The aphids that develop from overwintering eggs of Grylloprociphilus imbricator on American beech (known as fundatrices, not pictured) are approximately 5-6 mm long, and have been said to superficially resemble a termite queen. They have 4-segmented antennae and circular groups of wax pore plates on all segments. These circular groups have large central facets surrounded by very much smaller marginal ones. There are no siphunculi. Each beech blight aphid fundatrix produces thousands of nymphs (see first two pictures below) which often cover the fundatrix, obscuring her from view.
All Grylloprociphilus imbricator adults are winged. The offspring of a Grylloprociphilus imbricator fundatrix all mature to winged aphids (alatae), one of which is shown in the third picture above. The alatae have oval secondary rhinaria on antennal segments III-V or III-VI. The forewing of the alate has an unbranched media vein, and a broadly rounded cauda. First instars on the secondary host have thickened hind femora.
Grylloprociphilus imbricatorhost alternates between American beech (Fagus grandifolia) as the primary host and the roots of swamp cypress (Taxodium distichum) as the secondary host. In spring the fundatrices on beech give rise to large colonies with flocculent wax, which can persist and grow through the summer and autumn. Some of the alatae produced on beech migrate to Taxodium roots, where apterae can be found throughout the year. Sexuparae return to beech in November-February where they produce the sexual forms. Grylloprociphilus imbricator is found in eastern states of the USA.
Biology & Ecology
Over-wintering eggs of Grylloprociphilus imbricator hatch in spring and become wingleess stem mothers (= apterous fundatrices). These fundatrices develop on the underside of a leaf of American beech (Fagus grandifoliae). On maturity they move to the petioles and stems where they produce large numbers of offspring (see picture below).
In North Carolina, the fundatrix and her parthenogenetic offspring can be found from April until November. In Maryland Grylloprociphilus imbricator colonies may appear as early as May, but do not become common until late August/early September (Cook-Patton et al., 2014).
Smith & Denmark (1984) found some of these alatae produced migrate to the secondary host, the roots of swamp cypress (Taxodium distichum). These aphids can be found year-round on the roots of swamp cypress, indicating that the part of the population is anholocyclic. In late autumn (and early winter?) winged sexuparae are produced which fly back to the primary host, beech, and give birth to males (see picture below) and to females which lay overwintering eggs on the beech.
On the primary host, American beech, ants have not been recorded as tending beech blight aphid colonies. Aoki et al. (2001) observed no ants visiting their two experimental colonies, or five other colonies that they were able to examine at close range. When a twig on which a colony was formed was lightly touched some nymphs produced honeydew, but not many droplets of honeydew fell from the colony, contrary to the usual observation of aphids. Hottes & Frison (1931) mentioned that Grylloprociphilus imbricator often "produces so much honey-dew that the ground beneath the infestation becomes discolored." Thus, if ants were present, they were not effectively removing the honeydew from the observed colonies. Taken together, these observations strongly suggest that Grylloprociphilus imbricator does not depend upon defense by ants on their primary host.
Ants can however be found gleaning honeydew under the aphid colony.
On their secondary host, the roots of swamp cypress, Smith & Denmark (1984) recorded two species of ants (Pheidole moerens and Solenopsis invicta) tending Grylloprociphilus imbricator.
On exposed twigs of American beech, large wax-covered colonies of Grylloprociphilus imbricator are known to last over several months. Aoki et al. (2001) hypothesized that these colonies could not persist for such a long period without there being some sort of active defense behaviour by the aphids against predators. To test this hypothesis, they tried introducing tortricid moth larvae into the colony. Tortricid larvae are not natural predators of Grylloprociphilus imbricator, but the authors stated that, in their experience, if the aphids attack moth larvae, they will also attack actual predators (see for example Aoki, 1977).
Of ten tortricid larvae that were introduced on to a colony, all were attacked by nymphs of Grylloprociphilus imbricator. Eight were attacked almost immediately after introduction, and the other two were attacked 14 and 39 seconds after introduction. The attacked larvae responded by wriggling, and four fell off the colony within three minutes. A total of 69 nymphs attacked the ten tortricid larvae. Nymphs of all four instars participated in the attack and "stung" the larvae with their stylets, but of the 69 nymphs that attacked the larvae, 36 (52.2%) were fourth instar. Unlike older nymphs of other eriosomatines, wingpadded (alatiform) fourth instar nymphs of Grylloprociphilus imbricator are slender in shape with long legs. When the colony was disturbed, many fourth instar nymphs raised the tips of their abdomens covered with woolly wax and a few long wax filaments, and walked around while waving their abdomens back and forth (see picture below).
Aoki's is the first report that wingpadded fourth instar nymphs are the main defensive morph. In almost all aphid species that have soldiers, the main defenders are small first or second instar nymphs. Some species, such as Pseudoregma alexanderi and Colophina monstrifica have acquired larger soldiers by enlarging their sterile first instar nymphs (Aoki et al. 1981; Aoki, 1983). In contrast, Grylloprociphilus imbricator has acquired large defenders by modifying the behavior and morphology of its wingpadded fourth instar nymphs.
The boogie-woogie dance
Whilst the fourth instar soldiers may be effective in defending the colony from invertebrate predators such as coccinellid and syrphid larvae, and larvae of the Harvester butterfly (Fenseca tarquinius, see below), it is unlikely these soldiers would have much effect on a vertebrate predator such as an insectivorous bird. Aoki et al. (2001) did note that humans could detect the 'stings' (insertion of stylets) of the larvae when handling them, but their 'stings' only caused minor irritation. Most insectivorous vertebrates have thickened skin or feathers to protect themselves.
Large-scale disturbance of the beech blight aphid colony by (for example) an insectivorous bird or mammal provokes rather different defensive behaviour. These aphids will raise the posterior end of their body and sway. This action produces a dance-like effect that ripples throughout the colony, leading to Grylloprociphilus imbricator getting the name the "boogie-woogie aphid". This dance-like effect can be seen in a video: 'Dancing Boogie-Woogie Aphids'. It is not unlike a "Football" wave. The aphids' dance is thought to have evolved in order to distract and dissuade predators from focusing on single individuals. A similar strategy is followed by herds of impala in Africa - if ambushed by a predator, the group explodes in all directions in an attempt to confuse and distract the predator (Osborne, 2000).
Harvester butterfly larvae
Not surprisingly, the same predators that attack the wax-covered woolly alder aphid (Prociphilus tesselatus) also attack beech blight aphids. Best known amongst these is the larva of the harvester butterfly (Feniseca tarquinius). The harvester butterfly is found sporadically across its range, from Florida in the south to Nova Scotia in the north, and extends as far west as Texas in the south to Manitoba in the north. Up to 8 broods have been reported for the harvester butterfly, but more typically it has two to three broods, the first appearing in early May, the second in mid to late July, and occasionally, a third in August or September. The picture below shows a cluster of harvester larvae feeding on beech blight aphids.
Image reproduced by permission, copyright Jay Cossey, all rights reserved.
The butterfly lays its eggs among clumps of woolly aphids (including Eriosoma, Grylloprociphilus, Neoprociphilus, Pemphigus and Prociphilus species), on which the emergent larvae feed. The larvae are up to 1.9 cm in length and slug-like. Full-grown larvae are brightly patterned with gray, yellow and white, and covered with bristly hairs, although the pattern (see picture below) is often obscured with the white wax produced by their prey.
Image reproduced by permission, copyright Jay Cossey, all rights reserved.
Mathew et al. (2008) suggested that there may be acoustical signalling to facilitate the aphid-larva interaction. They showed that larvae of the harvester butterfly produce substrate-borne vibrations that possess a long pulse length and narrow bandwidth when compared with other lycaenid calls. They proposed that harvester larvae may be mimicking the acoustical signals produced by the woolly aphids upon which they feed. One has to note, however, Mathew et al. did not demonstrate the aphids produce any sound at all.
For aphid species that are regularly ant-attended, such as Prociphilus tessellatus, the ants have been observed to be distinctly hostile to the lycaenid larvae. This was thought to explain why early instar harvester larvae sometimes live in concealed locations under the aphids until fully grown, even spinning a silken web among the aphids. However, Youngstead & Devries (2005) have shown that harvester caterpillars are less likely to be concealed in the presence of the ants Camponotus pennsylvanicus and Formica obscuriventris than in the absence of ants. Instead, chemical analysis and behavioral assays suggested that chemical camouflage, not physical concealment, was responsible for the ants’ failure to detect and remove harvester caterpillars from aphid colonies. The cuticular lipid composition of caterpillars was shown to be similar to that of their aphid prey, and solvent extracts of harvester caterpillars and Prociphilus aphids evoke similar behavioural responses in the ants.
The pictures above show adult harvester butterflies. The proboscis of harvester adults is very short, and they do not feed on floral nectar. Instead they tend to stay around the aphid colonies, where they feed on aphid honeydew and sap; they also sip from mud and dung.
Birds are also known to predate beech blight aphids. The Tennessee warbler (Oreothlypis peregrina) is better known as a predator of spruce budworm (Choristoneura species, of the tortricid moth family). Bird numbers show a large and rapid response to budworm outbreaks, and there is evidence that birds may play a role in determining the mean level of oscillations. But Tennessee warblers will also feed on aphids and, from the observations below, birds appear to aggregate where there are large aphid populations.
Tracy, from Ohio USA, made a fascinating set of observations one autumn which she recounts in Autumn Warbler Incidents, part 3 - An insect feast. She watched a Tennessee warbler feeding on a vast colony of the beech blight aphid (Grylloprociphilus imbricator).
Image reproduced by permission, copyright Seasons Flow, all rights reserved.
It is unclear to what extent the dance of the boogie-woogie aphid (see above in 'Defensive behaviour') inhibits the predatory efforts of the warbler.
The picture below shows the specialist sooty mould (Scorias spongiosa) that grows exclusively on the copious amounts of honeydew deposited by colonies of Grylloprociphilus imbricator. Wherever a quantity of beech aphid honeydew falls Scorias spongiosa starts growing in a thin layer of yellow-brown tufts of asexual, flask-shaped, spore-bearing structures - known as pycnidia. As a result this fungus coats the leaves of seedlings directly beneath the aphid colonies. As honeydew accumulates the fungus grows larger, until it looks like a large yellow sponge sitting on the beech branches or leaves. At this stage, it is very soft and spongy and produces conidia (asexual, non-motile spores) in liquid droplets from its pycnidia.
As the fungus ages it blackens, becomes thicker, and harder, and produces sexual spores in flask-shaped structures called pseudothecia.
Cook Patton et al. (2014) investigated whether the beech aphid - sooty mould interaction had negative effects on beech seedling communities, and if so what the effect resulted from. They found that that tree seedlings, regardless of species identity, suffered higher mortality when they were positioned directly under aphid colonies. There are two ways in which this could happen: changes in soil quality and/or impairment of leaf function. Aphid honeydew represents a carbon rich input into the soil, which would alter C:N ratios and diminish soil fertility. However, seedlings grown in soil from infested and uninfested trees performed similarly. They suggested the seedling mortality beneath aphid colonies was not caused by changes in soil quality but by the sooty mould impairing leaf function. The researchers also found that the aphids preferentially and repeatedly colonized the same, large, beech trees, suggesting that the negative effects of this aphid-beech-fungal interaction were creating islands of seedling-poor patches. Note: this does not imply a lack of undergrowth is a disadvantage to the these beech trees.
Blackman & Eastop list 2 species of aphid as feeding on swamp cypress (Taxodium distichum): Illinoia morrisoniand Grylloprociphilus imbricator.Baker (2015) lists Illinoia morrisoni, but not as a species 'resident' to Britain - it being an invasive species to europe.
Damage and control
Barnd et al. (2008) commented that as the honeydew begins to get covered by sooty mould it can become quite unsightly. It is not, however, known to cause any serious injury to trees, although some limbs may die as a result of a heavy infestation. Cook Patton et al. (2014) note that the sooty mould does adversely affect seedling regeneration, albeit the likelihood of a seedling surviving directly under its parent tree is very low anyway.
We are very grateful to Jay Cossey for permiting us to use his excellent pictures of harvester butterfly caterpillars predating beech blight aphids, and to Seasons Flow for allowing us to use their excellent picture of a Tennessee Warbler eating beech blight aphids. We also thank Katja Schulz, who provided most of the pictures on this page under a creative commons licence.
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Aoki, S. et al. (1981). Observations on Pseudoregma alexanderi (Homoptera, Pemphigidae), an aphid species producing pseudoscorpion-like soldiers on bamboos. Kontyu49, 355-366. Full text
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Smith, C.F. (1974). Keys to and descriptions of the genera of Pemphigini in North America (Homoptera:Aphididae: Pemphiginae). North Carolina Agric. Exp. Sta., Tech. Bull. 226, 1-61.
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Youngstead, E. & Devries, P.J. (2005). The effects of ants on the entomophagous butterfly caterpillar Feniseca tarquinius, and the putative role of chemical camouflage in the Feniseca-ant interaction. Journal of Chemical Ecology31(9), 2091-2109. Full text