Issues in Aphid Biology
|"It has long been an axiom of mine that the little things are|
infinitely the most important"
Giant Willow Aphid (Tuberolachnus salignus)
Have we solved one of its mysteries?
Dransfield, R.D. & Brightwell, R.On this page: Cryptic or aposematic? Habitat and relatives Their mysterious life-cycle Their hiding place? Why hide in spring Why come-out in July
Compared to the boom-time of June and July, August can be a mite quiet for aphids. But on the plus side, it is when many of our larger species appear on the scene. Few rival the size of the giant larch aphid (discussed elsewhere) but the giant willow aphid is nearly as big, and has a much more spectacular appearance - especially when in vast numbers. We devote all this blog to these aphids because: Tuberolachnus salignus is quite spectacular, it reduces tree growth, it has recently been found for the first time over most of New Zealand, and (last but not least) there are several 'mysteries' surrounding this aphid...
They do look strange - but why?
When examined close-up Tuberolachnus salignus is a weird beastie indeed. Its abdomen has several rows of black sclerotic patches, and is covered with numerous fine hairs, which in good light give it a greyish-golden sheen. There is a large dark-brown thorn-like (or shark fin shaped) dorsal tubercle - in the centre of its back, just in front of the siphunculi which are atop large dark cones.
It is not immediately obvious whether their colour and morphology are cryptic (for camouflage) or aposematic (for warning) - or possibly both! Close-up and in good light the red legs, golden sheen and black tubercles strongly suggest aposematic colouration - possibly warning birds that Tuberolachnus salignus are distasteful.
In poor light or at a distance the effect is surprisingly cryptic. Take, for example, the colony shown below.
Like the giant aphids discussed elsewhere, they seemed to find the base of a dying branch very much to their taste.
Where is Tuberolachnus salignus found - and what is it related to?
It seems the giant willow aphid has a far east Asian origin, possibly Japan, because the only parasitoid known to be specific to it (Pauesia salignae) occurs there. The current distribution of Tuberolachnus salignus was described by Blackman & Eastop (1994, 2006) as being virtually cosmopolitan, apart from Australasia. The exemption of Australasia is no longer valid since Tuberolachnus salignus has very recently been found over much of New Zealand (Sopow, et al., 2014).
The Tuberolachnus genus is defined by the presence of a dorsal tubercle. Apart from Tuberolachnus salignus, there are only two other aphid species in this genus: Tuberolachnus macrotuberculatus and Tuberolachnus sclerata. These are classified in the subgenus Tuberolachniella, and feed on the evergreen shrub Eriobytra, in China and West Bengal respectively.
Basing a classification on a single taxonomic character is always a bit dodgy, and it seems especially so in this case. Blackman & Eastop (1994, 2006) believe that Tuberolachnus salignus (seen below being defended by a southern wood ant) is more closely related to some other Salix-feeding Lachnus species.
For example the little known Indian Lachnus salicis (sadly no photos available) is probably brownish in life and lives in large dense colonies on stems of Salix in Utar Pradesh, India. Like the giant willow aphid, it is attended by ants and no sexual morphs have ever been recorded. Note: Lachnus salicis is thought to overwinter as viviparae in bark crevices (Chakrabati & Raha, 1988). This seems a much more likely relative of the giant willow aphid and should probably be reclassified as Tuberolachnus, even though it lacks the dorsal tubercle.
Why no males - what is its life cycle?
Tuberolachnus aphids have only been found on willow trees from late July through to early March the following year. Numbers tend to peak in October, but by February few are left on the trees and none has been seen in April, May or June. They are said to be very active in January and February when they often wander around off the host. (Natural History Museum, 2011).
Adult Tuberolachnus salignus occur in two forms, wingless and winged. Density is the main factor affecting whether a nymph develops into an aptera or alate, although temperature may also have an effect. The picture below shows an winged giant willow aphid.
There are several possible reasons why aphids cannot be found at certain times of year (in this case during April, May and June):
One is therefore left with the 'mystery' of where the live viviparous aphids go in spring.
Where do they hide in spring - and do they reproduce during this period?
This year we were determined to answer this question, but regular searches throughout spring failed to reveal any aphids. Then in August we found our first colony of giant willow aphid (shown below) - on a branch of a damaged, but young, sallow tree. As usual, the colony was large and contained all stages of development. It had clearly been growing in size for some weeks (or months) - presumably out of sight.
Further examination of the tree then revealed the remains of a colony, still with many young nymphs, residing in deep crevices in split parts of the sallow trunk - where a branch was torn off (either in a gale, or by a passing vehicle). This, we think, is the hiding place of the giant willow aphid.
If our supposition is correct, their walk-about in March is presumably to find suitable damaged branches and bark crevices. They then live deep therein building up their numbers before 'bursting upon the world' in late July or August.
But why should an aphid want to hide itself in spring? After all, this is the time of year when many aphids increase hugely in numbers, often on the growing tips of plants in full view of the world.
Why do they hide in spring - for nutritional reasons, protection or what?
Why they do this is much the most interesting feature of the behaviour. Until appropriate experimental work is carried out, we can only speculate, but there are sufficient clues to at least formulate a working hypothesis.
Let us first address two unlikely possibilities:
Protection from predators offers a more plausible explanation. Specific aphid invertebrate predators are seldom found around Tuberolachnus colonies, albeit occasionally a harlequin ladybird attacks one. However, the colouration of giant willow aphids (cryptic at a distance, aposematic close up) strongly suggests that vertebrate predators may be the main selective pressure acting on their population.
So which vertebrate predators specialize in taking aphids from the bark of a tree? One obvious candidate here is the Eurasian treecreeper (Crithea familiaris). This bird is insectivorous, and climbs up tree trunks like a mouse searching for insects which it picks up with its fine curved bill. The period March to July would be the period of heaviest predation by treecreepers collecting aphid-sized insects for their young. The Eurasian tree creeper ranges from China and Japan across Asia to most of Europe. This is very similar to the 'natural' range of Tuberolachnus salignus, although man has now also spread the aphid to North America, South Africa and New Zealand.
Photo by Pawel Kuzniar
We cannot of course be certain that the common treecreeper was the source of the predation selective pressure. Other insectivorous bird species may also be involved, but the tree creeper does meet all the requirements.
Why do they emerge from concealment in July - is there adequate protection?
If we accept that bird predation may be an important selective pressure favouring concealment early in the year, why do these aphids emerge to face the world in August? One explanation is that spring hideaways become distinctly unhygienic with honeydew accumulation, and mould - even if ants are removing some of it. More importantly, predation pressures probably decline as once the nestlings fledge and disperse - and numbers of potential mutualists (wasps and ants) build up in numbers.
This assumes that the mutualists are successful in defending these aphids against predators. Wood ants are known to protect aphids from invertebrate predators, but are they as effective against birds?
The image below shows several southern wood ants tending a large colony of giant willow aphid on Sallow in October.
Aho (1997) carried out a study on the behavioural responses of Eurasian treecreepers, Certhia familiaris, to competition with ants. Wood ants share the same habitat as the treecreeper, and also feed on invertebrates on tree trunks. The Finnish researchers found that treecreepers spent a shorter time searching on spruce trunks visited by ants. They ascribed this to the fact that where the ants have been foraging there were fewer arthropods. But if there were large numbers of ants on spruce tree trunks, this was almost certainly because the ants were tending Cinara aphids on the trees. These would have been protected from the bird predators, whether because of shortage of other invertebrates (Aho's hypothesis) or direct irritation of the birds by the ants (our complimentary hypothesis).
Despite the presence of large quantities of honeydew colonies are not always ant attended, especially late in the season. Many years ago, Buckton (1876) recorded the behaviour of aphids when there were no ants to remove honeydew droplets. He reported that "if [the droplet] is not quickly withdrawn by an attendant ant ... it is projected by a peculiar jerk to a considerable distance". This ejected honeydew then attracts wasps and other honeydew feeders.
The two images above show social wasps (Vespula vulgaris left and Vespula germanica right) gleaning (collecting) the aphid honeydew from leaves beneath a Tuberolachnus salignus colony. Unlike ants they do not collect the honeydew directly from the aphids. However, Letourneau & Choe (1978) point out that honeydew foraging of bees and wasps involves various types of behaviour, ranging from little or no contact with Homoptera to displays of active herding and guarding, which would make this a mutually beneficial relationship - much as that between ants and aphids. Certainly the swarm of wasps around some colonies would dissuade some mammals (such as man) from approaching.