Ants as farmers, aphids in the slow lane

If you grow soft fruit such as currants or gooseberries, you are probably familiar with the sight of numerous aphids densely clustered around the stems, making the leaves wrinkled and deformed. You may also be aware that some ant species 'farm' aphids in order to consume the sugar-rich 'honeydew' that they excrete. However, this is a complex behaviour and so is worth a closer look.

A colony of Aphis schneideri on black-currant Ribes nigrum, attended by black garden ants Lasius niger

First of all, there are numerous aphid species that are found on cultivated fruits, and they can be difficult to tell apart. Those in the photo above are on black-currant Ribes nigrum - within the Ribes-feeding group, only one species has long, acute, erect to semi-erect hairs on the antennae (especially near the base), and that is what is seen here, Aphis schneideri (I couldn't get a clear photo of the antennal hairs, so you'll have to trust me on that). A. schneideri is also commonly associated with R. nigrum, causing clusters of terminal leaves to fold and distort, and the aphids are grey-green, with paler legs and often with a scattered coating of small pale waxy particles.

The ants seen attending the aphids here are the common black garden ant Lasius niger. Not all colonies of L. niger do this, although when it occurs, there is mutual benefit - the ants obtain sugar-rich honeydew and in turn protect the aphids from predators. So far, all straightforward, but exactly how the ants do this was not understood until a few years ago. It has been known for some time that, in order to ensure a dense crop of aphids, ants limit their dispersal (aphids otherwise disperse to new plants when overcrowded, the production of winged forms being triggered by the frequency of contacts between individuals) by biting off their wings (Kunkel 1973) or by secretions from the ants' mandibular glands interfering with the development of winged aphids (Kleinjan & Mittler 1975). Conversely, ants have been seen carrying aphids to suitable, good-quality host plants within their nest's home range. However, aphids also disperse by wandering (which may be more prevalent than dispersal by flying) and some decades ago, both Banks & Nixon (1958) and El Ziady (1960) noticed that the presence of ants seemed to slow aphids down, but no further research was undertaken until Oliver et al. (2007).

Ants are known to lay 'semiochemical' trails by touching glands onto the surface of their substrate, and these chemical marks can lead others from their nest sources of food (Hölldobler & Wilson 1990). Such chemicals can also be applied passively through shedding of cuticular hydrocarbons and this is important recognising nest-mates and, possibly, home-range territories (Devigne & Detrain 2002). Moreover, other insects, including herbivores and aphid predators, have  been found to respond to chemicals that indicate the presence of ants (Offenberg 2004). However, Oliver et al. (2007) found that these ant chemicals had a tranquilising effect on aphids, causing them to walk more slowly and thus - as with the other effects noted above - maintain higher densities which provide the ants with more honeydew.

Although ants have been seen deterring aphid predators such as ladybirds, this does not mean that the mutualistic arrangement is entirely positive for the aphids. Their manipulation by ants means that their dispersal is reduced (or at least delayed) which may have impacts on the wider population (or 'metapopulation') and increase competition between closely packed individuals. Also, dense aggregations may be repeatedly attacked, and sometimes wiped out, by specialist parasitoids which are able to evade ants, such as the small parasitic wasp Lysiphlebus cardui (Weisser & Völkl 1997). Lastly, ants are occasionally seen eating aphids and it appears that this primarily occurs when individual aphids are encountered away from the aggregation. Not only would this prevent aphids being used for the benefit of rival neighbouring ant nests, but presumably produces an evolutionary pressure to 'obey' ant chemical cues rather than be able to avoid the tranquilising effect.

A Lasius niger individual at a colony of Aphis schneideri

So, definitely a more complex story than it initially seemed (isn't it always!), but also a more interesting one, and something you may be able to witness in your own garden. If you are interested in identifying aphids, a standard work covering British Aphidini (the 'tribe' including the genus Aphis) is Stroyan (1984), but be warned - this is not an easy group to identify to species level, and the separation of some species can be uncertain.

References

Banks, C.J. & Nixon, H.L. (1958). Effects of the ant, Lasius niger L., on the feeding and excretion of the bean aphid, Aphis fabae Scop. Journal of Experimental Biology 35: 703-711.
Collins, C.M. & Leather, S.R. (200). Ant-mediated dispersal of the black willow aphid Pterocomma salicis L.; does the ant Lasius niger L. judge aphid-host quality? Ecological Entomology 27: 238-241.  
Devigne, C. & Detrain, C. (2002). Collective exploration and area marking in the ant Lasius niger. Insectes Sociaux 49: 357-362.
El Ziady, S. (1960). Further effects of Lasius niger L. on Aphis fabae Scopoli. Proceedings of the Royal Entomological Society A 35: 30-38.
Hölldobler, B. & Wilson, E.O. (1990). The Ants. Harvard University Press, Cambridge, MA.
Kleinjan, J.E. & Mittler, T.E. (1975). A chemical influence of ants in wing development in aphids. Entomologia Experimentalis et Applicata 18: 384-388. 
Kunkel, H. (1973). Die Kotagabe der Aphiden (Aphidina, Hemiptera) unter Einfluss von Ameisen. Bonner Zoologische Beiträge 24: 105-121.
Offenberg, J. (2004). Evidence that insect herbivores are deterred by ant pheromones. Proceedings of the Royal Society B 271: S433-S435.
Oliver, T.H., Mashanova, A., Cook, J.M., Leather, S.R & Jansen, V.A.A. (2007). Ant semiochemicals limit apterous aphid dispersal. Proceedings of the Royal Society B: Biological Sciences 274: 3127-3131.
Stroyan, H.L.G. (1984). Aphids - Pterocommatinae and Aphidinae (Aphidini). Homoptera, Aphididae. Handbooks for the Identification of British Insects 2(6): 1-232.
Weisser, W.W. & Völkl, W. (1997). Dispersal in the aphid parasitoid, Lysiphlebus cardui (Marshall) (Hym., Aphidiidae). Journal of Applied Entomology 121: 23-28.

After the rains and beyond the pale...

...or 'from floods and the 2012 wildlife apocalypse to meadow creation via the wordy worlds of genetics and biochemistry'.

If you've been in the UK during the middle of 2012, you will have noticed that it's been raining a bit. Well, I say 'a bit', I actually mean a lot. Really a lot - following an unusually hot spring, it was wet from April to mid-July, including the wettest April for a century, and the wettest June on record. It's well understood that this was because the jet stream looped south of the UK and stayed there, but what is less well known is why this happened - this is an area of active research (including links to climate change) and there is an excellent summary here.

It has also been widely reported in both national and local media (e.g. here and here) that this unusually lengthy and heavy rainfall has had a huge impact on British wildlife - some species such as ringlet (Aphantopus hyperantus) butterflies (which breed in damp grassy areas) can do well in wet conditions, but current predictions are that 2012 will be the worst year on record for British butterflies overall. Volunteer recording will be hugely important in determining the effects on this group and there is still time to join in with the Big Butterfly Count which runs until 5th August. Although slugs and snails have done well (much to the annoyance of gardeners and vegetable growers), winged insects (including those most eseential of pollinators, bees) have fared poorly, being unable to feed or find mates effectively in cold, wet conditions and therefore are also unable to reproduce successfully. Although some mollusc-feeders may have plenty of food, this may well not lead to a good year for amphibians as the hot spring dried up breeding ponds and the April rainwater was too cold for reproduction. Thus, despite a few winners, the effect has largely been an overwhelmingly negative one e.g. many birds have been unable to keep chicks warm and fed, while many species, such as puffins, have seen nests flooded.

A pair of common garden snails Cornu aspersum (often known as Helix aspersa)

With widespread breeding failures, local extinctions have been predicted and conservationists are rightly worried about how severe the impacts will be, especially as the summer of 2011 was also poor. However, with the weather changing to become hot and sunny about a week ago, hopes for a good late summer and autumn have been fuelled, and I have to wonder to what extent various species can make up for lost time while conditions are suitable. Certainly my own observations, and those of other naturalists I've been in contact with, suggest that there is currently a rapid burst of invertebrate adult emergence, including species usually encountered earlier in the summer. Some moths which have emerged late have been reported as unusually pale, although this is from a fairly small number of observations, so its importance remains unclear. Delayed moth emergence related to temperature is well documented (e.g. DuRant 1990) but there does not appear to be any mention in the literature of aberrant colouration due to such delays. Certainly, a pale colour does not suggest an adaptive response as darker colours are generally associated with cooler temperatures as they permit more rapid warming by absorption of solar radiation. So, my question is whether delayed emergence can lead to paler colouration through some effect on the mechanisms related to pigmentation. Although this idea is somewhat speculative, two possibilities (which are not mutually exclusive) spring readily to mind:

1. Delayed emergence affects the mechanism of pigment production.
2. A longer period as a pupa means energy reserves become depleted and less essential material (such as pigments) is metabolised to enable emergence to be postponed during unfavourable conditions.


Looking at pigment production, some relevant research has been undertaken by Sawada et al. (2002) who looked at the expression of an mRNA-encoding guanosine triphosphate-cyclohydrolase I (GTP-CH I), the first key enzyme in the synthesis of pteridines during pigment formation in the wings of the butterfly Precis coenia. The biochemical details are not important here, but the key result was that gene expression was strongest one day before butterfly emergence. So, if pigment production is timed to peak around emergence, could a delay lead directly to reduced pigmentation? From this example, I have to say that it doesn't appear so - the onset and duration of gene expression appears to be controlled by the decline in the ecdysteroid hormone 20-hydroxyecdysone (linked to moulting and metamorphosis and usually called 20E), and a short delay in emergence simply led to a later peak in expression such that pigmentation and emergence remained synchronised. It is still possible that low temperatures prevent pigment formation though this implies the retention of higher levels of 20E and/or one of more effects elsewhere in the chain of biochemical processes involved. Essentially it seems that no-one knows if such effects occur.

Moving onto pigment breakdown, I'll stick with pteridines as there are a number of other pigment groups and I want to keep this at least reasonably simple. However, as Watt (1967) shows, the pteridine pathway is anything but simple, which in turn means that there are many points at which it might be disrupted, and as above, there is no indication that anyone has looked at the effects of delayed emergence on pigmentation, including the breakdown of pigment compounds.

So, although this has been a somewhat limited look at possible pigmentation effects, it has at least shown that it is an area where future research is needed. However, this does not mean that there is no every-day or real-world relevance here. Coming back to the 'volunteer' aspect mentioned earlier, it is not just recording that is needed, but habitat creation - in particular, the small-scale improvements that anyone with a garden can make (or indeed councils who own open spaces) by cultivating more-or-less natural 'meadow' areas rather than ecologically sterile mown lawns. Our garden is not large but it does include a meadow patch with scabious, bird's-foot trefoil, clovers, meadow clary, cornflower, lady's bedstraw, knapweeds and others. Not only is it more interesting and attractive than a billard-table lawn, but it has been a haven for flying insects throughout the wet summer - I have still identified around 25 bee species alone this year, with flowers being used during even the briefest of lulls in rainfall, and very actively during genuinely warm conditions. Also, you don't have to be an expert/experienced entomologist, botanist or gardener to do this. Wild flowers are in fashion at the moment (let's hope they stay that way rather than gravel, paving-for-parking and swathes of decking) with thoughtful gardening writers and TV presenters such as Sarah Raven promoting this important subject, including easy how-to guides if you want a garden meadow - and this means that garden centres and plant nurseries are likely to be well-stocked with native insect-friendly species. If you do this, not only will invertebrates reap the benefits, but so will you.

The bee Andrena flavipes on white clover during the wettest summer on record.

References

DuRant, J.A. (1990). Influence of temperature on spring emergence of European corn borer moths (Lepidoptera: Pyralidae). Journal of Agricultural Entomology 7(3): 259-264.

Sawada, H., Nakagoshi, M., Reinhardt, R.K., Ziegler, I.& Koch, P.B. (2002). Hormonal control of GTP cyclohydrolase I gene expression and enzyme activity during color pattern development in wings of Precis coenia. Insect Biochemistry and Molecular Biology 32: 609–615.

Watt, W.B. (1967). Pteridine biosynthesis in the butterfly Colias eurytheme. Journal of Biological Chemistry 242(4): 565-562.

Lovely local longhorns

In Britain there are approaching 4,100 species of beetle and some of the most attractive and charismatic of these are the longhorns (Cerambycidae) known for their large size, bright patterns and long antennae. However, although some are strikingly coloured (such as the yellow and black Rutpela maculata), many are actually more sombre blacks and browns. One such species is the 'tawny longhorn' Paracorymbia fulva which I have found at three nearby locations during the last week or so, including my back garden.

Paracorymbia fulva

As you can see, it has yellow-brown elytra with black cut-off tips and is also otherwise black. It is very similar to male Anastrangalia sanguinolenta but has a pronotum wider than it is long and with rounded sides (in A. sanguinolenta the pronotum is more slender and less rounded), is 9-14mm long (excluding appendages) and is found in the adult stage between June and August. P. fulva is also interesting for a number of reasons.

Firstly, it is generally described as being associated with broadleaved woodland (e.g. Duff 2007a), but observations suggest that its habitats are more diverse than this. For example, my three recent sightings have been in a suburban garden, rough trackside vegetation and woodland edge while Michael Darby (in Wright 2011) reports that it is associated with chalk grassland in Wiltshire without any woodland or fallen timber.

Secondly, it is considered 'Rare' in the UK as it is listed as a Category 3 Red Data Book species (again e.g. Duff 2007a), but observations by mant recorders suggest that it is more common than this, even if still mainly associated with central and southern England. More widely, it is found across most of Europe, except the north and Turkey (Hoskovec & Rejzek 2007). Given that the northern limit is likely to be due to temperature, its expansion in the UK may be another example of a species spreading due to climate change.

Thirdly, no-one knows what it feeds on - or much else about it. This may seem surprising, and in some ways it is - as Martin Rejzec says in Wright (2011), P. fulva is one of the few remaining European species which has an unknown host plant, a larva that is completely undescribed, and an unknown life history. However, he goes on to explain that this may also be because, unlike most other longhorns, it does not develop in timber; instead it might do so in the underground parts of trees or shrubs, and the larvae may even be free-living in the soil, feeding for example on fungi. Whatever the case, it is clear that this is a species where there is clear opportunity for significant gains through targeted study and research, and as it is now more common in the UK, there may be a greater chance that this will happen.

If you are interested in longhorns in the UK, I strongly recommend acquiring a copy of Duff's excellent illustrated guide (2007, b) which will help you become familiar with this fascinating family of beetles.

A reminder that many longhorns are colourful, Rutpela maculata (sometimes placed in the genus Strangalia)

References

Duff, A. (2007a). Longhorn beetles: Part 1. British Wildlife 18(6): 406-414.
Duff, A. (2007b). Longhorn beetles: Part 2. British Wildlife 19(1): 35-43.
Hoskovec, M. & Rejzek, M.(2007). Paracorymbia fulva (De Geer, 1775). Cerambycidae. [accessed 19/07/2012].
Wright, R. (2011). Paracorymbia fulva - further information received. Beetle News 3(3): 6.

From loofahs to LEDs

I've been a bit quiet on the blogging front over the last couple of weeks - partly due to having too many assignments to mark and partly because the unusually wet weather has tended to keep me from doing much in the way of field ecology (this amount of rain is not good for most British terrestrial invertebrates). However, yesterday was the first dry day for a while and happily coincided with a wildlife walk I was due to lead for the Southampton Natural History Society.

We visited a conservation-friendly farm and the event provided an opportunity to record mainly invertebrates, but also anything else of interest that we came across - given the weather (and climate change links which I probably won't write much about here - other bloggers will be doing so) and the huge negative impact expected to be seen on British wildlife, records such as these are of great importance, especially when there is so little funding for professional survey work.

As it happens, we did see a reasonable diversity of invertebrates, though only in small numbers, and those that were numerous tended to be associated with wet or at least damp conditions (e.g. molluscs, woodlice, millipedes). One of these was the slime-mould Stemonitopsis typhina...

One of several clusters of Stemonitopsis typhina.

Just as one of my recent posts focused on a slime-mould that looked like a cluster of tiny loofahs, this species reminds me of little pearly-silvery LEDs. Each of the stalked sporangia is about 3-4 mm tall with a black stalk that is no more than half the overall height. Fresh specimens like this are silvery, but can become more lilac-grey with age. It is superficially similar to some of the more cylindrical species and forms within the genus Comatricha (e.g. the uncommon cylindrical form of the usually globular C. nigra) but can easily be separated by the presence of a silvery sheath around the stalk - here this is clearly visible as a pair of pale longitudinal lines running up either side of each stalk, although it actually goes all the way round but is translucent and the stalk shows through. S. typhina is a common and widespread species found on wet, rotten wood, usually of broad-leaved trees, and this example was found (along with several similar clusters) on fragments of sodden and well-rotted willow wood around the base of an old willow tree. A common, if unfamilar, example of the importance of dead wood habitats - more wet-summer observations here soon...

Twenty bees and counting

I've written on a few occasions about insect-friendly gardening and farming, and sometimes focused on a single species that has been attracted such as my recent observation of an unusual specimen of the wool-carder bee. I'd noticed that the combination of pollinator-friendly planting and the provision of habitat features such as bee-logs, so having seen a few more species yesterday during a welcome sunny patch, I decided to look through my list of garden species records for 2012 so far. I knew there was fairly good bee diversity in our garden, but was pleasantly surprised to find that I have already identified 20 species this year, with some others remaining unidentified so far. So, though the English drizzle has returned today, I thought I'd celebrate by sharing a few of these species...

First of all, a quick look at one of the species that has definitely made good use of the insect hotel I built in time for spring this year, the red mason bee Osmia rufa.

Bee-log with pre-drilled tunnels filled by Osmia rufa cells and sealed with mud.

Osmia rufa exiting a tunnel in the bee-log.

O. rufa is well-known to bee-friendly gardeners as it often entirely takes over artificial bee nest-boxes in the same way as it has used the bee-log above. It occasionally causes concern due its habit of burrowing into soft mortar between bricks, but is rarely if ever a problem. If you watch carefully, you can even see the females using special prongs on their faces to tamp the mud into position after bringing it to the nest as pellets held in their mandibles.

The second is a very different species, the parasitic bee Nomada marshamella.

Nomada marshamella posing helpfully on my finger.

N. marshamella is one of the commoner species in this genus of parasitic bees, and this specimen was seen crawling in through an open window. Like other Nomada, it is an effective wasp mimic, looking more wasp-like than bee-like, and can be confused with N. goodeniana (including by me, though courtesy of Nick Owens, I now know that they can be separated by the colour of the wing-base or 'tegula' - orange here as opposed to bright yellow). It is a parasite of the common mining bee Andrena carantonica (and possibly the rarer A. trimmerana), though interestingly none of those that I have so far recorded in the garden (which doesn't mean they aren't there of course). This is also a good point to plug the excellent BWARS (Bees, Wasps and Ants Recording Society) website, including a very fine photographic gallery.

Finally (I'm being relatively brief today), I'd like to introduce my 20th garden-bee identification of the year so far, a female Osmia caerulescens (I originally thought these photos were of Lasioglossum morio which has also been recorded here - thank you again to Nick Owens for letting me know).

Osmia caerulescens female approaching Lotus corniculatus flowers, tongue at the ready...

Osmia caerulescens female on Lotus corniculatus flower - note the blue-green metallic sheen and pale hairs.

This small bee is widespread and common (I'm pretty sure it's been using the garden for a while but I hadn't managed to get a close enough look), and feeds from a wide range of flowers. Females nest in existing holes such as in dead wood, including fence posts, and masonry (we have plenty of both) where it closes the hole with a plug of chewed leaves, and is well-known from both gardens and woodland edges.

So, just three of 20, but I hope they provide a little inspiration if you are thinking about planting bee-friendly plants and other garden features - for example, we have a small patch of open sand created to encourage invertebrates that like this sort of thing; it is possible to create a diverse habitat structure even in a tiny rectangle of Britain like ours. The list so far is below and I expect to identify more, especially as I have plenty of hosts with no parasites and parasites with no hosts...

• Bombus terrestris
• Anthophora plumipes
• Apis mellifera
• Bombus lapidarius
• Andrena haemorrhoa
• Osmia rufa
• Bombus hypnorum
• Bombus pascuorum
• Nomada flava
• Lasioglossum calceatum
• Lasioglossum morio
• Bombus lucorum
• Colletes daviesanus
• Sphecodes monilicornis
• Hylaeus communis
• Andrena flavipes
• Anthidium manicatum
• Hylaeus confusus
• Andrena labialis
• Osmia caerulescens
• Nomada marshamella

Wandering wool-carder?

One of Britain's most spectacular bees (in my opinion at least) is not a bumblebee, but the wool-carder bee Anthidium manicatum, one of the Megachilinae which includes the leaf-cutters. So, when I saw one basking on a Geranium leaf during a welcome burst of sunshine a few days ago (it then moved onto common bird's-foot trefoil Lotus corniculatus), I had to take a photo - however, when I looked more closely, it was almost, but not quite, as I expected.

The wool-carder bee Anthidium manicatum

At first glance, it looks much like any other individual of this species, however the yellow markings are far more strongly developed than is usual for a British specimen - they are usually spots to the sides of the abdomen with some in the midline and partially joined to form weak bands on the rear segments as shown in many books including Baldock (2008). A clearly striped individual like this is more like a continental European specimen - indeed, an experienced hymenopterist from BWARS remarked that he had never seen an individual like this in Britain. So, is this just an aberrant specimen, or - and I shall speculate a little - might something else be happening?

In Britain, A. manicatum is only locally common in the south, especially SE England, and becomes scarcer as you look further north. Until 1993 it was scarce even in the SE, after which it began to expand its range (Edwards, 1997) and become common is some southern locations. This suggests that temperature is a key factor in its distribution and to me indicates that this is one of many invertebrate species expanding it range as a result of climate change. Its common name of 'wool-carder' referes to its habit of shaving the hairs from downy plant leaves (such as Stachys) in order to line its nest - possibly a behavioural adaptation to provide insulation due to a requirement for high temperatures.

Considering the colour pattern, this specimen (like those in continental Europe) clearly seem to display wasp-mimicry, while typical British specimens do not, or at least only weakly. This would be a clear defensive adaptation, so why do British specimens tend not to show it? One possibility is that the relatively dark colouration permits more rapid warming when basking  - certainly this individual was also vibrating its wings at intervals, a typical insect behaviour used to warm the flight muscles. If, further south in Europe, this aid to warming is outweighed by the benefits from defensive mimicry, then the clearer stripes might be an advantage. This leads me to consider three possibilities:

1. This is an aberrant individual with no further significance.
2. It is a vagrant continental individual.
3. It is a British individual and increased temperatures are selecting for stronger stripes.

Of these, #3 is the most interesting but also the most speculative and there is no way of knowing from a single sighting. However, I intend to watch closely - males are highly territorial (and may kill other bees) so might use the garden regularly - and would be interested to hear from anyone else who has seen a specimen like this in Britain.

Anthidium manicatum basking on common bird's-foot trefoil Lotus corniculatus

References

Baldock, D.W. (2008). Bees of Surrey. Surrey Wildlife Trust, Woking.
Edwards, R. (ed.) (1997). Provisional Atlas of the Aculeate Hymenoptera of Britain and Ireland. Part 1. BWARS/BRC, Huntingdon.