Developmental patterns in wheat and resistance to cereal aphids

CROP PROTECTION (1985) 4 (3), 322-328

Developmental patterns in wheat and resistance to cereal aphids T. M. ACREMAN* and A. F. G. D I X O N

School of Biological Sciences, University of East Anglia, Norwich, NRd 7TJ, UK Abstract. As wheat develops it varies in its suitability for the grain aphid, Sitobion avenae, so the duration of each developmental stage determines aphid population growth. Simulations of aphid population development on spring and winter wheat cultivars revealed that, as the length of the preferred earing phase was found to be relatively constant, peak population size is determined by the number of aphids at ear emergence. This can be reduced by growing early-maturing varieties, which in terms of crop developmental stage effectively delays the start of the spring migration. Breeding wheat that matures as early as winter barley would greatly reduce the number of aphid outbreaks and make the prophylactic spraying of insecticides unnecessary.

Introduction Susceptibility of plants to insect-pest attack is often dependent on the developmental stage of the plant. Spring oats are poorer hosts for frit fly (Oscinella frit (L.)) after the four-leaf stage (Vickerman, 1978), young wheat plants are more resistant than older plants to the rose-grain aphid (Metopolophium dirhodum (Walker)) (Argandona, Luza, Niemeyer and Corcuera, 1980) and the fecundity and developmental time of the bird cherry-oat aphid (Rhopalosiphum padi (L.)) varies with the developmental stage of oats, barley and wheat (Leather and Dixon, 1981). However, the importance of the relative duration of the various developmental stages for the population growth of aphids is unknown. Sitobion avenae (Fabricius), the grain aphid, is a sporadic but important pest of wheat in Europe (Vickerman and Wratten, 1979; Carter, McLean, Watt and Dixon, 1980). It may reach high numbers on the ears and reduce yield by up to 42~o (Kolbe, 1969; George and Gair, 1979). The suitability of wheat for S. avenae also changes with plant developmental stage (Vereijken,1979; Watt, 1979) and this may explain some of the differences between laboratory- and field-based resistance rankings of wheat cultivars (Markkula and Roukka, 1972; Dean, 1973). However, there has been no attempt to manipulate the duration of the different developmental stages to improve host-plant resistance. *Present address: MAFF, Woodthorne, Wolverhampton, WV6 8TQ~ UK 0261-2194/85/03/322~)7503.00 © 1985 Butterworth & Co (Publishers) Ltd

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By using a simulation model of the population development of S. avenae on wheat (Carter, Dixon and Rabbinge, 1982) together with observations on the developmental patterns in wheat, this study assesses the potential for reducing aphid infestations through growing early-maturing cultivars. This is proposed as a possible alternative control strategy to the widespread and often prophylactic use of insecticides. Materials and methods Description o f the model

A full description of the model is given by Carter, Dixon and Rabbinge (1982). It describes the population development of S. avenae on wheat and includes aphid mortality due to the action of coccinellids, parasites and disease. Aphid immigration is estimated from the number of alates in suction trap catches. Aphid developmental, survival and reproductive rates derived from the literature are incorporated into the model and, together with estimates of adult longevity and the proportion of alatiform nymphs, are used to update aphid numbers on the crop. Aphid reproduction, survival and longevity are affected by crop developmental stage which is modelled using a polynomial equation. Developmental patterns in wheat

Two cultivars (Sandown and Newmarket) and 10 potential cultivars (1022/6, 320/30, 706/19, 1199/298, YY5/64, 1022/28, 1168/98, 896/12, 335/1 and 708/41)of spring wheat selected from the Plant Breeding Institute wheat stocks were sown in one-metre rows in three replicated blocks on 29 March, 1982. The developmental stages (Zadoks, Chang and Konzak, 1974) of 10 tillers of each variety were recorded at least weekly, until ripe. From these results and the associated accumulated day degrees > 6°C (the physiological threshold for wheat development, after Carter et al., 1982) polynomial equations were calculated for the relationship between day degrees and plant development for the two spring wheats with the most contrasting developmental patterns. These relationships were compared with that for winter wheat calculated from developmental data collected from three winter wheat fields in 1977 and day degrees > 6°C accumulated from the beginning of May by Carter et al. (1982). Simulations

The relationships between developmental stage and day degrees for spring wheat were used in the simulation model of the population growth of Sitobion avenae on winter wheat (Carter et al., 1982) together with the meteorological and aphidimmigration data and the numbers of natural enemies for Norfolk in the years 1976-81 to determine the influence of crop developmental pattern on peak aphid density. This was repeated using the relationship for a winter wheat that developed 1 week in advance of the earliest spring wheat and for a hypothetical early-maturing winter wheat that developed 3 weeks in advance of the earliest spring wheat, It was assumed that no aphids overwintered on the crop. Over the period 1976-81 the immigration of aphids into the crop each year

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Wheat development and cereal aphid resistance

varied in size, timing and duration, and predators and parasites also varied in abundance. This provided a good test of the relationship between crop developmental pattern and the peak number of aphids. Results

Developmental patterns in wheat There was no difference between the 12 spring wheat cultivars in the timetaken from sowing to ripening (developmental stage 90). There were, however, differences in the timing of intermediate developmental stages, for example, of 1 week from sowing to the completion of ear emergence (d.s. 59), and of 2 days from ear emergence to milky ripe (d.s. 73). Figure 1 shows the relationship between C

g t~ O c

50-

25"

o

0

200

400

6 0

Doy degrees ::=.6°C

FIGURE 1. Developmental patterns from 1 May for (A) YY5/64 (late spring, d.s.=0.141TOT-0-000038(TOT)2+6.68, n=16, r2=0"99); (B) Sandown (early spring, d.s. =0"174TOT-0"000082(TOT) 2 +5.42, n=16, r~ =0"99); and (C) winter wheat (after Carter, Dixon and Rabbinge, 1982, d.s. ----0.173TOT--0.000125 (TOT) 2 +26.34, n =48, r~ =0"97) where d.s. is developmental stage and TOT is the day degrees > 6°C accumulated from the beginning of May. developmental stage and cumulative day degrees > 6°C for winter wheat and for the two spring wheats with the earliest and latest ear emergence. The polynomial equations fit the observed developmental patterns very closely.

The effect of developmental patterns in wheat on population growth of S. avenae Using the relationships for crop development illustrated in Figure 1, a range of peak aphid densities were predicted for the six years 1976-81 (Table 1). For the

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TABLE 1. Predicted peak S . avenae densities (aphids/tiller) on early- to late-earing cultivars of wheat for the years 1976 81 Timing of earing for: Winter wheat

Year 1976 1977 1978 1979 1980 1981

Spring wheat

Early (s) Peak Date

Typical (s +2wk) Peak Date

Early (s + 3wk) Peak Date

Late (s +4wk) Peak Date

20"2 13"1 0"5 0"1 11"7 9"0

60"0 36"9 7.2 1-4 52"1 27-6

80.3 76.7 14.9 1.7 110.8 56.9

99"3 100.5 16"5 1"4 126'6 82"0

26~6 11/7 1017 1717 4/7 25/6

24/6 14/7 26.t7 22,'7 5/7 20/6

26/6 13t7 27 I7 22/7 5 t7 28t6

2716 13 f7 26/7 21 f7 6/7 2/7

spring wheats the largest populations were predicted for the late-earing line and the smallest for the early-earing line. Compared with the late-earing spring wheat, up to 66% fewer aphids were predicted for the 'typical' winter wheat, which ears 2 weeks earlier, and up to 97% fewer for the early-maturing winter wheat, which ears 4 weeks earlier. Discussion The crop developmental pattern has important consequences for aphid population growth, even on plants that are sown and ripen on the same dates (Table 1). The earlier the time of earing, the lower are the predicted aphid populations that result. For winter wheat, the time in spring is often too short to allow appreciable aphid population build-up before earing. Although aphid reproduction is highest on the ear from d.s. 59 to 73 (Watt, 1979) and the duration of this phase is slightly longer in winter wheat than in spring wheat, this is insufficient to compensate for the earlier earing, resulting in smaller aphid populations on winter wheat. As the length of the earing phase was found to be relatively constant it is, therefore, the population level at ear emergence that determines the peak number of aphids. The start of the immigration of S . a v e n a e into cereals is not dependent on the crop developmental stage but on winter weather (Waiters, 1982). Hence the effect of growing early-maturing wheat is equivalent to delaying this immigration, the timing of which is an important factor in determining the likelihood of an aphid outbreak (Waiters and Carter, 1981; Waiters, Watson and Dixon, 1983). Therefore the use of cultivars that ear early, especially winter cultivars, should be encouraged. Flowering of cereals grown in temperate regions is mainly dependent on daylength in the spring (Gill and Vear, 1980) so early maturity of winter and spring wheats is not closely linked to their respective sowing dates. Therefore further reductions in aphid infestations through early maturity will be achieved only by breeding earlier-earing cultivars, the potential of which is shown by the low aphid numbers on the hypothetical early-maturing winter wheat. If

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Wheat development and cereal aphid resistance

populations of five or more aphids/ear and rising at d.s. 60/61, which is equivalent to about 17 aphids/ear at peak (George and Gair, 1979), constitutes an outbreak, then the predicted number of outbreaks from 1976 to 1981 would have been reduced from four to one had such early-maturing winter wheat been sown. In reality, although an outbreak did not materialize in 1981, possibly because of heavy rainfall during the colonization of the crop (Watson and Carter, 1983; S. J. Watson and A. F. G. Dixon, unpublished work), the outbreaks of 1977 and 1980 would have been prevented. Such a reduction in outbreak frequency would make prophylactic spraying of insecticide very uneconomic. Watt (1983) suggested that, with an outbreak probability of 0.2 or less, prophylaxis should not be considered. These conclusions depend on the assumption that varying the timing of the developmental stages does not directly change the expression of other parameters in the system in a way which could cancel out the effects of early earing. For example, an interaction between late maturity and predation could, in some circumstances, result in later cuhivars supporting fewer aphids. In addition, overwintering of aphids within the crop may result in winter wheat supporting more aphids than spring wheat. This may explain the conflicting results of Lowe (1984) who found more aphids on early-earing wheat lines in 1980. Significantly, however, winter barley (the maturity of which is equivalent to that of the early winter wheat used in the simulations) supports fewer S. avenae than wheat in the field (Kolbe, 1970; Dean and Luuring, 1970) and this cannot be attributed entirely to its poorer performanceon barley (Watson and Dixon, 1984). Jones (1979) found more aphids on barley than on wheat when she compared winter wheat with spring barley, which mature at similar times. Di Pietro and Dedryver (1984) cited wheat cv. Maris Huntsman as more susceptible in the field than in the laboratory, because of its late-ripening character, and Ba-Angood and Stewart (1980) found that early-maturing wheat and barley escaped damage by cereal aphids. Carter et al. (1982) demonstrated the consequences of early earing in a parallel way by showing that increased ambient temperature speeds up crop development more than aphid growth, thus leading to smaller aphid infestations. The use of early-maturing cultivars has also been effective in reducing the pest infestations of other crops. In Texas, short-season cotton can be used to avoid infestations of boll weevil and cotto n fleahopper (Walker and Niles, 1971) and many high-yielding, early-maturing rice varieties have been developed to combat stem borers and leafhoppers (Russell, 1978). In conclusion, these results indicate that 'ontogenetic resistance' may be important and it merits further study, especially under field conditions. Together with the partial resistance recorded for wheat (Lee, 1980; Lowe, 1980, 1981; Kay, Wratten and Stokes, 1981; Sotherton and van Emden, 1982; Lowe and Acreman, 1984) it might be useful in suppressing the incidence of aphid outbreaks on cereals. It could also be an especially durable resistance (Johnson, 1978), as to overcome it the aphid would have to evolve lower temperature thresholds or faster developmental rates, which are constrained by other selection pressures.

Acknowledgements We would like to thank members of the aphid group at UEA, the PBI for supplying seed and Dr H. J. B. Lowe for helpful criticism of the manuscript. T. M. Acreman is indebted to the SERC for financial support.

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