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"It has long been an axiom of mine that the little things are infinitely the most important" (Sherlock Holmes)

 

 

  <September 2014>  

Autumn is not often regarded as a great time for insect hunting but, for aphidologists, it can be really good. Many conifer aphid populations peak in autumn, especially Cinara aphids. These are unusually large with long piercing mouthparts for piercing the bark of large trees. Many have a very limited host-range, often just one tree genus. Britain has 3 native conifers, thus few 'native' Cinara species. But in the last few hundred years many species were introduced, and some became naturalized. Following which we now have at least 25 Cinara species. Bedgebury Pinetum is a great place to hunt exotic Cinara aphids. Some can be serious pests, such as the cypress aphid. But some contribute positively to our biodiversity because they encourage wood ants, a keystone species. Some enable bees to produce high-quality 'forest' honey, and some host parasitoids never before reported in Britain

 

The black stem aphid (Cinara confinis) - hosting a new parasite species

Since parasites and predators require hosts, to best tell our story, let us begin with the aphids...

Towards the end of an early September day at Bedgebury  we noticed a small colony of the black stem aphid (the picture below shows an adult) beneath the lowest branch of a small Pacific silver fir. (And yes, we did find  their attendant wood ants first.)

Cinara confinis is somewhat variable in appearance, ranging from mottled dark brown to the vivid greenish-black shown here. It is best identified from the abdominal markings - a double row of black spots and lateral transverse rows of fine white wax. Like the giant larch aphids of our July blog  they seemed to find the base of a slowly dying branch very much to their taste.

Cinara confinis colonies are generally located on the trunk just below the first whorl of branches. If disturbed these colonies disperse rapidly. Apterous females tend to drop off but nymphs move rapidly up or down the stem and on to the branches. This species sometimes occurs in special earth galleries constructed by ants on the bark of fir trees. The Cinara confinis colony we found was 'strongly attended' by southern wood ants (Formica rufa) - and they did bite!

 

We have not found any predators attacking Cinara confinis at Bedgebury, despite the suggestion by Harding and Steenberg (2010) that the invasive harlequin ladybird (Harmonia axyridis) may assist in the natural regulation of this aphid. This is almost certainly because of the protection given by wood ants.

However, wood ants seem less effective against parasitoids - and several of the colony at Bedgebury had been parasitized, giving the black aphid mummies, shown in the first picture below. The adult parasitoid is shown in the second picture below.

On the basis of the extraordinary number of antennal segments (Baker, pers. comm.), this parasitoid is almost certainly Pauesia grossa. If so, this is the first record of this species in the UK.

Pauesia grossa is a specific parasitoid of Cinara confinis, and so far is only known to occur in Austria, the Czech Republic, France, Hungary and Switzerland.

 

Cinara confinis may become an important pest in Britain, given the switch from Norway Spruce to Noble fir (Abies procera) for Christmas trees (Norway Spruce can shed a lot of needles when placed in centrally-heated rooms). Hence finding a specific parasitoid is certainly interesting, and may be important.

The black stem aphid may have been in Britain a long time, probably ever since the first fir trees were planted in Britain in the 1600s. It therefore seems possible this parasitoid has also been here for some time, possibly unnoticed because the black mummies are so similar in colour to the live aphids. Even their ants were fooled (we have also observed this among ants attending Cinara juniperi ).

 

The green striped fir aphid (Cinara pectinatae) - a new, brown, colour-form

The green-striped fir aphid is large and (usually) shiny bright olive green, with three diffuse paler green longitudinal bands (see picture below). Like the black stem aphid is lives on fir trees (Abies species) but there the similarity ends.

The green-striped fir aphid is solitary and lives singly on small branches where it sits on the needles and feeds at the junction of petiole and stem as shown in the first picture below. One does not get large colonies with this species - the nymphs produced by a female gradually disperse away from their place of birth and are even better hidden than the adult.

Once they have found a suitable feeding site, Cinara pectinatae  do not move very much and are well anchored by means of their strong claws. They rely on their green cryptic coloration to protect them from predators such as coal tits.

 

Therefore, in September, we were very surprised upon finding brown females as well as green females. We thought at first they might be males, but (under the microscope) the brown ones were structurally identical to the green ones - except they were the wrong colour. Moreover they produced nymphs!

It soon became clear that the brown forms were just as well camouflaged as the green forms - except they were mimicking the buds and the stem, rather than the needles. A search through the literature revealed no other observations of brown C. pectinatae so we started e-mailing other aphid aficionados. Only Andrea Binazzi, an authority on Cinara aphids, recalled finding brown forms of Cinara pectinatae  in late summer and autumn - but his observation does not appear to have been published. In other words these brown Cinara pectinatae are an undescribed colour-form of the green striped fir aphid.

We normally find aphids by hand searching, but given the difficulty of finding Cinara pectinatae, we initially used beating to evaluate whether the aphids were present on a particular tree or not.

The presence of jet black ants (Lasius fuliginosus) on the beating tray strongly suggested that ants were attending the green striped fir aphid, but it proved very difficult to directly observe this. We did eventually observe them to be actively attending them as can be seen in the pictures below:

 

Our initial difficulty in observing and photographing this behaviour was because both the ants and the aphids were very sensitive to disturbance. The aphids left the scene rapidly and hid further along the branch, whilst the ants immediately attacked the intruder (me and the camera) with very little provocation.

 

The cypress aphid (Cinara cupressi) - now you see us, now you don't

We first looked at Cinara cupressi in our April blog  where we highlighted the damage they can do to cypress trees.

In April the aphids were on Nootka cypress (Xanthocyparis nootkotensis). In September we found the same aphid species on a different host - pencil cedar (Juniperus virginiana) - perhaps a mile from the previous location.

 

Aphid colonies were vigorously attended by wood ants, Formica rufa, (see the first picture above). The young tree they were on had apparently suffered extensive dieback from the infestation and possibly previous years' aphid populations. However, searching other similarly-damaged specimens failed to locate the beasties. Presumably, having caused their damage, those colonies had 'burnt themselves out'. In other words, predators, parasitoids, and fungi feeding upon the honeydew had killed the colonies - or reduced them to a few survivors, or eggs. Being extremely cryptic such survivors are very difficult to find unless ant attended.

Cypress trees can recover from the damage caused by Cinara cupressi, providing they are in a favourable environment - although we doubt that such a young tree can recover. In the urban environment where cypress hedges are highly stressed, death of the bush is the rule and it is usually better to replant with a different species.

 

The bow-legged fir aphid (Cinara curvipes) - why sometimes waxy?

The bow-legged fir aphid lives on the trunk or branches of fir (Abies spp.) and cedar (Cedrus deodora). It was originally confined to North America, but was first recorded in the UK in the 1990's at Kew Gardens in London from where it soon spread to other parts of the UK. The species has also spread to continental Europe, although whether this was via the UK or by separate introductions from the USA is unclear.

We first found Cinara curvipes  in England in July 2012, on a fir at Oaken Wood in Surrey, so it was no surprise to find it at Bedgebury in September this year. There it was, living on western hemlock (Tsuga heterophylla), one of its less commonly-used hosts. 

Wingless adults are dull grey-black with a shiny broad sclerotized cross band on the last abdominal segment, clearly visible in the picture above.

Both wingless and winged adults (see picture above) have the hind tibiae long and curved, hence their English name: the bow-legged fir aphid.

Cinara curvipes nymphs develop a covering of pale grey wax on the thorax and the abdomen. This may or may not persist to the adult stage. Our own observations suggest that the adults are only heavily waxed if there are no attendant ants. If anyone else has noticed this effect of ant attendance on Cinara aphids please let us know - defence strategies of aphids is a fascinating topic which has been hardly explored.

Cinara curvipes also uses the same leg-kicking defense against possible predators as the oak aphid Lachnus roboris, possibly giving a reason for the rather unusual curved shape of the tibiae in this species. They seem to maintain that posture, as shown below, even when undisturbed.

This aphid tends to worry foresters more than most because it is one of the few Cinara species that is not restricted to a single genus of conifers. Once Cinara curvipes is established in a country it may well switch to favour another tree, possibly a species critical to local forestry concerns. Jurc et al. (2009) for example expresses concern that its capacity for host-switching could lead to it spreading to silver fir (Abies alba) forests in Slovenia.

So why 'hunt' for aphids?? 

Acknowledgements

We are grateful to the UK Forestry Commission Bedgebury Pinetum  for their kind assistance, and permission to sample.

We are also very grateful to Ed Baker, Tree Preservation Officer, Cardiff Council, for provisional identification of the Cinara confinis parasitoid, Pauesia grossa, a new hymenoptera species to Britain.

We have made provisional identifications from high resolution photos of living specimens, along with host plant identity. In the great majority of cases, identifications have been confirmed by microscopic examination of preserved specimens. We have used the keys and species accounts of Blackman & Eastop (1994)  and Blackman & Eastop (2006)  supplemented with Blackman (1974) , Stroyan (1977) , Stroyan (1984) , Blackman & Eastop (1984) , Heie (1980-1995) , Dixon & Thieme (2007)  and Blackman (2010) . We fully acknowledge these authors as the source for the (summarized) taxonomic information we have presented. Any errors in identification or information are ours alone, and we would be very grateful for any corrections. For assistance on the terms used for aphid morphology we suggest the figure  provided by Blackman & Eastop (2006).

Useful weblinks 

References

  •  Jurc, M. et al. (2009). The first record of Cinara curvipes (Patch, 1912) (Homoptera, Aphididae) in Slovenia and its possible impact. Zbornik gozdarstva in lesarstva 88, 21 - 29. Full text 

  •  Harding, S. & Steenberg, T. (2010). Is Harmonia axyridis a potential biocontrol agent in Christmas tree plantations. In Babendreier, D. et al. (Ed.) Proceedings of the first meeting on Harmonia axyridis and other ladybirds. Benefits and risks of exotic biological control agents. IOBC/wprs Bulletin 58, 195-201.  Full text