A compound gall - assembly instructions
Imagine this. Dozens of newborn young housed in a nursery, side by side with their siblings. Additional babies being produced all the time.
The nursery must grow to accomodate these new arrivals, which will ultimately number several hundred.
The young must feed continuously to sustain their rapid growth and development.
They must be protected from predators as they are totally defenceless.
Their mother is close by but cannot care for her progeny as she is encased in her own protective chamber which she cannot leave.
Sounds like a logistical nightmare. However, the creature in question - the coccid bug Apiomorpha pharetrata - has found solutions to all of these challenges.
The compound gall of Apiomorpha pharetrata – nursery and food source
In my earlier blog Galls - a home you can eat, I introduced the gall of the coccid bug Apiomorpha pharetrata. These are familiar objects on leaves of saplings of the White Stringybark, Eucalyptus globoidea in our forest. Figs. 1, 2 show one of these galls I saw in late summer 2024.
Each gall has two parts:
A globular gall, shaped like an avocado, which houses a single female bug.
An irregular, plate-shaped structure - the compound gall - made up of many fused, tubular chambers. Each chamber is home to an individual male bug.
The galls are produced, not by the bugs living within, but by the host plant itself. The resident insect triggers the plant to produce gall tissue instead of leaf or petiole. The bug then uses its mouthparts to suck nutritious fluids from the vascular system of that induced plant tissue.
Compound gall development
I was curious to know how compound galls are formed. I had a number of questions.
Where do the bugs, which will populate a new gall, come from?
How do they get to that new gall site?
Does each bug move into an existing gall chamber? Or does it grow and develop in parallel with its housing?
How do the male galls chambers come to be so closely packed?
Do all of the male bugs set up home at the same time or progressively?
Let’s start at the beginning - the birth of a new bug.
Where are baby bugs made?
New bugs are produced by adult females. In early October 2024, I spotted a new cohort of A. pharetrata galls on the leaves of eucalyptus saplings (figs. 3-5).
These looked similar to the female galls I had observed in the preceding summer, but were of varying size and shape. The smallest were tubular, while the largest had the familiar avocado shape.
Ants were regularly seen collecting honeydew from the pore at the apex of the gall, suggesting there were living females within.
Three different size classes of bugs were found inside the galls (figs. 6-8), representing the three nymphal instars females pass through as they develop into adults (Cook & Gullan, 2001).
The largest bugs (fig. 8) were identical to the adult females I had found in the previous summer.
These females were clearly mature. There were many baby bugs inside their galls - as seen in this video. A female gives birth to these nymphs inside her gall (fig. 9).
Cook & Gullan (2001) report that A. pharetrata females take at least 14 months to reach sexual maturity. So it’s likely that these largest female galls had been there for over a year.
At this stage, none of these galls had a compound male gall attached.
newborn nymphs inside female gall
Fig. 9. a chain of nymphs emerging from the female’s vulva
The newborn bugs, called crawlers (figs. 10-12) exit the female gall through its apical pore.
These tiny creatures are the start of the next generation of bugs and the founders of a new gall.
How do crawlers get to their new gall site?
Female crawlers move to the end of a leaf and try to catch an air current or simply crawl to a leaf at a different site. They are the main agents for dispersal of A. pharetrata (Cook et al., 2000).
Male nymphs on the other hand just crawl onto the surface of their natal gall. This is where the new compound gall forms, within which they will develop to adulthood.
A detailed look at the development of the compound gall
Having access to a set of ‘naked’ adult female galls enabled me to follow compound gall growth from start to finish.
Here are the major events of that developmental sequence:
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I saw the first signs of a male gall on these female galls in late November.
At that time, it took the form of a dark red, low mound, close to the apical pore of the female gall. Around 15 crawlers had clustered within the central area of the mound (fig. 13). Some were seen en route from the apical pore to the mound (fig. 14). Note the female gall which aberrantly, has formed on the side of the larger female gall.
Over the next couple of days, the mound grew higher and developed a shallow depression, within which additional nymphs gathered (fig. 15). At this stage, all nymphs lay on the surface, closely packed together (fig. 16).
In some cases, the mound was split by a cleft (figs. 17-18). Crawlers were packed on the inner walls of the mound with some spilling over onto its edges. A "lost” one can be seen wandering over the surface of the female gall in fig. 17.
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Fig. 19 shows a later stage of male gall development. The galls on these adjacent female galls are much larger and span the entire width of the female gall. They have taken on a shallow cup shape and each houses a large number of crawlers, which cover the bowl of the cup (fig. 19).
Some of the crawlers have disappeared beneath the surface, their positions indicated by patches of wax (white arrows in fig. 20). The nymph indicated by a red arrow appears to be burying itself.
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The surface of the galls is almost clear of crawlers. They have apparently tunnelled downwards to form tubular chambers. Waxy patches on the surface betray their location (figs. 21, 22). Slices through the gall reveal the chambers (figs. 23, 24) and their occupants, which range from 1st to 3rd instar nymphs (figs. 25, 26).
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Galls increase in size (compare gall in fig. 21, with same gall in fig. 27 one week later and fig. 28 three and half weeks later; compare same gall in fig. 29, with fig. 30 three weeks later). Chambers (indicated by reddish or yellow circular patches with a wax covering) are regularly spaced. A ring of small patches around the periphery (figs. 28, 30) indicates chambers that have been newly added. There is little change in the arrangement of chambers elsewhere - the original set of chambers maintain their relative positions.
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All chambers have opened to the surface (fig. 31, 32). The gall tissue is firmer and dryer, a process which continues until the chambers become quite woody. Continuing development of nymphs generates a full range of stages, right through to the winged adult. The anal filaments of the adults (shown in fig. 37) project from their chambers (fig. 31).
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Dissection of a gall shows the identity of nymphs at different positions. This gall had started to form 8 weeks previously. There is a progression in nymphal stages from the centre to the periphery (fig. 33). Adults and late nymphal stages – instars 4 (fig. 34), 5 (fig. 35) and winged adult (figs. 36, 37) – occupy the bulk of the gall. Early stage nymphs – instars 1, 2 (fig. 38) and 3 – are restricted to outer regions. Winged adults are quiescent within their chambers.
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The gall in fig. 39 is 15 weeks old. I followed it through from its first appearance (see fig. 13) to this stage in late summer. All of its chambers were either empty or contain dead, parasitised nymphs. The winged males had departed in search of a mate. This compound gall was attached to the female gall shown in figs. 40, 41. The female within was still alive at this time and producing crawlers.
A model for male gall development
My observations suggest the following model for the growth and development of the compound gall of Apiomorpha pharetrata.
A low mound forms on the surface of the female gall, close to its apical pore.
Crawlers move from the female gall onto the top of the mound.
The gall takes on the shape of a shallow cup as it grows. Crawlers continue to arrive, eventually covering the bowl.
The initial cohort of crawlers moves beneath the surface. They create regularly spaced chambers in the gall tissue as they continue their nymphal development. The size of the gall increases substantially during this phase but the chambers maintain their original relative positions.
Newly arriving crawlers take up positions on the periphery of the gall, which continues to grow to accomodate them.
Nymphs complete their development to the adult stage within the chambers and remain there in a quiescent state. Eventually, they crawl out of their chambers and fly away.
Questions for further study
My observations provided answers to some of the questions posed at the outset of this project. But we are left with a number of new questions.
Is a crawler required to trigger the initial formation of the mound? In some female galls, I observed what appeared to be incipient mounds which failed to develop further. No crawlers were ever seen on these mounds.
What causes crawlers to assemble on the mound? Cook et al. (2000) note that A. pharetrata crawlers fail to settle if transferred to the gall of another female. They describe likely chemosensory pores on the antennae of these crawlers, which they suggest may enable the nymph to recognise conspecific females and/or other male crawlers.
How do the gall chambers come to be regularly spaced? The crawlers are closely spaced in a non-overlapping pattern when seen on the gall surface just before they disappear into the interior. This may contribute to the regular spacing of their chambers.
What triggers the winged males to leave the gall and seek out a mate? Presumably chemosensory cues released by the females play a role in attracting them.
References:
Cook, L.G. & P.J. Gullan, P.J. (2001) Longevity and reproduction in Apiomorpha Rübsaamen (Hemiptera: Sternorrhyncha: Coccoidea) Boll. Zool. agr. Bachic. Ser. II 33: 259-265
Cook, L.G., P.J. Gullan & A.C. Stewart (2000) First-instar morphology and sexual dimorphism in the gall-inducing scale insect Apiomorpha Rübsaamen (Hemiptera: Coccoidea: Eriococcidae) J. Natural History 34: 879-894.