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Balsam twig aphidOn this page: Identification & Distribution Biology & Ecology: Life cycle Wax coating and honeydew Natural enemies Other aphids on the same host Damage & Control: Damage assessment & economic injury level Resistance Biological Control: Augmentative Conservation Chemical Control Integrated Control
Identification & Distribution:
The wingless viviparae of Mindarus abietinus are yellowish green and covered with wax powder and long tendrils of accumulated wax (cf. Prociphilus fraxinii and Prociphilus bumeliae which are also wax covered, but feed on the roots of Abies). The antennae and legs are distinctly darker. Wax pore plates are almost always absent from the prothorax and abdominal tergites I & II, and only constantly present on abdominal tergites VI & VII (cf. most other Mindarus species feeding on Abies, which have wax pore plates on the prothorax and often also on abdominal tergites II-VII). The body length of Mindarus abietinus apterae is 1.7-2.0 mm.
The winged viviparae of Mindarus abietinus (see second picture above) have dark dorsal abdominal cross-bands. Antennal segment III has 12-27 rhinaria in a single row, mostly extending across the complete width of the segment. The alate body length is 1.5-2.7 mm. The images below show an apterous adult Mindarus abietinus, dorsal and ventral, in alcohol.
The balsam twig aphid is found on young shoots of fir (Abies species), especially silver fir (Abies alba) and Nordmann fir (Abies nordmanniana). (Note: During heavy infestations Naumann-Etienne & Remaudière (1995) found many nymphs fell from their preferred hosts onto accidental hosts in the forest undergrowth, and often reached maturity on them.) The eggs hatch in spring, and there are then three generations. Small apterous sexual forms are produced in June, and the females lay the eggs which hatch the following spring. Mindarus abietinus is found throughout Europe, as well as the Middle East, Pakistan and possibly India and parts of the Far East. It may cause serious damage or kill young shoots, or cause deformation and loss of needles. There is also some evidence that infestations affect susceptibility to spruce budworm.
Biology & Ecology:
Fondren & McCullough (2002) describe the biology of the Balsam twig aphid (Mindarus abietinus) on balsam fir (Abies balsamea) and Fraser fir (Abies fraseri ) in the USA. There are only 3 generations per year. The eggs are black and are covered with short white strands of wax (see picture below).
They are laid on needles near the bases of buds in June-July. They overwinter as eggs and do not hatch until around late March to mid-April the following year. Hatching is completed in one to two weeks. The newly hatched aphids are very small and difficult to see, but by mid- to late April they have grown enough to be easily visible against a dark background. These fundatrices (not pictured) feed on 1-year-old needles, or through the bud scales of unopened buds, but cause little damage. They mature in about three to four weeks, then reproduce, each one producing 20 to 40 live young.
The second generation of aphids, called sexuparae (see picture below), is the only stage that causes appreciable damage to tree foliage. The sexuparae aphids first appear just after bud break as the new needles begin to expand. These aphids will suck sap from the soft, current-year needles for three to four weeks until they mature.
When the density of sexuparae aphids is high, the growing needles become curled, distorted or stunted (see picture below).
The sexuparae mature to either apterous or alate adults (see pictures below).
Some of the alates may fly to other trees, while others are carried on the wind to new trees. Balch (1950) encountered large flights of Mindarus abietinus at altitudes from 500 to 5000 ft. Small buoyant insects of this kind can be carried considerable distances in horizontal air currents after being lifted by convection currents. Although proof of ability to survive at high altitudes is lacking, these observations suggest that mass 'flights' occur in the upper air in warm weather with light winds and thus ensure the wide distribution and intermingling of populations of such species.
Mature sexuparae give rise to the final generation of aphids, the sexuales which includes both males and females. These aphids are very small and do little feeding. After mating, the tiny aphids produce the eggs that will overwinter. The life cycle is completed by late June, and the aphids do not reappear until the next spring.
Wax coating and honeydew
All stages of Mindarus abietinus have a dense wax covering. Even the eggs have short white strands of wax (see picture above). This is secreted afresh after each moult, so newly moulted individuals have little or no wax, whilst adults often have long tendrils of accumulated wax (see picture below).
Secreted wax in the form of threads passes out of the cuticle as filaments, the arrangement of these filaments in the cuticle above each epidermal cell gives rise to the distinctive wax skein found in each species: hollow, solid or honeycombed. Smith (1999) suggests that the primary role of the secreted wax is to coat the droplets of honeydew secreted by the aphids, thus preventing the aphids becoming contaminated by their own honeydew (see pictures below) and that of other members of the colony. This view is supported by Pike et al. (2002).
Other, secondary, roles of wax may include individual microclimate isolation and protection from fungi, parasites and predators, as well as waterproofing and frost protection. Mindarus abietinus is not attended by ants.
Fondren & McCullough (2002) give a general account of natural enemies of Mindarus abietinus in North America. Hoverfly larvae (Syrphidae) are voracious predators of balsam twig aphids. These larvae live inside the expanding buds and curled needles, where the sexuparae aphids feed. The adult syrphids tend to hover around the buds and current-year shoots, searching for aphid colonies where they will lay their eggs. Brown lacewings (Hemerobiidae) are predators of aphids as both adults and larvae (see picture below).
Brown lacewing adults overwinter in the litter layer, emerge early in spring and lay eggs that will hatch about a month later. Green lacewing (Chrysopidae) larvae actively hunt for aphids in the buds and shoots, and adults are frequently observed on or near infested firs. Ladybird (Coccinellidae) adults and larvae are common and important predators of balsam twig aphid. Several species feed on balsam twig aphids during the spring and summer, including Harmonia axyridis and Anatis mali.
Berthiaume et al. (2000) evaluated the impact of natural coccinellid larval predation on the balsam twig aphid by systematically removing coccinellid egg masses in a balsam fir (Abies balsamea) Christmas tree plantation in southwestern Quebec. Among coccinellid species hunting on fir foliage during development of Mindarus abietinus fundatrices in May, the indigenous Anatis mali (see picture below) was by far the most abundant and the main one to oviposit on trees.
Image copyright Whitney Cranshaw, Colorado State University / Bugwood.org under a Creative Commons Attribution 3.0 License
Comparison of trees on which coccinellid larval predation was excluded with control trees showed that Anatis mali had a marked impact both during and after the phase of rapid Mindarus abietinus population growth that followed fundatrix maturation. On trees where coccinellid larvae were allowed, aphid colonies became inactive (i.e. no live aphids in the colony) about two weeks earlier than on controls. A strong dampening effect on aphid density was also observed in those colonies that remained active until the end of the aphid life cycle. Predation on aphid colonies reduced production of sexual forms, as the density of Mindarus abietinus overwintering eggs per shoot subsequently was reduced by 32%. Predation by coccinellid larvae occurred too late to prevent needle damage to current year shoots, which affects the aesthetic value of Christmas trees. However, current year shoots measured in the mid-crown of trees late in the season were 19% longer on trees where aphid predation by coccinellid larvae was allowed, compared with trees where they were excluded. It was concluded that Anatis mali is an important natural control factor of balsam twig aphid in Christmas tree plantations, hence its activity should be protected and possibly stimulated by favourable pest management.
Berthiaume (2001) evaluated predation by the cantharid beetle Podabrus rugosulus an opportunist predator of Mindarus abietinus in Christmas tree plantations. Infested shoots develop into pseudogalls characterised by stunting and needle distortion, thus reducing the aesthetic value of trees. In a recent field study of natural mortality affecting the balsam twig aphid in Christmas tree plantations in Quebec, arthropod predation on this aphid was frequently observed. Aphidophagous specialists, including various coccinellid and syrphid species, were most frequently involved, although predation by adults of the cantharid beetle Podabrus rugosulus was also observed. This is the first report of cantharid predation on the balsam twig aphid. Podabrus rugosulus is widespread in eastern Canada and the United States.
Berthiaume et al. (2007) compared the efficacy of two coccinellids, the native Anatis mali and the exotic Harmonia axyridis, in predation of Mindarus abietinus. They hypothesized that the exotic coccinellid Harmonia axyridis, which has recently expanded its range into eastern Canada, should be less well adapted to the prey (Mindarus abietinus) on balsam trees than the native coccinellid Anatis mali which evolved in close association with aphids on conifers in North America. They found that the seasonal life cycle of Anatis mali was better synchronized with that of Mindarus abietinus compared with that of Harmonia axyridis. In spring, Anatis mali adults appeared nearly two weeks earlier on trees than Harmonia axyridis and were active predators of the aphid fundatrices. Anatis mali oviposition thus began before the aphid population started to grow, and its larvae were most active during peak aphid colonies. Behavioral observations showed that both adults and larvae of the nativeAnatis mali searched for prey more actively than those of Harmonia axyridis. The adult-to-adult net reproductive rate of Anatis mali was three times higher than that of Harmonia axyridis. Thus the native Anatis mali was better adapted than Harmonia axyridis to prey on Mindarus abietinus, possibly because it evolved for a much longer period of time with this prey in conifer habitats.
Other aphids on same host:
Mindarus abietinus has been recorded from 22 Abies species.
Damage and control:
Fondren & McCullough (2002) reviewed damage to fir caused by Mindarus abietinus. Trees that break bud relatively late in spring generally sustain less aphid damage than trees that flush early. This probably occurs because late bud-breaking trees provide few feeding sites for the newly hatched sexuparae aphids. In a recent study at Michigan State University, trees that began to break bud after May 7 escaped aphid injury, while trees that broke bud before May 7 were likely to be damaged. Overall growth rates of trees that break bud relatively late are similar to trees that break bud early - the late-flushing trees simply catch up once the new needles begin to grow. In the future, it may be possible to decrease long-term problems with balsam twig aphid by selectively planting fir species or varieties that break bud relatively late. Feeding by the second generation of aphids (the sexuparae) in the swelling buds and expanding needles can affect the growth and appearance of trees. At low aphid densities, some needles on infested shoots will bend or curl slightly, but this rarely causes noticeable damage. When aphid densities are high, however, current-year needles become distorted and appear to be curled or wrapped around the shoot.
When this level of damage occurs, needle growth may be reduced, causing the current-year shoots to appear stunted.
If heavy feeding occurs in consecutive years, tree vigour and growth rates may decline. Balsam twig aphid rarely kills trees, but reduced tree growth and appearance can decrease tree value and reduce profits for growers.
A unique aspect of the interaction between fir trees and Mindarus abietinus is the ability of trees to outgrow much of the aphid damage. Feeding by the aphids is typically completed by mid- to late June. Current-year needles, however, will continue to grow during the remaining summer months. By autumn, many of the needles will have recovered their form. Studies consistently show that trees outgrow 40 to 50 percent of balsam twig aphid damage by autumn. This means that trees that have moderate or high levels of aphid damage in late June will look much better at harvest time (December). Some aphid damage can also be removed by clipping off affected shoots when trees are sheared. The timing of bud break in spring is an important factor affecting the extent of aphid damage.
Damage assessment & economic injury level
Kleintjes et al. (1999) compared methods for monitoring Mindarus abietinus and their potential damage in Christmas tree plantations. Mindarus abietinus causes distortion, loss, or both, of needles on balsam fir Christmas trees. Insecticides are often applied for control of twig-feeding aphids with little monitoring of population levels or their subsequent damage. This study compared the utility of 2 aphid monitoring techniques (beating discs, and visual counts of infested shoots) that could easily be used by Christmas tree growers. A beating technique was better than visual counts for detecting numbers of fundatrices before and during budbreak, whereas visual counts of midcrown infested shoots were more feasible for estimating aphid abundance after budbreak. Sample-size analysis indicated that a minimum of 15 trees could be used for either method to estimate mean numbers of fundatrices or mean proportions of potentially infested shoots. Correlation analyses between mean numbers of aphids or proportions of infested shoots and resulting proportions of undamaged shoots were variable with a significant and negative correlation between infested shoots and subsequent undamaged shoots. Paired comparisons were also made between selected and nonselected Choose-and-Cut Christmas trees to evaluate public perception of aphid damage. The public did not differentiate between aphid-damaged and undamaged trees, but they did show a preference for larger trees. Their results indicate that growers need to monitor aphids before budbreak and limit insecticide applications to trees with predictable levels of infestation.
Fondren and McCullough (2003) sought to (1) monitor the numbers of Mindarus abietinus in fir plantations; (2) assess relationships between Mindarus abietinus density, tree seasonality, and damage to tree foliage; and (3) develop an aesthetic injury threshold for Mindarus abietinus on Christmas trees. They monitored seasonal changes of Mindarus abietinus and fir trees on three commercial Christmas tree plantations in central and northern Lower Michigan for 3 years. The seasonal abundance of Mindarus abietinus fundatrices and sexuparae was strongly correlated with accumulated degree-days (DD) where base = 10°C. (DD°C = sum((Tmax-base)+(Tmin-base))/2 for n days, and Tmax and Tmin are the max and min temperature each day.) Fundatrices matured by 83 DD°C and sexuparae were first observed at 83-111 DD base 10°C. Trees that broke bud 1 week later than other trees in the same field escaped Mindarus abietinus damage, and the shoot expansion rate in spring was generally positively correlated with Mindarus abietinus damage. Retail customers surveyed at a choose-and-cut Christmas plantation over two years did not consistently differentiate between similarly-sized trees with no, light, and moderate Mindarus abietinus damage - but heavy damage (more than 50% damaged shoots) did affect customer perception.
DeHayes (1981) looked at genetic variation in susceptibility of Abies balsamea to Mindarus abietinus. Balsam fir from eastern origins had 15-60% greater incidence of attack and averaged nearly twice the crown injury than did that from western origins. Fraser fir suffered little or no injury and appears to avoid twig aphid attack when planted in the north because it begins growth after the aphid population has peaked. The concentration of β-phellandrene in twigs was strongly correlated with twig aphid injury in balsam fir, whereas height, date of budbreak, needle length, and concentrations of other monoterpenes were weakly or only indirectly correlated with twig aphid injury.
Carter (1985) looked at some resistance features of trees that influence the establishment and development of aphid colonies. One of the aphid species covered was Mindarus abietinus. Seasonal changes in soluble amino-acids of leaves and their relationship with the annual life cycle of several aphid species including Mindarus abietinus is discussed. The authors suggested that trees with a different seasonal growth pattern, or containing certain secondary compounds, as well as those trees with physical barriers that can exclude aphids from feeding, could be adopted to lessen the attacks by aphids.
Mattson et al. (1989) found that Mindarus abietinus infested nearly all trees in a range-wide provenance plantation of balsam fir, Abies balsamea in Michigan. Infestation levels were highest on eastern and lowest on western seed sources of fir. Large populations of the aphid were correlated with low survival and reduced developmental rates of the spruce budworm Choristoneura fumiferana . They proposed that chronic, high susceptibility of trees to aphids could reduce concomitant susceptibility to budworm through direct (competition) and indirect (host and community-level) effects.
Fondren & McCullough (2002) posed the question of whether host plant resistance can be a long-term management tool. Genetic factors appear to play a role in the timing of bud break, which affects the extent of aphid damage that fir trees sustain. Many varieties of balsam fir, for example, break bud before Fraser fir trees, even when they are growing side by side. Even within a species, some trees are genetically programmed to break bud relatively late in spring. Identifying the individual trees, varieties or species of fir that break bud late may help reduce aphid damage in he short term as well as the long term. For example, it may be beneficial to harvest trees with early bud break as soon as they reach saleable size. Trees with late bud break are less likely to be affected by aphid feeding and could be retained until they reach a larger size. In the long term, identification and selective propagation of trees that have consistently late bud break may help to reduce balsam twig aphid populations in Christmas tree plantations throughout Michigan.
Biological control can be an important part of an integrated management program for balsam twig aphid. Fondren & McCullough (2002) described two biological control strategies to consider in Christmas tree plantations.
Fondren et al. (2004) identified insect predators associated with Mindarus abietinus in three Christmas fir-tree fields in Michigan. They also conducted laboratory and field studies to assess the effectiveness of augmentative releases of the chrysopid Chrysoperla rufilabris for Mindarus abietinus control. A diverse complex of predators, primarily generalists including syrphids, coccinellids, and lacewings, was observed on infested trees. Predator abundance was generally low early in spring when Mindarus abietinus fundatrices were present, but predators became more common as sexuparae and later aphid stages appeared. In controlled laboratory tests, Chrysoperla rufilabris were capable of consuming at least 35 Mindarus abietinus per day, but were able to develop on 10 aphids per day. In field studies, release of one Chrysoperla rufilabris larva on to caged branches with moderate Mindarus abietinus infestations significantly reduced the density of Mindarus abietinus overwintering eggs. In open field releases, Chrysoperla rufilabris larvae significantly reduced the density of Mindarus abietinus sexuparae and overwintering Mindarus abietinus eggs in two of three fields.
Saunders (1969) described control operations in western Washington, USA. Mindarus abietinus attacked Abies grandis and Abies concolor and caused severe stunting, needle fall, and twig distortion of Christmas trees. They found that ultra-low-volume application of 0.25 g oxydemetonmethyl per 4- to 6-ft-tall tree gave effective seasonal control. Oxydemetonmethyl, dimethoate, and Azodrin® applied to the trunk at 2.5 g per tree in water alone or with the adjuvants Estab® or Roplex® gave excellent control, but this high rate and application expense was only economically practical for high-value trees.
Nettleton & Hain (1982) described the life history, foliage damage, and control of the balsam twig aphid, Mindarus abietinus, in the Fraser fir Christmas tree plantations of western North Carolina, USA. Mindarus abietinus causes leaf-curl and shoot-stunting of the new foliage of Fraser fir in North Carolina. Although this injury usually has a minimal impact on the trees' health and vigour, the injury can reduce the aesthetic quality and hence the marketability of Christmas trees. Most of the injury can be minimized by maintaining vigorous growth, and timing necessary insecticide applications. Under most circumstances chemical control should only be considered during the last year or two before harvest. Dimethoate, pirimicarb, acephate, or chlorpyrifos will provide adequate control after egg hatch, but before bud break.
Kleintjes et al. (1997) evaluated the impact of a growers' application of the insecticide Phosphamidon-8 upon populations of aphids and their arthropod predators in a plantation in western Wisconsin, USA. Spraying occurred late May as a result of aphids visibly damaging Christmas trees targeted for December 1994 sales. Aphids and predators were sampled by visual counts of infested shoots before and after insecticide treatment. Percentages of treated aphid-infested shoots significantly decreased from 86% prespray to 3% postspray, whereas percentages of untreated infested shoots increased from 75-88%. Two weeks postspray, percentages of both sprayed and unsprayed infested shoots were 5%. Numbers of aphidophagous predators significantly decreased on sprayed trees and significantly increased on unsprayed trees. Spiders increased on all trees. Assessment of needle damage 9 months after treatment revealed no significant differences in the mean number of damaged shoots between sprayed and unsprayed trees. However, during the following growing season, treated trees contained significantly fewer aphids and predators than did unsprayed trees. This indicates that insecticide treatment of the shoot-feeding stages (fundatrigenia and sexuparae) can reduce numbers of aphids and their predators in the current and subsequent year, but will not necessarily reduce needle damage.
Cloutier (2001) reviewed control programmes for Mindarus abietinus in Canada from 1981-2000. Control of Mindarus abietinus in managed plantations was mainly based on insecticide spraying against fundatrices, which prevented pseudogall formation. In the mid-1990s, it was estimated that 18,000 litres of diazinon were applied annually to control Mindarus abietinus in Quebec.
Kleintjes (1997) examined the effects of integrating cultural tactics into the management of Mindarus abietinus in balsam fir Christmas tree plantations. A complete randomized block split-plot design incorporating whole plot treatments (fertilizer/mowing, fertilizer/Simazine herbicide, white Dutch clover intercrop and no treatment) with subplot treatments (Imidacloprid, Diazinon, Azadirachtin and no treatment) was used to determine treatment effects upon numbers of aphids and their natural enemies. Numbers of aphids and aphid-infested shoots were low on all treatments (<12 aphids per subplot) although fertilized treated plots had slightly higher numbers of aphids. Diazinon treated subplots had significantly lower, albeit marginally, mean numbers of aphids/subplot. All treatments and their interactions had little effect upon proportions of infested shoots and resulting undamaged shoots (>80% undamaged). Predator abundance were too low to detect significant effects of treatments.
Fondren & McCullough (2002) discuss timing of insecticide sprays using degree-days to avoid harming predators. They suggest that mMonitoring degree-day accumulation helps growers estimate when stem mothers are likely to hatch and when the sexuparae aphids will begin feeding. Degree-day accumulation is a way of keeping track of how quickly temperatures warm up in the spring. It is more accurate and reliable to base scouting and control activities on accumulated degree-days than on the calendar. Degree-day accumulations for Mindarus abietinus are usually based on a threshold temperature of 50 degrees F. Accumulated degree-days are calculated weekly by Michigan State University (MSU). A grower can estimate when balsam twig aphid fundatrices and sexuparae will appear by monitoring the accumulation of degree-days in spring. When spraying is necessary, it is critical to apply insecticides at the proper time to prevent damage to current-year foliage. The ideal time to spray is at 100 to 140 day degrees, after the fundatrices have hatched, but before the sexuparae (second generation) aphids are present. Typically at this point, buds are swelling, but have not yet broken, and the fundatrices have hatched and are exposed at the ends of the shoots. It is very important to control the fundatrices before they produce the sexuparae. The sexuparae typically feed inside the expanding bud and are well protected from insecticides. Spraying after the sexuparae are present will not prevent damage to the current-year foliage, and will harm beneficial predatory insects and possibly lead to more pest problems later.