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«Biology and Management of Woolly Apple Aphid S. D. Cockfield and E. H. Beers Washington State University, Tree Fruit Research and Extension Center, ...»

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Biology and Management of Woolly Apple Aphid

S. D. Cockfield and E. H. Beers

Washington State University, Tree Fruit Research and Extension Center,

1100 North Western Avenue, Wenatchee, WA, 98801

___________________________________

WOOLLY APPLE APHID, Eriosoma lanigerum (Hausmann), is native to eastern North

America, where it originally occurred on American elm, Ulmus americana L., hawthorn

Crataegus spp., and mountain ash, Sorbus spp. (Patch 1913). It has since adapted to apple, Malus × domestica (Borkhausen), after cultivated apple was introduced into North America, and has spread to other apple-growing regions of the world. It has been the subject of research in many countries, such as the United States, England, Holland, France, Israel, India, Japan, South Africa, New Zealand, and Australia. Research has centered on phenology, behavior, biological control, chemical control, and host plant resistance. The purpose of this paper is to review the major contributions to the literature on woolly apple aphid, especially as they pertain to management of the pest in Washington.

Life cycle Woolly apple aphid occurs on American elm as the primary host in eastern North America (Baker 1915). Overwintering eggs on elm hatch in the spring and produce stem mothers, or fundatrices, a morph found only on the primary host. Their feeding on elm produces a growth irregularity known as elm leaf rosette (Patch 1916). The nymphs have wax glands, much like the forms on the secondary host. Several generations are produced on elm parthenogenetically, which eventually give rise to the alate spring migrants. These alates disperse to a secondary host, e.g., apple or mountain ash. Multiple generations of apterous virginoparae are produced on the secondary host. These morphs are the familiar, purplish aphids which form numerous colonies on shoots, especially leaf axils, and wounds, characterized by covered by white, waxy filaments, giving rise the common name “woolly”. They are capable of reproducing indefinitely on apple and can overwinter on either roots or aerial portions of the tree. As colonies increase, alate virginoparae are produced, which migrate to another secondary host (apple) and produce additional apterous virginoparae. In the summer and fall, colonies on apple can produce alate sexuparae, which migrate back to the primary host. Sexuparae produce apterous males and oviparae (females), which lay overwintering eggs (Baker 1915). Males and oviparae are about the size of first instar virginoparae. The ovipara lays a single, dark brown egg, which fills her abdomen (Sandanayaka and Bus 2005).

Woolly apple aphid was apparently originally a holocyclic, heteroecious aphid species alternating between American elm and one or more secondary hosts (Crataegus or Sorbus).

Sometime after the introduction of the cultivated apple with European settlers in eastern North America, this species adapted to use apple as a secondary host. Since that time, this species has been introduced throughout the world where apple is grown, mostly in the absence of the primary host. Where the primary host was lacking, the spread of woolly apple aphid must perforce be dependent on adaptation to using apple as a host year round. Thus the species has transitioned from holocyclic/heteroecious to anholocyclic/monoecious. This is likely the case in most countries in which woolly apple aphid occurs. Even in eastern North America, the spread of the Dutch elm disease after WWII has made U. americana scarce in many regions; thus even in the region of origin, it is likely anholocyclic/monoecious. In some countries, these strains only produce alate or apterous virginoparae, i. e., completely lacking the alate sexuparae and sexuals.

In other areas of the world, some strains produce alate sexuparae which seek apple instead of elm, eventually producing overwintering eggs on apple (Sandanayaka and Bus 2005).

Injury

Woolly apple aphid can be a mere nuisance, a detriment to apple production, or a threat to the tree’s survival, depending on the level of infestation and where colonies are located. Many of the host’s tissues can be attacked, including shoots (bark), wounds, and roots. In severe infestations, colonies near spurs can deposit honeydew on fruit, which can in turn cause russetting and serve as a substrate for sooty mold. Historically, nursery trees and newly planted trees are at higher risk, and tree mortality can be substantial (Sherbakoff and McClintock 1935).

The insects can directly infest fruit by entering the core through the calyx (Essig 1942, Madsen et al. 1954). Cultivars with an open calyx are particularly susceptible. The presence of insects either in or on the fruit can present a problem for the phytosanitary protocols for import/export to some countries.

Woolly apple aphids feed from phloem tissue and reduce tree vigor by removing carbohydrates in transport from the leaves to growing cells (Madsen and Bailey 1958). Saliva injected into the host as the aphids feed causes additional damage to plant tissues. Shoots develop splits in reaction to feeding in as little as eight weeks (Weber and Brown 1988). Eventually stem galls form and enlarge where the aphids feed in leaf axils (Madsen and Bailey 1958). The wounds on the trunk and stems caused by aphid colonies or other factors serve as long-term feeding and overwintering sites, where they become infested with perennial canker. Continued feeding interferes with healing of wounds and prolongs and spreads the fungal infection (Childs 1929).





Heavy infestations of woolly apple aphid can lead to the death of planting stock (Sherbakoff and McClintock 1935) and even occasionally cause tree death or visible decline in mature trees (Klimstra and Rock 1985).

Edaphic colonies on apple roots cause damage to roots, and can eventually debilitate the entire tree. Root galls form around colonies in as little as four weeks, and can enlarge for years (Weber and Brown 1988). The galls grow by the proliferation of nonfunctional xylem tissue, which greatly reduces water conductivity of roots. Their rapid growth serves as a nitrogen sink in competition with shoots. Galled roots contain decreased stored carbohydrates compared with healthy roots (Brown et al. 1991). Thus, root infestations can decrease the growth rate of shoot tissue, and decrease trunk diameter in newly-planted trees (Brown and Schmitt 1990, Weber and Brown 1988). Even in mature trees, linear shoot elongation can be reduced. In years of high crop-load, the number and weight of fruit per tree can be reduced, leading to economic losses (Brown et al. 1995).

Phenology

Aerial populations of apterous virginoparae, in cold regions of Europe, Asia, and North America, vary throughout the season. Colonies often show a peak of population growth in July, followed by a decrease in August and September, a possible second peak in October, followed by a sharp decrease in winter (Lohrenz 1911, Evenhuis 1958, Bonnemaison 1965, Kozár et al. 1979, Walker 1985, Brown and Schmitt 1994). In warmer regions, aerial colonies can be present in small branches throughout the year with no discernable pattern, except for a population decline in winter or in summer (Hoyt and Madsen 1960, El-Haidari et al. 1978, Asante et al. 1993).

In cold climates such as Washington, aerial colonies decrease in winter as late-instar nymphs and adults are killed by low temperatures. First instars survive in bark crevasses, but in some severe winters, survival can be as low as 1% (Walker 1985). Development of first instars and recolonization of leaf axils can begin in early spring, because the aphid is adapted to cool weather. The developmental rate peaks at relatively low temperature, 26 C in Washington (Walker et al. 1988), and the estimated developmental threshold is 5.2 C (Asante et al. 1991).

Poor adaptation to heat explains much of the population decline usually seen in late summer (Walker 1985, Mols and Boers 2001).

Seasonal changes in aerial colonies are also influenced by movement of individuals. The production of alates, which leave aerial colonies, corresponds to a decrease in population growth (Walker 1985). Growth of aerial colonies in spring and summer is supplemented by alate virginoparae from elm only in eastern North America (Brown and Schmitt 1994). Unlike other aphid species on apple, apterous virginoparae of woolly apple aphid are mostly sessile, except for the first instar. First instars can move great distances on the host plant searching for a place to insert their stylets and begin feeding (Schoene and Underhill 1935). In all apple-growing regions, first instars from root colonies can crawl up the trunks and join existing shoot colonies or establish new ones. Some early observers noted a change in first instar movement in response to the seasons. Theobald (1922) noted that aphids moved up the trunks from root colonies in early spring and primarily down the limbs from aerial colonies in the fall, potentially forming larger or new root colonies. In California, movement up from root colonies began in May, peaked in July and August, and declined in September and October. A second peak occurred in December and January. Crawlers moving from the roots peaked just before aphid populations began to increase in aerial colonies. Movement down from aerial colonies peaked in August and September (Hoyt and Madsen 1960). First instar migration showed no seasonal trend in Washington (Walker 1985). There were two peak periods of both up and down movement: mid to late summer, and late September to November. Bodenheimer (1947) observed that root colonies in the Middle East could be established by infested fruit or twigs that dropped to the ground.

First instar woolly apple aphid move in a non-random manner when seeking new feeding locations. Although young usually settle next to established adult females, nymphs wander as the original colonies increase and become crowded. Nymphs in the field actively move away from heat and strong sunlight (Schoene and Underhill 1935), and are inhibited by temperatures below 10 C (Hoyt and Madsen 1960). Nymphs from a lab colony oriented movement towards cool to moderate temperatures in the range of 15-20 C. Most individuals were repelled by light and showed positive geotropism, a tendency to move down (Hoyt and Madsen 1960)). Thus, high temperatures may cause migration of first instars to the roots (Lohrenz 1911, Hoyt and Madsen 1960). However, nymphs collected from the field in the process of moving up the trunk moved towards light and showed a neutral geotropism (Hoyt and Madsen 1960).

Migration of first instars on the trunks of trees can be exploited in sampling programs. Sticky tape with a band of insect trapping medium placed around the trunks of trees can be used to trap crawlers. A count of presence and absence of crawlers at petal fall determined the extent of trees with significant root colonies in West Virginia (Brown 1993).

Biological control

Little is known of the natural mortality factors that regulate edaphic populations. However, biological control of the aerial colonies has been studied extensively. (Asante 1997) compiled a review of the world literature. The parasitoid Aphelinus mali (Haldeman) is native to eastern North America, and has been introduced in many regions around the world to control woolly apple aphid (DeBach 1964). Woolly apple aphid was first recorded in Washington in 1892, and became a serious pest (Johansen 1957). The parasitoid was brought to the Hood River Valley in Oregon from Michigan in 1928 and 1929, and successful releases were made in 1930 and 1931 (Childs and Gillespie 1932). Specimens from Hood River, Oregon were brought to Yakima in 1930 and 1931, while some from Oregon and some from Ontario, Canada, were brought to Wenatchee in 1931 and released in 1931 and 1932. By 1934, the parasitoid was reproducing in many orchards in Wenatchee.

Improvement of biological control has been a concern in many regions of the world, because of the chronic infestations of woolly apple aphid. In cold, northern regions, population regulation of woolly apple aphid is erratic or insufficient (DeBach 1964). Colonies of woolly apple aphid on apple roots are completely protected from the parasitoid. The size and shape of aerial colonies cause A mali to have a poor numerical and functional response to host density in the event of an outbreak. Percent parasitism declines as colonies increase in size, because parasitoids can’t reach inside the center of dense colonies. If woolly apple aphid forms large colonies quickly in spring, A. mali would be less and less efficient (Mueller et al. 1992).

The response of A. mali to growth of woolly apple aphid population is further diminished by low temperatures. The low developmental threshold of A. mali is higher than that of its host (Asante and Danthanaryana 1992), and the development rate of the parasitoid peaks at higher temperatures than that of the host (Walker 1985). Nevertheless, the reproductive rate of A. mali is much lower than that of woolly apple aphid, especially at low-intermediate temperatures (Walker 1985). Thus, field experiments indicate the development time lags behind, even in hot weather (Asante and Danthanaryana 1992, Bonnemaison 1965, Evenhuis 1958, Walker 1985).

This explains early season outbreaks of the aphid, especially in Europe (Bonnemaison 1965, Evenhuis 1958). After an analysis of simulated reproduction of both the host and parasitoid, Walker (1985) believed that summers were too brief in Wenatchee for the parasitoid to eliminate the host locally. Mols and Boers (2001) proposed introduction of a strain from Nova Scotia, Canada, to the Netherlands, because the Dutch strain, originally from Virginia, is less adapted to a cold climate. Asante and Danthanarayana (1992)) advocated introduction of a better biological control agent in northern New South Wales, Australia, because of inability of A. mali to suppress outbreaks.

Endogenous species of predators often cause substantial mortality of woolly apple aphid.

Without the presence of natural enemies, aphid colonies in Wenatchee steadily increased throughout the summer (Walker 1985). When parasitoids were allowed access, the colonies still increased. Only predators and parasitoids together showed an ability to reduce aphid colonies.

Predators often reject mummified wooly apple aphids, thus favoring the parasitoid (Walker 1985).



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