What's in a gall? Part 3: Secrets of the bedeguar

About a week ago, I was on top of St. Catherine's Hill nature reserve near Winchester (Hampshire, England), leading a wildlife walk entitled 'Galls and other wildlife' as the heavens opened and the rain came down... and down... However, although few invertebrates were visible, there was one aspect of entomology that was visible whatever the weather - galls. Last month, I wrote about an undescribed gall species which can be found on this chalk grassland reserve, and before that I investigated the complex inner workings and inhabitants of a common gall species, the Knopper. So, when I saw a cluster of old woody bedeguar galls (Diplolepis rosae) on a sweet-briar (Rosa rubiginosa), I had to collect one and bring it back for closer examination.

A live gall of D. rosae

Bedeguar galls (also known as Robin's Pincushion in Britain) are the galls of the cynipid wasp D. rosae and are quite familar due to their large (a few cm across) spiky shape as shown above. Bedeguar is a Persian word relating to thistles (either their spininess or being wind-blown like thistledown), and there is evidence that ancient writers such as Pliny were familiar with these structures.

Most (well over 90%) of D. rosae wasps are female and it may well be that males are redundant and disappearing. As described in, for example, Csoka et al. (1998), this appears to be due to infection by the bacterium Wolbachia which causes reproduction to occur via thelytokous parthenogenesis (i.e. production of females from unfertilised eggs). Wolbachia has various effects on its different hosts (other wasps, woodlice, gnats, fruit flies) and comes in different strains, but it can interefere with meiosis (meaning females could not produce haploid eggs), cause sexual incompatibility, prevent production of males, or even feminise males (this happens in woodlouse hosts even though they have males genes). In any case, females emerge during May and June and lay eggs in leaf buds which are beginning to swell - whatever the precise criteria for bud selection, females can investigate a bud for up to an hour before deciding on its suitability. Inserting the ovipositir under a bud scale, eggs are laid between the developing leaflets inside  without damaging the plant tissues, and 30+ eggs can be laid, each in an individual cell.

As is usual in cynipid gallers, the leaflet cells around and below the egg immediately become highly active, enlarging and producing RNA, proteins and other substances, and a small pad is formed after about two days. Cell walls break down forming a cavity in the pad, and around a week after the egg was laid, it hatches and the larva enters the cavity. As it begins to feed, nutritive cells develop near its head - these line the chamber while the outside produces cambium. The epidermis meanwhile grows bulges which develop into the familiar multicellular hairs forming the outside of the gall which is familiar to us, the whole mass containing a number of cells. Also, new vascular tissues grow inwards to supply the nutritive layer and out into the hairs as well as linking with leaf veins. The gall is fully developed by July or August and at this point the larvae feed rapidly, being fully fed by October. They overwinter in the gall, pupate there in late spring, and new adults use their jaws to tunnel out (Redfern 2011).

An old bedeguar gall c. 25mm across showing exit holes in individual cells. The gall is also covered with lichens and moss.

The gall broken open to show vascular strands and the inside of a single cell.

The pictures above, especially the lower one, show the complex structure of the vascular tissues, shown here as spaghetti-like threads having grown through the outer layers before they became woody. As shown by the colonising lichens etc., this is quite an old gall and so no D. rosae or associated parasites/inquilines are present, but the complex structure is of interest, especially given the possibility of non-galling invertebrate colonists. A variety of structures is shown in the following pictures:

Enlarged cells similar to those seen in the Knopper gall (see link at top of article)

Layering of cells in the bedeguar gall.

Spongy texture of woody cells surrounding a gall cell.

Some of the vascular tissues, now woody, linked to various parts of the gall and host plant, including the hairs - elongate plant cells are visible.

A section from around a gall cell showing the same elongate structures and their association with the spongy layer.

Looking inside an individual gall cell, it is clear that there is colonisation by, for example, lichens and fungi, but there is evidence of other biota using these ready-made structures.

The inside of a gall cell showing a white membrane suggesting a cocoon, plus black specks of 'frass' (invertebrate faeces).

Looking behind this membrane, among the green algae and black frass, there appears to be an empty skin (exuvium) - the small linear structures in the centre are probably legs.

Having found an exuvium, I had to wonder what had left it there. I didn't expect to find anything, but then there was a tiny flash of reddish movement as I looked down the microscope.

In the bottom of the open cell, a small, round (and quickly moving) red shape.

After some time, I managed to capture this tiny creature (the inner chamber of the cell is only a few mm across, so this is only about 0.5mm long) and took some pictures. It turns out that unlike many invertebrates, it is unable to walk on glass, so although its limbs were moving, the organism itself stayed still on a slide...

The tiny beast in question - a mite, possibly an oribatid. Note the shiny round carapace, bristly appendages and rostrum with transverse wrinkles.

The dorsal surface of the mite showing the even sculpturing.

The best close-up I could get of the head and front appendages/bristles.

So, as always when I decide to investigate a gall in detail, I have come away finding more than expected - it has induced me to read up on the unusual bacterium-mediated reporductive strategy of D. rosae, scrutinise the fine structure of something that is familiar on a macro scale only, and find an invertebrate that I genuinely can't identify (I await a friendly acarologist - should one appear, I'll post any updates). However, with its shiny single carapace, it does look like an oribatid (moss mite, order Oribatida). These vary in their diet, but different species feed on dead plant matter, fungi, carrion or lichens, while some are predatory. Given the microhabitat here, I suspect fungal and/or lichen feeding, and after a further search of the gall cells I found four of these mites. The gall and mites are now in a tiny vivarium, so I may get to see more behaviour and maybe young. If so, pics and details will of course appear here. Thanks for reading!


References

Csoka, G., Mattson, W.J., Stone, G.N. & Price, P.W. (eds) (1998). The Biology of Gall-Inducing Arthropods. General Technical Report NC-199, Forest Service, North Central Research Station, USDA, St Paul, MN. Contains many useful papers and used as a general reference in the publication below.

Redfern, M. (2011). Plant Galls. Collins, London. The source of much of the gall biology here, and a must for gall-nerds!