Insects: slaves in a fungal nation

Imagine you are a Yellow Dung-fly, let’s say a common species like Scathophaga stercoraria. It is a warm summer’s day and you are flying around a grassy meadow peppered with juicy cow-pats. Just the sort of cow-pats frequented by the other flies you prey upon, and where your species’ larvae will develop. Marvellous. Then however, you get a strange urge. The urge is telling you to climb to the top of a tall grass stem. You obey. When you get there, the urge tells you to do the following:

1. Turn so that your head is facing downwards;
2.  Evert your proboscis and attach it to the plant;
3. Raise your abdomen and spread your wings;
4. Stay!

And this is exactly what you do, until some hours later you die in this position and sporangia erupt from your remains, spore dispersal enhanced by the position you have adopted... Yes, you were infected by a fungus of the genus Entomophthora (literally ‘insect-destroyer’) which parasitised you, changed your behaviour (causing what is sometimes known as ‘summit disease’), then killed you, after which spores were dispersed physically (e.g. by wind) or directly to male flies that tried to mate with you. But how did the fungus do that?

The changed behaviour described above was investigated by Maitland (1994) and has been written about widely, including no doubt many ‘Introductory Mycology’ texts and modules. Unsurprisingly however, fewer column-inches seem to have been devoted to the detailed processes that occur after infection by spores, particularly what takes place after hyphae reach the fly’s brain.

Scathophaga stercoraria assumes the position - note released spores...

...and in plan view.

Looking at somewhat older work, Humber (1976) noted that fungi of the related genus Strongwellsea produced numerous fungal nuclei in the brain neuropile and thoracic ganglia of host flies. Having penetrated the abdominal nerves, hyphae grew forward between the neurons without apparent damage and without affecting host's behaviour. Could this be the route through which Entomophthora subsequently does affect host behaviour? Possibly, but this still doesn’t explain how behaviour is changed, only how the fungus gets into a position to do so.

One reason why a clear answer isn’t forthcoming is that, as yet, there isn’t a clear one – however, research is ongoing e.g. at Harvard’s Rowland Institute where they are investigating whether the neural circuitry infected by Entomophthora includes geotactic (‘which way’s up?’) Polarity Control Neurones.

[** STOP PRESS ** Ben de Bivort from the Harvard lab mentioned above has just been in touch to let me know that their research on Entomophthora has ceased, for now at least. They have a working culture system  for the fungus, but couldn't establish an infection in their model system, Drosophila melanogaster, even by injecting high concentrations of cultured cells directly into the abdomen. Research may restart at some point, but for now it seems that either D. melanogaster was resistant, cell injection doesn't work (maybe another process is needed prior to infection?), and/or something else is going on entirely.]

There are however interesting parallels with Entomophthora infection in other species groups. For example, in Wood Ants Formica rufa, the fungus E. ovispora appears to release a dormant Hymenopteran sleeping behaviour which manifests as ‘summit disease’ as the ants climb grass stems which they then grip with their mandibles; some individuals are even glued to the stem by fungal attachments (Roy et al. 2006). Infected ants contain the greatest density of hyphae around the sub-oesophageal and protocerebral nerve ganglia (Loos-Frank & Zimmermann 1976) and it will be interesting to see how this compares with findings from the Rowland Institute. Certainly, Salwiczek & Wickler (2009) consider that parasites such as Entomophthora can only utilise existing, if dormant, behaviour rather than inducing entirely new behaviours.

The taxonomy bit: The genus Entomophthora is generally placed in the family Entomophthoraceae, order Entomophthorales within the Zygomycetes, those fungi which produce sexual spores and have a vegetative mycelium largely lacking septa. For more detailed descriptions of relevant taxa, see here. Taxonomic and descriptive work is ongoing although not all molecular systematic evidence agrees, for example see James et al. (2006) and Thorn et al. (2007).

References

Humber, R.A. (1976). The systematics of the genus Strongwellsea (Zygomycetes: Entomophthorales). Mycologia 68: 1042-1061.

James, T. Y., Kauff, F., Schoch, C.L., Matheny, P.B., Hofstetter, V., Cox, C.J. & Celio, G. (2006). Reconstructing the early evolution of Fungi using a six-gene phylogeny. Nature 443: 818-823.

Loos-Frank, B. & Zimmermann, G. (1976). Über eine dem Dicrocoelium-Befall analoge Verhaltensänderung bei Ameisen der Gattung Formica durch einen Pilz der Gattung Entomophthora. Zeitschrift für Parasitenkunde 49: 281-289.

Maitland, P. (1994). A parasitic fungus infecting yellow dungflies manipulates host perching behaviour. Proceedings of the Royal Society of London B 258: 187–193.

Roy, H.E., Steinkraus, D.C., Eilenberg, J., Hajek, A.E. & Pell, J.K. (2006). Bizarre interactions and endgames: Entomopathogenic fungi and their arthropod hosts. Annual Review of Entomology 51: 331-357.

Salwiczek, L.H. & Wickler, W. (2009). Parasites as scouts in behaviour research Ideas in Ecology and Evolution, 2, 1-6 DOI: 10.4033/iee.2009.2.1.c

Thorn, R.G., Tibell, L., Untereiner, W.A, Walker, C., Wang, Z., Weir, A., Weiss, M., White, M.M., Winka, K., Yao, Y.-J. & Zhang, N. (2007). A higher-level phylogenetic classification of the Fungi. Mycological Research 111(5): 509-547.

The walnut orb-weaver: not always where you think it is

A common and widespread species of spider in Britain (and with females up to 15 mm body-length, fairly large for this country), the walnut orb-weaver (Nuctenea umbratica) is usually found in concealed locations in wood, such as under bark or in cracks in old fence- and gate-posts. As such, it is found in woodland, hedges, gardens and around buildings – anywhere with old ‘woodwork’, natural or man-made. However, the picture below shows that it can be more varied in its hiding-places – seen on 22nd September 2010 at Highbridge Farm, this female was hidden in the head of a common reed Phragmites australis on the bank of the River Itchen. Admittedly there was an old jetty nearby, so it may not have had to move far to find its usual woody crevice, but I’m not aware of any other records of this species using a plant head as a refuge. Has anyone else made a similar observation?

N. umbratica taking refuge in a reed

All the lonely beetles, where do they all come from?

Shortly before World War II, London’s Natural History Museum published the first edition of Common Insect Pests of Stored Food Products (Hinton & Corbet 1943), a slim volume providing a guide to the identification of such insects. Although not specifically covering beetles or non-native species, the topic is such that many of the species covered were indeed beetles, and that are number of these were introduced to Britain. However, it was not until the publication of Volume 1 of Insect Travellers (Aitken 1975) that the beetles recorded from cargoes imported into Britain were surveyed and presented comprehensively, whether or not they were seen as pest species. In Volume II (Aitken 1984), which covered insects other than beetles, the numbers, types and origins of cargoes were updated,  and extended to cover the period 1957 to 1977. The 1970s saw a shift from cargo stowage in ships’ holds towards the use of freight containers; in turn this led to the decline of ‘traditional’ ports with piecemeal unloading which allowed for easier inspection and application of insecticides. Therefore, ship and wharf inspection was virtually superceded by increased vigilance inland by the 1970s e.g. at the end points of cargo distribution such as factories, warehouses, mills and farms.

Fast-forwarding to 2010, a lot has changed. Britain now has a Non-native Species Secretariat (NNSS) with its associated Non-native Species Information Portal (NNSIP) of factsheets currently in development. In 2005, Natural England undertook an ‘Audit of Non-native Species in England’ which tabulated 2721 species and hybrids, of which 98 were beetles. Looking at these, the origins/native ranges can be approximately split as follows:

Europe 43

Australasia 16

North America 10

Asia (as a whole) 5

Eurasia 5

East Asia 3

South America 3

‘Tropics’ 3

Central America 2

Palaearctic 2

Africa 1

Europe & Africa 1

South Atlantic islands 1

Unknown 3

Although there is some doubt about the origins of some of these (e.g. a few listed under ‘Europe’ could turn out to be Eurasian), by far the most prevalent source of non-native beetle species is elsewhere in Europe, even though Asia, and especially China, is often cited anecdotally as such a source. It is true that many non-native plants originated in China, and that increased Chinese exports are likely to increase the transport of species from East Asia. However,  it should also be remembered that some Chinese beetles found in Britain and elsewhere are particularly striking such as the Asian longhorn beetle (Anoplophora glabripennis) and the citrus longhorn beetle (Anoplophora chinensis). These have in turn induced the production of many factsheets and column-inches about their invasiveness and damage to timber (e.g. Haack et al. 2010) and that the Internet allows much faster and broader familiarisation with such species than was the case when introductions were first being catalogued.

Asian longhorn beetle (Anoplophora glabripennis)

While other invertebrates may show a similar pattern (of 34 spiders on the NNSIP register, 20 are from Europe and none are strictly Asian), looking at new and potential invasive species as a whole (i.e. including all animal taxa) shows a different pattern. For example, since their 2005 audit, Natural England’s horizon-scanning (Parrott et al. 2009) highlights 63 species across its red ‘alert’, yellow ‘watch’, ‘black’ and ‘climate’ lists; of these, North America (13), East Asia (12) and Asia (9) are the key areas of origin with only 5 species originating elsewhere in Europe and 7 more widely in Eurasia.

There are many factors here, but some seem to stand out; 

• Beetles move by many means, often helped by humans, but many introductions into Britain are likely to be from Europe as their ranges expand northwards with climate change.
• Many terrestrial invertebrates, especially small species, can spread to new areas unaided – this is seen with ‘ballooning’ spiders.
• Larger species, particularly invertebrates are often spread intentionally such as fish species introduced for angling or ornamental purposes and subsequently escaping or being released.

So, to return to the title question ‘...where do they all come from?’, the answer is that they are from more-or-less everywhere, but often just across the English Channel – for those of us interested in species recording and finding new beasties, they are likely to keep us busy and there will no doubt be further striking exotics hitting the headlines as they appear in fruit shipments and imported houseplants. Meanwhile, the small and less obvious beetles will be making their quiet way from continental Europe...

References

Aitken, A.D. (1975). Insect Travellers. Volume I. Coleoptera. Technical Bulletin 31. Ministry of Agriculture, Fisheries and Food. HMSO, London.

Aitken, A.D. (1984). Insect Travellers, Volume II. MAFF Agricultural Development and Advisory Service Reference Book 437. HMSO, London.

Hinton, H.E. & Corbet, A.S. (1943). Common Insect Pests of Stored Food Products. British Museum (Natural History), London.

Haack, R., Hérard, F., Sun, J., & Turgeon, J. (2010). Managing invasive populations of Asian longhorned beetle and Citrus longhorned beetle: a wWorldwide perspective Annual Review of Entomology, 55 (1), 521-546 DOI: 10.1146/annurev-ento-112408-085427

Parrott, D., Roy, S., Baker, R., Cannon, R., Eyre, D., Hill, M., Wagner, M., Preston, C., Roy, H., Beckmann, B., Copp, G.H., Edmonds, N., Ellis, J., Laing, I., Britton, J.R., Gozlan, R.E. & Mumford, J. (2009). Horizon Scanning For New Invasive Non-native Animal Species in England. Natural England, Sheffield. (Natural England Contract No. SAE03-02-189, Natural England Commissioned Report NECR009).

Thank you to the US Fish & Wildlife Service for putting this image in the public domain. Much appreciated.

Playing with cars - can crows make their own roadkill?

It is well known that carrion crows (Corvus corone) frequently feed from roadkill. As they lack a bill specialised for tearing into flesh, they may need a carcass to be opened by another animal before being able to scavenge – a job done very effectively by the impact of a vehicle.

In Japan, they have been seen to use cars to crack walnuts, placing them on pedestrian crossings when the traffic stops, and after traffic has passed, waiting for the lights to change again in order to collect the opened nut safely; if the nuts are missed, they even hop down and shift them (see video here) (Nihei 1995). This is astonishing behaviour, first noted in Japan in 1990, but in hindsight not that difficult to imagine developing – after all, crows already drop prey items such as molluscs onto hard surfaces to break them. As well as being an area where research has been undertaken (Zach 1979), I have seen this on a stony beach in southern England, and a road is a hard surface. From this starting point – (1) drop hard food onto the road, (2) notice and remember that cars aid the food-opening process, (3) learn to avoid the dangerous cars, (4) notice that pedestrian crossings have safe traffic-free periods handily announced by lights and bleeping, (5) adapt points 1-4 by moving nuts if necessary. So, most impressive, but it still follows from development of a well-known behaviour in a new urban setting.

However, what about roadkill? I am not aware of crows dropping unopened carcasses onto roads (though suddenly it seems plausible if the carcass is small...), but on two occasions I have witnessed what looked, from my human perspective, like a crow ‘herding’ a pigeon into traffic... could it be creating its own roadkill? Speculative, yes, but also plausible I feel. Of course, it could simply be aggression with the crow pushing the pigeon roadwards by chance, but as the pigeon moved back towards the grass verge, the crow did appear to be trying to prevent it. I didn’t see the pigeon being run over on either occasion, but still I have to wonder and on both occasion I had a witness who agreed what the event looked like... Now, all that’s lacking is some evidence, so any similar observations would be really interesting and much appreciated, or of course indications that I’m talking scribble!

References

Nihei, Y. (1995). Variations of behaviour of Carrion Crows Corvus corone using automobiles as nutcrackers Japanese Journal of Ornithology, 44 (1), 21-35 DOI: 10.3838/jjo.44.21


Zach, R. (1979). Shell Dropping: Decision-making and optimal foraging in northwestern crows Behaviour, 68 (1), 106-117 DOI: 10.1163/156853979X00269

Bird song vs urban noise

It's now well known that some birds can adapt their songs to different environments. For example, great tits (Parus major) have been shown to sing faster and at a higher pitch in urban areas (Slabbekoorn & den Boer-Visser 2006). This may be because urban noise, mostly from traffic, tends to be at a lower pitch and drowns out low-pitched birdsong. Also, the relative openness of city landscapes compared to woodland means that high-pitched songs are less likely to be lost in reflections in dense foliage – the reason why songs in dense woodland are slower and lower-pitched.

Exactly how city birds adopt a higher pitch is not so well understood. As great tits are known to learn songs from their neighbours (I have heard one incorporating car-alarm sounds), one hypothesis states that young birds may simply not hear the low notes produced by other birds and so lose them from their song. However, this would imply that urban songs had fewer notes than forest songs, which is not the case. Instead, songs with low notes may be dropped entirely, leaving birds with an exclusively high-pitched repertoire. Alternatively, as songs are used for attracting mates or defending territory, it may be that urban birds are forced to use higher-pitched songs because the low-pitched ones do not prompt the required response. However, without urban noise, females generally prefer males with lower-pitched songs and it is unknown as yet what the effect of song change will be on mate selection (Mockford & Marshall 2009). Certainly, noise in the urban environment does appear to be exerting evolutionary pressure with birds using higher-pitched songs being more successful at mating.

Does this mean urban noise will eventually have no effect as birds adapt? Well, no – it has become clear that not all birds are able to adapt. With low-pitched species unable to sing effectively near main roads, man-made noise may lead to a decrease in biodiversity around towns and main roads. Urban development does tend to lead to a similar, limited, range of species being found and recent research in the US (Francis et al. 2009) shows that noise reduces the diversity of bird species present (absent species being those with lower-pitched calls and songs), but not necessarily the overall number of birds, as those that remain fledge their young more successfully due to the relative absence of avian predators, many of which have low-pitched calls. Of course, there may also be knock-on effects of reduced biodiversity e.g. an absence of species which are important for dispersing seeds (such as jays) would be harmful to the ecosystem as a whole by reducing plant regeneration.

The behavioural flexibility that may be key to urban success, or the lack of it in many species, is likely to at least partly explain the detrimental effects on bird communities in noisy urban areas or along main roads. Mockford and Marshall (2009) also show that birds from noisy areas respond less strongly to the song of birds from quieter areas, and vice versa, even when the songs come from only a mile or two away. As great tits can disperse up to 3km (1.8 miles) in their first year, this means that young males may have difficulty establishing and defending a territory, or attracting a mate, if they move to an area with more or less noise than they are used to – something that may have implications for great tits' ability to communicate and breed successfully, especially as great tits are thought to learn their song in their first year and can only make small changes after this. Potential barriers to breeding could mean they eventually stop recognising each other, reducing genetic flow between urban and rural populations and it is unknown whether small populations in small cities will suffer from lower genetic diversity.

Other species are also affected such as the blackbird (Turdus merula) which is also shown to sing faster and at a higher pitch in noisy environments (Nemeth & Brumm 2009), while nightingales (Luscinia megarhynchos) are known to sing more loudly and in Germany even break noise regulations, reaching 95 decibels (Brumm 2004). Showing a different adaptation, the highly territorial robin (Erithacus rubecula) sings during the night in areas that are noisy during the day, with light pollution (often considered to be the cause of nocturnal singing in urban birds) appearing to have less of an effect than daytime noise (Fuller et al. 2007). This study also found that nocturnal singing was, on average, 10 decibels louder than daytime songs. This may mean that robins are highly adaptable to the urban environment, but equally they may well be suffering from what noise has rendered poor-quality habitat and having trouble attracting mates. If so, nocturnal singers could be sacrificing other activities such as feeding and preening in order to maximise their singing time. Female robins judge the quality of males by how creatively they sing and prefer males using a greater diversity of songs. Therefore, noise pollution could have a negative effect on males by making it more difficult to hear their full repertoire.

The effect of noise on communication also has effects outside of breeding e.g. the need to hear approaching predators or locate prey, and noise does not just affect birds. Frogs croak, crickets chirp, bats use ultrasound to navigate and find insect prey, and there has been much research relating to the effects of shipping noise on navigation and communication by whales and dolphins. Therefore it is becoming increasingly clear that, when thinking about conservation, good quality habitat requires reduced noise pollution as well as high-quality habitat, and reduced pollution from light and unpolluted air and water.

References

Brumm, H. (2004). The impact of environmental noise on song amplitude in a territorial bird Journal of Animal Ecology, 73 (3), 434-440 DOI: 10.1111/j.0021-8790.2004.00814.x

Francis CD, Ortega CP, & Cruz A (2009). Noise pollution changes avian communities and species interactions. Current biology, 19 (16), 1415-1419 PMID: 19631542

Fuller RA, Warren PH, & Gaston KJ (2007). Daytime noise predicts nocturnal singing in urban robins. Biology letters, 3 (4), 368-370 PMID: 17456449

Mockford, EJ, & Marshall, RC (2009). Effects of urban noise on song and response behaviour in great tits. Proceedings of the Royal Society of London B , 276 (1669), 2979-2985 PMID: 19493902

Nemeth, E., & Brumm, H. (2009). Blackbirds sing higher-pitched songs in cities: adaptation to habitat acoustics or side-effect of urbanization? Animal Behaviour, 78 (3), 637-641 DOI: 10.1016/j.anbehav.2009.06.016

Slabbekoorn, H., & den Boer-Visser, A. (2006). Cities Change the Songs of Birds Current Biology, 16 (23), 2326-2331 DOI: 10.1016/j.cub.2006.10.008

Note that a version of this article appeared as:
Hubble, D. (2010). British birds and urban noise. Southampton Natural History Society Annual Report 2009: 11-14.

Leaf miners & climate change?

OK, I'm going to be a bit speculative here... In April this year, I found abut 20 leaf mines of the agromyzid fly Chromatomyia aprilina on honeysuckle (Lonicera periclymenum) in Stoke Park Woods near Eastleigh in Hampshire. Although probably under-recorded in the county (the local records centre had a single record, and I found one more on the excellent British Leafminers site), there is nothing inherently astonishing about finding this species, except for the date when I found it and the form its mine took.

Spring mine of C. aprilina (note pupa just above the midrib).

The usual more-or-less stellate start to C. aprilina mines in summer & autumn.

C. aprilina is usually considered to have two generations ('bivoltine') - one in early summer and one in the autumn. However, in February 2009 a new 'spring' form was found in Kent with further records in March that year from Gloucestershire. This appears to be an early generation and has a different mine structure with the initial stellate section much reduced and mining occurring away from the leaf midrib.

Again, this may not be astonishing in itself, but it does raise some interesting questions:

1. Why has this new form of mine appeared; is it an adaptive reponse to the earlier spring seasons associated with climate change allowing an extra generation to be squeezed in? This appears to be a well-known miner, so it seems unlikely that the spring form was simply overlooked until last year. I wonder if the spring generation will begin to appear further north as temperatures increase, and if so whether this spread could be separated from the distribution of the species as a whole.
2. Whatever the cause, why does it have a different form? Are conditions in the leaf different in spring in some way that affects mining?
3. Are other leaf miners exhibiting similar changes?

Any thoughts on this are most welcome - with only two years of records, maybe little can be inferred but it will be interesting to see if the above questions can be tackled.

Pupa (c. 3mm) of C. aprilina in the leaf. Note spiracles to the left. This pupa was raised to an adult.

References

D. Hubble (2010). Hampshire records of Chromatomyia aprilina Goureau 1851 (Diptera, Agromyzidae) - an under-recorded leaf miner? Dipterists Digest, 17 (1), 63-64

Spencer, K.A. (1972). Diptera, Agromyzidae. Handbooks for the Identification of British Insects 10(5g): 1-136.

Another beetle new to Britain

I've recently received the latest edition of 'The Coleopterist' and in it is an article about a chrysomelid (leaf or 'flea' beetle) new to Britain (Harrison 2010). It's called Longitarsus symphyti and is a small (1.5-2.8 mm) yellowish beast which is found only on Common Comfrey Symphytum officinale. It has been found by the author in Berkshire in August 2009, so being in the south of England too, and knowing the location of an abundant comfrey patch nearby, I will be out looking for it next summer, although it appears to be wingless and therefore may be slow to arrive...

Until then, I'll be familiarising myself with its identification features that allow it to be separated from the similar L. pellucidus & L. succineus (it has a translucent cuticle allowing the dark gut contents to be seen, longer male antennae, more elongate antennal segments 4-11 with unicolorous segment 11, and a distinctive aedeagus median lobe & spermatheca). I'll need to as it will have to be added to my key to the British Chrysomelidae (more on that and the related recording scheme on my Chrysomelid page soon - a Chrysomelid website including online recording is on its way).

I don't have a pic of this species, but to see collection specimens, look here.

Reference

Harrison, T. (2010). Longitarsus symphyti Heikertinger, 1912 (Chrysomelidae) new to Britain. The Coleopterist 19(2): 41-43.

Britain's aquatic moths

When we think about aquatic insects, various groups spring to mind – caddis, dragonfly and damselfly nymphs, and water beetles among others. However, moths do not often appear on this list.

Worldwide there are several hundred moth species with aquatic larvae, and more are being discovered as research unravels the biology of previously unknown larve. Those considered truly aquatic feed on or mine aquatic vegetation, with a few species consuming diatoms from the surfaces of rocks. Some species construct portable cases similar to caddis and may produce submerged silken spinnings. Most species, especially the external plant-feeders, are in the family Pyralidae; some others are in the family Arctiidae. Truly aquatic larvae often have filamentous gills on the body and may produce a portable case as mentioned above. Also, they usually have small abdominal prolegs with crotchets (small hooks) in an oval pattern, as opposed to terrestrial forms which have well-defined, raised prolegs with crotchets in a circle (Bouchard 2009). Aquatic moth larvae usually live in still or slow-flowing waters such as ponds and marshes, with some found in streams. 

In most aquatic moth species, females swim to the bottom of the water-body to lay their eggs; a few species lay eggs on the surface (e.g. species where wingless females wait on the water surface until mated). In at least one species, the adult female moth is completely aquatic and never emerges from the water.

Larva of Parapoynx showing gills © Hugh Clifford

In Britain, four native pyralid species can be considered truly aquatic and will be covered first; the Brown China-mark (Elophila nymphaeata), the Beautiful China-mark (Nymphula stagnata), the Ringed China-mark (Parapoynx stratiotata) and the Water Veneer (Acentria ephemerella). Of these, the first three are in the subfamily Nymphulinae, while the Water Veneer is in the closely related Acentropinae. Some other species have semi-aquatic larvae such as those feeding low down in the stems of emergent vegetation and those which raft between food-plants; these will be covered secondly.

The larvae of the three nymphuline species all have aquatic larvae which live submerged in spinnings among aquatic vegetation (Goater 1986):

Elophila nymphaeata

Larvae feed on pondweeds (Potamogeton spp.), frogbit (Hydrocharis morsus-ranae) and bur-reeds (Sparganium spp.) from September to June. The initial stage is a leaf-miner, later living in a floating case made of leaf fragments. To facilitate feeding, the larva attaches the case to the underside of a leaf with silk; pupation occurs in a silk cocoon covered with further leaf fragments, attached to a plant stem just below the water surface. This is a common and widespread species in Britain, found where there are suitable pond and lake margins, as well as abundant vegetation in slow-flowing rivers and canals. Adults differ from Nymphula stagnata by being larger in size and having broader, browner wings; a smaller dark brown form is known from bogs in the New Forest and Dorset (Manley 2008).

Nymphula stagnata

Larvae feed mainly on yellow water-lily (Nuphar lutea), also on bur-reeds (Sparganium spp.) and probably other water-plants from August to May. The initial stage is a miner within the pith of the stem where it hibernates until April. Post-hibernation feeding occurs in the stem or in a chamber of leaves spun just below the water surface; pupation occurs in a white silk cocoon attached to the food plant. This is a common and widespread species in Britain, found at the margins of rivers, streams and lakes, although it is more locally distributed north of southern Scotland.

Parapoynx stratiotata

Larvae are more specialised for aquatic life than the first two species, with a profusion of branched gills, and feeding on pondweeds (Potamogeton spp.), Canadian waterweed (Elodea canadensis), hornworts (Ceratophyllum spp.) and other water-plants from July to May. The larva spins leaves together, forming an open web, and makes wriggling movements to aid gas exchange; pupation occurs in a large pinkish cocoon attached to a plant beneath the water surface. Habeck (1983) researched the various food plants of this species, including its possible use as a control agent of invasive aquatic plants in the USA. It is locally distributed at the margins of ponds, lakes, slow-flowing rivers, canals and ditches; commonest in the south of England and Wales, but recorded as far north as Yorkshire and Lancashire.

Acentria ephemerella

Larvae are found to 2m depth in loose spinnings among food plants which include Canadian waterweed (Elodea canadensis), pondweeds (Potamogeton spp.), stoneworts (Chara spp.) and filamentous algae. Hibernation takes place from October to May with larvae becoming fully-fed by May or June; pupation occurs in a silk cocoon at up to a metre depth beneath the water surface. Adult females are usually flightless with much-reduced wings, remaining submerged and swimming with long-fringed middle and hind legs until mating occurs on the water’s surface; fully winged females do occur and are larger than the males. It is locally abundant in ponds, lakes and slow-flowing rivers throughout Britain.

A number of other fully aquatic nymphulines have been recorded in Britain, but these are non-native species generally with sparse records associated with greenhouses specialising in aquatic plants and are detailed in Goater (1986). However, there are some other species which produce larvae with some aquatic aspect to their life history. For example, Schoenobius gigantella and Donacaula forficella (subfamily Schoenobiinae) both have larvae that feed on plants such as common reed (Phragmites australis) and reed sweet-grass (Glyceria maxima), floating to new stems on rafts made from sections of the previous stem. D. mucronellus may not raft, but feeds and pupates in the lower sections of reed, G. maxima and sedge (Carex spp.) stems, and as such may need to tolerate wet conditions, especially if water-levels are high. Similarly, within the subfamily Crambinae, the boggy heathland specialist Crambus silvella (known mainly from Surrey, Hampshire, Dorset and Norfolk) pupates in a cocoon in the soil which, in wet conditions, may again require tolerance of inundation, although this is not certain. C. uliginosellus is very local in wet bogs, but its larval biology is unknown and so its tolerance of wet conditions is less certain still.

Therefore, although it is clear that a number of species require research to determine their larval life history, Britain does have a known aquatic moth fauna, which – along with the global fauna – may expand as knowledge of larval biology increases.

References

Bouchard, R.W. (2009). Guide to Aquatic Invertebrate Families of Mongolia. Identification Manual for Students, Citizen Monitors, and Aquatic Resource Professionals. Draft Chapter 11: Lepidoptera: Aquatic Moths available here [accessed 17/11/2010].

Goater, B. (1986). British Pyralid Moths. A Guide to their Identification. Harley, Colchester.
Habeck, D.H. (1983). The potential of Parapoynx stratiotata L. as a biological control agent for Eurasian watermilfoil. Journal of Aquatic Plant Management 21: 26-29.
Manley, C. (2008). British Moths and Butterflies: A Photographic Guide. A&C Black, London.

Thanks to BioDiTRL at the University of Alberta for the image of Parapoynx.

Further reading

For more detail about one European species invasive to North America (Acentropus niveus) visit here.


For more about the diversity of aquatic moth species, see:
Mey, W. & Speidel, W. (2008). Global diversity of aquatic moths (Lepidoptera) in freshwater. Hydrobiologia 595(1): 521-528.

Grey Phalarope: Feeding association with Coot?

The Grey Phalarope (Phalaropus fulicarius) breeds in the high Arctic, usually in remote areas such as northern Siberia, Alaska/Canada, Greenland and Svalbard - in fact, Iceland is its most southerly breeding location. It winters at sea around cold current upwellings where food is abundant, mainly off the west coasts of South Africa and South America. As it also migrates across the sea, it is rarely seen on passage, although a few appear on the mainland (generally coastal locations) especially if blown by strong winds. 

Grey Phalarope © Dean Eades

With breeding in such inaccessible locations, and both wintering and migration taking place out at sea, it's not often that the opportunity arises to see one in southern England. Most British records are from Scotland, though I had seen two before at Strumble Head, Pembrokeshire, Wales - one of the most regular areas for sightings. So, it was a pleasant surprise to see one at Fishtail Lagoon in the Keyhaven & Pennington Marshes, Hampshire while out for a group walk on 7th November 2010. British sightings like this are in winter plumage (as above) and the bird, although a wader, looks superficially like a tiny gull - the individual at Fishtail Lagoon did however have a faint blush on the throat, an indication that it was a 1st-winter bird.

Grey phalarope show interesting feeding behaviour, spinning, often in tight circles, to stir up the invertebrate food that they take from the surface. Studies (e.g. Hohn 1971) have shown a tendency to spin clockwise, especially if there are many in the same feeding area, although individuals may spin both ways.

To add to the interst, this individual was seen apparently feeding in association with Coot (Fulica atra), closely following one actively foraging bird and feeding from the surface around it, presumably taking food particles stirred up by its diving. Having since looked for sightings of this individual (which I now know had been present for a week or two), this behaviour had been noted at least once previously. I am however unaware whether this feeding association is typical behaviour for the species - certainly the similarity in scientific names between Grey Phalarope and Coot is simply due to the coot-like structure of the phalarope's feet. So, although it is likely that observations are limited by the remore areas this species frequents, I would be interested to hear if anyone knows more about this type of feeding association.

Reference

Hohn, E.O. (1971). Observations on the breeding behaviour of grey and red-necked phalaropes. Ibis 113(3): 335-348.