Eucallipterus tiliae

Identification & Distribution:

All adult viviparae of Eucallipterus tiliae are alates (see first picture below). The body is pale yellow with black markings, including lateral stripes on head and prothorax and two rows of black dorsal abdominal spots. The forewing has a dark front edge and dark spots at the tips of the oblique veins. The antennae are black with the middle part of segment 3, the bases of segments 4, 5 and 6 and the terminal process paler. The terminal process is 0.55-0.7 times the length of the base of the last antennal segment. The short, truncate, siphunculi are dark or dusky. The body length of winged female Eucallipterus tiliae is 1.88-3.0 mm.

The winged male of Eucallipterus tiliae (see second picture above) is similar to the alate vivipara, but has secondary rhinaria on antennal joints III-VI. The claspers are blackish.

The common lime aphid feeds on the undersides of leaves of lime (Tilia species). It does not host alternate. Alate males and apterous oviparae develop in mid-late summer, earlier in the year than in most species. Eucallipterus tiliae is found in Europe, south-west and central Asia and north Africa, and has been introduced to North America and New Zealand.

Biology & Ecology

Dixon (1971a) established that lime aphids have an clumped or aggregated distribution within each leaf. Kidd (1976a) sought to find out whether this behaviour was the result of social attraction or mutual preference for certain areas of the leaf. He first assessed leaf vein selection in the lime aphid. Small veins confer greater nutritional benefits and have no lignified barriers. But there are advantages to feeding on the larger veins for those more mature aphids which can penetrate the sclerenchyma - the large veins of the upper surface are situated in grooves, which may provide protection against dislodgement. The picture below shows several third instar nymphs (and one first instar nymph) feeding on the leaf veins.

Kidd concluded that aggregation partly results from the selection by large aphids of the larger leaf veins, which cover only a small proportion of the leaf area. But a more important factor for both nymphal and adult Eucallipterus tiliae is social aggregation, the aphids themselves being the attractive stimulus (Kidd, 1976b). In adults aggregation comes about through responses to visual stimuli from the wing patterns of other adults.

Kidd (1977) looked at the effects of high population density on the flight behaviour. Aphids show a heightened flight response to direct crowding and to the effects on the leaves of their host plant of previous high numbers of aphids. Sensitivity to direct crowding occurs at stages, the effects being additive in determining the likelihood of an aphid flying. The adults respond to the increased tactile stimulation from other aphids brought about by crowding.

Dixon (1972) examined the mechanisms by which the production of sexual males and females (oviparae) is regulated. In this species there are two "interval timers" or "biological clocks". One controls the production of oviparae (see picture below), whilst the other controls the production of males (see next two pictures below).

One unusual feature of the ovipara is the presence of subsiphuncular wax glands (see wax secretion in picture above). The wax is secreted as a defense against predators.

Both interval timers are sensitive to day-length and temperature, but they respond in different ways. With the approach of autumn the waning effect of the timer inhibiting oviperae production combined with the short day-lengths results in an increasing proportion of the aphids developing into sexual females. The restraining effect of the "interval timer" results in a gradual transition from parthenogenetic to gamic reproduction over a period of several generations and is still operational in the autumn. However, in this species even relatively long day conditions (17 h) can induce the development of oviparae. This low threshold of response to day-length combined with the short generation time results in the sexual morphs appearing very early in the year. This is of considerable adaptive significance in years when, as frequently happens, the aphids disappear locally before the onset of autumn.

Dixon (1971) analysed the changes in numbers of Eucallipterus tiliae over a number of years. In the course of a year the lime aphid typically shows a single peak of abundance, the timing of which varies from year to year. Dixon found there was an overcompensated density dependent factor acting within years, and an inverse density dependent factor acting between years. Because of its effect on the aphid's rate of development and reproduction the variation in temperature from year to year acts as a density disturbing factor. There is no evidence from laboratory experiments to suggest that the quality of its food influences the numbers of the lime aphid. However, qualitative changes in the aphid following period of aphid abundance were shown to be important in the overcompensated density dependent response. Modelling studies supported the conclusion that numbers of the lime aphid in Britain are regulated by an interaction between predation and aphid flight (Dixon & Barlow, 1979). These normally pre-empt regulation by aphid induced changes in plant quality which would otherwise cause increased flight and mortality later in the year.

Barlow (1981) modelled populations of Eucallipterus tiliae in both Britain (where it is native) and New Zealand (where it is an introduced exotic pest). In Britain, populations of this aphid characteristically build up to a single peak each season, reached early in the year if densities are initially high and later if they are low. Following the peak, numbers decline and over-wintering eggs are laid by sexual forms at the end of each season. The result is an inverse relationship between densities at the beginning of successive years. In New Zealand the picture appears to be somewhat different. Densities remain low, with only slight peaks in spring and autumn and a depression during summer. Sexual forms are produced about 6 weeks later than in Britain, relative to the time of appearance of the first generation. Predators are very few. It appears that wind is a significant mortality factor in these populations.

Dixon (1973) compared sycamore (Drepanosiphum) and lime (Eucallipterus) aphids with respect to their ability to adapt metabolically to changes in temperature. It seems that sycamore aphids can adapt, but lime aphids cannot. The difference in ability of these two tree-dwelling aphids to adapt metabolically to changes in temperature can be related to their mode of life. The sycamore aphid lives on sycamore which is native to the mountainous areas of southern and central Europe where conditions are cool. Sycamore also has a longer growth period than lime as its buds burst earlier and it sheds its leaves later. Sycamore aphids are therefore naturally exposed to a wider range of temperatures than lime aphids.

Wratten (1973) looked at the effectiveness of the coccinellid beetle, Adalia bipunctata, as a predator of the lime aphid. He concluded that this predator did not influence the timing or intensity of major peaks in aphid numbers, as the predator larvae soon became satiated. However, the large numbers of larvae present after a peak inflicted a heavy mortality and accentuated the population decline, suppressing the production of oviparae and (presumably) reducing the initial population the following year. In recent years the role of Adalia bipunctata seems to have been taken over by the invasive Harmonia axyridis (see pictures below).

Glen (1975) looked at the searching behaviour and prey-density requirements of another lime aphid predator, the black-kneed capsid (Blepharidopterus angulatus). High levels of emigration by adult females prevented predator populations from responding to high aphid populations.

Dahlsten et al. (1999) carried out long term sampling of introduced populations of Eucallipterus tiliae and its natural enemies in northern California. Eucallipterus tiliae was more abundant in the lower canopy, but had no consistent pattern regarding inner versus outer canopy. Aphid population densities fluctuated irregularly each season and were not associated with parasitoid or predator densities. Trioxys species were the most numerous associated natural enemies, and most abundant on the inner leaves of the lower canopy on the north-eastern sides of trees. Both the aphid and parasitoids were significantly more abundant on trees with Argentine ants ( Linepithema humile) present. In Europe Eucallipterus tiliae is not usually attended by ants, and it is not clear in this work whether the ants were simply collecting (gleaning) honeydew from the leaves or actively attending the aphids.

Other aphids on same host:

Eucallipterus tiliae has been recorded from 12 Tilia species.

Blackman & Eastop list 3 species of aphid as feeding on common lime (Linden, Tilia x europaea) worldwide, and provide formal identification keys (Show World list). Of those aphid species, Baker (2015) lists all three as occurring in Britain (Show British list).

Damage & Control:

Lime aphids are generally considered to have little direct effect on tree growth (Alford, 2012). However, Dixon (1971b) detected effects of Eucallipterus tiliae on the growth of lime saplings. Although the growth above ground in girth, height increment, leaf number and leaf size was normal, the roots of aphid infested saplings did not grow. Saplings infested with aphids shed their leaves earlier. Aphid infestation in one year resulted in smaller leaves in the following year, but these leaves were a darker green and had a net production 1.6 times greater than the leaves of previously uninfested saplings.

Llewellyn (1972) calculated the energy budgets of lime aphid populations on two mature lime trees. Each year the aphid population utilizes 6% of its energy intake in production, 4% in metabolic heat loss, and 90% in defaecation and excretion. An energy drain of 28,055 kcal per year was imposed on the trees by this energy turnover. Llewellyn (1975) did further work on the energy drain imposed by the aphid populations. Each leaf supported an average of five aphids throughout the season and their feeding resulted in an energy drain of 19% of the trees annual net production. Llewellyn calculated that twenty-six aphids/leaf would completely drain the net primary production of the tree.

The major problem with Eucallipterus tiliae is not its impact on tree growth, but the effects of the copious quantities of sticky honeydew which descend on anything below infested trees. - Since lime is widely planted in the urban environment, this means cars and the various street architecture. A black mould grows on the honeydew, coating any item affected. To date no environmentally friendly method has been demonstrated to yield effective control of lime aphids. Attempts have been made in some European cities to control lime aphids by releasing larvae of the native two-spot ladybird beetle, Adalia bipunctata. Unfortunately, adult ladybird beetles disperse soon after release, and there is little indication they provide control of the aphids. Recently Lommen et al. (2013) demonstrated experimentally that releases of both larvae and adult of a flightless strain of Adalia bipunctata, obtained from natural variation in wing length, can reduce the impact of honeydew from lime aphid outbreaks on two species of lime in an urban environment.

Eucallipterus tiliae was first found in the United States as an invasive more than 100 years ago in the area of Washington, D. C. It has occurred in the western United States for more than 50 years, having apparently spread from the east. It causes a nuisance problem on urban lime trees with the sticky honeydew dropping on cars beneath them. In 1970 the aphidid parasitoid Trioxys curvicaudus was introduced in Berkeley, California, marking the first use of a parasitoid for biological control against an ornamental shade tree aphid pest (Olkowski et al. 1982a). Because aphid populations were lower by 1978, and because there was less honeydew and fewer complaints, the project was initially considered successful. However, Dahlsten & Hall (1999) did not consider this a fully successful biological control effort. For a start, the parasitoid did not spread far from the original release site. Additionally Trioxys curvicaudus was found to have several hosts, and was not specific to the linden aphid as previously believed.

Zuparko & Dahlsten (1994) point out that biological control works much better if combined with some degree of host resistance. Host resistance comes from glandular hairs or pubescence. Zuparko & Dahlsten (1996) have highlighted a new potential for classical biological control of Eucallipterus tiliae in California. Previous biological control efforts in California directed against Eucallipterus tiliae had assumed that the aphid was native to Europe. Although several European parasitoids have become established and attack Eucallipterus tiliae in California, complete control has not been achieved. New records of Eucallipterus tiliae from eastern Asia suggest that the aphid may have evolved there rather than Europe. This area has the greatest species diversity of both the host genus (Tilia) and the other linden-feeding drepanosiphid aphids. Zuparko & Dahlsten recommended that any further efforts for locating importable natural enemies be focused in this region.

Acknowledgements Whilst we make every effort to ensure that identifications are correct, we cannot absolutely warranty their accuracy. We have mostly made identifications from high resolution photos of living specimens, along with host plant identity. In the great majority of cases, identifications have been confirmed by microscopic examination of preserved specimens. We have used the keys and species accounts of Blackman & Eastop (1994) and Blackman & Eastop (2006) supplemented with Blackman (1974), Stroyan (1977), Stroyan (1984), Blackman & Eastop (1984), Heie (1980-1995), Dixon & Thieme (2007) and Blackman (2010). We fully acknowledge these authors as the source for the (summarized) taxonomic information we have presented. Any errors in identification or information are ours alone, and we would be very grateful for any corrections. For assistance on the terms used for aphid morphology we suggest the figure provided by Blackman & Eastop (2006).

Useful weblinks

References Alford, D.V. et al. (2012). Pests of ornamental trees, shrubs and flowers. 2nd Edn. Manson Publishing. Barlow, N.D. (1981). Modelling aphid populations. New Zealand Journal of Ecology 4, 52-55. Full text Dahlsten, D.L. et al. (1999). Long-term sampling of Eucallipterus tiliae (Homoptera: Drepanosiphidae) and associated natural enemies in a Northern California site. Environmental Entomology 44(5), Abstract Dahlsten, D.L. & R.W. Hall. (1999). Biological control of insects in outdoor urban environments. In: Bellows, T. S. & T. W. Fisher (eds.), Handbook of Biological Control: Principles and Applications. Academic Press, San Diego, New York. 1046 p. Abstracth Dixon, A.F.G. (1971a). The role of intra-specific mechanisms and predation in regulating the numbers of the lime aphid, Eucallipterus tiliae L. Oecologia 8(2), 179-193. Abstract Dixon, A.F.G. (1971b). The role of aphids in wood formation. II. The effect of the lime aphid, Eucallipterus tiliae L. (Aphididae), on the growth of lime, Tilia x vulgaris. Journal of Applied Ecology 8(2), 393-399. Full text Dixon, A.F.G. (1972). The "interval timer", photoperiod and temperature in the seasonal development of parthenogenetic and sexual morphs in the lime aphid, Eucallipterus tiliae Ln. Oecologia 9(4), 301-310. Abstract Dixon, A.F.G. (1973). Metabolic acclimatization to seasonal changes in temperature in the sycamore aphid, Drepanosiphum platanoides (Schr.), and lime aphid, Eucallipterus tiliae L. Oecologia 13(3), 205-210.Abstract Dixon, A.F.G. & Barlow, N.D. (1979). Population regulation in the lime aphid. Zoological Journal of the Linnean Society 67(3), 225-237. Abstract Glen, D.M. (1975). Searching behaviour and prey-density requirements of Blepharidopterus angulatus (Fall.) (Heteroptera: Miridae) as a predator of the lime aphid, Eucallipterus tiliae (L.), and leafhopper, Alnetoidea alneti (Dahlbom). Journal of Animal Ecology 44(1), 115-134. Full text Kidd, N.A.C. (1976a). Aggregation in the lime aphid (Eucallipterus tiliae L.) 1. Leaf vein selection and its effect on distribution on the leaf. Oecologia 23(3), 247-254. Abstract Kidd, N.A.C. (1976b). Aggregation in the lime aphid (Eucallipterus tiliae L.) 2. Social aggregation. Oecologia 25(2), 175-185. Abstract Kidd, N.A.C. (1977). The influence of population density on the flight behaviour of the lime aphid, Eucallipterus tiliae. Entomologia Experimentalis et Applicata 22(3), 2511/2"261. Abstract Llewellyn, M. (1972). The effects of the lime aphid, Eucallipterus tiliae L. (Aphididae) on the growth of the lime Tilia x vulgaris Hayne. I. Energy requirements of the aphid population. Journal of Applied Ecology 9(1), 261-282. Abstract Llewellyn, M. (1975). The effects of the lime aphid (Eucallipterus tiliae L.) (Aphididae) on the growth of the lime (Tilia X vulgaris Hayne). II. The primary production of saplings and mature trees, the energy drain imposed by the aphid populations and revised standard deviations of aphid population energy budgets. Journal of Applied Ecology 12(1), 15-23. Abstract Lommen, S.T.E. et al. (2013). Releases of a natural flightless strain of the ladybird beetle Adalia bipunctata reduce aphid-born honeydew beneath urban lime trees. BioControl 58(2), 195-204. Abstract Olkowski, W.H. et al. (1982a). Linden aphid parasite establishment. Environmental Entomology 11: 1023-1025. Abstract Wratten (1973). The effectiveness of the coccinellid beetle, Adalia bipunctata (L.), as a predator of the lime aphid, Eucallipterus tiliae L. Journal of Animal Ecology 42(3), 785-802.  Abstract Zuparko, R.L. & Dahlsten, D.L. (1994). Host plant resistance and biological control for linden aphids. Journal of Arboriculture 20(5), 278-281. Abstract Zuparko, R.L. & Dahlsten, D.L. (1996). New potential for classical biological control of Eucallipterus tiliae (Homoptera: Drepanosiphidae). Biological Control 6(3), 407-408. Abstract