f u r t h e r inoculate non-infected p l a n t s . These experiments have shown that the importance of predators in reducing aphid populations may be overridden by t h e i r e f f e c t on the spread of v i r u s by dislodged aphids.  Even though populations were lower in the  experimental cages than i n the c o n t r o l , v i r u s 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 v i r u s e s .  41  Table 6.  Spread of Bean Yellow Mosaic v i r u s by pea aphids in predatorcontaining and predator-free cages.  Plot  Total no. aphids in plot a f t e r 3 days  Total plants colonized by aphids from infected plant  No. of infected plants a f t e r 12 days  Infection spread (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  1  47  3  1  14  2  27  1  1  14  Control  42  F i g . 7.  The spread of BYMV by pea aphids i n cages with and without c o c c i n e l l i d predators.  42a  o infection source • new infection  Plots with Predators  •• • o••  • o• •  Control  •o ••  •  Chapter  III  ADAPTATION OF ALARM PHEROMONE RESPONSES OF THE PEA APHID  44  Introduction  When attacked by natural enemies, many aphids release a c o r n i c l e secretion.  Although t h i s secretion may be employed i n a defensive  manner (Edwards, 1966), an a c t i v e 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 r e c e p t i o n .  This escape response i s considered to be an adaptation  for avoiding predators (Nault, 1973).  The s u r v i v a l value of t h i s w i l l  vary, however, depending upon the circumstances.  For example, an i n d i v i d u a l  which leaves the host plant reduces the p r o b a b i l i t y of being captured by a predator on that p l a n t , but now must face the a d v e r s i t i e s of being on the ground. I used the pea aphid Acyrthosiphon pi sum (Harris) to t e s t the hypot h e s i s that the response of aphids to alarm pheromone has been adjusted by t h e i r a g i l i t y in avoiding predators on the plant and by the p r o b a b i l i t y of t h e i r s u c c e s s f u l l y f i n d i n g another host plant a f t e r leaving the o r i g i n a l plant.  This suggests two hypotheses: f i r s t , v a r i a t i o n in  m o b i l i t y and host plant f i n d i n g a b i l i t y among i n s t a r s (see chapter 1) leads to the p r e d i c t i o n that young i n s t a r s should be more conservative than adults in responding to alarm pheromone.  Second, aphids l i v i n g i n  hot, dry climates are exposed to more severe stress on the ground than those l i v i n g i n more salubrious surroundings.  I p r e d i c t , t h e r e f o r e , 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 s k s of leaving the plant are higher i n the hot, dry region.  Materials and Methods Age Class Responses A colony of pea aphids was started from many i n d i v i d u a l s c o l l e c t e d from a l f a l f a on the U n i v e r s i t y of B r i t i s h Columbia campus, Vancouver. Aphids were reared on broad bean V i c i a faba cv E x h i b i t i o n Long Pod, under a l i g h 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 i z e from three to  eleven i n d i v i d u a l s 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 i n d i c a t e pheromone release.  In over  73% of the times that aphids released c o r n i c l e s e c r e t i o n s , there was response by aphids i n d i c a t i n g presence of b i o l o g i c a l l y a c t i v e l e v e l s of alarm pheromone.  This i s consistent with the estimate f o r adult pea aphids  by Nault ejt a]_. (1973).  Cornicle secretions w i l l be c a l l e d alarm pheromone  throughout t h i s paper since i t i s t h i s a c t i v e component which i s of i n t e r e s t here. One of three s t i m u l i were presented to each of the groups of aphids: (1) Pheromone - A fourth i n s t a r aphid was removed from the main colony and brought w i t h i n 0.5 to 1.0 cm of the group being t e s t e d .  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 microforceps near the group being t e s t e d . presence of a natural enemy.  This was done to simulate the  This stimulus did not d i f f e r in i t s e f f e c t  from that of a s t r u g g l i n g aphid (Dixon and Stewart, 1975). (3) Pheromone-vibratory stimulus - This i s the presentation of the two s t i m u l i described above, applied simultaneously. The aphids were allowed three seconds to respond i n each t e s t . group was tested only once, with one of the three s t i m u l i .  A  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 f o r an i n d i v i d u a l or i f i t v a r i e d . Environmental and rearing conditions were the same as in the previous t e s t . Adults were exposed to alarm pheromone from a squeezed aphid.  Those that  dropped i n response were placed on a new plant with two others that r e s ponded s i m i l a r l y .  The aphids were again exposed to alarm pheromone twenty-  four hours l a t e r and t h e i r responses recorded.  Aphids that did not drop  on the f i r s t day were a l s o exposed to alarm pheromone on the f o l l o w i n g day.  47  Behaviour of Kami oops aphids Pea aphids were c o l l e c t e d from a l f a l f a in the i n t e 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  i n s t a r Kamloops aphids were exposed to alarm pheromone and adult Kamloops aphids were exposed to alarm pheromone or pheromone-vibratory s t i m u l i . Methods employed were the same as in the age class experiments,  Results  A l l s i g n i f i c a n c e tests employed e i t h e r the Chi-square t e s t or Dixon and Massey's (1969) proportions t e s t .  Results of t e s t s are followed with  * or * * r e s p e c t i v e l y to i n d i c a t e which t e s t was used. Less than 20% of any i n s t a r showed a v i s i b l e response to the v i b r a tory stimulus alone ( F i g . 8).  Older i n s t a r s tended to respond more f r e -  quently. A greater proportion of fourth i n s t a r and adult aphids (p < 0.01**) responded to the pheromone than the younger i n s t a r s .  Figure 9 shows the  proportion of each type of response with back up behaviour being the most prevalent response by the oldest i n s t a r s .  The proportions of the d i f f e r e n t  responses by i n s t a r s two and three (not shown) was s i m i l a r to i n s t a r one. At l e a s t 78% of a l l i n s t a r s responded to the pheromone-vibratory stimulus.  More than 80% of the responses were the dropping type i n the  f i r s t four i n s t a r s (Figure 10). The dropping behaviour demonstrated by some i n d i v i d u a l s was repeatable.  48  Individuals which l e f t the plant i n 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 a n t l y less on day two (p < 0.05**) than did the t o t a l group of the f i r s t day.  Data of day one were not s i g n i f i -  c a n t l y d i f f e r e n t from the data c o l l e c t e d f o r adults i n the age class experiments. Fourth- i n s t a r nymphs and adult aphids from Kamloops responded less than t h e i r counterparts from Vancouver (p < 0.05*) (Figure 11).  Aphids  from the h o t t e r , 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 r e l u c t a n t to leave the host plant when stimulated by pheromone alone.  However, both groups reacted s i m 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 p h y s i o l o g i c a l state.  The pea aphid displays p l a s t i c i t y i n the response to alarm phero-  mone between i n s t a r s and biotypes.  Adult and fourth i n s t a r pea aphids  are about three times larger than f i r s t i n s t a r pea aphids.  Adults c o l -  lected from the f i e l d were 3.175 mm i n length (SE=0.025, N=l05) from antennal tubercle to anal plate while f i r s t i n s t a r aphids were only 1.041 mm long (SE=0.014, N=94). Related to s i z e d i f f e r e n c e s are the r i s k s of predation associated with each i n s t a r .  For example, a l l stages of the p i r a t e 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  48  0)  c -6 c  oa  C  oa o  48 53 48  J2-  3.  4. Instar  Adult  50  F i g . 9.  Types of responses to pheromone stimulus by pea aphids.  Second  and t h i r d i n s t a r aphids respond s i m i l a r l y to f i r s t i n s t a r aphids.  x O  Z Q. 3  U D CO  {  OO  €  i  i  i  i  i  CN  J  !  I  O  I  L  CN  J  •3 "S + 6uipuodsej  I  I  1  UOIIJOCIOJJ  L  CN  51  F i g . 10.  Types of responses to a pheromone-vibratory stimulus by pea aphids.  Second and t h i r d i n s t a r aphids respond s i m i l a r l y to  f i r s t i n s t a r aphids.  Instar 1 N = 6 4  Instar 4 N r 5 5  + Run  Jump  Back up  No Rx  Type of response to stimulus  Adult N = 5 0  52  Table 7. The r e p e a t a b i l i t y of pea aphid responses when exposed to alarm pheromone on consecutive days.  Type of Response Proportion Run ± SE  Proportion Drop ± SE  Proportion Back up ± SE  71  .07 i .03  .18 ± .05*  .44 ± .06  F i r s t day droppers  18  .05 ± .05  .28 ± .11**  .33 ± .11  F i r s t day non-droppers  45  0  .07 + .04  .22 + .06  Day  Group  1  A l l aphids  2 2  N  * S i g n i f i c a n t l y d i f f e r e n t from day 1 non-droppers (p  0.05)  * * S i g n i f i c a n t l y d i f f e r e n t from day 1 non-droppers (p  0.01)  53  Fig. It.  Comparative responses of Vancouver and Kami oops aphids to pheromone and pheromone-vibratory s t i m u l i .  ra  /y //  Kamloops E3 N - 51 Vancouver L_J N" 46 __»lnstar 4  I r  71  Pheromone  Kamloops Vancouver I  1*1 No R>  Adult  Pheromone only  Kamloops Vancouver lult  N- 41 N* 41  N* 35 N* 50  Pheromone-Vibratory  54  nemorum (L.) (Heteroptera: Anthocoridae) are more e f f i c i e n t at capturing f i r s t i n s t a r than fourth i n s t a r pea aphids (Evans, 1976).  In the l a b o r -  a t o r y , Frazer and G i l b e r t (1976) found that when a c o c c i n e l l i d was present on an aphid i n f e s t e d , the p r o b a b i l i t y of a f i r s t i n s t a r pea aphid being captured and eaten was 3.5 times greater than f o r an a d u l t .  In the f i e l d ,  they found that most of the aphids captured by the beetles were the younger i n s t a r s .  These observations are to be expected i f one examines  the probable success of each escape option a v a i l a b l e to the d i f f e r e n t instars. When predator:aphid s i z e r a t i o i s l a r g e , the p r o b a b i l i t y of avoiding capture by running i s low (Evans, 1976). generally unsuccessful  F i r s t and second i n s t a r s are  at escaping predators whereas the older i n s t a r s may  be s u c c e s s f u l , e s p e c i a l l y i f the predator i s small (e.g. young c o c c i n e l l i d larvae). Back up behaviour requires the removal of the s t y l e t from the feeding site.  The s t y l e t lengths of e a r l i e r i n s t a r s of aphids are d i s p r o p o r t i o n -  a t e l y large.  For example, f i r s t i n s t a r green peach aphid Myzus persicae  (Sulzer) nymphs possess s t y l e t s only s l i g h t l y smaller than the adults (Forbes, 1969).  Presumably, the f i r s t i n s t a r needs a d i s p r o p o r t i o n a t e l y  longer s t y l e t i n order to reach the same feeding s i t e s as the a d u l t s . S t y l e t removal may be more awkward and e n e r g e t i c a l l y c o s t l y to the younger i n s t a r 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, t h i s expenditure may appear i n s i g n i f i c a n t , however, with numerous exposures to alarm pheromone, constant removal of the s t y l e t may be d e t r i mental to the young i n s t a r s .  The younger i n s t a r s are r e l u c t a n t to move  about on the plant compared to the fourth i n s t a r s and a d u l t s .  Unprovoked  55  movements in the former tend to occur only around moulting time when the s t y l e t s must be removed. Dropping behaviour ensures the success of escaping predation on the plant but t h i s response may be c o s t l y . warm weather can be very low.  Aphid s u r v i v a l on the ground i n  Greenbugs, Schizaphis graminum (Rondani),  pushed o f f t h e i r host plants on a hot sunny day were unable to survive high ground temperatures f o r more than four seconds (Ruth et a]_., 1975). Frazer and G i l b e r t (1976) reported that young i n s t a r s of A. pisum have a more d i f f i c u l t time f i n d i n g a host plant when knocked o f f a plant. Young i n s t a r s s u f f e r a s i g n i f i c a n t l y higher m o r t a l i t y (p < 0.01) on the ground than adults (see chapter 1), in dispersal experiments in f i e l d cages.  The m o r t a l i t y 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 o n l y , the younger i n s t a r s may drop or stay.  Other options such as running do not s i g n i f i c a n t l y reduce the  p r o b a b i l i t y of capture and can e n t a i l even greater r i s k s once o f f the plant. Pheromone alone signals a disturbed aphid nearby, but the signal i s not d e f i n i t e enough to warrant d r a s t i c a c t i o n .  Nearby t a c t i l e stimulus  accompanying the pheromone probably does i n d i c a t e more imminent danger, r e q u i r i n g an immediate response.  Aphid predators show a much higher  turning frequency once an aphid has been contacted (Dixon, 1959).  In  t h i s s i t u a t i o n , the p r o b a b i l i t y of m o r t a l i t y from predation may be higher than the p r o b a b i l i t y of death on the ground.  The dual stimulus of pheromone  and v i b r a t i o n caused over 90% of the f i r s t i n s t a r aphids to leave the plant. The older i n s t a r s improve t h e i r chances of s u r v i v a l with a l a r g e r  56  repetoire of escape responses. and i s the l e a s t u t i l i z e d .  Dropping has the highest p o t e n t i a l cost  Pheromone-vibratory s t i m u l a t i o n e l i c i t s a  high p r o b a b i l i t y of,dropping and t h i s complies with the argument presented f o r the smaller i n s t a r s : when a l l i n d i c a t i o n s are that a predator i s near, i t i s time to leave.  But, other avoidance behaviours are also successful  f o r these i n s t a r s 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 i n the summer  months f o r 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 d i f f e r e n c e s are even greater at ground l e v e l 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 r e s p e c t i v e l y . In the summer of 1977, I ran aphid dispersal t e s t s i n f i e l d cages in Kamloops, s i m i l a r to those conducted i n Vancouver i n 1976.  On-ground mor-  t a l i t y was much higher f o r the Kamloops adults and f i r s t i n s t a r s than i t was f o r t h e 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.  S e l e c t i o n would favour those i n d i v i d u a l s that  u t i l i z e non-dropping escape options because of the harsh on-ground environment in Kamloops.  Other p h y s i o l o g i c a l and behavioural d i f f e r e n c e s are  known to occur between d i f f e r e n t biotypes of the pea aphid.  Frazer (1972)  has shown d i f f e r e n c e i n population dynamics between the Vancouver and Kamloops biotypes.  The Kamloops adult pea aphid i s more r e l u c t a n t to drop  i n a d i r e c t confrontation with a c o c c i n e l l i d than the Vancouver type (see  57  chapter 4). Some i n d i v i d u a l s show a repeatable tendency to drop in response to alarm pheromone.  The o f f s p r i n g of one female consists of droppers and  non-droppers, so i t appears that the t r a i t i s not c h a r a c t e r i s t i c of the whole clone.  This mixed strategy i s s i m i l a r to the production of both  alates and apterae by one female which allows her o f f s p r i n g to better e x p l o i t a v a i l a b l e resources  (McKay, 1974).  Those o f f s p r i n g which drop  from the host plant may possibly f i n d new resources.  Those that stay and  are not captured by predators, ensure the s u r v i v a l of the group of a known resource.  Way and Cammell (1971) have reasoned s i m i l a r l y f o r aphid popu-  l a t i o n s 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 i n d i v i d u a l s 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 i s often very d i f f e r e n t from that on the plant. on the ground may be. hot and dry or wet and muddy.  Conditions  An aphid that leaves  a plant must be able to move on the ground f o r long enough to f i n d a host plant i f i t i s to survive. In B r i t i s h Columbia, pea aphids occur i n 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 f e r e n t biotypes and d i f f e r e n c e s between the two have been shown for population dynamics (Frazer, 1972) and behaviour (chapter  III).  In Kamloops, ground temperatures and evaporation rates at ground l e v e l are much higher than those i n Vancouver, and t h i s would be a greater stress on dispersing apterae in Kamloops than in Vancouver.  Aphids i n  Kamloops could cope with t h i s problem i n two ways: (1) through reduced tendency to drop in response to predator a c t i v i t y , (2) through greater p h y s i o l o g i c a l resistance to heat and d e s i c c a t i o n . 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 t h e r run, drop, or  back up escape responses from aphids which are near the aphid that releases the pheromone.  Kamloops aphids of a l l i n s t a r s and Vancouver aphids i n the  f i r s t three i n s t a r s do not r e a d i l y drop when exposed to alarm pheromone, whereas adult Vancouver aphids do.  Higher m o r t a l i t i e s on the ground in  the former groups was suggested as the force s e l e c t i n g against dropping  60  in response to reception of an alarm pheromone.  Relative responses to  alarm pheromone provide an i n d i r e c t measure of w i l l i n g n e s s to disperse. In t h i s chapter I examine the predator-escape responses of adult aphids from Vancouver and Kamloops, to t e s t the hypothesis that Kamloops aphids are conservative about leaving the host p l a n t .  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 t e s t the p h y s i o l o g i c a l tolerance of the two aphid b i o types to heat and d e s i c c a t i o n .  If aphids from hotter regions are more  r e s i s t a n t to heat and d e s i c c a t i o n , 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 i n s t a r pea aphids can survive temperatures of 41°C at near 100% r e l a t i v e humidity for up to 25.5 minutes.  Harrison and Barlow's (1973) data cannot be used to t e s t  the hypothesis of temperature e f f e c t s on pea aphid dispersal  success  because they did not i n d i c a t e what e f f e c t s the high temperatures had on behaviour.  Ruth et_ al_. (1975) showed that greenbugs, Schizaphis  graminum  (Rondani), ceased moving w i t h i n 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 e f f e c t s high evaporation rates might have on aphid s u r v i v a l at high temperatures.  On hot, sunny days, evaporation rates at ground  l e v e l 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 s t a r t e d from many i n d i v i d u a l s c o l l e c t e d from a l f a l f a on the U n i v e r s i t y of B r i t i s h Columbia campus, Vancouver, i n the m i l d , moist coastal region of B r i t i s h Columbia.  A second colony was  c o l l e c t e d from a l f a l f a at the A g r i c u l t u r e Canada Research S t a t i o n , Kamloops which i s s i t u a t e d i n 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 E x h i b i t i o n 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 t h r e e day-old adult aphids f o r the escape-reaction experiments and one-day-old f i r s t i n s t a r s and three-day-old adults f o r the temperature treatment t e s 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 o c c i n e l l i d C o c c i n e l l a c a l i f o r n i c a Mannerheim (starved f o r twenty-four hours) was released onto a plant holding a group of three-dayold adult aphids.  The beetle was allowed to search u n t i l i t confronted  and e l i c i t e d a r e a c t i o n 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 p l a n t ; (2) drop - the aphid drops from the p l a n t ; (3) back up - the aphid removes i t s s t y l e t from the plant and, i n so doing, moves i t s body backwards and then remains r i g i d . If the aphid ran or dropped w i t h i n one second of e x h i b i t i n g a back  62  up r e a c t i o n , then the reaction was not recorded as the back up type. Only r e s u l t s from d i r e c 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 t e s t e d . 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 ated by 14 cm.  separ-  Measurements were taken at 0900, 1100, 1300, 1500 and  1700 hr (PDT) over 2 five-day periods i n Kamloops and 6 five-day periods i n Vancouver.  At the same time, evaporation was measured using a 1 mm  bore glass c a p i l l a r y tube described by Wellington (1949) over a t h r e e minute period. The locomotory response and o r i e n t a t i o n of insects can be a f f e c t e d 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 o o 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 o o r .  The arena was kept i n a Hot-  pack temperature-controlled growth chamber at 40°C.  Aphids were released  into the centre of the arena and allowed to search f o r p l a n t s .  Of the  20 aphids tested ( i n groups of 5 ) , 14 were able to f i n d plants before e x h i b i t i n g signs of heat stupor.  This showed that aphids are able to  locate plants u n t i l they are paralyzed by the heat.  63  Temperature Chamber Experiments Aphids were removed from t h e i r plants and immediately placed into open glass P e t r i dishes whose w a l l s 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 f o r t e s t i n g at two temperatures, 42°C and 37.5°C. Twenty-four hours before a group of aphids was t e s t e d , 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 f o l l o w i n g morning, three hours before the experiment  began, the s i l i c a was renewed.  In a f u r t h e r set of treatments, s i m i l a r  procedures were used but water was used instead of s i l i c a , to provide a moist atmosphere. Aphids were tested i n groups of f i v e , two groups at one time.  The  p l a s t i c box had a c l e a r cover that allowed me to observe the aphids without d i s t u r b i n g them.  Observations were made every 5 minutes at 37.5°C and  every 2 minutes at 42°C.  A r e p l i c a t e was terminated when a l l aphids  exhibited signs of p a r a l y s i s  ( i . e . heat stupor); aphids that remained  motionless a f t e r having f a l l e n on t h e i r backs or sides with t h e i r legs curled inwards were considered paralyzed. remained that way u n t i l death. temporarily.  Aphids in t h i s condition usually  On a few occasions, an aphid would recover  I did not record such an aphid as having been paralyzed  u n t i l the condition was permanent. Each of the four aphid groups, adult and f i r s t i n s t a r Kamloops and Vancouver aphids, were tested with the f o l l o w i n g 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 c a l c u l a t e the P T (the time at which 50% of the aphids were paralyzed) and ou cn  the 95% confidence l i m i t s for P T . 5Q  A non-parametric t e s t (Mann Witney  U Test) was used to compare group mean p a r a l y s i s times because the experimental design was such that p a r a l y s i s times were not independent w i t h i n any one group t e s t e d .  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 f o r immediate dropping, should i t become necessary.  However, the aphid does  not commit i t s e l f to leaving the p l a n t , and i f the threat of predation diminishes, the aphid can r e i n s e r t 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 u n t i l they contact i t (Dixon, 1959).  Therefore, an aphid which faces high m o r t a l i t y  r i s k s on the ground, should wait u n 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 p o t e n t i a l m o r t a l i t y on the ground i s less than i f the aphid were to remain on the p l a n t . Adult aphids in Kamloops s u f f e r higher m o r t a l i t y on the ground than the adult pea aphids i n Vancouver (.33 ±.0 8 compared to .06 * .02) (p > 0.01).  65  Therefore, the p r o b a b i l i t y of capture by an approaching predator should exceed .33 before a Kamloops adult aphid drops, whereas the p r o b a b i l i t y of capture need not be very high before an adult pea aphid in Vancouver should drop to improve i t s chances of s u r v i v a 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 p l a n t , an aphid may o c c a s i o n a l l y be captured while e x h i b i t i n g back up behaviour.  However, the potential m o r t a l i t y 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 e x h i b i t back up behaviour as a preliminary step f o r dropping and then only drop when necessary. Ground temperatures in Vancouver were not as high as those measured i n 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 c o n t r a s t ,  I recorded temperatures exceeding 40°C on f i v e d i f f e r e n t occasions on three d i f f e r e n t days during J u l y 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 a n 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 i n s t a r aphids from Kamloops and Vancouver e x h i b i t e d signs of p a r a l y s i s f a r sooner (p > 0.001) at 42°C than at 37.5°C (Table 8).  F i r s t i n s t a r aphids always succumbed to heat p a r a l y s i s sooner than  the adults.  In the 42°C treatments, aphids r e s i s t e d p a r a l y s i s longer i n  the moist treatments but the d i f f e r e n c e s were not s i g n i f i c a n t at the 5% level.  At 37.5°C, Kamloops adults became paralyzed sooner (p > 0.02)  the dry atmosphere than i n moist c o n d i t i o n s .  None of the other three  in  66  classes of aphids tested became paralyzed sooner in the dry atmosphere. In f a c t , Vancouver adults r e s i s t e d p a r a l y s i s longer (p > 0.04) i n the dry than the moist treatment at 37.5°C.  I am unable to explain t h i s unex-  pected r e s u l t , although there i s some evaporative c o o l i n g of the aphids i n the dry atmosphere f o r a short time. There was no c l e a r pattern of a greater inherent resistance to heat p a r a l y s i s by Kamloops aphids compared with Vancouver aphids.  Kamloops  adults r e s i s t e d p a r a l y s i s 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 a n t l y d i f f e r e n t ,  I  suspect that the treatment temperatures are so high that p h y s i o l o g i c a l resistance at these extreme temperatures cannot be selected f o r without high costs to other p h y s i o l o g i c a l or enzymatic functions which normally occur at lower temperatures. Since Kamloops adult aphids do not appear to be any more r e s i s t a n t to high temperatures, I conclude that the high ground temperatures observed i n Kamloops would be s t r e s s f u l to t h e i r d i s p e r s i n g apterae. F i e l d conditions i n the dispersal experiments were s i m i l a r f o r both b i o types, except f o r temperature and evaporation r a t e s .  Therefore, high  ground temperatures should be considered as a f a c t o r i n the higher mort a l i t y rates of Kamloops aphids since p a r a l y s i s times are r e l a t i v e l y short at high temperatures. Kamloops aphids appear to have adjusted t h e i r escape behaviour i n order to cope with higher r i s k s on the ground rather than to adjust physiologically.  F i r s t i n s t a r s 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 l o c a t i n g plants and walking over the t e r r a i n i n the f i e l d (chapter I ) .  F i r s t i n s t a r s appear to have made a s i m i l a r behavioural  67  adjustment as the Kamloops adult aphids.  However, f i r s t i n s t a r aphids  and Kamloops adult aphids w i l l drop from the plant when the dropping s t i m u l 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 f o r dropping response i n high r i s k s i t u a t i o n s f o r Kamloops adult aphids. I consider p a r a l y s i s times a more r e a l i s t i c i n d i c a t o r of p o t e n t i a l m o r t a l i t y f o r aphids on the ground than l e t h a l times at a given temperature. A paralyzed aphid w i l l probably die while l y i n g 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 q u i c k l y an aphid can recover from heat stupor. Therefore, p a r a l y s i s can be viewed as an i n d i c a t i o n 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 f a c t o r i n the d i s p e r s a l of apterous pea aphids in the f i e l d .  This i s e s p e c i a l l y important from an a g r i c u l t u r a l point  of view, since the actions of predators may increase the spread of plant diseases by inducing i n f e c t i o u s aphids to disperse to v i r u s f r e e plants. Pea aphids show a p l a s t i c i t y i n behaviour not only between popul a t i o n s but also w i t h i n i n d i v i d u a l clones.  This means that the clone  as an " i n d i v i d u a l " can react to a v a r i e t y of s i t u a t i o n s by containing a number of b e h a v i o u r a l l y - d i f f e r e n t aphids, some of which w i l l react  68  Table 8.  P a r a l y s i s times of f i r s t i n s t a r and adult pea aphids from Vancouver and Kamloops at 2 temperatures and 2 humidity treatments.  DRY  MOIST PT™ (95% confidence limits)  N  PT  Kn b U  (95% confiden limits)  Temp.  N  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)  b U  ADULTS  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)  P a r a l y s i s times are i n minutes.  69  Figure 12.  Responses of adult Kamloops and Vancouver pea aphids i n a d i r e c t confrontation with an adult c o c c i n e l l i d .  .5 Kamloops p 3 Vancouver I—1  o  2  Run  Drop  Back up  70  optimally to a given s i t u a t i o n .  If we imagine two clones of aphids  l i v i n g i n two c o n s i s t e n t l y d i f f e r e n t environments, we can expect natural s e l e c t i o n to act upon the clones to promote greater numbers of those i n d i v i d u a l s whose behaviour best s u i t s the environment they are i n . Dixon (1971) stated that i t would be s u r p r i s i n g i f d i f f e r e n t morphs of the b i r d cherry-oat aphid Rhopalosiphum padi L. exhibited s i m i l a r reproductive s t r a t e g i e s since they are exposed to d i f f e r e n t 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 r e n t environments.  If aphid clones are able to a l t e r the propor-  t i o n of behavioural and p h y s i o l o g i c a l types contained w i t h i n , to best s u i t environmental s i t u a t i o n s , they may be able to track t h e i r environment.  However, i t i s important that they maintain enough v a r i a t i o n  w i t h i n the clone so that a l l responses are a v a i l a b l e f o r a given si tuation. Janzen (1977) stated that we know almost nothing of aphid population dynamics because what we view as an e n t i r e f i e l d population of aphids, may i n r e a l i t y be a few i n d i v i d u a l clones spread wide and t h i n over a large area.  I support t h i s concensus and suggest that i t i s very d i f -  f i c u l t to determine f i t n e s s values of a p a r t i c u l a r behavioural of physiol o g i c a l reaction i n 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 d u a l " contributes to the gene pool and i n d i v i d u a l s are d i f f i c u l t to recognize i n the f i e l d .  These very impor-  tant problems should not discourage further: research i n t o population processes and the e f f e c t s of natural enemies on aphids, but instead should provide d i r e c t i o n for future i n q u i r i e s . The past decade has seen a resurgence i n the use of natural enemies  f o r the control of insect pests (cf Debach, 1974).  Although there  have been some dramatic successes i n b i o l o g i c a l c o n t r o l , I feel that i n t r o d u c t i o n of natural enemies to control pests must be done i n a cautious and wel1-developed manner.  The r e s u l t s of the virus spread  experiments described i n t h i s t h e s i s point to the f a c t that the actions of predators may not always be economically b e n e f i c i a l i n the final analysis.  72  BIBLIOGRAPHY  Adams, R., L i l l y , J . and G e n t i l e , A. 1976. Evaluation of some i n s e c t i c i d e s in c o n t r o l l i n g and reducing flower losses f o r virus diseases  in  g l a d i o l a plantings. J . Econ. Ent. 69_: 171-2. Barlow, C.A. and Kerr, W.D. 1969. Locomotery responses to temperature in the grain w e e v i l , Si tophi 1 us granarius  (L.) (Coleoptera: C u r c u l i o n -  idae). Can. J . Zool. 47: 217-24. Batschelet, Edward. 1965. S t a t i s t i c a l methods f o r the analysis of problems in animal o r i e n t a t i o n and c e r t a i n b i o l o g i c a l rhythms. AIBS Monograph. Blanchard, R.A. 1934. Control of aphids on a l f a l f a i n the Antelope V a l l e y , C a l i f . USDA C i r . 307. Booker, R.H. 1962. The e f f e c t of sowing date and spacing on rosette disease on groundnut i n Nigeria with observations on the vector Aphis c r a c c i v o r a Koch. Ann. Appl. B i o l . 52_: 125-31. Bowers, W.S., Nishino, C., Montgomery, M.E., Nault, L.R. and N i e l s o n , M.W. 1977. Sesquiterpene progenitor, Germacrene A: An alarm pheromone i n aphids. Science 196: 680-1. Bradley, R.H.E., Moore, C.A. and Pond, D.D. 1966. Spread of potato v i r u s Y c u r t a i l e d by o i l . Nature (Lond.) 209:  1370-1.  Broadbent, L. 1965. The importance of a l a t e aphids in virus spread w i t h i n crops. Proc. 12th Int. Cong. Ent. 1964: 523-4. Burns, M.D. F l i g h t in the vetch aphid, Megoura v i c i a e Buckton. Unpublished Ph.D. t h e s i s , U n i v e r s i t y of Glasgow. Busvine, J.R. 1971. A c r i t i c a l review of the techniques f o r t e s t i n g  73  i n s e c t i c i d e s . Commonwealth A g r i c u l t u r a l Bureaux, p. 345. Campbell, A., Frazer, B.D., G i l b e r t , N., G u t i e r r e z , A.P. and Mackauer, M. 1974. Temperature requirements of some aphids and t h e i r p a r a s i t e s . J . Appl. E c o l . H:  431-8.  Cooke, W.C. 1970. Ecology of Acyrthosiphon pi sum i n the Blue Mountain area of Eastern Washington and Oregon. USDA Tech. B u l l . 1287. Darby, H.H. and Kapp, E.M. 1933. Observations on the thermal death points of Anastrepha ludens (Loew.). USDA Tech. B u l l . 400. DeBach, P. 1974. B i o l o g i c a l control by natural enemies. Cambridge Univers i t y Press, Cambridge. Dixon, A.F.G. 1958. Escape responses shown by c e r t a i n aphids to the presence of Adalia decempunctata. Trans. Royal Ent. Soc. London 110: 319-34. Dixon, A.F.G. 1959. An experimental study of the searching behaviour of the predatory c o c c i n e l l i d beetle A d a l i a bipunctata ( L . ) . J . Anim. Ecol. 28: 259-81. Dixon, A.F.G. 1971. Reproductive s t r a t e g i e s of the a l a t e morphs of the b i r d cherry-oat aphid Rhopalosiphum padi L.  J . Anim. E c o l . 45_: 817-30.  Dixon, A.F.G. and Stewart, W.A. 1975. Function of the siphunculi in aphids with p a r t i c u l a r reference to the sycamore aphid, Drepanosiphum platanoides. J . Z o o l . , Lond. 175_: 279-89. Dixon, W.J. and Massey, F.J. 1969. Introduction to s t a t i s t i c a l a n a l y s i s . McGraw-Hill Book Co., Toronto, p. 249. Doodson, J.K. and Saunders, P.J.W. 1970. Some e f f e c t s of barley yellow dwarf virus on spring and winter cereals in f i e l d t r i a l s . Ann. Appl. B i o l . 66: 361-74.  74  Eastop, V.F. 1977. Worldwide importance of aphids as virus vectors. Chapter 1 Ln Aphids as virus vectors. (K.F. Harris and K. Maramorosch, eds.). Academic Press, New York. Evans, H.F. 1976. The r o l e of predator-prey s i z e r a t i o i n determining the e f f i c i e n c y of capture by Anthocoris nemorum and the escape reactions of i t s prey, Acyrthosiphon pi sum. E c o l . Entomol. 1_: 85-90. Farrar, C L . 1963. Large cage design f o r insect and plant research.  U.S.  Dept. A g r i c . A.R.S. 33-77. Ferrar, P. 1969. Interplant movement of apterous aphids with special reference to Myzus persicae ( S u l z . ) . B u l l . Ent. Res. 60: 653-60. Forbes, A.R. 1969. The s t y l e t s of the green peach aphid Myzus persicae. Can. Ent. 101_: 31-41. Frazer, B.D, 1972. L i f e tables and i n t r i n s i c rates of increase of apterous black bean aphids and pea aphids, on broad bean (Homoptera: Aphididae). Can. Ent. 104: 1717-22. Frazer, B.D. 1972. Poluation dynamics and recognition of biotypes i n the pea aphid. Can, Ent. 104:  1729-33.  Frazer, B.D. 1977. Plant virus epidemiology and computer simulation of aphid populations. Chapter 17 In_ Aphids as virus vectors  (K.F.  Harris and K. Maramorosch, eds.). Academic Press, New York. Frazer, B.D. and G i l b e r t , N. 1976. C o c c i n e l l i d s and aphids: A q u a n t i t a t i v e study of the impact of adult ladybirds (Coleoptera: C o c c i n e l l i d a e ) preying on f i e l d populations of pea aphids (Homoptera: Aphididae). J . Entomol. Soc. B r i t . Columbia 73_: 33-56. F u j i s a k i , K. 1975. Breakup and reformation of colony in the f i r s t - i n s t a r larvae of the winter cherry bug, Acanthocoris sordidus Thunberg  75  (Hemiptera: Coreidae), in r e l a t i o n to the defense against t h e i r enemies. Res. P o l . E c o l . Kyoto Univ. 16: 252-64. G i l b e r t , N., G u t i e r r e z , A.P., Frazer, B.D. and Jones, R.E. 1976. E c o l ogical Relationships. W.H. Freeman & Co., San Francisco, p. 157. G r y l l s , N.E. 1972. Aphid i n f e s t a t i o n and virus i n f e c t i o n of peas and beans on the Central Tablelands of New South Wales. Aus. J . A g r i c . Anim. Husb. 12.: 668-74. Harrison, J.R. and Barlow, C.A. 1972. Population growth of Acyrthosphon pi sum a f t e r exposure to extreme temperatures. Ann, Ent. Soc. Amer. 65: 1011-15. Harrison, J.R. and Barlow, C.A. 1973. Survival of the pea aphid Acyrthosiphon pi sum (Homoptera: Aphididae), at extreme temperatures. Can. Ent. 105: 1513-18. Hughes, R.D, 1963. Population dynamics of the cabbage aphid Brevicoryne brassicae ( L . ) . J . Anim. E c o l . 32: 393-424. Janzen, D.H. 1977. What are dandelions and aphids? Am. Nat. 111_: 586-9. Jones, R.E. 1977. Search behaviour: a study of 3 c a t e r p i l l a r species. Behaviour 60: 237-60. Kennedy, J . S . , Day, M.F. and Eastop, V.F. 1962. A Conspectus of Aphids as Vectors of Plant Viruses. Commonwealth A g r i c u l t u r a l Bureau, Farnham Royal, 114 pp. Kislow, C . J . and Edwards, L . J . 1972. Repellent odours in aphids. Nature (Lond.). 235: 108-9. Klingauf, F. 1967. P r o t e c t i v e and avoidance reactions of aphids when threatened by predators and p a r a s i t e s , Z. Angew. Ent. 60: 269-317. Kring, J.B. 1972. F l i g h t behaviour of aphids. Ann. Rev. Entomol. 1_7:  76  461-92. L i d i c k e r , W.Z. 1962. Emigration as a possible mechanism permitting the regulation of population density below carrying capacity. Am. Nat. 96: 29-33. MacArthur, R.H. and Wilson, E.O. 1967. The Theory of Island Biogeography. Princeton U n i v e r s i t y Press, Princeton, N.J. MacKay, P.A. 1974. Studies of maternal age as a source of v a r i a t i o n i n two insect species. Ph.D. t h e s i s , U n i v e r s i t y of B r i t i s h Columbia, Vancouver. MacKay, P.A. and Wellington, W.G. 1975. A comparison of the reproductive patterns of the apterous and a l a t e virginoparous Acyrthosiphon pi sum (Homoptera: Aphididae). Can. Ent. 107: 1161-6. Messenger, P.S. and Force, D.C. 1963, An experimental host-parasite system. Therioaphis maculata (Buckton) - Praon p a l i t a n s Muesebeck (Homoptera: Aphididae - Hymenoptera: Braconidae). Ecology 44_: 532-40. Murdie, G. 1969a. The b i o l o g i c a l consequences of decreased s i z e caused by crowding or rearing temperatures in apterae of the pea aphid, Acyrthosiphon pi sum H a r r i s . Trans. R. ent. Soc. Lond, 121: 443-55. Murdie, G. 1969b. Some causes of s i z e v a r i a t i o n in the pea aphid, Acyrthosiphon pisum H a r r i s . Trans. R. ent. Soc, Lond. 121: 423-42. Murdoch, W.W. and Oaten, A. 1975. Predation and population s t a b i l i t y . I_n Advances in Ecological Research (ed. A. Macfadyen). V o l . 9. Academic Press, New York. Myers, J.H. and Campbell, B.J, 1976. D i s t r i b u t i o n and dispersal in popul a t i o n s capable of resource d e p l e t i o n : A f i e l d study. Oecologia 24: 7-20.  77  Nault, L.R. 1973. Alarm pheromones help aphids escape predators. Ohio Rep. 58: 16-17. Nault, L.R. and Bowers, W.S, 1974. M u l t i p l e alarm pheromones in aphids. Ent. exp. appl. ]7_: 455-7. Nault, L.R.,  Edwards, L . J . and Styer, W.E. 1973. Aphid alarm pheromones:  secretion and reception. Envir. Entom. 2_: 101-5. Niku, B. 1972. Der E i n f l u s s rauberischer Feinde auf die Ausbreitung von Erbenlausen (Acyrthosiphon pi sum (Harr.)) in Bestand. Z. Ang. Entomol. 70: 359-64. Niku, B. 1973. Die Orientierung von Erbsenlciasen (Acyrthosiphon pi sum (Harr.)) nach einer F a l l r e a k t i o n . Z. P f l . Krankh. und P f l . Schutz 79: 729-42. Niku, B. 1975. Verhalten und Frochtbarkeit ungefluegetter Erbsenlause (Acyrthosiphon pi sum) nach einer F a l l r e a k t i o n . Entomol. exp. Appl. 18: 17-30. Petterson, J . 1969. Tagging aphids. Opusc. Ent, 33: 219-29. Phelan, P.L., Montgomery, M.E. and Nault, L,R, 1976. Orientation and locomotion of apterous aphids dislodged from t h e i r hosts by alarm pheromone. Ann. Entomol. Soc. Amer. 69_: 1153-6. Randolph, P.A., Randolph, J.C. and Barlow, C.A. 1975. Age s p e c i f i c energetics of the pea aphid Acyrthosiphon pisum. Ecology 56_: 359-69. Ribbands, C R . 1964. Spread of apterae of Myzus persicae (Sulz.) and of yellows virus in sugar beet. B u l l . Ent. Res. 54_: 267-83. Ribbands, C R . 1965. The s i g n i f i c a n c e of apterous aphids i n the spread of viruses w i t h i n a g r i c u l t u r a l crops. Proc. 12th Int. Congr. Ent. 1964:  525-6.  78  Roff, D. 1977. Dispersal  in dipterans: i t s costs and consequences. J .  Anim. Ecol. 46: 443-57. Ruth, W.E., McNew, R.W., Caves, D.W. and Eikenbary, R,D. 1975. forced from host plants by Lysiphlebus testaceipes.  Greenbugs  Entomophaga.  20: 65-71. Shaw, M.J.P. 1970. E f f e c t s of population density on a l i e n i c o l a e of Aphis fabae (Scop.).  II.  The e f f e c t s of crowding on the expression of  migratory urge among alatae i n the laboratory. Ann. appl. B i o l . 65: 197-203. Smith, F.F, and Webb, R.E. 1969. Repelling aphids by r e f l e c t i v e surfaces, a new approach to the control of i n s e c t - t r a n s m i t t e d v i r u s . J_n Viruses, vectors and vegetation. 631-9. New York:  Interscience.  Sutherland, O.R.W. 1969. The r o l e of crowding in the production of winged forms by two s t r a i n s of the pea aphid Acyrthosiphon pi sum. J . Insect P h y s i o l . 15_: 1385-1410. Tamaki, G., Halfhi 11, J.E. and Hathaway, D.0, 1970. Dispersal and reduct i o n of colonies of A. pi sum by Aphidius s m i t h i i . Ann. Ent. Soc. Amer. 63: 973-80. Ulchanco, L.B. 1921. Reproduction in the Aphididae with a consideration of environmental f a c t o r s . Psyche, Cam. Mass. 28: 95-109. Ulchanco, L.B. 1924. Studies on the embryogeny and post natal development of the Aphididae with special reference to the "symbiotic organ" or "mycetome". P h i l i p p i n e Journ. of Science 24_: 143-247. Van Valen, L. 1971. Group s e l e c t i o n and the evolution of d i s p e r s a l . Evolution 25_: 591-8. Watson, M.A. and Healy, M.J.R. 1953. The spread of beet yellows and  79  beet mosaic viruses i n the sugar-beet root crop II.  The e f f e c t s of  aphid numbers on disease incidence. Ann. Appl. B i o l . 40: 38-59. Way, M.J. 1968. I n t r a - s p e c i f i c mechanisms with special reference to aphid populations. J j i : Insect Abundance, ed. T.R.E. Southwood, Sym. Roy. ent. Soc. Lond. 18-36. Way, M.J. 1973. Population structure in aphid colonies. J_n Perspectives in Aphid Biology (ed. A.D. Lowe). Ent. Soc. New Zealand. Way, M.J. and Cammell, M.E. 1971. S e l f regulation in aphid populations. In Dynamics of populations (ed. P . J . den Boer and G.R. Gradwell). Proc. NATO adv. Study I n s t . , Oosterbeek, 1970. pp. 232-42. Pudoc, Wageningen. Wellington, W.G. 1949. The e f f e c t s of temperature and moisture on the behaviour of the spruce bud worm Ghoristoneura fumiferana (Clem.) (Lepidoptera: T o r t r i c i d a e ) I. The r e l a t i v e importance of graded temperature and rate of evaporation in producting aggregations  of  larvae. S c i . A g r i c . 29_: 201-15. Wellington, W.G. 1960. The need f o r d i r e c t observation i n studies of temperature e f f e c t s on l i g h t r e a c t i o n s . Can. Ent. 92: 438-48. Wientjens, W.H.J.M., Lakwijk, A.C. and van der Marel,.T. 1973. Alarm pheromone of grain aphids. Experientia 29_: 658-60. Wolfenbarger, D.O., C o r n e l l , J.A. and Wolfenbarger, D.A. 1974. Dispersal distances attained by insect populations of d i f f e r e n t d e n s i t i e s . Res. Pop. E c o l . j_6: 43-51. Woodford, J.A. 1973. The climate w i t h i n a large aphid proof f i e l d cage. Ent. Exp. Appl. 16:  313-21.  

Cite

Citation Scheme:

        

Citations by CSL (citeproc-js)

Usage Statistics

Share

Embed

Customize your widget with the following options, then copy and paste the code below into the HTML of your page to embed this item in your website.
                        
                            <div id="ubcOpenCollectionsWidgetDisplay">
                            <script id="ubcOpenCollectionsWidget"
                            src="{[{embed.src}]}"
                            data-item="{[{embed.item}]}"
                            data-collection="{[{embed.collection}]}"
                            data-metadata="{[{embed.showMetadata}]}"
                            data-width="{[{embed.width}]}"
                            async >
                            </script>
                            </div>
                        
                    
IIIF logo Our image viewer uses the IIIF 2.0 standard. To load this item in other compatible viewers, use this url:
http://iiif.library.ubc.ca/presentation/dsp.831.1-0094299/manifest

Comment

Related Items