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Simulations of bird cherry—Oat aphid population dynamics: A tool for developing strategies for breeding aphid-resistant plants
Agriculture, Ecosystems and Environment, 14 (1985) 159--170
159
Elsevier Science Publishers B.V., Amsterdam -- Printed in The Netherlands
SIMULATIONS OF BIRD CHERRY--OAT APHID POPULATION DYNAMICS: A TOOL FOR DEVELOPING STRATEGIES FOR BREEDING APHID-RESISTANT PLANTS
S. WIKTELIUS and J. PETTERSSON
Swedish University of Agricultural Sciences, Department of Plant and Forest Protection, Box 7044, S-750 07 Uppsala (Sweden) (Accepted for publication 13 June 1985)
ABSTRACT Wiktelius, S., and Pettersson, J., 1985. Simulations of bird cherry--oat aphid population dynamics: a tool for developing strategies for breeding aphid-resistant plants. Agric. Ecosystems Environ., 14: 159--170. A model of the population dynamics of the bird cherry--oat aphid (Rhopalosiphum padi (L.)) has been used to study the likely effects of plant resistance on aphid population growth. The sensitivity to changes in aphid population variables (landing, wing formation, birth, mortality, development) and their timing were simulated. Based on the simulations, we suggest that resistant plant genotypes should have the following characteristics in their effects on the aphid: (i) cause high nymphal mortality, (ii) cause prolonged development during early plant stages and (iii) cause low birth rate close to ear emergence. The simulations also stress the need for further research on the damaging effects of R. padi on the plant.
INTRODUCTION
The bird cherry--oat aphid (Rhopalosiphum padi (L.)) is a serious pest in spring-sown cereals in Scandinavia. Damage is caused both by direct feeding and by transmission of virus diseases. R. padi is a host-alternating aphid with bird cherry (Prunus padus L.) as primary host and many different grasses and sedges as secondary hosts. After hatching and development on the winter host, alate emigrants invade cereal fields. In central Sweden, this usually happens in the end of May-middleQf June (Wiktelius, 1984). The first generation born in the cereal fields is mainly apterous. The population reaches a peak after about 1 month. It then decreases rapidly due to the combined effect of a less nutritious crop, mortality 6au~ed by natural enemies and the production of a large proportion of alatae that leave the fields (Ekbom and Wiktelius, 1985; Wiktelius and Ekbom, 1985). Overwintering in Sweden takes place exclusively in the egg stage on the primary host, while parthenogenetic overwintering is common in countries with milder winters (Carter et al., 1980). 0167-8809/85/$03.30
© 1985 Elsevier Science Publishers B.V.
160
Screening of cereal varieties for resistance against R. padi has been done under field, greenhouse and laboratory conditions. Several variables, i.e., aphid weight, number of offspring and developmental time have been used to measure the differences in plant resistance (Hsu and Robinsson, 1961, 1962; Rautap~, 1970; Markkula and Roukka, 1972; Kieckhefer et al., 1980; Lowe, 1980). These attempts to find sources of resistance have met with variable success. The variation in resistance is comparatively small and laboratory and field tests often produce contrary results. The goal for a resistance-breeding program should not be to change a certain aphid parameter per se, but to relate such a change to aphid population growth and ultimately to plant damage. We believe that population models are very useful for developing strategies for resistance breeding because they make it possible to predict the likely effects of a resistance character tested in the laboratory on aphid populations in the field. Carter and Dixon (1981) showed the usefulness of population models in a resistance-breeding program for the English grain aphid (Sitobion avenae F.). Their sensitivity analysis of the model showed that changes in mortality, birth rate and developmental rates had strong effects on population growth while landing rate and wing formation were less effective. The objectives of this study were to show how a population model can be used to determine which parts in an aphid's life cycle should be manipulated in attempts to reduce population size and to study when during population development those manipulations would have the strongest effect. The results are discussed in relation to present knowledge on plant damage by R. padi. THE MODEL The simulation model is a deterministic one written in Continuous Simulation Modelling Program (CSMP). The driving variable is temperature and its dally variation is approximated by a sinus function through maximum and minimum temperatures each day. The time step in the calculations is 0.1 day. A relational diagram of the model is shown in Fig. 1. Adults are separated into three different groups: {i) emigrants (EM), (ii) first adult generation following the emigrants (A1) and (iii) later adult generations (A2). The adult pass through six age classes, each with its own temperature-dependent reproductive rate. Reproductive rates and longevities for adults other than emigrants were obtained from Dean (1974). Emigrants have shorter lifespans and a higher reproductive rate early in life than other morphs {Wiktelius and Chiverton, 1985) and these differences have been incorporated into the model. Juveniles are separated into two groups: (i) juveniles from emigrants (J1) and (ii) "other" juveniles (J2). The two groups differ in one character: juveniles from emigrants do not develop into alates. The developmental rates for juveniles were also obtained from Dean {1974).
161
(Flying aphids) variable
rl ~
Rate variable
~ .... l I G
rmm
Auxiliary variable
Flow of P material Flow of - - - - ' P information
~
?
[
I
!
L.
t Fig. 1. A simplified relational diagram of the population development of R, padi. For further explanation see text.
The development of the juveniles and the ageing of the adults are treated as a "boxcar train without dispersion" (for an explanation see de Wit and Goudriaan, 1978). Wing formation is density dependent according to a relationship found by Rautap~i (1976). Wing formation occurs during the fourth juvenile stage. The alatae (AL) are assumed to leave the population immediately. Natural mortality for all instars was estimated from data presented by Dean (1974). Emigrants are assumed to have the same natural mortality as other adults.
162
The developmental rate (DVR) of the crop, expressed in decimal units (Zadoks et al., 1974), is calculated according to the equation: DVR = 0.1 • T E M P - 0.5 The relationship was estimated from field trials conducted at the Institute of Plant Husbandry, Swedish University of Agricultural Sciences (S. Larsson, unpublished results, 1980). SIMULATIONS
The term "normal rates" for birth, development and mortality, hereafter refer to those given by Dean {1974). Plant density in all simulations was set at 400 m -~. Simulations started at crop developmental stage (DVS) 12 and terminated at DVS 50 (beginning of ear emergence). The simulations were initialized by a landing rate of one (low level) or 10 (high level) emigrants per m 2 per day during the first 5 days. In a first set of simulations, the effect of small changes in temperature was tested by using data from years with different temperature conditions for the period 1 June --10 July. Those simulations were done using normal rates and only for the high level of emigrants. Temperatures from 1978 were used in all subsequent simulations. Temperature data were obtained from the meteorological station at the Swedish University of Agricultural Sciences, Uppsala. In a second set of simulations, landing rate, wing formation, daily mortality during first juvenile stage, birth rate or developmental rate of nymphs were changed by 20, 50 or 75%. These simulations were carried out using both high and low levels of emigrants. In a third set of simulations, rates were changed by 20% during certain periods in crop phenology. The rates tested in this way were birth rate, developmental rate of nymphs and first stage juvenile mortality. The changes were in effect during either tillering (DVS 20--30, Day 8--20) stem elongation (DVS 30--40, Day 20--30) or booting (DVS 40--50, Day 30--40). Those simulations were only carried out using the high level of emigrants. Population size was measured as numbers of aphids per plant or the cumulative number of aphids per plant per day, i.e., aphid days. RESULTS
Figure 2 summarizes the phenology of population development at normal rates and at the high level of emigrants. The number of J2 increased rapidly from Day 15 and by Day 24 about 90% of the population consisted of J2. The population peaked at Day 38 with 125 aphids per plant. The first AL appeared on Day 21 and reached their maximum on the last day, when 22% of the population were AL. The general trend in population development
163
No (log n÷l)
J2
2
AL 1
A2
J1 A1 20
10
12
15
2"0
25
3"0
30 :35
4()
40 Day
4'5
5~) DVs
Fig. 2. The s i m u l a t e d n u m b e r in various juvenile and adult stages at n o r m a l c o n d i t i o n s . EM - - emigrants; J1 - - juvenile f r o m emigrants; J2 - - o t h e r juveniles; A1 - - first adult g e n e r a t i o n s after emigrants; A2 - - o t h e r adult generations; A L - - alatae. The lower x-axis indicates d e v e l o p m e n t a l stage o f the crop (DVS).
150
-80 -78 -81 "O
"~ 100 6 z
50.
10
2C)
3()
40
50 Day
Fig. 3. The s i m u l a t e d g r o w t h o f t h e p o p u l a t i o n up t o t h e beginning o f ear e m e r g e n c e using t e m p e r a t u r e c o n d i t i o n s for t h r e e d i f f e r e n t years. Mean t e m p e r a t u r e s for the simulated period: 1978 = 15.2°C; 1980 = 16.3°C; 1981 = 13.2°C.
164
was similar when using the low level of emigrants, but peak number was lower (14 by Day 39) and the proportion of AL was less (0.25%). Changes in temperature altered the day of the peak, but had little effect on its magnitude (Fig. 3). Increases in nymphal mortality caused the most pronounced decreases in peak population and in total numbers of aphid days, independent of the strength of the increase (Table I, Fig. 4). Changes in developmental rate and birth rate were of intermediate importance, while changes in landing rate and wing formation caused relatively small reductions in population size. Small changes in developmental rate had proportionally the strongest effect. The relative magnitudes of the reduction in population size were the same for both high and low levels of emigrants, although the reductions were slightly stronger at the low level. Increased nymphal mortality had a relatively strong effect throughout population development. The relative importance of changes in birth rate was greater early in the development of the population, while the impor-
TABLE I The effects of changes in various population parameters on population size at two levels of emigration* Parameter
Simulated Emigration level change (%) High
Low
Population peak
Total aphid days**
Population peak
Total aphid days**
20 50 75
18 45 72
21 47 73
20 50 75
20 50 75
Nymphal mortality 20 rate 50 75
70 94 98
64 91 97
72 95 99
66 92 97
Birth rate
20 50 75
42 83 97
39 79 95
45 85 97
42 80 95
Developmental rate
20 50 75
57 79 84
42 68 76
57 81 86
45 71 78
Wing formation rate
20 50 75
21 47 67
12 31 46
19 46 67
12 31 46
Landing rate
*Figures are presented in terms of percentage reduction o f normal population size. **Cumulative number of aphids per day up to beginning of ear emergence.
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0
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E to
"N
e~ 0
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0
0
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0 -J
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5 O~ I
o
oo
o
sp!qd0 ~0 "ON
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166 TABLE II Relative importance of changes of various parameters on population size. Parameters are listed in order of decreasing importance within each section Simulated change (%)
Cumulative number of aphids per day after: 20 days
30 days
40 days
20
Mortality Birth Landing Developm. Wingf.
Mortality Developm. Birth Landing Wingf.
Mortality Deveiopm. Birth Landing Wingf.
50
Mortality Birth Landing Developm. Wingf.
Mortality Birth Developm. Landing Wingf.
Mortality Birth Developm. Landing Wingf.
75
Birth Mortality Landing Developm. Wingf.
Mortality Birth Landing Developm. Wingf.
Mortality Birth Developm. Landing Wingf.
tance of changes in developmental rate increased towards the end of the population development period (Table II). A change in developmental rate had the strongest influence when it occurred during the early stages of crop development, while a change in birth TABLE III The effects on population size of changes (20%) in various population parameters at different crop developmental stages (DVS)* Rate
DVS
Cumulative number of aphids per day after: Population peak 20 days 30 days 40 days
Development
20--30 30--40 40--50
17 ---
27 7 --
29 22 +0.4
29 19 13
Birth
20--30 30--40 40--50
12 ---
10 13 --
8 12 11
6 11 16
Mortality
20--30 30--40 40--50
22 ---
22 22 --
19 26 17
13 28 28
*Figures are presented in terms of percentage reduction of normal population size.
167 125"
~751125Z5 ] Oevelopment
!
1 2
Birfh
3
75
25
b
3'0
~.'o
3O
s'o
~0
50
125
Mortahty 75
25 2'0
f
~o
~o
Crop development stoge
so
Fig. 5. The effect on population development of changes (20%) in different rates during crop developmental stage 20--30 (1), 30--40 (2) and 40--50 (3). rate had a stronger influence when occurring closer to ear emergence (Fig. 5, Table III). A late reduction in developmental rate lowered the population peak, b u t slightly increased the number of aphid days at Day 40. The effect of increases in nymphal mortality during different plant stages is obscure, since there was little congruence between the size of peak population and number of aphid days. DISCUSSION This model has not been tested thoroughly against field data, b u t the general trend in population development produced by the model agrees well with that observed in the field (Wiktelius and Ekbom, 1985). Wing formation was treated as a strictly density-dependent process in this model. Thus, alate production decreases as aphid density goes down. Watt and Dixon (1981) and Ankersmit and Dijkman (1983) have shown that both crowding and plant age affect wing formation in Sitobion avenae. This may also be true for R. padi, b u t experimental data are lacking. We believe, however, that the effect of the plant on alate production is more pronounced after ear emergence. We chose to terminate the simulations at the beginning of ear emergence (DVS 50), because t o o little is known a b o u t aphid--host
168
interactions during later plant stages. Alate formation, as well as developmental rates, birth rates and survival are likely to be affected during these later stages and further studies are necessary before this period can be simulated with any accuracy. Furthermore, for the purpose of resistance breeding, we believe that effects on the aphid population before ear emergence are of more importance than effects afterwards. The simulations have indicated the parts of the aphid's life cycle which should be changed in order to cause the largest reductions in population size. Changes in nymphal mortality, developmental rate and birth rate caused relatively large reductions, while changes in landing rate and wing formation were of lesser importance. Theoretical effects can be studied with a model, but reality sets the limits. Available data on ranges of variation found in screening experiments relevant to this study are compiled in Table IV. Although changes in landing rate, according to the simulations, seem to be of little importance, the great variation shown by this variable makes it a potential resistance-breeding factor. On the other hand, the small range of variation in developmental rate probably makes this a less useful factor, in spite of its theoretical potential. No data on nymphal mortality are available for R. padi, but studies on other aphids have shown the importance of this factor (Dielman and Eenink, 1981). Mechanical obstacles, e.g., halryness or accessibility of the phloem vessels are likely to be important to the survival of the earlier instars. It should be possible to develop such mechanical obstacles through resistance breeding. Considering the ranges in Table IV and the results from the simulations, the effects of a single factor are likely to cause only moderate reductions in population size and several factors in combination should be considered in breeding work.
TABLE IV Range of variation observed in screening experiments for plant resistance to R. padi Screened factors
Range of variation
Reference
Comments
75
Kieckhefer et al., 1980
The results were obtained during low infestation levels (0.25--1 per plant)
Developmental rate 10
Adams and Drew, 1964
0.6 days difference from birth to adult
Birth rate
69
Adams and Drew, 1964
Total number of offspring
62
Hsu and Robinson, 1961, 1962
Number of offspring during first 5 days
(%) Landing rate
169 A p l a n t ' s s u i t a b i l i t y f o r an a p h i d is likely t o c h a n g e d u r i n g d e v e l o p m e n t . T h e p r e s e n t w o r k s h o w s t h a t t h e relative i m p o r t a n c e o f changes in d i f f e r e n t a p h i d p o p u l a t i o n p a r a m e t e r s can d e p e n d on t h e p l a n t stage a n d this f a c t s h o u l d be c o n s i d e r e d w h e n designing screening m e t h o d s . R e s i s t a n c e b r e e d i n g against a p h i d s can o n l y be o f use w h e n it is r e l a t e d t o p l a n t d a m a g e . T h e n a t u r e o f d a m a g e o n cereals caused b y aphids is far f r o m u n d e r s t o o d . A p h i d s can cause b o t h q u a n t i t a t i v e a n d qualitative d a m a g e , b u t t h e results f r o m m a n y such e x p e r i m e n t s are a m b i g u o u s ( R a u t a p ~ i , 1 9 7 2 , 1 9 7 5 ; Lee et al., 1 9 8 1 a , b; H o l t et al., 1984). O u r s i m u l a t i o n s s h o w t h a t t h e relative i m p o r t a n c e o f d i f f e r e n t r e s i s t a n c e - b r e e d i n g e f f o r t s change during p l a n t d e v e l o p m e n t and t h a t r e d u c t i o n s in p e a k p o p u l a t i o n a n d a p h i d d a y s o f t e n deviate. M o r e k n o w l e d g e o n w h e n a n d h o w d a m a g e is caused is urgently needed.
REFERENCES Adams, J.B. and Drew, M.E., 1964. Grain aphids in New Brunswick. II. Comparative development in the green house of three aphid species on four kind of grasses. Can. J. Zool., 42: 741--744. Ankersmit, G.W. and Dijkman, H., 1983. Alatae production in the cereal aphid Sitobion avenae. Neth. J. Plant Pathol., 89: 105--112. Carter, N. and Dixon, A.F.G., 1981. The use of insect population simulation models in breeding for resistance. I.O.B.C./W.P.R.S. Bull., IV/l: 21, 24. Carter, N., McLean, J.F.G., Watt, A.D. and Dixon, A.F.G., 1980. Cereal aphids -- a case study and review. Appl. Biol., 5: 271--348. Dean, G.J., 1974. Effect of temperature on the cereal aphids Metopolophium dirhodurn (Wlk.), Rhopalosiphum padi (L.) and Macrosiphum avenae (F.) (Hem. Aphididae). Bull. Entomol. Res., 63: 401--409. Dielman, F.L. and Eenink, A.H., 1981. Resistance of lettuce to Nasonovia ribis nigri: research on the occurrence of differential interactions between host and aphid genotypes and on the inheritance of resistance. SROP/WPRS Bull., 81/4: 41--46. Ekbom, B. and Wiktelius, S., 1985. Polyphagous arthropod predators in cereal crops in central Sweden 1975--1982. Z. Angew. Entomol., 99: 433--442. Holt, J., Griffiths, E. and Wratten, S.D., 1984. The influence of wheat growth stage on yield reductions caused by the rose--grain aphid, Metoplophium dirhodum. Ann. Appl. Biol., 105: 7--14. Hsu, S.-J. and Robinson, A.G., 1961. Resistance of barley varieties to the aphid Rhopalosiphum padi (L.). Can. J. Plant Sci., 42: 247--251. Hsu, S.-J. and Robinson, A.G., 1962. Further studies on resistance of barley varieties to the aphid Rhopalosiphum padi (L.). Can. J. Plant Sci., 43: 343--348. Kieckhefer, R.W., Jedlinski, H. and Brown, C.M., 1980. Host preferences and reproduction of four cereal aphid on 20 Arena selections. Crop Sci., 20 : 400--402. Lee, G., Wratten, S.D. and Kenyi, K.B.L., 1981a. The effects of growth stage in cereals on yield reductions caused by aphids. Proc. Br. Crop Prot. Conf. Pests and Diseases, BCPC Publications, Croydon, pp. 449--456. Lee, G., Stevens, D.J., Stokes, G. and Wratten, S.D., 1981b. Duration of cereal aphid population and the effects on wheat yield and breadmaking quality. Ann. Appl. Biol., 98: 169--178. Lowe, H.J.B., 1980. Resistance to aphids in immature wheat and barley. Ann. Appl. Biol., 95: 129--135.
170
Markkula, M. and Roukka, K., 1972. Resistance of cereals to the aphids Rhopalosiphum padi (L.) and Macrosiphum avenae (F.) and fecundity of these aphids on Graminae, Cyperaceae and Juncaceae. Ann. Agric. Fenn., 11: 417--423. Rautap~i~i, J., 1970. Preference of cereal aphids for various cereal varietiesand species of Graminae, Juncaceae and Cyperaceae. Ann. Agric. Fenn., 9 : 267--277. Rautap~i~i, J., 1972. The importance of Coccinellaseptempunctata L. (Col. Coccinellidae) in controlling cereal aphids, and the effect of aphids on the yield and quality of barley. Ann. Agric. Fenn., 11: 424--436. Rautap~i~i, J., 1975. Control of Rhopalosiphum padi (L.) (Horn., Aphididae) with Coccinella septempunctata L (Col., Coccinellidae) in cages, and effect of late aphid infestation on barley yield. Ann. Agric. Fenn., 14: 231--239. Rautap~i~i, J., 1976. Population dynamics of cereal aphids and method of predicting population trends. Ann. Agric. Fenn., 15: 272--293. Watt, A.D. and Dixon, A.F.G., 1981. The role of cereal growth stages and crowdig on the induction of alatae in Sitobion avenae and its consequences for population growth. Ecol. Entomol., 6: 441--447. Wiktelius, S., 1984. Studies on population development on the primary host and spring migration of Rhopalosiphum padi (L.) (Horn., Aphididae). Z. Angew. Entomol., 87: 217--222. Wiktelius, S. and Chiverton, P.A., 1985. Ovariole number and fecundity for the two emigrating generations of the bird cherry--oat aphid (Rhopalosiphum padi) in Sweden. Ecol. Entomol., 10: 349--355. Wiktelius, S. and Ekbom, B., 1985. Aphids in spring sown cereals in central Sweden: abundance and distribution 1980--1983. Z. Angew. Entomol., 100: 8--16. Wit, C.T. de and Goudriaan, J., 1978. Simulation of Ecological Processes. Pudoc, Wageningen, 103 pp. Zadoks, J.C., Chang, T.T. and Konzak, D.F., 1974. A decimal code for the growth stages of cereals.Weed Res., 14: 415--421.
159
Elsevier Science Publishers B.V., Amsterdam -- Printed in The Netherlands
SIMULATIONS OF BIRD CHERRY--OAT APHID POPULATION DYNAMICS: A TOOL FOR DEVELOPING STRATEGIES FOR BREEDING APHID-RESISTANT PLANTS
S. WIKTELIUS and J. PETTERSSON
Swedish University of Agricultural Sciences, Department of Plant and Forest Protection, Box 7044, S-750 07 Uppsala (Sweden) (Accepted for publication 13 June 1985)
ABSTRACT Wiktelius, S., and Pettersson, J., 1985. Simulations of bird cherry--oat aphid population dynamics: a tool for developing strategies for breeding aphid-resistant plants. Agric. Ecosystems Environ., 14: 159--170. A model of the population dynamics of the bird cherry--oat aphid (Rhopalosiphum padi (L.)) has been used to study the likely effects of plant resistance on aphid population growth. The sensitivity to changes in aphid population variables (landing, wing formation, birth, mortality, development) and their timing were simulated. Based on the simulations, we suggest that resistant plant genotypes should have the following characteristics in their effects on the aphid: (i) cause high nymphal mortality, (ii) cause prolonged development during early plant stages and (iii) cause low birth rate close to ear emergence. The simulations also stress the need for further research on the damaging effects of R. padi on the plant.
INTRODUCTION
The bird cherry--oat aphid (Rhopalosiphum padi (L.)) is a serious pest in spring-sown cereals in Scandinavia. Damage is caused both by direct feeding and by transmission of virus diseases. R. padi is a host-alternating aphid with bird cherry (Prunus padus L.) as primary host and many different grasses and sedges as secondary hosts. After hatching and development on the winter host, alate emigrants invade cereal fields. In central Sweden, this usually happens in the end of May-middleQf June (Wiktelius, 1984). The first generation born in the cereal fields is mainly apterous. The population reaches a peak after about 1 month. It then decreases rapidly due to the combined effect of a less nutritious crop, mortality 6au~ed by natural enemies and the production of a large proportion of alatae that leave the fields (Ekbom and Wiktelius, 1985; Wiktelius and Ekbom, 1985). Overwintering in Sweden takes place exclusively in the egg stage on the primary host, while parthenogenetic overwintering is common in countries with milder winters (Carter et al., 1980). 0167-8809/85/$03.30
© 1985 Elsevier Science Publishers B.V.
160
Screening of cereal varieties for resistance against R. padi has been done under field, greenhouse and laboratory conditions. Several variables, i.e., aphid weight, number of offspring and developmental time have been used to measure the differences in plant resistance (Hsu and Robinsson, 1961, 1962; Rautap~, 1970; Markkula and Roukka, 1972; Kieckhefer et al., 1980; Lowe, 1980). These attempts to find sources of resistance have met with variable success. The variation in resistance is comparatively small and laboratory and field tests often produce contrary results. The goal for a resistance-breeding program should not be to change a certain aphid parameter per se, but to relate such a change to aphid population growth and ultimately to plant damage. We believe that population models are very useful for developing strategies for resistance breeding because they make it possible to predict the likely effects of a resistance character tested in the laboratory on aphid populations in the field. Carter and Dixon (1981) showed the usefulness of population models in a resistance-breeding program for the English grain aphid (Sitobion avenae F.). Their sensitivity analysis of the model showed that changes in mortality, birth rate and developmental rates had strong effects on population growth while landing rate and wing formation were less effective. The objectives of this study were to show how a population model can be used to determine which parts in an aphid's life cycle should be manipulated in attempts to reduce population size and to study when during population development those manipulations would have the strongest effect. The results are discussed in relation to present knowledge on plant damage by R. padi. THE MODEL The simulation model is a deterministic one written in Continuous Simulation Modelling Program (CSMP). The driving variable is temperature and its dally variation is approximated by a sinus function through maximum and minimum temperatures each day. The time step in the calculations is 0.1 day. A relational diagram of the model is shown in Fig. 1. Adults are separated into three different groups: {i) emigrants (EM), (ii) first adult generation following the emigrants (A1) and (iii) later adult generations (A2). The adult pass through six age classes, each with its own temperature-dependent reproductive rate. Reproductive rates and longevities for adults other than emigrants were obtained from Dean (1974). Emigrants have shorter lifespans and a higher reproductive rate early in life than other morphs {Wiktelius and Chiverton, 1985) and these differences have been incorporated into the model. Juveniles are separated into two groups: (i) juveniles from emigrants (J1) and (ii) "other" juveniles (J2). The two groups differ in one character: juveniles from emigrants do not develop into alates. The developmental rates for juveniles were also obtained from Dean {1974).
161
(Flying aphids) variable
rl ~
Rate variable
~ .... l I G
rmm
Auxiliary variable
Flow of P material Flow of - - - - ' P information
~
?
[
I
!
L.
t Fig. 1. A simplified relational diagram of the population development of R, padi. For further explanation see text.
The development of the juveniles and the ageing of the adults are treated as a "boxcar train without dispersion" (for an explanation see de Wit and Goudriaan, 1978). Wing formation is density dependent according to a relationship found by Rautap~i (1976). Wing formation occurs during the fourth juvenile stage. The alatae (AL) are assumed to leave the population immediately. Natural mortality for all instars was estimated from data presented by Dean (1974). Emigrants are assumed to have the same natural mortality as other adults.
162
The developmental rate (DVR) of the crop, expressed in decimal units (Zadoks et al., 1974), is calculated according to the equation: DVR = 0.1 • T E M P - 0.5 The relationship was estimated from field trials conducted at the Institute of Plant Husbandry, Swedish University of Agricultural Sciences (S. Larsson, unpublished results, 1980). SIMULATIONS
The term "normal rates" for birth, development and mortality, hereafter refer to those given by Dean {1974). Plant density in all simulations was set at 400 m -~. Simulations started at crop developmental stage (DVS) 12 and terminated at DVS 50 (beginning of ear emergence). The simulations were initialized by a landing rate of one (low level) or 10 (high level) emigrants per m 2 per day during the first 5 days. In a first set of simulations, the effect of small changes in temperature was tested by using data from years with different temperature conditions for the period 1 June --10 July. Those simulations were done using normal rates and only for the high level of emigrants. Temperatures from 1978 were used in all subsequent simulations. Temperature data were obtained from the meteorological station at the Swedish University of Agricultural Sciences, Uppsala. In a second set of simulations, landing rate, wing formation, daily mortality during first juvenile stage, birth rate or developmental rate of nymphs were changed by 20, 50 or 75%. These simulations were carried out using both high and low levels of emigrants. In a third set of simulations, rates were changed by 20% during certain periods in crop phenology. The rates tested in this way were birth rate, developmental rate of nymphs and first stage juvenile mortality. The changes were in effect during either tillering (DVS 20--30, Day 8--20) stem elongation (DVS 30--40, Day 20--30) or booting (DVS 40--50, Day 30--40). Those simulations were only carried out using the high level of emigrants. Population size was measured as numbers of aphids per plant or the cumulative number of aphids per plant per day, i.e., aphid days. RESULTS
Figure 2 summarizes the phenology of population development at normal rates and at the high level of emigrants. The number of J2 increased rapidly from Day 15 and by Day 24 about 90% of the population consisted of J2. The population peaked at Day 38 with 125 aphids per plant. The first AL appeared on Day 21 and reached their maximum on the last day, when 22% of the population were AL. The general trend in population development
163
No (log n÷l)
J2
2
AL 1
A2
J1 A1 20
10
12
15
2"0
25
3"0
30 :35
4()
40 Day
4'5
5~) DVs
Fig. 2. The s i m u l a t e d n u m b e r in various juvenile and adult stages at n o r m a l c o n d i t i o n s . EM - - emigrants; J1 - - juvenile f r o m emigrants; J2 - - o t h e r juveniles; A1 - - first adult g e n e r a t i o n s after emigrants; A2 - - o t h e r adult generations; A L - - alatae. The lower x-axis indicates d e v e l o p m e n t a l stage o f the crop (DVS).
150
-80 -78 -81 "O
"~ 100 6 z
50.
10
2C)
3()
40
50 Day
Fig. 3. The s i m u l a t e d g r o w t h o f t h e p o p u l a t i o n up t o t h e beginning o f ear e m e r g e n c e using t e m p e r a t u r e c o n d i t i o n s for t h r e e d i f f e r e n t years. Mean t e m p e r a t u r e s for the simulated period: 1978 = 15.2°C; 1980 = 16.3°C; 1981 = 13.2°C.
164
was similar when using the low level of emigrants, but peak number was lower (14 by Day 39) and the proportion of AL was less (0.25%). Changes in temperature altered the day of the peak, but had little effect on its magnitude (Fig. 3). Increases in nymphal mortality caused the most pronounced decreases in peak population and in total numbers of aphid days, independent of the strength of the increase (Table I, Fig. 4). Changes in developmental rate and birth rate were of intermediate importance, while changes in landing rate and wing formation caused relatively small reductions in population size. Small changes in developmental rate had proportionally the strongest effect. The relative magnitudes of the reduction in population size were the same for both high and low levels of emigrants, although the reductions were slightly stronger at the low level. Increased nymphal mortality had a relatively strong effect throughout population development. The relative importance of changes in birth rate was greater early in the development of the population, while the impor-
TABLE I The effects of changes in various population parameters on population size at two levels of emigration* Parameter
Simulated Emigration level change (%) High
Low
Population peak
Total aphid days**
Population peak
Total aphid days**
20 50 75
18 45 72
21 47 73
20 50 75
20 50 75
Nymphal mortality 20 rate 50 75
70 94 98
64 91 97
72 95 99
66 92 97
Birth rate
20 50 75
42 83 97
39 79 95
45 85 97
42 80 95
Developmental rate
20 50 75
57 79 84
42 68 76
57 81 86
45 71 78
Wing formation rate
20 50 75
21 47 67
12 31 46
19 46 67
12 31 46
Landing rate
*Figures are presented in terms of percentage reduction o f normal population size. **Cumulative number of aphids per day up to beginning of ear emergence.
("
."
"0
.o
o
°
.
,o
0
.o
c o~ E o_ o 0~
0
,o
N E
&
\\
0
C~
\, o
E to
"N
e~ 0
'~.-k
.o
0
0
~e
0 -J
-sN
5 O~ I
o
oo
o
sp!qd0 ~0 "ON
r~
m e~
166 TABLE II Relative importance of changes of various parameters on population size. Parameters are listed in order of decreasing importance within each section Simulated change (%)
Cumulative number of aphids per day after: 20 days
30 days
40 days
20
Mortality Birth Landing Developm. Wingf.
Mortality Developm. Birth Landing Wingf.
Mortality Deveiopm. Birth Landing Wingf.
50
Mortality Birth Landing Developm. Wingf.
Mortality Birth Developm. Landing Wingf.
Mortality Birth Developm. Landing Wingf.
75
Birth Mortality Landing Developm. Wingf.
Mortality Birth Landing Developm. Wingf.
Mortality Birth Developm. Landing Wingf.
tance of changes in developmental rate increased towards the end of the population development period (Table II). A change in developmental rate had the strongest influence when it occurred during the early stages of crop development, while a change in birth TABLE III The effects on population size of changes (20%) in various population parameters at different crop developmental stages (DVS)* Rate
DVS
Cumulative number of aphids per day after: Population peak 20 days 30 days 40 days
Development
20--30 30--40 40--50
17 ---
27 7 --
29 22 +0.4
29 19 13
Birth
20--30 30--40 40--50
12 ---
10 13 --
8 12 11
6 11 16
Mortality
20--30 30--40 40--50
22 ---
22 22 --
19 26 17
13 28 28
*Figures are presented in terms of percentage reduction of normal population size.
167 125"
~751125Z5 ] Oevelopment
!
1 2
Birfh
3
75
25
b
3'0
~.'o
3O
s'o
~0
50
125
Mortahty 75
25 2'0
f
~o
~o
Crop development stoge
so
Fig. 5. The effect on population development of changes (20%) in different rates during crop developmental stage 20--30 (1), 30--40 (2) and 40--50 (3). rate had a stronger influence when occurring closer to ear emergence (Fig. 5, Table III). A late reduction in developmental rate lowered the population peak, b u t slightly increased the number of aphid days at Day 40. The effect of increases in nymphal mortality during different plant stages is obscure, since there was little congruence between the size of peak population and number of aphid days. DISCUSSION This model has not been tested thoroughly against field data, b u t the general trend in population development produced by the model agrees well with that observed in the field (Wiktelius and Ekbom, 1985). Wing formation was treated as a strictly density-dependent process in this model. Thus, alate production decreases as aphid density goes down. Watt and Dixon (1981) and Ankersmit and Dijkman (1983) have shown that both crowding and plant age affect wing formation in Sitobion avenae. This may also be true for R. padi, b u t experimental data are lacking. We believe, however, that the effect of the plant on alate production is more pronounced after ear emergence. We chose to terminate the simulations at the beginning of ear emergence (DVS 50), because t o o little is known a b o u t aphid--host
168
interactions during later plant stages. Alate formation, as well as developmental rates, birth rates and survival are likely to be affected during these later stages and further studies are necessary before this period can be simulated with any accuracy. Furthermore, for the purpose of resistance breeding, we believe that effects on the aphid population before ear emergence are of more importance than effects afterwards. The simulations have indicated the parts of the aphid's life cycle which should be changed in order to cause the largest reductions in population size. Changes in nymphal mortality, developmental rate and birth rate caused relatively large reductions, while changes in landing rate and wing formation were of lesser importance. Theoretical effects can be studied with a model, but reality sets the limits. Available data on ranges of variation found in screening experiments relevant to this study are compiled in Table IV. Although changes in landing rate, according to the simulations, seem to be of little importance, the great variation shown by this variable makes it a potential resistance-breeding factor. On the other hand, the small range of variation in developmental rate probably makes this a less useful factor, in spite of its theoretical potential. No data on nymphal mortality are available for R. padi, but studies on other aphids have shown the importance of this factor (Dielman and Eenink, 1981). Mechanical obstacles, e.g., halryness or accessibility of the phloem vessels are likely to be important to the survival of the earlier instars. It should be possible to develop such mechanical obstacles through resistance breeding. Considering the ranges in Table IV and the results from the simulations, the effects of a single factor are likely to cause only moderate reductions in population size and several factors in combination should be considered in breeding work.
TABLE IV Range of variation observed in screening experiments for plant resistance to R. padi Screened factors
Range of variation
Reference
Comments
75
Kieckhefer et al., 1980
The results were obtained during low infestation levels (0.25--1 per plant)
Developmental rate 10
Adams and Drew, 1964
0.6 days difference from birth to adult
Birth rate
69
Adams and Drew, 1964
Total number of offspring
62
Hsu and Robinson, 1961, 1962
Number of offspring during first 5 days
(%) Landing rate
169 A p l a n t ' s s u i t a b i l i t y f o r an a p h i d is likely t o c h a n g e d u r i n g d e v e l o p m e n t . T h e p r e s e n t w o r k s h o w s t h a t t h e relative i m p o r t a n c e o f changes in d i f f e r e n t a p h i d p o p u l a t i o n p a r a m e t e r s can d e p e n d on t h e p l a n t stage a n d this f a c t s h o u l d be c o n s i d e r e d w h e n designing screening m e t h o d s . R e s i s t a n c e b r e e d i n g against a p h i d s can o n l y be o f use w h e n it is r e l a t e d t o p l a n t d a m a g e . T h e n a t u r e o f d a m a g e o n cereals caused b y aphids is far f r o m u n d e r s t o o d . A p h i d s can cause b o t h q u a n t i t a t i v e a n d qualitative d a m a g e , b u t t h e results f r o m m a n y such e x p e r i m e n t s are a m b i g u o u s ( R a u t a p ~ i , 1 9 7 2 , 1 9 7 5 ; Lee et al., 1 9 8 1 a , b; H o l t et al., 1984). O u r s i m u l a t i o n s s h o w t h a t t h e relative i m p o r t a n c e o f d i f f e r e n t r e s i s t a n c e - b r e e d i n g e f f o r t s change during p l a n t d e v e l o p m e n t and t h a t r e d u c t i o n s in p e a k p o p u l a t i o n a n d a p h i d d a y s o f t e n deviate. M o r e k n o w l e d g e o n w h e n a n d h o w d a m a g e is caused is urgently needed.
REFERENCES Adams, J.B. and Drew, M.E., 1964. Grain aphids in New Brunswick. II. Comparative development in the green house of three aphid species on four kind of grasses. Can. J. Zool., 42: 741--744. Ankersmit, G.W. and Dijkman, H., 1983. Alatae production in the cereal aphid Sitobion avenae. Neth. J. Plant Pathol., 89: 105--112. Carter, N. and Dixon, A.F.G., 1981. The use of insect population simulation models in breeding for resistance. I.O.B.C./W.P.R.S. Bull., IV/l: 21, 24. Carter, N., McLean, J.F.G., Watt, A.D. and Dixon, A.F.G., 1980. Cereal aphids -- a case study and review. Appl. Biol., 5: 271--348. Dean, G.J., 1974. Effect of temperature on the cereal aphids Metopolophium dirhodurn (Wlk.), Rhopalosiphum padi (L.) and Macrosiphum avenae (F.) (Hem. Aphididae). Bull. Entomol. Res., 63: 401--409. Dielman, F.L. and Eenink, A.H., 1981. Resistance of lettuce to Nasonovia ribis nigri: research on the occurrence of differential interactions between host and aphid genotypes and on the inheritance of resistance. SROP/WPRS Bull., 81/4: 41--46. Ekbom, B. and Wiktelius, S., 1985. Polyphagous arthropod predators in cereal crops in central Sweden 1975--1982. Z. Angew. Entomol., 99: 433--442. Holt, J., Griffiths, E. and Wratten, S.D., 1984. The influence of wheat growth stage on yield reductions caused by the rose--grain aphid, Metoplophium dirhodum. Ann. Appl. Biol., 105: 7--14. Hsu, S.-J. and Robinson, A.G., 1961. Resistance of barley varieties to the aphid Rhopalosiphum padi (L.). Can. J. Plant Sci., 42: 247--251. Hsu, S.-J. and Robinson, A.G., 1962. Further studies on resistance of barley varieties to the aphid Rhopalosiphum padi (L.). Can. J. Plant Sci., 43: 343--348. Kieckhefer, R.W., Jedlinski, H. and Brown, C.M., 1980. Host preferences and reproduction of four cereal aphid on 20 Arena selections. Crop Sci., 20 : 400--402. Lee, G., Wratten, S.D. and Kenyi, K.B.L., 1981a. The effects of growth stage in cereals on yield reductions caused by aphids. Proc. Br. Crop Prot. Conf. Pests and Diseases, BCPC Publications, Croydon, pp. 449--456. Lee, G., Stevens, D.J., Stokes, G. and Wratten, S.D., 1981b. Duration of cereal aphid population and the effects on wheat yield and breadmaking quality. Ann. Appl. Biol., 98: 169--178. Lowe, H.J.B., 1980. Resistance to aphids in immature wheat and barley. Ann. Appl. Biol., 95: 129--135.
170
Markkula, M. and Roukka, K., 1972. Resistance of cereals to the aphids Rhopalosiphum padi (L.) and Macrosiphum avenae (F.) and fecundity of these aphids on Graminae, Cyperaceae and Juncaceae. Ann. Agric. Fenn., 11: 417--423. Rautap~i~i, J., 1970. Preference of cereal aphids for various cereal varietiesand species of Graminae, Juncaceae and Cyperaceae. Ann. Agric. Fenn., 9 : 267--277. Rautap~i~i, J., 1972. The importance of Coccinellaseptempunctata L. (Col. Coccinellidae) in controlling cereal aphids, and the effect of aphids on the yield and quality of barley. Ann. Agric. Fenn., 11: 424--436. Rautap~i~i, J., 1975. Control of Rhopalosiphum padi (L.) (Horn., Aphididae) with Coccinella septempunctata L (Col., Coccinellidae) in cages, and effect of late aphid infestation on barley yield. Ann. Agric. Fenn., 14: 231--239. Rautap~i~i, J., 1976. Population dynamics of cereal aphids and method of predicting population trends. Ann. Agric. Fenn., 15: 272--293. Watt, A.D. and Dixon, A.F.G., 1981. The role of cereal growth stages and crowdig on the induction of alatae in Sitobion avenae and its consequences for population growth. Ecol. Entomol., 6: 441--447. Wiktelius, S., 1984. Studies on population development on the primary host and spring migration of Rhopalosiphum padi (L.) (Horn., Aphididae). Z. Angew. Entomol., 87: 217--222. Wiktelius, S. and Chiverton, P.A., 1985. Ovariole number and fecundity for the two emigrating generations of the bird cherry--oat aphid (Rhopalosiphum padi) in Sweden. Ecol. Entomol., 10: 349--355. Wiktelius, S. and Ekbom, B., 1985. Aphids in spring sown cereals in central Sweden: abundance and distribution 1980--1983. Z. Angew. Entomol., 100: 8--16. Wit, C.T. de and Goudriaan, J., 1978. Simulation of Ecological Processes. Pudoc, Wageningen, 103 pp. Zadoks, J.C., Chang, T.T. and Konzak, D.F., 1974. A decimal code for the growth stages of cereals.Weed Res., 14: 415--421.