Maintenance Of The Phenology Of The Winter Moth

Transcript

Biological Journal of the Linnean Society (1985), 25: 221-234. With 1 figure Maintenance of the phenology of the winter moth (Lepidoptera: Geometridae) N . J. HOLLIDAY Department of Entomology, University of Manitoba, Winnipeg, Manitoba R3T 2N2, Canada ,hepled for publication September I984 Adult winter moths (Operophtera brumata (L.)) are active in late autumn or early winter. The eggs overwinter in the canopy of trees and hatch simultaneously with the bursting of host tree buds. Many young larvae disperse on the wind on silk strands. Larvae are polyphagus and feed until late spring when they pupate in soil or leaf litter. The duration of the egg and pupal stages is genetically determined and varies with latitude. The egg stage is long in the north and short in the south, while the pupal stage is short in the north and long in the south. The literature on the ecology and physiology ofwinter moth is reviewed. The factors maintaining the unusual phenology are discussed. It is concluded that the larval stage is early because mature leaves of many host trees are unsuitable as food, because parasitism against later larvae is more intense, and because summer temperatures may be injurious to larvae. The adult period is late in the year so that the final stages of pupal development occur in cool conditions and so that adults emerge after most insect predators have ceased activity. Throughout most of the range retarding the adult emergence period would cause activity to be impeded by severe winter weather; in the south this is not so and i t is suggested that eggs must be on the trees for a minimum period to ensure synchronization of egg hatch with bud burst. The protracted adult emergence period may be an adaptation reducing predation by birds. KEY WORDS:-Operophtera brumata - winter moth - phenology - selection CONTENTS Introduction . . . . . . . . Literature review . . . . . . . General biology . . . . . . Phenology . . . . . . . The effect of temperature . . . . Population biology . . . . . Discussion . . . . . . . . . Phenology of the larval stage . . . Phenology of the adult stage . . . Duration of the adult emergence period Conrlusions . . . . . . . . Acknowledgements . . . . . . References. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 22 I 222 222 222 223 225 228 228 229 23 I 232 233 233 INTRODUCTION The ecology of the winter moth (Operophtera brumata (L.)) has received more attention than that of most other insects. The population dynamics of the winter 0024-4066/85/07022 1 + 14 $03.00/0 22 1 0 1985 The Linnean Society of London Downloaded from https://academic.oup.com/biolinnean/article-abstract/25/3/221/2670667/Maintenance-of-the-phenology-of-the-winter-moth by guest on 21 October 2017 222 N. J. HOLLIDAY moth have been studied in several localities and on a number of host trees (Embree, 1965; Varley, Gradwell & Hassel, 1973; Holliday, 1975, 1977; Dale, 1980). The effects of temperature upon the insect and upon its phenology have also received considerable study (e.g. Kozhanchikov, 1950; Wylie, 1960a; Bonnemaison, 197 1 ; Holliday, 1983). Factors already identified as affecting the phenology of winter moth larvae include the increasing levels of host plant defences as leaves develop (Feeny, 1970; Wint, 1983). Dierl & Reichholf (1977) proposed that the phenology of the adult stage is an adaptation to avoid predation by vertebrates. However, the literature dealing with winter moth phenology does not integrate information from population ecology with data from physiological studies. This paper reviews both physiological and ecological factors affecting the phenology of the winter moth, and discusses alternative hypotheses on the maintenance of that phenology. A future paper will discuss how the phenology and other unusual characters of winter moth may have evolved. LITERATURE REVIEW General biology A detailed description of the life cycle of the winter moth was given by Varley et al. (1973). Adults emerge from pupation in autumn or winter. They are nocturnal; males are weak fliers and the females are brachypterous and incapable of flight. Females climb trees and mating usually occurs during the climb. Females lay an average of about 150 eggs in bark crevices on twigs in the tree canopy. Eggs hatch in spring and newly hatched larvae may disperse by spinning silk strands and drifting on the wind. Larvae feed on the leaves of deciduous trees and, after passing through five instars, descend to pupate in an earthen cocoon in leaf litter or the upper layers of soil. There is one generation each year. Winter moth inhabits the deciduous forest biome where i t feeds on over 100 species of deciduous trees and shrubs (Tenow, 1972). It is found in most of Europe and in parts of western and eastern Asia (Kozhanchikov, 1950). It was introduced to N America and is now spreading on both east and west coasts (Embree, 1966; Gillespie, Finlayson, Tonks & Ross, 1978). Phenology Most winter moth eggs hatch during a period of about 3 weeks (Briggs, 1957; Cuming, 1961) at the time of opening of the leaf buds of deciduous trees (Wylie, 1960a). Because of seasonal differences, eggs hatch in mid-May in Norway (Edland, 1971), in late March or early April in southern Britain (Briggs, 1957; Holliday, 1977) and northern France (Bonnemaison, 1971); and in early March in southern Italy (Silvestri, 1941). In all of these localities the duration of the larval feeding period is about 6 weeks, but in the more continental climate of the Ukraine eggs hatch in early May and pupation is no more than 1 month later (Moravskaya, 1960). Adults emerge in September in Finland; in September and October in the Leningrad area; in October and November in the Ukraine; from November to Downloaded from https://academic.oup.com/biolinnean/article-abstract/25/3/221/2670667/Maintenance-of-the-phenology-of-the-winter-moth by guest on 21 October 2017 223 WINTER MOTH PHENOLOGY Months J F M A M J J A S O N D 10 - 50- A I I 0 c r" 20- c 15 - C 1 I Figure 1. Typical phenology of winter moth and average monthly temperature for three localities: A, Leningrad (60"N);B, S England (51"N);C, Italy (41"N).Bars indicate time when each stage is present (filled bars, eggs; vertical shading, larvae; open bars, pupae; diagonal shading, adults). Sources of phenological data are given in the text, temperatures are from Thran & Broekhuizen (1965). February in Transcaucasia; and in February in Cyprus (reviewed in Kozhanchikov, 1950). Emergence of adults is mainly during November and December in Britain (Varley et al., 1973) and near Paris (Bonnemaison, 1971). In the Alps adults emerge earlier at high altitudes than in adjacent lower areas (Schneider-Orelli, 1916). The period during which adults emerge is usually at least 2 months long. Females live about 12 days (Moravskaya, 1960) but lay most of their eggs within 2 or 3 days of emergence (Briggs, 1957). The duration of the larval feeding period and of the adult stage is relatively constant throughout the range but the length of the egg and pupal stages is extremely variable (Fig. 1). In the northern parts of the range the pupal stage is short and the egg stage is long, while in the southern part of the range the pupal stage is long and the egg stage is short. The efeect of temperature Larvae The upper and lower limits for development of larvae are 28 and 3.5"C, respectively; caterpillars are increasingly susceptible to starvation as the temperature increases above 20°C (Kozhanchikov, 1950). The effect of temperature on the duration of larval development near Leningrad (Kozhanchikov, 1950) is similar to that near Paris (Grison & Silvestre de Sacy, 1948; Bonnemaison, 1971). At 10°C larval development takes between 40 and 50 days, and at 20°C about 17 days. Downloaded from https://academic.oup.com/biolinnean/article-abstract/25/3/221/2670667/Maintenance-of-the-phenology-of-the-winter-moth by guest on 21 October 2017 224 N. J. HOLLIDAY Pupae The upper and lower limits for pupal development are 25 and 4"C, respectively, but the optimal range for development is 10-15°C (Kozhanchikov, 1950). Towards the end of the pupal period pupae are less tolerant of temperatures above the optimal range (Wylie, 1960a; Holliday, 1983), and die if kept for long periods at or above 18.6"C (Kozhanchikov, 1950; Holliday, 1983). Kozhanchikov (1950) and Wylie (1960a) found a direct relationship between pupal duration and temperature. Kozhanchikov suggested that the delaying effect of high temperatures on adult emergence was sufficient to explain the differences in phenology at different latitudes. Conflicting results were obtained by Speyer (1938), Grison & Silvestre de Sacy (1948) and Bonnemaison (1971) who observed no effect of temperature on the duration of the pupal period. An explanation for this contradiction was offered by Holliday (1983) who found that the duration of the pupal period is increased at temperatures above the favourable range but below the upper lethal limit, but is independent of temperature at all temperatures within the favourable range. The extended pupal period found at temperatures above 15°C by Kozhanchikov (1950) and Wylie (1960a) seems to be a symptom of heat stress. Speyer (1938) and Wylie ( 1960a) reared pupae from different localities under identical temperatures and found that pupal duration is different for each locality. Speyer ( 1941) showed by breeding experiments that these differences are genetically determined. Adults During the adult emergence period, temperatures below 0°C reduce the number of females climbing trees (Briggs, 1957; Cuming, 1961; East, 1974). Emergence from pupation may be inhibited by cold, or adults may emerge normally and the females remain on the ground until warmer weather prevails. Heavy snowfalls also reduce catches of females on trees (Cuming, 1961). Adults can survive temperatures within the range - 15 to +27"C but the most favourable range for activity is between 4 and 12°C (Kozhanchikov, 1950). The minimum temperature for flight of the males is about 5°C (Alma, 1970) and the optimum temperatures for response to the sex attractant pheromone are between 7 and 15°C (Roelofs, Mill, Linn, Meinwald, Jain, Herbert & Smith, 1982). Flight is not essential for copulation, which has been observed at -0.8"C (Cuming, 1961). Females can oviposit at - 1.6"C (Cuming, 1961). Winter moth adults are most active at and shortly after dusk, which is usually within 2 4 h of the highest temperature of the day (Alma, 1970). Eggs The eggs of the winter moth are extremely cold-hardy: their average supercooling point is -31°C (Macphee, 1967). The upper limit for egg development is 26°C (Kozhanchikov, 1950). Moravskaya (1960) reported that eggs in the Ukraine go through an obligatory diapause, a result earlier found by Kozhanchikov ( 1950) for eggs from the Leningrad area. Kozhanchikov reported that there are three phases of embryonic development: a pre-diapause phase, a diapause which can only be broken by at least 2 months of temperatures below O"C, and a post-diapause phase in which development is continuous until Downloaded from https://academic.oup.com/biolinnean/article-abstract/25/3/221/2670667/Maintenance-of-the-phenology-of-the-winter-moth by guest on 21 October 2017 WINTER MOTH PHENOLOGY 225 eclosion. However, workers using eggs from Versailles (Gaumont, 1950; Wylie, 1960a; Bonnemaison, 1971), Czechoslovakia (Mrkva, 1968), Britain (Briggs, 1957), and northern Germany (Wylie, 1960a) found no diapause. Gaumont (1955) found three stages of development in eggs from Versailles. In the middle stage metabolic activity is reduced, the egg is very resistant to unfavourable conditions, and exposure to cold results in very slow development; however, the egg is not in diapause. Gaumont proposed that the winter moth exhibits different types of life cycle in different localities. He recognized a northern type which has an obligate diapause broken only by exposure to cold, and a southern type which has no diapause. Gaumont predicted that the northern type would be found in Scandinavia as well as in the U.S.S.R.; however, Wylie (1960a) showed that there is no obligate diapause in eggs from southern Sweden. In addition to the possibility of geographic variation in the presence or absence of embryonic diapause, winter moth eggs from different localities, when reared under identical conditions, hatch at different times (Speyer, 1938; Wylie, 1960a). Speyer (1941) and Wylie (1960a) crossed winter moths from different localities and showed that the duration of egg development under identical conditions is genetically determined. Within a locality there is variation in the duration of egg development so that families of eggs laid at different times hatch at about the same time (Briggs, 1957). In addition to these sources of variation, the duration of the egg stage is inversely related to temperature (e.g. Wylie, 1960a; Bonnemaison, 197 1). However, the different phases of development through which eggs pass have made it difficult to establish a developmental threshold. Embree (1970) found that the eclosion of eggs collected from the field in January could be predicted using temperature summations above 5°C. Population biology The population dynamics of winter moth have been studied on oak (Quercus spp.) near Oxford (Varley et al., 1973) and in Nova Scotia (Embree, 1965), on elm and oak in the Ukraine (Moravskaya, 1960), and on apple (Malus sylvestris Mill.) near Bristol (Holliday, 1975, 1977; Dale, 1980). Table 1 summarizes the major mortality factors identified in these studies; these factors are discussed in more detail below. Larvae The degree of synchronization of egg hatch with the bursting of buds of the host trees is extremely important to the survival of first instar winter moth larvae (Embree, 1965; Holliday, 1977). Eggs usually hatch in the morning (Embree, 1970), a time when there are often light winds and convection currents. These are favourable conditions for wind-borne larvae to reach suitable feeding sites (Embree, 1970). When a dispersing larva lands it may begin to feed, but if the landing site is unsuitable it will disperse again. Hence, though dispersal is random, selection of a food plant is not. As a result, foliage clusters open at the time of egg hatching have higher densities of feeding larvae than clusters which open later (Holliday, 1977), and larvae show active preference for some tree 10 Downloaded from https://academic.oup.com/biolinnean/article-abstract/25/3/221/2670667/Maintenance-of-the-phenology-of-the-winter-moth by guest on 21 October 2017 226 N. J. HOLLIDAY species (Wint, 1983). During the process of dispersal larvae d o not feed, but normally 2-3 days of starvation does not cause appreciable mortality nor affect the strength of host-plant preference (Wint, 1983). Despite these adaptations which reduce the hazards associated with hatching on an unsuitable host plant, mortality of first instar larvae before they commence feeding may reach 85"10 (Embree, 1965). Mortality of feeding larvae may result from environmental factors, predation or parasitism. Holliday (1977) found that there was no significant reduction in density of larvae on apple trees during the feeding period; parasitism in the study site never exceeded 1% (Holliday, 1975). Near Oxford, parasitism is usually less than 30% and is mainly caused by the tachinid flies, Cyeenis albicans (Fallen) and Lypha dubia (Fallen) (Cheng, 1969; Varley el al., 1973). Although 60 other parasitoids attack winter moth larvae (Wylie, 1960b), their impact on the population of the winter moth at Oxford is small (Varley et al., 1973). Winter moth larvae are an important item in the diet of nestling titmice (Parus spp.), nevertheless only 2-5% of the population of larvae is eaten (Betts, 1955). Great tit nestlings (P. major L.) are fed only the early instars of winter moth larvae: later in the spring other species of caterpillars are preferred (Royama, 1970). In contrast, blue tit nestlings (P.cueruleus L.) are fed on winter moth larvae as long as these are available in the canopy (Betts, 1955). In Nova Scotia, at the very high population densities prevalent before biological control, predation by birds and starvation following complete defoliation of trees killed up to 95% of large larvae (Embree, 1965). Feeny (1970) showed that as oak leaves (Q. robur L.) become more mature, they become less suitable as food for winter moth caterpillars. If the fourth and fifth instars are fed on mature leaves the resulting pupae are much lighter in weight than if they are fed on young leaves. A similar phenomenon occurs when larvae are fed on mature leaves of hazel (Corylus auellana L.), hawthorn (Crataegus monogyna Jacq.), blackthorn (Prunus spinosa L.), or apple ( M . sylvestris) (Wint, 1983). Since pupal weight and the fecundity of resulting females are correlated (Holliday, 1975), the reproductive capacity of larvae feeding on mature leaves is diminished. Near Oxford reproductive capacity is greatest in larvae which commence feeding on Q. robur at the time of its bud burst (Wint, 1983). Wint predicted that females from such larvae would produce over 30% more eggs than those from any other combination of date of eclosion and food plant which he tested. At Oxford, first instar larvae exhibit feeding preference for Q robur and the phenology of eclosion is synchronized with bud burst of this species. However, in many years the synchronization is imperfect and larvae are forced to disperse and feed on alternative hosts with a consequent reduction in their reproductive capacity (Wint, 1983). Pupae Holliday (1977) found that mortality of pupae in an apple orchard exceeded 88%; of this up to 72% could be attributed to predation by vertebrates and invertebrates (Holliday, 1975); similar figures were obtained by Moravskaya (1960) in the Ukraine. In oak woodland near Oxford, between 1950 and 1962, predation frequently accounted for 80% or more of the pupae and, of those that survived predation, an average of about 35% were parasitized by an ichneumon wasp, Cratichneumon culex (Mueller) (Varley et al., 1973). The estimate of pupal Downloaded from https://academic.oup.com/biolinnean/article-abstract/25/3/221/2670667/Maintenance-of-the-phenology-of-the-winter-moth by guest on 21 October 2017 WINTER MOTH PHENOLOGY 22 7 predation at Oxford includes mortality of larvae seeking pupation sites and of adult females before they ascend trees to oviposit. East (1974) estimated that in the Oxford site 14:/, of larvae die after descending from the tree but before pupation, and that 72% of pupae are eaten between June and November. The major predators are shrews, and carabid and staphylinid beetles. Adults East’s (1974) estimate of the mortality of female winter moth after emergence but before climbing trees was 23%. Many adults are taken by great tits which feed mainly on the ground; 70% of the moths eaten are female (Betts, 1955). Other potential predators of adults on the ground are shrews and the carabid beetle Nebria brevicollis Fabricius; the more voracious carabid and staphylinid beetles which attack pupae are not active this late in the year. Spiders are active both on the ground and on tree trunks at the time of adult emergence; for example Meta segmentata (Clerck) kills male moths on the trunks of trees (Holliday, 1975). There are no quantitative data on the mortality of male winter moths: the numbers of males on tree trunks greatly exceed the number of unmated females (Holliday, in prep,) so predation of males probably does not reduce subsequent egg numbers. When exposed to light, males rest on horizontal surfaces with the wings held horizontally; when placed in the dark males seek a vertical surface and rest with their wings perpendicular to that surface (Alma, 1970). Thus when the male rests on the ground during the day the cryptic upper surfaces of the wings are exposed. Presumably this is a defence against visually hunting predators such as birds. In England the major predator of female moths in the tree canopy is probably the blue tit (Betts, 1955). Betts estimated that titmice could eat up to 20% of the population of winter moth females, either on the ground or in the canopy. Females in the canopy spend the day motionless on twigs where they resemble buds in shape and size. This, and the rapidity with which the moths complete oviposition (Briggs, 1957), reduces the impact on the number of eggs laid of birds eating female moths. Holliday (1975) estimated that this predation reduced egg density by 12% in an apple orchard; Dale (1980), in the same orchard, obtained estimates as high as 33%. Predation of winter moth females by birds may not be as important in southern central Europe where titmice eat seeds in winter, and other insectivorous birds migrate (Dierl & Reichholf, 1977). Eggs In localities where the egg stage lasts 4 months (Holliday, 1975), 5 months (Embree, 1965) and 5.5 months (Mrkva, 1968), over 95% of eggs hatch if exposed in the field but protected from predators. Eggs are highly resistant to low humidity except at high temperatures unlikely to occur in the field (Kozhanchikov, 1950). There are no published estimates of egg mortality due to predation. Titmice are very active predators on insects on apple trees and, in captivity, will readily and repeatedly eat winter moth eggs (Holliday, 1975). However, winter moth eggs were never found in the gizzards of titmice taken from oak woodland in which winter moth were abundant (Betts, 1955). Eggs are seldom parasitized (Wylie, 1960b) and probably only small numbers are eaten by invertebrates (Holliday, 1975). Downloaded from https://academic.oup.com/biolinnean/article-abstract/25/3/221/2670667/Maintenance-of-the-phenology-of-the-winter-moth by guest on 21 October 2017 N. J. HOLLIDAY 228 DISCUSSION The rate of spread in eastern Canada (Embree, 1966) indicates that the winter moth is not a very vagile insect. In Europe this lack of movement has permitted the evolution of local, genetically determined variants with respect to the duration of the egg and pupal stages (Fig. 1). Thus the amount of mixing of genetic material among distant winter moth populations is probably small, and selective pressures favouring a particular phenological regime must be sought in the same locality as the regime is found. At this point a shortcoming in the literature becomes apparent: the ecological data and the physiological data have seldom been collected in the same locality. Therefore, in the discussion that follows it is often necessary to extrapolate between localities. Phenology of the larval stage Synchronization of egg hatch with bud burst is important to the population dynamics of winter moth in all localities (Table 1). If eggs hatch before bud burst, first instar larvae must disperse to avoid starvation; high mortality is associated with such dispersal, and larvae may starve anyway. Although larval polyphagy and resistance to starvation may reduce the risks of dispersal (Wint, 1983), the selective advantages of early eclosion must be considerable, since later eclosion would avoid these risks entirely. The increasing level of host-plant defences is a powerful selection pressure favouring early completion of feeding. The weight of pupae, and the corresponding reproductive capacity, is greater when larvae commence feeding Table 1. Summary of estimates of percentage apparent mortality for winter moth populations. Further details and sources of information are given in the text Stage of winter moth Mortality factor Range of percentage mortality Dispersal or starvation of first instars Parasitism by tachinid flies 6-85 0-30 Other parasitoids 0-15 Diseases Starvation of large larvae and predation by birds Predation of larvae seeking pupation sites 0-10 Pupae Parasitism by Cratichneumon culex Predation and other pupal mortality M 5 10-85 Adults Predation of females on the ground 23 Eggs Not oviposited Larvae Infertility Egg mortality in the canopy 2-95 Remarks Very important in all localities Important in most of Europe, and when introduced to N America, not important in orchards About 60 individually unimportant parasitoid species Only important in high-density populations 14 12-33 Important at Oxford, less so elsewhere Important in most localities. Predators are shrews, carabid and staphylinid beetles Includes loss due to predation of females on trees 1-5 8 Downloaded from https://academic.oup.com/biolinnean/article-abstract/25/3/221/2670667/Maintenance-of-the-phenology-of-the-winter-moth by guest on 21 October 2017 WINTER MOTH PHENOLOGY 229 early in the season (Feeny, 1970; Wint, 1983), and is maximum when the larvae begin feeding on oak at the time of its peak bud burst (Wint, 1983). Because of the much higher reproductive capacity of larvae which commence feeding on oak at its bud burst, and the preference larvae exhibit for foliage of Q. robur, Wint (1983) suggested that winter moth is an oak-feeding species, selected to synchronize with Q,! robur, and that other trees can be regarded as ‘a reserve food supply’. While this may be true in a predominantly oak woodland near Oxford, it is not so throughout the range of winter moth. Near Leningrad, willow (Salix fragilis L.) is the preferred host (Kozhanchikov, 1950), while in Fennoscandia birch (Betula spp.) and fruit trees are preferred (Tenow, 1972); in both these areas Q. robur occurs and is also fed upon by winter moth larvae. I suggest that, for each locality, the fittest phenology of egg hatch will be the average date of bud burst of all suitable host-tree species, weighted both by host abundance and by the reproductive capacity of larvae which feed on them. This would explain the variations in host-plant preference between Britain and Fennoscandia, but does the same effect result in much more local variations in phenology? There are no data for the winter moth, but in Alsophila pometaria (Harris), a parthenogenetic species with a similar life history, phenology varies between neighbouring pure stands of host trees of different species, but not between different species of trees within a mixed stand (Mitter, Futuyma, Schneider & Hare, 1979). In addition to host-plant defences, mortality factors which are more intense near the end of the feeding period would also tend to favour early pupation. If the upper lethal temperature and the preferred temperatures of the larvae found by Kozhanchikov (1950) apply throughout the range, then in the south, and in areas of continental climate, rapid completion of the feeding period may be necessary to avoid the high temperatures of late spring and summer. Natural enemies might also affect larval phenology. In England predators of larvae do not appear to exert a selection pressure favouring early pupation (Betts, 1955; Royama, 1970). Cyzenis albicans is widespread through much of Europe and parasitizes the later instars of winter moth larvae more than the earlier instars (Wylie, 1960b). In England in some years C. albicans is poorly synchronized with its host so that winter moth larvae which pupate early suffer a lower rate of parasitism than those which pupate later (Hassell, 1969). Lypha dubia also inflicts higher mortality upon winter moth larvae which develop slowly: parasitoids are killed if they fail to reach second instar before the host becomes a pre-pupa (Cheng, 1970). In England both these tachinid parasitoids exert selection pressure favouring early pupation, but this is not so throughout the range. In Canada, where it was introduced to control winter moth, C. albicans is well synchronized with its host (Embree & Sisojevic, 1965). No doubt the relative importance of host-plant defences, physiological limitations of the larva, and natural enemies, varies throughout the range of the winter moth. These selective forces will favour reduction of the duration of the larval stage to the extent that physiological constraints allow, and the development of a mechanism synchronizing eclosion with bud burst. Phenology of the adult stage Dierl & Reichholf (1977) suggested that brachyptery and the adoption of walking as the mode of locomotion allow females to be active at low Downloaded from https://academic.oup.com/biolinnean/article-abstract/25/3/221/2670667/Maintenance-of-the-phenology-of-the-winter-moth by guest on 21 October 2017 230 N. J. HOLLIDAY temperatures. Although male flight (Alma, 1970) and response to the sex pheromone (Roelofs et al., 1982) are inhibited by low temperatures, the behaviour patterns of males appear to enable mating to occur even when temperatures are below those needed for flight (Holliday, in prep.). For these reasons the range of phenological alternatives for winter moth is greater than for moths in which flight is an important element of reproductive behaviour. Although the phenology of larval feeding is tightly constrained, it is clear from the variation in the duration of the pupal and egg stages throughout the geographic range that there is potential for considerable flexibility in the timing of the adult stage. However, in each locality there is a characteristic length of the pupal period which results in adult emergence just before winter; this must indicate a selective advantage to this unusual timing of adult activity. Why is the adult stage not later? Except in the southern part of the range, the selective pressures against later adult emergence are presumably climatic in nature. Adult activity is inhibited by cold and by snow (Cuming, 1961)) and late emergence would increase the probability of such conditions impeding reproduction. I n the southern part of the range snow and prolonged cold are unusual except in mountainous areas. Perhaps synchronization of egg hatch with bud burst can occur only when the eggs are in the tree for some minimum period. The time of egg hatch is determined by thermal accumulations following a period of exposure to cold (Embree, 1970); in many species of trees the time of bud burst is determined in a similar way, although the process is more complex because of the interaction of factors such as photoperiod (Kozlowski, 1971). Synchronization is probably more reliable when winter moth is present as an egg in the tree canopy and experiencing a similar thermal regime to the buds, than would be the case if the moth were in the pupal stage in the soil during part of the post-dormancy bud development. Why is the adult stage not earlier? A number of hypotheses will be examined which fall into two categories. Firstly there are hypotheses concerned with selective advantages in having the egg stage short and the pupal stage long. A second type of hypothesis relates to mortalities affecting the adult stage directly. The first type of hypothesis concerns the length of the pupal stage relative to the egg stage. Perhaps increasing the duration of the egg stage would increase egg mortality, from dehydration or depletion of food reserves. However, the egg is very resistant to dehydration (Kozhanchikov, 1950). Over 95% of eggs hatched in all the studies, and survival was similar for durations of 4 and 5.5 months (Embree, 1965; Mrkva, 1968; Holliday, 1975), so if mortality does increase with increasing duration of the egg stage, it does so only when the egg stage lasts longer than 5.5 months. Egg mortality might also result from the activities of natural enemies. If the rate of loss per day of newly laid eggs was higher than the rate of loss per day of pupae at the end of the pupal period, then the number of eggs hatching per larva pupating would be decreased by an extension of the egg stage. Thus, high rates of predation or of parasitism of eggs might be the selection pressure favouring a late adult emergence period. However, there is little predation or parasitism of Downloaded from https://academic.oup.com/biolinnean/article-abstract/25/3/221/2670667/Maintenance-of-the-phenology-of-the-winter-moth by guest on 21 October 2017 WINTER MOTH PHENOLOGY 23 I eggs, and predators kill many pupae (Table 1). Some predators are active throughout the pupal period. Thus, there is no evidence to suggest that the impact of natural enemies would favour a shorter egg stage. The final hypothesis in this group concerns the effect on the pupa of shortening the pupal stage. This would expose the final stages of pupal development to higher temperatures which may cause stress or death (Kozhanchikov, 1950; Holliday, 1983). After hot summers the effects of temperature stress have been observed in the field (Paillot, 1934). Advancing the adult emergence period could expose pupae to high, injurious temperatures throughout much of the range of the winter moth: as far north as Leningrad the mean temperatures in July and August are sufficient to cause stress (Fig. 1). Hypotheses relating to adult mortality propose that the adult phenology is an adaptation to avoid predators. Both males and females are eaten by vertebrate and invertebrate predators; however, there are no quantitative data on the resulting mortality to males. Females on the ground are eaten by birds, small mammals and arthropods. The ground-feeding great tit eats many females and fewer males (Betts, 1955); other predators are shrews (Sorex araneus L.) (East, 1974), and spiders (Holliday, 1975). The most voracious surface-feeding insect predators cease activity shortly before the time of winter moth adult emergence (East, 1974; Holliday, 1975). If adults emerged earlier in the season they would no doubt be eaten by these insects, and this may be a selection pressure favouring late emergence. The major predators of female winter moths in the tree canopy are probably birds. Dierl & Reichholf (1977) suggest that at the time of adult emergence the risk of being eaten by birds is reduced: most insectivorous birds have migrated, and the resident titmice have switched to a granivorous diet. They suggest that avoidance of predation by birds is the main reason for the observed phenology of adult emergence. In England however, predation of females in trees by birds reduces egg numbers by 12 to 33% (Table 1). Both males and females exhibit adaptations which may make them less vulnerable to visually hunting predators, and this further supports the hypothesis that predation by birds is important at the time of adult emergence. Duration of the adult emergence period The period of egg hatch lasts less than 1 month but the adult emergence period extends over 2 months (Fig. 1 ) . This long period may be because the selection pressures acting to maintain adult phenology are not as intense as those maintaining the phenology of egg hatch. Alternatively, the prolonged adult emergence period may be another adaptation to reduce the impact of predation by birds. Titmice searching trees for insects in winter can inflict densitydependent mortality upon their prey (Gibb, 1958; Solomon & Glen, 1979). Solomon & Glen found that high densities of codling moth larvae are rapidly reduced by titmice, but that the resulting low-density population suffers a much-reduced rate of predation. If the emergence period of winter moth were short, high densities of moths would be present on the ground and in trees; these would probably suffer intense predation by birds. The prolonged emergence period results in low densities of moths a t any one time and consequently a lower rate of predation. Downloaded from https://academic.oup.com/biolinnean/article-abstract/25/3/221/2670667/Maintenance-of-the-phenology-of-the-winter-moth by guest on 21 October 2017 N. J. HOLLIDAY 232 CONCLUSIONS Throughout the range of the winter moth, larval eclosion is synchronized with bud burst of deciduous trees and adult activity occurs in cool conditions. Consequently, the duration of both the egg and the pupal stages varies considerably throughout the range. Both egg and pupal duration are genetically determined and characteristic for each locality (Speyer, 1941; Wylie, 1960a). The proposed reasons for maintenance of winter moth phenology are summarized in Table 2. The phenology of the larval stage is maintained as early as possible by the increase in intensity of host-plant defences described by Feeny (1970) and Wint ( 1983). Additional selection pressures for early completion of the larval stage are tachinid parasitoids, which attack the latest larvae most intensively, and the sensitivity of larvae to the high temperatures of summer. The most widespread factors maintaining the phenology of the adult emergence period are climatic: adult activity must be completed before severe weather sets in, but the final part of the pupal period must occur when it is cool. In the southern part of the range severe winter weather may not be an important factor preventing retardation of adult emergence; however, synchronization of egg hatch with bud burst may require a minimum period of egg development in the same microclimate as the buds. An additional factor favouring late adult emergence is the avoidance of voracious predatory beetles which cease activity in early autumn; however, the range over which this phenomenon operates is unknown. The avoidance of predation by birds was suggested by Dierl & Reichholf (1977) as the most important factor favouring the late activity period of adult winter moth. I do not believe that this is generally applicable, for birds do inflict Table 2. Summary of selection pressures thought to be responsible for maintaining winter moth phenology. Factors which do not act throughout the range are enclosed in brackets Potential change i n phenology Selection pressure favouring change Selection pressure opposing change E d i e r cgg hatrh Greater reproductive capacity through longer feeding period Risk of hatching before buds burst Earlier pupation Increasing host plant defences [Increasing parasitism of larvae] [Temperatures rising to upper lethal limit of larvae] Reduced reproductive capacity because of reduction in length of feeding period Edrlirr adult rmrrgence [Risk of severe winter weather] [Better synchronism of egg hatch with bud burst] Heat stress to later pupal stages [Increased predation of adults by insects] Longer pre-reproductive period in adult None Predation of adults before reproduction complete [Risk of severe winter weather] Prolongation of adult emergence season [Density-dependent predation of adults by birds] Factors listed under 'Earlier adult emergence' Downloaded from https://academic.oup.com/biolinnean/article-abstract/25/3/221/2670667/Maintenance-of-the-phenology-of-the-winter-moth by guest on 21 October 2017 WINTER M O T H PHENOLOGY 233 mortality on adult moths, and moths exhibit adaptations which may tend to reduce this mortality. The prolonged period of emergence of winter moth adults may be such an adaptation. In autumn and winter titmice inflict densitydependent mortality on insects, and given the same total number of adults emerging, emergence over a long period with low densities at any one time would result in less predation than emergence over a short period with correspondingly higher densities. Whether or not eggs undergo a diapause in any part of the range is in doubt: those authors reporting a diapause may have been observing the period of quiescence seen by others. It is clear that an important function of any regulatory mechanism of egg development is to synchronize egg hatch with bud burst, and that such a mechanism must be able to compensate for the variability in the time of oviposition. ACKNOWLEDGEMENTS During the gestation period of this review many colleagues assisted by their discussions-and criticisms: special thanks go to M r M . E. Solomon, Dr D. M . Glen, Dr M. C. Singer, and Dr L. J. 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