THE SURVIVAL OF APHIDS DÜRING A SEVERE
WINTER
G . D . HEATHCOTE
It is generally recognised that a severe winter is of some benefit to the gardener and the farmer in that it decreases the attack from pests and diseases in the following spring. Clearly some aphids and other pests do survive, even the most severe winters we experience in Suffolk (and the winter of 1984/85 was undoubtedly a severe one) but the whole question of winter survival of animals and plants is a complex one. For many years part of my job was to forecast the severity of the forthcoming attack of 'virus yellows' (a disease caused by a complex of viruses, all carried by aphids) in the sugar-beet crop from a study of the winter weather. The most important weather factor taken into consideration in the south of England was the number of frosts (when the grass minimum temperature feil below -0-3°C) from January to March (Watson, et a/., 1975), the greater the number of frosts the smaller the risk of a bad attack of yellows. A forecast had to be made as early in the season as possible, to help the farmer who had to decide whether to apply granules of insecticide with the sugar-beet seed in the furrow at sowing to give the emerging plants some protection from 'greenfly'. (Let me claim that my forecast was more often right than wrong.) The severity of the winter judged by the number of frosts, proved more useful than the average winter temperature or any of several other statistics which could have been used. When aphids become frozen they die, and a severe winter kills many of the aphids which would otherwise survive in mangold clamps, on weeds, or on crops such as brassicas in the field. It also kills many of the weeds and other plants infected with the disease. Therefore, both the number of sources of the disease and of the potential carriers are decreased. The aphid particularly involved in the study was the peach-potato aphid, Myzuspersicae (Sulz.), which has a large host ränge, including such common weeds as chickweed (Stellaria media (L.) Vill.), groundsel (Senecio vulgaris L.), shepherd's purse (Capsella bursa-pastoris (L.) Medic.) and small nettle (Urtica urens L.), some of which can also carry the viruses causing yellows of sugar beet. Under suitable conditions aphids can survive short exposure to very low temperatures. Their survival depends upon many factors, including the temperature at which they were reared, the degree of acclimatisation, the length of the cold period, whether they were wet ordry, the age of the aphid, the cold-hardiness of the host plant and the position of the aphid of the plant. When they are cooled rapidly they suffer from 'thermal shock' and die, but they can be acclimatised and become 'supercooled' (i.e. no ice crystals form in their body fluids at temperatures much below the freezing point of water) with a lower limit of about - 2 0 ° C (Parry, 1978). They are most likely to survive if reared at a low temperature. Such individuals are often darker than normal. The mean supercooling temperature of M. persicae is lowered by
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T H E SURVIVAL OF A P H I D S DÜRING A SEVERE WINTER
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0-125 for every 1°C decrease in the rearing temperature (Solomon, 1967). The supercooling point is relatively high if the aphid is wet at the beginning of the cold period because it suffers from exogenous freezing - ice crystals forming in the body fluids due to inoculation by outside contact with ice, in addition to endogenous freezing. Düring a cold period an aphid is prevented from feeding and starves, and while the maximum temperature is below about 6°C the aphid remains in a 'chill coma'. Starvation reduces the supercooling ability of aphids, but newly-born young of M. persicae which have not fed can be supercooled to exceptionally low temperatures, even below — 20°C (Parry, 1978). The nature of the food supply and the cold-hardiness of the host plant strongly influences an aphid's ability to survive. At —2°C about 50% of M. persicae survive on potato plants, but 85% survive on brassicas (Adams, 1962). Potato 'groundkeepers' (tubers left in the ground after harvest) are likely to be killed if the mean temperature is below 2°C in any month (Croxall & Smith, 1976), but it requires long exposure to temperatures below 9°C to kill groundsel plants (Salisbury, 1961). Even differences in the sap of different parts of plants may affect an aphid's survival. Parry (1978) found that small nymphs (young) of M. persicae feeding on subsidiary leaf veins could survive lower temperatures than larger individuals feeding on the main vein. Some individuals are able to survive the lowest temperatures they are likely to experience in England. Adams (1962) found that about 1% of M. persicae could survive at - 1 2 ° C for 48 hr., and one survived 96 days at —2°C. An aphid on a herbaceous plant in winter will be at the 'grass temperature' (approximately 2-3° lower than the 'Stevenson screen' temperatures recorded by meteorological stations and given as 'air temperatures'). However, when there is snow cover temperatures are taken above the snow and 'grass temperatures' may be considerably lower than the actual temperature on the lower leaf surface of plants under the snow. I have found aphids on plants under snow which appeared to be dead, but which began to twitch after about 30 min. at room temperature and eventually recovered completely. Some aphids are better able to face the winter than others. For example, Bevan and Carter (1980) found that the green spruce aphid, Elatobium abietinum (Walker), a common aphid in Suffolk, was well able to feed and breed on spruce during the trees' period of winter dormancy and survive frost. The scanning electron microscope showed that this aphid has a coating of curly filaments of wax on the body which is totally absent on less 'frost proofed' aphids such as the vetch aphid, Megoura viviae (Bückt.). This wax probably functions as an anti-wetting layer, holding off frost crystals from the aphid's body and preventing or delaying fatal inoculative freezing. Relatively few species of aphids survive in the active S t a t e on plants during the winter in Suffolk, but they do so as eggs, which are extremely cold-hardy. For example, the very common black bean aphid, Aphis fabae Scop. overwinters almost exclusively as eggs on spindle,Euonymus europaeus L. These eggs contain a number of Compounds which act as 'antifreeze', the best
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Suffolk
Natural History,
Vol. 21
known of which is p r o b a b l y glycol. T h e s e act as solvents, keeping potentially harmful salts in Solution during ice formation. S o m e a p h i d eggs will remain viable through t h e coldest winters we e x p e r i e n c e , but s o m e aphids survive without producing eggs in Suffolk. T h e c o m m o n e s t aphid f o u n d on weeds r o u n d t h e arable fields of t h e a r e a is the shallot a p h i d , Myzus ascalonicus D o n c . ( H e a t h c o t e & B y f o r d , 1975), and this species d o e s not p r o d u c e eggs - in fact males a r e u n k n o w n and all r e p r o d u c t i o n is p a r t h e n o g e n e t i c . It is t r u e that a severe winter decreases the attack of aphids in t h e following spring, b u t a few always survive and these can r e p r o d u c e so rapidly (a Single f e m a l e m a y p r o d u c e 3 0 - 4 0 young, without mating, during 2 or 3 w e e k s ) that we can n e v e r expect to be entirely f r e e f r o m the pest species. References A d a m s , J. B. (1962). A p h i d survival at low t e m p e r a t u r e s . Canad. J. Zool., 40,951. B e v a n , D . & C a r t e r , C. I. (1980). Frost p r o o f e d aphids. Antenna, 4, 6. Croxall, H . G . & Smith, L. P. (1976). T h e epidemiology of p o t a t o blight in the E a s t Midlands 1923-74. Ann. appl. Biol., 82, 451. H e a t h c o t e , G . D . & B y f o r d , W . J. (1975). Surveys of sugar-beet s e e d c r o p s , m a n g o l d clamps and w e e d s in E n g l a n d for aphids and viruses, 1963-73. J. agric. Sei. Camb., 84, 87. Parry, W . H . (1978). Supercooling of Myzus persicae in relation to gut c o n t e n t . Ann. appl. Biol., 90, 27. Salisbury, Sir E d w a r d (1964). Weeds and aliens. Collins, L o n d o n . S o l o m o n , M . G . (1967). Supercooling point of t h e aphid Myzus persicae Sulzer. M. Sc. Thesis, Univ. London. W a t s o n , M . A . , H e a t h c o t e , G . D . , L a u c k n e r , F. B. & Sowray, P. A . (1975). T h e use of w e a t h e r d a t a and c o u n t s of aphids in the field to predict t h e incidence of yellowing viruses of sugar beet crops in E n g l a n d in relation to the use of insecticides. Ann. appl. Biol., 81, 181. D r G . D. Heathcote, 2, St M a r y ' s S q u a r e , Bury St E d m u n d s
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