Banking on bees

Much has been written about the importance of sunny banks for invertebrates - they are often included (sometimes as 'beetle banks') in habitat management plans and as sometimes appear as recommended features related to mitigation of various types of site development. There is much about this and other aspects of habitat management for invertebrates in e.g. the excellent Kirby (2001), but I want to focus on a local example of a feature that has just this function, albeit unintentionally - a south-facing bank alongside the footpath leading to the front of a nearby church in Hampshire, southern England.

The south-facing bank in a nearby churchyard

This is not a huge feature - it's around 10 metres long and no more the around a metre high at most (as the path rises, the bank gets lower until it merges with the rest of the churchyard). However, there are nearby flowers as pollen sources, plus small bare patches of light soil, just right for burrowing. It is also south-facing and hence sunny and warm - this is key as the north-facing slope on the other side of the path does not support the range of pollinators described below. A couple of days ago, these were found and photographed during less than an an hour on a sunny day in what is currently proving to be an unusually warm spring (I'll leave out discussion of climate change on this occasion). So, what did I find?

The bee-fly Bombylius major

The commonest bee-fly in the UK, B. major can be identified by its broad, dark wing-bands (not to mention the long proboscis characteristc of this gorup) and parasitises a number of solitary bee species - so, as well as being a herald of spring, it's also an indicator that there are bees around somewhere. However, in this case, a indicator of bee activity wasn't needed - I just needed to look at the grassy bank to see a flurry of activity.

Andrena cineraria - an attractive black and white ground-nesting species

The most obvious bee species was A. cineraria - I spotted around 15 at one time (it's difficult to be more precise as they rarely stop flying around), including some using entrance holes to burrows, plus brief 'tussles' between pairs of individuals. In some places, this species nests in huge aggregations of thousands of females and attendant males (Baldock, 2008) and I wonder if these 'tussles' are aggressive encounters related to access to nest-burrows, or are failed mating attempts - they are too fast to be certain about the sex of the participants. Of course, where one species is found, its parasites often follow - in this case the cleptoparasite Nomada lathburiana which can be very numerous in the large aggregations mentioned above. Cleptoparasites are also known as 'cuckoo bees' as they lay their eggs in nests of other bee species, their  larvae feeding on the food provided for the host larvae. Needless to say, I was on the lookout for N. lathburiana and it wasn't long before I saw one investigating the entrances to A. cineraria nests.

Nomada lathburiana showing the yellow spots and bands seen in several species of this genus.

However, although this was an interesting find, there were other bee species, including a small (aroung 6mm long) fairly dark bee that was extremely difficult to photograph due to its rapid darting flight and tendency to re-launch whenever I got near. However, I did manage to get a shot and it turned out to be another cleptoparasite, N. flavoguttata.

Nomada flavoguttata - note the reddish-brown bands on the abdomen, including a pair of tiny yellowish dots (the species name means 'yellow spots').

Although possibly not that familiar, this is a fairly common species which parasitises several small Andrena species. This is important because at this point I hadn't seen any small Andrena, only A. cineraria, so I continued looking. Then, among the flurry of black & white bee bodies, I noticed a likely candidate - a small bee crawling around under the leaf litter. Again, photography was tricky as, when on the ground, it crawled underneath leaves, and flew rapidly away as soon as it emerged - definitely camera-shy! However, I did get the following picture, and (from other views, including while feeding on dandelion Taraxacum flowers) enough detail to identify it as A. minutula, the commonest of several similar species and a known host of N. flavoguttata.

Andrena minutula crawling underneath leaves.

Two host-parasite pairs was good for an hour's work, but there was more bee-biodiversity to be found as I saw another Andrena species exiting a burrow.

Andrena flavipes flying away from its burrow

A. flavipes is identified by the pale abdominal hair-bands and orange-yellow pollen-hairs in the hind tibiae, and like A. cineraria, can be found in large nesting aggregations. It also has its own cleptoparasite, N. fucata although I could not find this although it is present at almost all of its host's nest sites - more hunting will be required.

So, I hope these observations have reinforced the importance of sunny banks as invertebrate habitat - including for our often-declining, yet essential, populations of pollinators. If you have a little spare space in your garden or another piece of land, why not add a little bank - even a small one will attract invertebrates.

An insect's-eye view of the bank with A. cineraria flying overhead.

References

Baldock, D.W. (2008). Bees of Surrey. Surrey Wildlife Trust, Pirbright.
Kirby, P. (2001). Habitat Management for Invertebrates: a Practical Handbook (revised reprint). RSPB, Sandy.

Keep feeling fasciation

Apologies for the terrible 1980s music pun - if you don't know what I'm talking about, Wikipedia will explain... Anyhow, today's topic is fasciation - the flattened expansion of plant parts into flattened bands or ribbons, sometimes with multiplication of flower heads (the phenomenon is also known as 'cresting'). Although generally considered rare as a whole, fasciation has been documented in well over 100 plant species in 107 families (Presland et al., 2009), including some very common ones such as the dandelion - often called Taraxacum officinale agg., but in the UK this is incorrect as T. officinale does not occur and there are around 235 species with intermediates and much variability. If you want to investigate this tricky taxonomic area in more detail, see Dudman & Richards (1997).

A common species of dandelion (Taraxacum sp., probably T. subhamatum) showing a fasciated stem with normal stems in the background.

Fasciation is not well understood in all cases, and can be caused by a number of factors - mutation of meristematic cells (i.e. abnormality of the growing tip), bacterial infection (particularly by Rhodococcus fascians), attack by mites or insect attack, or chemical, frost and/or mechanical damage - and in some cases can be inherited. In most cases, a single stem is affected (as in the photo above) and does not recur the following year.

Dandelion showing a fasciated flower-head.

One area where active research has explained fasciation well is the action of the bacterium R. fascians. Infection leads to hyperdosage of plant hormones, especially auxins and cytokinins which it may induce or may produce itself (Vandeputte et al., 2005). Induced overexpression of plant hormones can be complex, involving biochemical/transcription pathways which include genes and their homologues, hormone-inactivating compounds, hormone precursors, cofactors in various aspects of mineral metabolism and so on (Simon-Mateo et al., 2006). The visible effect of this occur by apical dominance being broken and secondary or auxiliary meristems being activated (hence the proliferation of flowers in the second photo).

Other causes are less well understood and may overlap with gall-causing agents in the case of mites and insects, while R. fascians is itself known as a causer of 'leafy gall' as well as fasciation (Redfern & Shirley, 2011). So, a feature to look out for, and one with plenty of opportunities for research - now, where's that funding application..?

References

Dudman, A.A. & Richards, A.J. (1997). Dandelions of Great Britain and Ireland. BSBI, London.
Presland, J., Oliver, J. & Barber, M. (2009). Abnormalities in Plants. Wiltshire Botanical Society.
Redfern, M. & Shirley, P. (2011). British Plant Galls (2nd ed.). FSC, Shrewsbury.
Simon-Mateo, C., Depuydt, S., de Oliveira Manes, C.L., Cnudde, F., Holsters, M., Goethals, K. & Vereeke, D. (2006). The phytopathogen Rhodococcus fascians breaks apical dominance and activate auxiliary meristems by inducing plant genes involved in hormones metabolism. Molecular Plant Pathology 7(2): 103–12.
Vandeputte, O., Oden, S. & Mol, A. (2005). Biosynthesis of auxin by the gram-positive phytopathogen Rhodococcus fascians is controlled by compounds specific to infected plant tissues. Appl. Environ. Microbiol. 71(3): 1169–77.

Diary of a farm pond: March 2012

It's been a while since I posted an update about the development of the farm pond at our local community farm project at Highbridge in Hampshire, southern England. Originally a left-over from gravel extraction, the pond has been extended and serves a dual purpose as both wildlife habitat and a source of water for irrigation. As southern England is currently experiencing a period of drought, balancing these functions will be an ongoing concern...

As a 'working pond', one key characteristic has been disturbance, especially recently as part sof the banks have been re-profiled and landscaped to prevent the sides collapsing (there's a track running along one edge), and to make it easier to access the pump when water is needed for irrigation. So, at first glance, the pond currently looks a bit sparse.

The farm pond following re-landscaping. The irrigation pump and piping can be seen to the left.

However, there's more going on than this first picture suggests. The foreground is the area that has been re-landscaped and has therefore been largely returned to 'stage one' as far as species colonisation goes. However, in the background you can see the small reedbed which has not been affected by recent works.

A slightly different viewing angle reveals more marginal vegetation.

As well as the reedbed, this photo shows that there is still marginal vegetation - this extends up the bank to the right which is gravelly and has a variety of common wildflower species along with some rough grassland and small fruit and nut trees planted as part of the community farm. Last summer this showed considerable invertebrate activity, and I expect it will be the same this year. The pond itself supported various species including several dragonflies and damselflies, plus several fly species, whirligig beetles (Gyrinus) and frogs. It is inevitable that some overwintering larvae, pupae or adults will have been affected by pond works, but hopefully this will be minimal. Despite the unusually warm weather (around 20degC for the last couple of days), it is still very early for most invertebrates to be active, although there were numerous Gyrinus, plus the spring cranefly Tipula vernalis. I shall of course be looking out for the appearance of other species, including some of the less popular groups I began searching for at the site last year (such as springtails AKA Collenbola) and updates will appear here.

Pied Wagtail Motacilla alba, one of a pair using the margins of the pond in warm weather.

Oh, my rusty hollyhocks!

As my wife knows, I don't have to be at work to get distracted by an interesting bug, plant or fungus. So, nobody was very surprised when, during a leisurely walk following a family pub lunch yesterday, I bent down to take a sample of an interesting-looking hollyhock (Alcea rosea) leaf.

Hollyhock leaf showing orange fungal structures and something small indicated by a red arrow...

As you can see from this photo, the leaf bears numerous orange fungal structures on both the blade and petiole (stalk), plus there's a small invertebrate indicated by the red arrow. Staring with the fungus, a closer look highlights some familiar structures...

Elongate orange fungal structures on the petiole. These are blister-like and the dark orange masses are spores that have become exposed as the blisters have ruptured.

On the leaf blade, similar (but more globular) spore-filled structures are seen (red arrows), while some appear greyer in colour (blue arrow).

Although small, these blisters clearly include some abnormal growth and colouration of the plant's tissues and thus can be considered to be galls. A quick look in Redfern & Shirley (2011) provides an easy identification - there is a single galling species species found on hollyhock (and some other Malvacaeae), the rust fungus  Puccinia malvacearum. This specimen clearly matches the description, including the grey colour of older spores. Although this species may be unfamiliar, the genus is found on many plants with those on lords-and-ladies (Arum maculatum) and nettles (Urtica dioica) being particularly common and widespread - just look out for the little orange rings and pustules. Now onto the potentially trickier tiny invertebrate...

Small (3 mm long) leafhopper on the hollyhock leaf. See below for the meaning of the red arrows and circle.

If you are familiar with generalist insect books such as Chinery (1986), you can quickly tell that this is a leafhopper (Cicadellidae) of some sort, possibly a relative of the often-illustrated Eupteryx aurata. However, there are numerous species in this group (the subfamily Typhlocybinae) and the more technical Le Quesne & Payne (1981) may well be needed to identify them by keying out. So, back to a bit of taxonomic morphology - important diagnostic features are as follows:

• The three apical forewing veins (indicated by red arrows in the above photo) join the same cell (indicated by the red circle), noting that two of the veins merge to form a 'Y'.
• In the same photo, you can see the white 'waxy area' on the front edge of the forewing. Just behind thisthere is an irregularly shaped black spot cut into two by a pale wing vein. In some species this spot marges into one.
• In side view the front of the face (running down to the piercing mouthparts) is flat without a clear angle part of the way down (see top photo below).
• The pattern on the pronotum is distinctive - two clear black dots near the front edge with fuzzy longitudinal brown marks attached to them, plus other smaller black dots to the sides (see lower photo).
• The pattern on the head shows a triangle of three large black spots; the single rear spot does not have a dent in its front edge.
• The front of the 'face' is not clearly shown here, but in the above photo you can just see that there are two more black spots in front of the three on the head, but not another pair further to the side by the eyes.

Side view of the leafhopper showing the flat front to the 'face'.

More-or-less dorsal view of the leafhopper showing the patterns on the head and pronotum.

Combining these features and using them in the key, the species can be identified as Eupteryx melissae. This is a leafhopper which, like the rust fungus above, is known from hollyhocks and related Malvaceae. It is very similar to E. thoulessi but can be separated using the features on the front of the face (E. thoulessi has the extra pair of lateral spots near the eyes which are absent here), and of course the food-plant is a helpful clue. Although this specimen was seen in mid-March, it is usually not recorded until May. However, it may have emerged following a recent spell of warm weather; when collected it appeared dead, but was probably simply torpid as the temperature had fallen considerably over a couple of days - certainly it became active again under the microscope.

More soon...

References

Chinery, M. (1986). Collins Guide to the Insects of Britain and Western Europe. Collins, London.
Le Quesne, W.J. & Payne, K.R. (1981). Cicadellidae (Typhlocybinae) with a checklist of the British Auchenorhyncha (Hemiptera, Homoptera). Royal Entomological Society Handbooks for the Identification of British Insects 2(2c): 1-95.
Redfern, M. & Shirley, P. (2011). British Plant Galls (2nd ed.). FSC, Shrewsbury.

Antscape: ghosts in the graveyard

Despite the title, it's early March and so couldn't be much further from Halloween, but wildlife respects its own calendar, not ours... Anyhow, having gone for a wander in the woods a few days ago, I took my usual shortcut through the nearby churchyard and noticed something intriguing. On many of the graves, especially on the corner-stones, tussocks of soil and grass had developed. I must have seen this dozens of times before but it had never really grabbed my attention - this time however, I stopped to take a closer look...

Tussocks on the corners of a grave.

From a distance, these tussocks just look like long grass that the mower has missed. However, close up it is clear that they are actually formed of fairly loose soil with grass and moss growing on it. Like any good ecologist, I began to delve...

Yellow Meadow Ants (Lasius flavus) in a churchyard 'tussock'

As soon as pulled open one of these tussocks, it was clear how they had formed - they are actually anthills of the Yellow Meadow Ant (Lasius flavus). L. flavus is a common species, associated with the formation of 'antscapes' comprised of hundreds of closely spaced anthills on undisturbed grasslands (although sometimes they don't form anthills). In Britain it is the only species building long-term nests of the 'unthatched mound' type - a couple of others such as L. niger produce occasional small, temporary mounds, while the Wood Ant Formica rufa produces much bigger mounds covered ('thatched') with bits of twig etc. (Skinner & Allen 1996). L. flavus nests are up to about 30 cm tall, the mound effectively being the spoil heap from soil dug out when the colony builds its underground nest of tunnels and chambers. Being subterranean, L. flavus is rarely seen unless sought out, despite probably being Britain's commonest ant - the underground habit has led to reduced eye development and even soil is brought to the surface at night (Pontin 2005), so daytime activity is unlikely to be seen in passing - certainly I saw no ants on the surface. This also keeps different species apart - in this case, L. flavus lives in the same areas as L. niger, but the latter lives on the surface forming much larger territories (active L. flavus mounds can be as little as 2 m apart, below which inter-colony competition is too intense and queens are attacked prior to establishment of a new colony) (Pontin 2005). As the ants cannot make mounds in mowed (or heavily grazed) areas, it is clear that their use of the graves as a focus for their anthills allows them to avoid disturbance by mowers. In meadows, I have seen newly forming nests being built around plant stems - possibly to provide an initial scaffolding for the loose soil particles.

Like many ant species, L. flavus feeds on the sugary 'honeydew' produced by aphids that are tended by the colony. However, the ant-aphid relationship is more complex than this as L. flavus has 'collected' a number of subterranean aphid species (e.g. of the genera Forda, Geoica, Aphis, Tetraneura and Baizongia) which, in Britain, have lost their sexual generation associated with woody plants and are now entirely asexual on the roots and stolons of grasses. Others such as Sappaphis bonomii lay over-wintering eggs on plants above ground, and L. flavus tends them as if they were ant eggs (at the wrong time of year). Not only that, but as well as using aphids as sources of honeydew, L. flavus also uses them as prey to feed its larvae (Donisthorpe 1927, Pontin 2005). The aphids rarely disperse openly above ground level, suggesting that despite the possibility of being eaten by ant larvae, the protection of subterranean ants outweighs this risk. Further, this may effectively form a type of 'culling', keeping aphid density below levels where they tend to start producing winged forms for dispersal.

So, although this is a common and widespread species, it hides a symbiotic lifestyle that is rarely seen despite taking place beneath our feet as we walk across many an old pasture or other undisturbed grassland. I'm certainly tempted to ask permission to investigate these churchyard mounds more closely and maybe learn more about the aphids and other 'guest' invertebrates that can be found within. As the church (St. Mary's, Bishopstoke) was consecrated in 1891, there has been plenty of time for the ant community to develop. Lastly, I want to look briefly at the landscape, or 'antscape', effects of L. flavus. In an old pasture, the anthills are close together (active ones may abut or overlap old inactive ones), but their arrangement is effectively patchy and random. In the churchyard, the association with graves means that this is not the case and the anthills are arranged more or less in a grid matching the positions of graves - even where these have since disappeared - in such cases the pattern of anthills marks the outlines of old graves - ghosts in the graveyard!

Pattern of L. flavus anthills following the locations of current and missing graves.

References

Donisthorpe, H.St.J.K. (1927). Guests of British Ants. Routledge, London. [An old classic; can be a bit expensive, and a lot of the taxonomy has changed, but still worth having].
Pontin, J. (2005). Ants of Surrey. Surrey Wildlife Trust, Woking. [Maps of ant distribution in Surrey, but plenty of other more widely applicable information about British ants].
Skinner, G.J. & Allen, G.W. (1996). Ants. Richmond, Slough. [An excellent little book in the Naturalists' Handbooks series. Includes species-level keys to the British ant fauna. If you want just one book on British ants, I recommend this].

Further reading

Agosti, D., Majer, J.D., Alonso, L.E. & Schultz, T.R. (2000). Ants. Standard Methods for Measuring and Monitoring Biodiversity. Smithsonian, Washington DC. [Takes a global approach with particular emphasis on the tropics and Americas, but covers a range of widely applicable techniques and ideas].

Hampshire's newest slug, a lover of logs

Yesterday at the annual HBIC Recorders' Forum, local members of the Conchological Society brought a display stand including a live specimen of Limacus maculatus. This was found in the Lyndhurst area of the New Forest and represents a species new to Hampshire as of 2011.

Limacus maculatus

L. maculatus (previously in the genus Limax as is the case in many key British texts) is also known as the Irish Yellow (sometimes Green) Slug; it is widespread in Ireland (see map) where it is found commonly in towns and gardens as well as being associated with rotting wood in natural habitats (NMNI 2010). emerging at night to feed and climb. It is medium to large (70-130 mm long), yellowish to greenish and blotchy, with grey to blue-grey tentacles and colourless to yellow or orange slime. A common pattern variation has the darker mottling more fragmented such that the animal has a spotty appearance, similar to that of Limacus flavus (the Yellow Slug) which is similarly often given as genus Limax. These two species were previously considered to be the same (Cameron et al. 1983), though L. flavus is usually a paler yellowish colour and spotty, with a pale zone extending above the fringe of the foot whereas in L. maculatus there is dark pigmentation to the fringe of the foot, and the animal usually has larger dark blotches (though note the spotty variant mentioned above). As a rule of thumb, though care is needed as they are variable, L. maculatus is usually a darker and blotchier green while L. flavus is usually a paler and spottier yellow. See here for photographs of extended specimens showing the tentacles.

More widely, as well as Britain, it is known from France, the Canary Isles, Romania, Bulgaria, Ukraine, Russia, the Black Sea coast and the mountains of Transcaucasia (Turkey to Azerbaijan and NW Iran). Its full distribution is not known with certainty (Kerney, 1999), though it is considered to have been introduced by humans into the British Isles (as well as around Moscow and St. Petersburg), with its native range being the deciduous forests of the Crimea and Caucasus (Wiktor & Norris 1982, Sysoev & Schileyko 2009, Schütt 2010).

In Britain, most records of L. maculatus (see map) are from northern England, with a scattering elsewhere. While L. flavus is largely associated with humans (garden rubbish, damp cellars and outbuildings etc) with occasional records in woodland, L. maculatus is more strongly associated with woodlands, particularly beneath large logs, bark or in tree-holes where moist conditions are maintained (although it can be found in situations similar to those of L. flavus, as well as under stones in fields). The Hampshire specimens seemed to be associated particularly with large logs. Though found sometimes on rubbish, food put out for other animals, dead plants, or on lichens on walls and stones (Cook & Radford 1988, Schütt 2010), its strong association with large logs means that L. maculatus probably feeds on wood-decay fungi, suggesting that large fallen timber may provide both food and shelter. This diet (fungi, algae, lichens, dead plant material) is common among slugs and although many gardeners and vegetable growers dislike slugs, only a few species such as the common Field Slug Deroceras reticulatum actually feed on living higher plants (Kerney & Stubbs, 1980).

As a final note, the 'new to Hampshire' tag is a close one as it was found in Christchurch in 1884 (Kerney 1986) - though now in the county of Dorset, back then the town was in Hampshire...

Found L. maculatus in Britain? Let your local Biological Records Centre know...

References

Cameron, R.A.D., Eversham, B. & Jackson, N. (1983). A field key to the slugs of the British Isles. Field Studies 5: 807-824.
Cook, A. & Radford, D. J. (1988). The comparative ecology of four sympatric limacid slug species in Northern Ireland. Malacologia 28: 131-146.
Kerney, M. (1986). A 19th-century record of Limax maculatus in the British Isles. Conchologists' Newsletter 97: 361.
Kerney, M. (1999). Atlas of the Land and Freshwater Molluscs of Britain and Ireland. Harley, Colchester.
Kerney, M. & Stubbs, A. (1980). The Conservation of Snails, Slugs and Freshwater Mussels. NCC, Shrewsbury.
National Museums Northern Ireland (2010). MolluscIreland: Limacus maculatus (Kaleniczenko 1851) Irish Yellow Slug. [accessed 04/03/2012]
Schütt, H. (2010). Turkish Land Snails. Verlag Natur & Wissenschaft, Solingen.
Sysoev, A. & Schileyko, A. (2009). Land Snails and Slugs of Russia and Adjacent Countries. Pensoft, Sofia.
Wiktor, A. & Norris, A. (1982). The synonymy of Limax maculatus (Kaleniczenko, 1851) with notes on its European distribution. Joural of Concholology 31: 75-77.