Elder aphid networks

The photo above shows a dense colony of Elder aphids, Aphis sambuci, many individuals of different ages feeding close together. They are likely to be all a clone, female descendants of a single founding female that emerged from an egg early in spring, and identical genetic copies of her. Elder aphids forms this characteristic ash grey patches on tender elder stems. The aphids suck the elder sap using their piercing mouthparts. Having a close look at elder aphids gives you an opportunity to learn to learn about ecological networks in a few minutes of observation. All the photos in this post were taken in the space of seven minutes this morning on my way to work on the same young elder bush.

 Despite the fact that elder, Sambucus nigra, has relatively few insect predators, most likely due to it having cyanogenic chemicals in its leaves, elder aphids are an important link in networks making use of elder sap. 

Ants have a mutualistic relationship with the aphids. They benefit from the aphids honeydew by soliciting them to excrete it, taping them with their antennae. The sugary rich liquid is consumed by the ants and their larvae. The ants treat the aphids as their domestic animals. The aphids benefit too, as potential predators or parasites are pursued or attacked by the ants.

But the ants can't totally defend the aphids from their numerous predators. Here a female hoverfly, Epistrophe eligans, lays eggs on a patch of elder aphids.

A hoverfly egg is visible on the centre of this photo, on the edge of the aphid colony.

See the patches cleared of aphids in this patch? They are due to predation by the green hoverfly larvae just visible amongst them. Surrounded by food, the larvae will gorge on the aphids and grow rapidly.

This hoverfly larvae (possibly Epistrophe eligans) is likely to be ready to pupate.

Not only hoverflies, ladybirds are attracted by this aphid bonanza and adults land on the elder, possibly attracted by the smell of aphids. A Harlequin sunnies itself on a leaf...

...while an active 2 spot searches about.

Ladybirds have laid their bright yellow egg clutches on or under the leaves, near the aphid colonies.

...here visible on the background. I couldn't find any ladybird larvae today on this elder. 

This fly enjoyed licking the honeydew on a leaf. Some species of butterflies, like the Speckled Wood, also takes advantage of honeydew.

Five species (2 ladybirds, a fly, an ant and a hoverfly) thriving on elder aphids. If I had waited a bit longer, or being a bit luckier, I could have witnessed tiny parasitoid wasps that lay their eggs inside the aphids and eat them from the inside!

Waking up to served breakfast

 I ventured out to the garden today despite the wind and occasional shower. Plants are starting to awaken: leaves sprouting, two daffodils about to open and a single bowed down Hellebore flower. 7 spot ladybirds like to hibernate between the waterproof leaves of the spurge and today the bright sun woke some of them up. They must have felt very lucky, as colonies of aphids were sitting on the very same shoots. I didn't see any eat aphids, in fact the aphid in the photo below was sitting on the ladybird's head just before I took the shot. But give them time and the spurge might be cleared up of aphids. Something I found surprising is that the aphids are reproducing, and it is february, weren't they supposed to be eggs at this time of year?

Ants tending aphids

Ants have a sweet tooth. They gather nectar from flowers, buds and nectaries but also farm animals to obtain their sweet honeydew. These farmed animals are scale insects and aphids. Ants tend the aphids (above), protect them from their predators and parasites and keep them together for easy "milking". To obtain the honeydew produced by aphids, ants stimulate them with their antennae, after which the aphid will secrete a droplet of sugar rich liquid. These ants are tending groups of aphids on an Iris leaf. To soften the built-in flash light I put a piece of kitchen paper in front of it, holding it with my left finger.

Dropping aphids and their alarm pheromones

Fortunately for the organic gardener, aphids have many predators: hoverfly larvae, lacewings, ladybirds, shield bugs and spiders eat them in numbers. Although aphids appear defenceless against their predators, they have evolved a suite of antipredator responses. Some aphids have warning coloration and sequester chemicals from their feeding plants that are distasteful or toxic to their predators, other release toxic chemicals or waxes and a few have a hard-skinned soldier caste to defend the colony, yet others maintain an army of ants that defend them. The most common form of defence - both against predators or parasitoids - is however, behavioural: the aphids move away or drop from the leaf they are feeding on when they sense an approaching predator.
 Dropping is very effective in reducing immediate risk: aphids fall away from the approaching danger onto the ground. Once there other costs become apparent: the aphid may be far from the host plant and is exposed to ground predators or to desiccation.
 The orange tree in my conservatory is infested with aphids. I took advantage of the abundance of 7 spot ladybirds in the garden and brought a few onto the tree, placing them on particularly infested branches. I was pleasantly surprised by the eagerness with which the ladybirds took to the intended job. They started munching aphids straight away, clearing whole shoots in a few minutes. After a little observation, however, it became apparent that it was the aphid's behaviour which was mostly responsible for the shoots being cleared. The undisturbed aphids sat motionless, on a living carpet feeding on the tender leaf sap nearby. In contrast, as soon as a ladybird attacked, the aphids on the same leaf came alive and some started to move away, going into another leaf, while many aphids dropped to the ground as the ladybird fed on their unfortunate siblings. The following two photos illustrate this. They were taken about 27 seconds apart. In the first one, notice the three aphids on the tip of the leaf. In the second photo, these aphids have dropped to the ground, leaving just a couple of aphid molts stuck to the leaf tip, while the ladybird is still feeding on an aphid, motionless.

 Ladybirds are very effective at eliciting the drop response from aphids, especially when compared to smaller, less energetic feeders, as demonstrated in experiments by John Losey and Robert Denno on pea aphids feeding on alfalfa exposed to a predator insect.

This means that on average 60% of aphids feeding on a plant stem dropped to the ground when a 7 spot ladybird (Coccinella septempunctata) was introduced, in sharp contrast to the lower dropping response to the bugs and the control. Given the higher mortality of aphids on the ground, it follows that ladybirds would be very effective clearing aphid infestations through direct predation, and their indirect effect on aphids dropping from the plant.
 What mechanisms are responsible for this dropping behaviour? or, put differently, how do aphids sense that a predator is approaching? Dropping behaviour happens in response to predator contact, vibrations generated by the predator, or in response to an alarm pheromone secreted by individual aphids when attacked. This chemical signal, (E)-ß-farnesene (EBF), is secreted in dropplets by the cornicles, little tubes at the rear of the aphid, and they may impregnate the predator, which in its next move will elicit the dropping response before actually attacking another aphid.
 The release of an alarm pheromone by an individual that is likely to be eaten by a predator seems paradoxical. What benefit can this individual gain from its production? An alarm pheromone can be adaptive when the benefit is shared by relatives. This is indeed the case in aphids: groups of aphids feeding in close contact are likely to be members of the same clone, that is, they are genetically identical, as aphids often reproduce parthenogenetically. The alarm pheromone also has longer lasting effects benefiting the individual relatives, as the aphids that have been exposed to the chemical tend to produce winged offspring, which will likely disperse away from predators, in the case of the ladybird attacker, they will be likely to avoid the following generation of ladybird larvae.

References
LOSEY, J., & DENNO, R. (1998). The escape response of pea aphids to foliar-foraging predators: factors affecting dropping behaviour. Ecological Entomology, 23 (1), 53-61 DOI: 10.1046/j.1365-2311.1998.00102.x
Schwartzberg, E., Kunert, G., Stephan, C., David, A., Röse, U., Gershenzon, J., Boland, W. & Weisser, W. (2007). Real-Time Analysis of Alarm Pheromone Emission by the Pea Aphid (Acyrthosiphon pisum) Under Predation. Journal of Chemical Ecology, 34 (1), 76-81 DOI: 10.1007/s10886-007-9397-8

Hoverflies to the rescue!

Despite being so early in the year, aphids are already covering the shoots of many plants. I saw my first Episyrphus balteatus of the year today. Basking on the warm, springy sun and then taking an interest in a small rose. I watched her while it flew away and back to the rose, chosing a fresh shoot and then adopting an egg-laying posture. I was surprised, but the camera was ready in my hands. The first one of the year and it was already mated! The hoverfly left and I looked at the rose stem.

 A bright white egg sat surrounded by fat aphids. What a well chosen place! Hopefully the aphid infestation will soon be under control thanks to the voracious hoverfly larvae.

Ants as scavengers and herders

So far I have overlooked two important aspects of garden ant foraging behaviour, mainly due to the lack of suitable photos. Yesterday, I spotted a strange large insect walking on the concrete yesterday, when I got closer I realised it was actually a dead bluebottle being dragged by a garden ant (Lasius niger). Another ant run frantically back and forth, but a single one seemed to do most of the work. The strength of an ant is quite formidable, able to lift or drag objects much heavier than themselves. This illustrates the role of ants as scavengers. Any dead animal will either be dragged to the nest or bits of it will.

The second aspect is one of the most surprising of ants - showing their adaptability -  but also a reason why they are hated by many gardeners: their role as aphid herders. Ants behave as farmers with their aphids and will try to keep the numerous aphid predators at bay as well as milking their honeydew. This is considered a mutualistic relationship and aphids also benefit from the behaviour. Even when aphid predators are excluded, aphids multiply faster in the presence of ants. The photo, taken today, shows two garden ants stimulating Elder Aphids (Aphis sambuci) to excrete their honeydew. Elder aphids form very compact groups on tender growing stems of Elder.

Hoverflies laying

I posted on hoverfly larvae feeding on aphids a few days ago, but I was able to photograph several species laying eggs and thought that deserved a post on itself. My mock orange (Philadephus) has dense aggregations of black aphids and several hoverflies have been laying eggs on the buds and leaves on Philadelphus and Pyracantha. On the top photo Eupeodes luniger. Her swollen abdomen curling to deposit an egg on a bud. She patiently moved from a clump of buds to another, spreading her eggs in the whole bush. The carnivorous, aphid loving larvae that will hatch from these eggs will contribute to keeping the aphid numbers on check.

Syrphus

Epistrophe eligans

And to end the post, just to say that this is a special post for BugBlog: Number 100. I am quite happy to have taken on blogging, and it has been a lot of fun researching the posts. I hope I can mark many more returns for BugBlog in the future.

Greenflies clouds and networks

There were raining greenflies today, whole clouds of them causing a visible effect on people, talking about them, swatting them and taking them from their clothes, glasses and skin (above). The warm weather has encouraged the winged forms of aphids (greenflies) to take to the air and search for new feeding plants. Aphids are a central part complex ecological networks. For example, a study by Muller and coworkers in an abandoned field in the south of England found:

Twenty-six species of plants were attacked by 25 species of aphid which were parasitized by 18 species of primary parasitoids. The primary parasitoids were attacked by 28 species of secondary parasitoids, of which 18 directly attacked the still living aphid (hyperparasitoids) and 10 attacked the aphid after mummification (mummy parasitoids). The aphids were attended by three species of ants.

Only the bean aphid (Aphis favae) is parasitized (or superparasitized) by no less than 12 species of small wasps which lay single eggs inside individual aphids. Some of the wasps, the secondary parasitoids, lay eggs in parasitized aphids. Then the sweet sap produced by aphids is enjoyed by ants, butterflies and bumblebees. Aphids are eaten by lacewings, ladybirds, hoverflies and small spiders; and swifts and swallows who pick them in the air plankton. You could say that the presence of aphids generates a lot of added biodiversity.

This figure taken from the study mentioned earlier summarised the parasitoid network over two years of monthly study. The middle bar represents the different aphid species (each is a number and the length of each section represents the abundance of each species. The bottom bar are the primary parasitoids and the top bar the secondary parasitoids. The conecting lines represent the strength of the interaction between a particular pair of species.
Back at the garden, on the roses newly growing shoot, covered on rose aphids (Macrosiphum rosae) this was beautifully illustrated.

A 7 spot happily munching a rose aphid 

A hoverfly larvae crawling around also eating them. This one seems to be showing off!

A weeks old garden spider has caught a winged one.

A parasitic wasp lurking about in the rose bush. I cannot say it is an aphid parasitoid for sure, but keep surveying the rose leaves, leaving and coming back to another leaf.

There are lots of fascinating things about aphids and they surely will come back to these pages in the future.

More information

Muller, C., Adriaanse, I., Belshaw, R., & Godfray, H. (1999). The structure of an aphid-parasitoid community. Journal of Animal Ecology, 68 (2), 346-370 DOI: 10.1046/j.1365-2656.1999.00288.x

Predator and prey

The sure destiny of many aphids these days is to end up as an ladybird meal

In the last couple of weeks, the number of ladybird larvae in the garden has increased noticeably. All sizes from tiny newborn larvae to full sized, ready to pupate ones are found on a large variety of threes and shrubs in which, so far, aphids were happily eating and reproducing. Most of these larvae are Harlequins, the new invasive ladybird with generalist feeding habits. I have mixed feelings for this species. On the one hand, as I already wrote in another post it is quite invasive and could compete and affect adversely native ladybirds. On the other, given that we do not use pesticides in our garden the Harlequin aphid-munching could mean I have some nice cherries to eat in a couple of weeks time. I am not for demonising invasive species or believing gloomy, apocalyptic scenarios relating to them. It is us humans who put them here in the first place. The Harlequin was used to control greenhouse aphids and scale insects (biological control gone wrong, again!) and I get the feeling it is here to stay. Lets hope for the best regarding our native ladybirds and enjoy the Harlequin as the beautiful insect it is.

Tiny larvae

Fully grown larvae

Ladybird pupae

A shiny recently emerged Harlequin considering its meal