Pineus pini
(pine woolly aphid)

P. pini (sensu lato) can cause problems on exotic species of two-needled pines (subgenus Haploxylon) even within its native range, as reported for P. pini from Germany by Steffan (1970b), from France by Gaumont (1978) and from Italy by Covassi and Binazzi (1981).

Infestation by P. pini (sensu lato) causes premature needle shedding and reduction in the length of infested needles, reducing productivity and leading to up to 50% loss of growth increment (Day et al., 2003) and up to 20% tree mortality (Odera, 1974). Stress can make pine trees more vulnerable to attack (Madoffe and Austara, 1993; Day et al., 2003). Damage to trees is most severe under warm, dry conditions (Mailu et al., 1978a).

Wind can facilitate the spread of Pineus (McClure, 1989a), but transmission between countries and between continents is mainly by human transport of infested planting material of two-needled pines (Barnes et al., 1976). The cryptic habit of these insects make them very difficult to detect at plant quarantine inspection, and after introduction they may be overlooked for years because the attention of forest entomologists is often focused on more easily detected pests. In Zimbabwe, the pest was accidentally introduced in 1962 but was not noticed until 1968 (Barnes et al., 1976).

Once introduced and established, alien P. pini (sensu lato) can spread at an average rate of spread of 15 km per year (McClure, 1989b). In Zimbabwe it spread rapidly and reached all the important areas of afforestation within 12 years of its introduction; nearly all the hard pines were attacked with varying degrees of severity, whereas introduced species of soft pine were not (Barnes et al., 1976).

P. pini (sensu lato) has been recorded outcompeting native insects on pines in Kyrgyzstan (Ponomareva and Gabrid, 1981) and in north-eastern North America (McClure 1984a, 1989b).

P. pini is native to western and Central Europe (Blackman and Eastop, 1994) and P. boerneri may be of eastern Asian origin (Blackman and Eastop, 1994). Records of these species from other parts of the world represent introduced populations.

The geographical records listed for P. pini sensu lato can be tentatively assigned to the following species:

P. pini: Western and Central Europe, Australia, New Zealand.

P. boerneri: China, Taiwan, Hawaii, California, north-eastern USA, Chile and Argentina, eastern and southern Africa, Australia, New Zealand and probably Malaysia; also possibly Pakistan.

P. pini (sensu lato) are very small, cryptic insects that are easily overlooked. They have already been accidentally introduced to a number of countries on infested planting material of two-needled pines, and have subsequently become pests. Cuttings and seedlings of two-needled pines should be subject to very close examination before being exported/imported to a country where P. pini (sensu lato) does not occur.

Pineus boerneri has been recorded preferentially attacking the 3-year-old growth of the lower canopy of Pinus resinosa in the north-eastern USA, feeding beneath bark flakes or at the base of the needle sheaths (McClure, 1982).

All the recorded host plants of P. pini sensu lato are members of the subgenus Diploxylon (two-needled pines), not subgenus Haploxylon (pines with needles occurring in groups of more than two) (Anon., 1971). In former Czechoslovakia, with only one exception, infestations of Pineus found on members of Hapoxylon were always Pineus cembrae or P. strobi, not P. pini (Hochmut, 1969).

Pineus boerneri was recorded attacking 39 species of Pinus in Kenya (Odera, 1974), including all the species listed in this datasheet. Host plants that have evolved together with an aphid species have usually evolved defences against aphid infestation that result in slower aphid reproduction on that host.

McClure (1990) suggested that the native host of P. boerneri was Pinus thunbergii; the aphid had significantly greater survival and fecundity on Pinus resinosa (native to America) than on P. thunbergii (native to China).

Genetics

Steffan (1970a) discussed the evolution of asexual lines in species of adelgids including P. pini, and remarked that the asexual strain often had a different number of chromosomes to the sexual strain. P. pini may have arisen as an asexual strain of P. orientalis (Marchal, 1911; Carter, 1969, 1971).

Blackman et al. (1995) found that different populations of Pineus ?boerneri varied in their chromosome number, as might be expected of an asexual species. Specimens with 2n=16 were recorded from Hawaii and California, USA; samples with 2n=17 were recorded from California, Africa, Australia and New Zealand. Some samples from Australia and New Zealand had 2n=19 and 2n=21. Blackman et al. (1995) postulated that the 17-chromosome form of P. boerneri could have arisen from the 16-chromosome form through a single dissociation of one of the longest pair of chromosomes. Such dissociations are common in permanently parthenogenetic populations of aphids (Blackman, 1980).

Physiology and Phenology

In North America, Pineus boerneri is parthenogenetic, trivoltine and passes through six stages of development (McClure, 1989b); however, the generation overlap was so pronounced that all the developmental stages were present at almost all times of the year.

The following is based on Carter (1971). The life cycle of P. pini (sensu lato) differs from that of most adelgids by its simplicity. There may be a partial migration of alatae (sexuparae) to Picea (the ancestral primary host) each year, but males are never produced and sexual reproduction and gall formation on Picea does not occur.

In the absence of sexual reproduction, gall-forming females (gallicolae) do not occur, and asexual reproduction by wingless and winged (alate) females continues throughout the year. There are at least three overlapping generations annually. Clutches of eggs are laid (one egg at a time) over a period of several weeks, resulting in considerable differences between the hatching times of the first and last eggs laid. There are five immature instars before an adult is produced. Overwintering is as wingless adult females (hiemosistentes) that are heavily sclerotized, and as second- and third-instar larvae. In spring, the larvae develop into apterous progredientes (the summer form of the adult female, which is lightly sclerotized) and alate (winged) females.

Reproductive Biology

Reproduction is asexual all year, by the parthenogenetic production of eggs.

Environmental Requirements

Stress can make pine trees more vulnerable to attack by P. boerneri (Madoffe and Austara, 1993; Day et al., 2003). Air pollution was found to make pines more susceptible to attack by P. pini in Finland, possibly due to a resultant reduction in predatory mite populations (Heliovaara and Vaisanen, 1989).

In the north-eastern USA, survival of P. boerneri was higher on branches than on needles during winter, but was higher on needles than on branches in spring and summer (McClure, 1984a). Wind facilitated the spread of P. boerneri in north-eastern North America, and extremes of summer and winter temperatures determined the ultimate limits of its latitudinal distribution; heavy rain reduced its abundance (McClure, 1989a).

In Malawi, the biological performance and pest status of P. boerneri is influenced by external factors especially the within-tree and seasonal fluctuations in the level of nitrogen, total rainfall and canopy structure (Chilima and Leather, 2001). Prolonged, heavy rainfall reduced population levels significantly, mainly through eggs and crawlers being washed off the tree, whereas numbers increased in hot, dry weather; other causes of mortality were found to be excessive heat and crawler dispersion (Mailu et al., 1980).

In the UK, Carter and Barson (1973) found that the threshold temperature for flight by winged Pineus was 16°C, and at least 64% of the catch was taken in the afternoon; fluctuations in the mean date of flight each year were probably related to the phonological condition of the food plant.

Associations

In Scotland, UK, P. pini is sometimes associated with a covering of the fungus Cucurbitaria pithyophila [Curreya pityophila] on the lower branches of Pinus sylvestris, occasionally killing the bark (Murray and Parry, 1969).

In north-eastern America, where the introduced P. boerneri and the native P. coloradensis occur together on Pinus resinosa, P. boerneri was found to maintain numerical dominance over P. coloradensis (McClure, 1984a) and displaced P. coloradensis in the majority of stands over a 5-year period (McClure, 1989b). However, where P. boerneri and Matsucoccus resinosae (an introduced scale insect) occurred together, the presence of M. resinosae on the branches resulted in significantly reduced numbers of P. boerneri on both branches and needles, whereas the presence of P. boerneri had no significant effect on numbers of M. resinosae. In one-third of the affected stands, P. boerneri was excluded by the scale insect within 3 years (McClure, 1990).

Introduced populations of P. boerneri have been successfully controlled by the introduction of predatory species of Leucopis. The most effective control agent recorded is L. tapiae in Hawaii, where Leucopis tapiae (as L. obscura, on Maui, Molokai and Kauai islands) and L. nigraluna (on Hawaii island) were found to maintain P. boerneri (as P. pini) populations below economically significant levels (Nakao et al., 1978; Culliney et al., 1988).

In Kenya, predatory Exochomus spp. were found to remove 12% of the Pineus boerneri population (Mailu et al., 1980). In Zimbabwe, coccinellid beetles were responsible for a marked decline in the infestation (Anon., 1971).

Biological control attempts have also been made in Australia (Waterhouse and Sands, 2001). Only Exochomus quadripustulatus, imported from the UK, became established there. The native predator Diomus pumilo is considered an important predator.

Pineus are such small insects that they are normally prepared as slide mounts so that morphological detail can be studied at high magnification. Carter (1971) provides a method for the preparation of slide mounts and keys to identify the genus Pineus and to more-or-less separate the four species that occur in the UK; the key covers P. pini and P. orientalis, but not P. boerneri.

Strong light and magnification are required, and the bark and needle sheaths need to be destructively examined. P. pini (sensu lato) occur as brownish-red ovoids in nests of white wax fibres beneath bark flakes and bud scales, and concealed within the needle sheaths. Clusters of yellow or brownish-red eggs may also be present in the wax nests; the eggs are not attached to the host plant.

P. pini is morphologically indistinguishable from P. orientalis, a species that reproduces sexually and alternates between Picea (the primary host) and Pinus sylvestris. At present, P. boerneri is not reliably morphologically distinguishable from P. pini and P. orientalis because morphological variation in these species has not been sufficiently well analysed and no identification key is available.

Due to the variable regulations around (de)registration of pesticides, your national list of registered pesticides or relevant authority should be consulted to determine which products are legally allowed for use in your country when considering chemical control. Pesticides should always be used in a lawful manner, consistent with the product's label.

Phytosanitary Measures

Restricted movement and thorough inspection of planting material of Haploxylon pines is the most effective way to prevent P. pini (sensu lato) entering a country.

Cultural Control and Sanitary Methods

Stress can make pine trees more vulnerable to attack by P. boerneri (Madoffe and Austara, 1993); avoidance of marginal growing conditions through more attention to the selection of suitable planting sites can avoid problems with Pineus infestation (Day et al., 2003).

Possible management of P. boerneri in Malawi, through the regulation of nitrogen nutrition and canopy structure, was discussed by Chilima and Leather (2001).

In response to problems with adelgids (including P. pini) on exotic conifers grown in the numerous tree nurseries east of Oldenburg, Germany, Steffan (1970b) recommended that these tree species should not be planted in shelter belts, parks or forests within the growing region.

Host-Plant Resistance

Different species of pine tree, and different provenances of any one pine species, vary in their susceptibility to attack by P. pini (sensu lato) (Simpson and Ades, 1990b; Falkenhagen, 1991a, b). The level of susceptibility of a particular pine species may vary also between one locality and another, reflecting different levels of environmental stress between sites. Simpson and Ades (1990b) called for more research on the planting of multi-clonal mixtures and the pattern in which they are planted, to minimize losses.

Replanting with species or provenances of pines less susceptible to attack is an option for the control of P. pini (sensu lato), but is a long-term and possibly expensive solution that may incur hidden costs in reduced yield or quality, e.g. Pinus radiata has been replaced with the less susceptible P. patula in East Africa, but the latter species is inferior in fibre quality (Day et al., 2003).

Odera (1974) mentioned that Pinus ayacahuite and P. strobes var. chiapensis are resistant to attack by Pineus boerneri (as Pineus pini) in Kenya.

Biological Control

Where members of P. pini (sensu lato) have been accidentally introduced, they are good candidates for classical biological control (Mills, 1990). Pineus boerneri has been controlled successfully by introduced natural enemies in Hawaii, New Zealand and Chile.

Introduced populations of P. boerneri have been successfully controlled by the introduction of predatory species of Leucopis. The most effective control agent recorded is L. tapiae in Hawaii, where Leucopis tapiae (as L. obscura, on Maui, Molokai and Kauai islands) and L. nigraluna (on Hawaii island) were found to maintain P. boerneri (as P. pini) populations below economically significant levels (Nakao et al., 1978; Culliney et al., 1988).

In 1991 L. tapiae was also found to have accidentally entered Malawi, but has not provided such effective control there as in Hawaii (Greathead, 1995; Day et al., 2003). An account of various (mostly unsuccessful) introductions of alien predator species to East Africa against P. boerneri is given by Day et al. (2003).

In Kyrgyzstan, P. pini (sensu lato) (as P. pini) outcompeted the native Oligonychus piceae in the same ecological niche; local natural enemies were ineffective against it, suggesting it was an introduction, and Pineus numbers were only reduced after Leucopis spp. were released (Ponomareva and Gabrid, 1981).

Introduction of the predatory bug Tetraphleps raoi to Kenya in 1975 resulted in some reduction in P. boerneri populations, but not sufficient to prevent reduction of tree growth and occasional tree mortality (Karanja and Aloo, 1990).