Many insects eat plants. But some use them for more than just a food source.

They hijack growth of part of the plant, usually a leaf or stem, triggering it to develop into a protective chamber inside which they develop to the adult stage.

Certain groups of bugs (true bugs, as opposed to bug=small insect) are masters of this strategy. The weird, distorted plant structures they induce - galls - provide food as well as protection for the developing bug nymph. And when females reach sexual maturity the gall becomes a maternity ward and nursery for their offspring.

Bugs belong to the order Hemiptera, a very diverse group of insects. But they all have one common feature - a highly modified mouthpart, the stylet. They use this to suck fluids from plants (or in some cases animals).

Our forest is home to several species of gall forming bugs and each makes a distinctive type of gall. I’ve focussed on one of these species in this post - Apiomorpha pharetrata - which belongs to the family Eriococcidae.

We have found these galls on saplings of the eucalypt Eucalyptus globoidea, one of the most common trees in our forest.

1. Introducing the extraordinary gall of Apiomorpha pharetrata

The gall of Apiomorpha pharetrata is a major piece of engineering, constructed from two parts.

It generally forms on the petiole at the base of a leaf. As it develops, nutrients in the plant’s vascular system are diverted away from the leaf to the gall and the leaf withers and dies.

Male gall

The larger part, an irregular plate- or cup-shaped structure, consists of many individual tubular galls fused together. A single male gall insect develops inside each of these tubes.

Female gall

The globular structure on the other side of the compound male gall houses a single female insect. The female gall is attached directly to the base of the petiole, while the male gall grows on the surface of the female gall.

The female gall has an opening in the form of a small pore at the opposite end to its attachment to the petiole. In some of the galls I collected, this pore was covered in wax.

Sometimes the female gall is positioned on the surface of a leaf, rather than on its petiole. One or two veins of the leaf become thickened and woody as they are co-opted for the delivery of nutrients to the gall.

Development of the male gall

As they grow, the tubular male galls become dryer and woody, changing from a pale to dark green or brown colour.

An opening forms on each tube at the opposite end of its attachment to the female gall. This provides an escape route for the developing male nymph when it becomes an adult insect and a way for the nymph to discharge honeydew from its chamber as it develops.

Inside the gall chambers

The female gall houses a single breeding female bug. She produces thousands of nymphs, called crawlers.

The female crawlers move away from their natal gall to set up a new breeding site.

The male crawlers, on the other hand, move directly from their mother’s gall to the growing compound gall. Each settles there and continues its development within a chamber that forms around it.

Eventually the compound male gall contains hundreds of developing male bugs. When mature, these become winged insects, which fly away in search of a mate.

Establishing a new gall

This schematic summarises what happens after a female crawler arrives at a new site.

1. She settles on a petiole of a leaf or the leaf blade itself and induces the formation of a new gall.

2. The gall grows around her as she develops further into an adult female.

3. She attracts adult winged males by releasing pheromones. One of these mates with her.

4. She gives birth to many crawlers and the gall bug life cycle begins anew.

2. Inside the female’s world

The female gall bug lives her entire life inside her gall

By some totally unknown mechanism (Cook & Gullan, 2008), the female nymph induces a change in the developmental program of the plant tissue on which she settles. What would normally become a leaf or twig, becomes gall tissue.

The female nymph passes through 3 instars as she develops into an adult, the gall growing around her during this process (Cook & Gullan, 2001). By the time she is mature, the gall looks like a small avocado – the insect being the ‘seed’ inside the thick walled ‘fruit’. It’s a tight fit but there is enough room for her to move around a little.

By carefully cutting slices from the top of the gall, I was able to expose the mature female lying within, as seen in the panel of images below.

She is covered in wax, which is secreted from tiny pores present on almost every body segment. This wax prevents the female from being covered by her excreta of honeydew and/or protects her from dessication.

The female’s form befits life in a tight space

The female gall bug is a seriously stripped-down creature. Legs, wings, antennae, eyes, mouthparts and the other body parts you’d expect to find in a typical adult bug are not at all obvious.

She does have some of these components, but they’re present in a form appropriate for life in a tightly constrained space. She can’t make use of the wings, eyes and long legs of a typical bug in her tiny, dark home inside the gall.

So she stops nymphal development before these structures appear or when they are still small. But she continues developing gonads and other kit needed for the task of reproduction.

This style of development is called neoteny. An adult animal that develops in this way is sexually mature and can reproduce, but the rest of its body has stalled in an immature, larval state. Axolotls provide a familiar example - a salamander with a tadpole-like body that can breed.

While her ability to move around is obviously limited, the female can wriggle back and forth quite actively in the gall cavity - as you can see from the response of this female when I touch her with a probe.

To get a better view of their morphology, I fixed females in ethanol and then removed their body wax with detergent.

The adult female has the usual insect complement of 6 legs. These are undeniably short, but they do the job required, given her lifestyle.

Other structures visible include her tiny antennae, spiracles (entry holes to her internal respiratory system), spine- and hair-like setae (hairs), a pair of pointed lobes at the end of her body and the labium (mouthpart). The latter houses the stylets, which she thrusts into the tissue in the wall of the gall to suck up fluid from the phloem, the plant tissue for sugar transport.

Insects that feed in this way must find a means of getting rid of the excess sugar in their diet. One solution is to excrete it as honeydew. But that presents a problem if you live permanently in a small, almost sealed enclosure as the sticky, sugar-filled solution threatens to gum up your body parts. The anal lobes at the rear of the female’s body enable her to direct her honeydew excreta through the pore of the gall to the outside.

The female’s vulva surrounds a simple hole on the anterior margin of the second to last abdominal segment. It is normally barely visible, but becomes very obvious when she gives birth to nymphs - which you can see happening in the 3rd image in the panel above.

The female bug is a breeding machine

Housed in a safe chamber, with no need to search for food, the female can focus all of her efforts on reproduction.

She excels at this task. Cook & Gullan (2001) state that females of most Apiomorpha species can produce thousands of offspring over several weeks. A. pharetrata females become sexually mature at 14 months and can live for up to 2.5 years - providing an extended period for reproduction.

Embryonic development - from egg to fully developed bug nymph - takes place inside the body cavity of the female, which is packed with embryos.

At birth the nymphs are covered by a membrane. This dries over 5-30 minutes, then the nymph breaks free and becomes mobile (Cook & Gullan, 2001).

These videos made after opening a female gall show the active movements of the first instar nymphs.

The technical and very apt name for these endearing creatures is ‘crawlers’. Note that they, like their mother become covered in wax, secreted from glands on their bodies.

Crawlers remain in the gall chamber for several days before emerging from its pore. They then wander around the plant for several more days (Cook et al, 2001).

Their next challenge is to find a construction site for a gall in which to develop to the adult stage.

Their body structure suits them admirably for that task.

3. Baby bugs

A closer look at crawlers

The crawlers have a flattened, disc-shaped body, about 0.4 mm long, surrounded by a fringe of spine-like setae.

Each of these setae bears a transparent wing-like membrane, which abuts or overlaps that on the adjacent setae - giving the appearance of a continuous thin ‘wing’ around the body.

The head has a pair of six-segmented antennae, which bear fine setae, and a pair of ocelli (simple eyes).

The legs are relatively long. Needs must as the nymph does a good deal of walking en route to the site where it will develop into an adult insect.

A pair of long filamentous, wax-covered setae projects from the end of the abdomen.

Female crawlers disperse

Crawlers are the main agents for dispersal in Apiomorpha and indeed most species of the superfamily Coccoidea.

In general, the further away the nymphs can get, the better, as this increases the probability of outbreeding - usually a good thing. A common dispersal strategy used by a crawler is to move to the end of a leaf, raise its abdomen and try to catch an air current to transport it away - either to a different leaf on the natal tree or to a different tree. Or the nymph may simply crawl to a different site.

The flattened body shape of the crawler with low front cross-sectional area, the wing around the body margin, the hairy antennae and the long, thin rear setae are clear adaptations for aerial dispersal (Cook & Gullan, 2000). They reduce the fall speed of the nymphs as they drift on the wind.

In most Apiomorpha species, both male and female crawlers are engaged in the task of dispersal. However in A. pharetrata, only the female crawlers attempt to disperse.

When it eventually settles in a new location, the female nymph begins crawling around, searching for a stem, petiole or leaf surface on which to induce the formation of a new gall.

Undoubtedly, only a tiny fraction of crawlers finds a suitable site for gall construction, which accounts for the vast numbers of offspring produced by each mother gall insect.

It takes 3-4 weeks for the female gall to become a full enclosure and 2.5 months for the A. pharetrata female to complete development. She passes through 3 nymphal instars before finally eclosing as an adult.

She spends the rest of her life of 2.5 years in that same gall chamber (Cook & Gullan, 2001), which ultimately becomes her sarcophagus.

Male crawlers take just a short walk

In contrast to their sisters, male crawlers make only a short journey to reach their site of gall construction. After exiting the cavity of their natal gall via its pore, they simply crawl up onto its lateral surface.

They settle there and make their home inside a compound gall which forms at that site.

Development of male nymphs

Within its gall home, the male nymph goes through 5 instars as it develops into an adult bug. I made vertical slices through male galls to reveal the developing insects within.

This panel shows how the male nymph changes as it develops. Each of the insects shown was found inside its own chamber in the compound gall and was imaged after removal from the gall. Some are covered with the wax they produce, while in others I have removed it by treating with alcohol and paraffin oil. I judged the instar stage based on morphology and size.

4. Males are flyers

This panel shows fully developed adult males, which I dissected from their gall chambers. They remain in their galls in a quiescent state, which can last for several months, until triggered to emerge. This occurs when females are ready to mate.

They have a very unusual appearance with 4 simple eyes (ocelli) - two dorsal and two ventral. These eyes are not used to locate a female gall visually. Rather, they give the male a view of the horizon (which many flying insects do with their ocelli), and he uses this image to maintain a vertical position during flight.

How then does the male find a mate if not by sight? He is guided by pheromones released by the female. This chemical signal is detected by chemoreceptors housed in the male’s long, fuzzy antennae.

So male gall insects fly with their bodies held vertically. Quite a bizarre creature!

Those long waxy filaments dangling from the end of the body are thought to stabilise this vertical flying position.

Another special adaptation, the male’s sharply pointed abdomen, enables him to couple with the female through the narrow pore of her gall.

The adult males have no mouthparts. They don’t feed and they live for fewer than 5 days after eclosing (Cook et al, 2001).

Given their high mortality rate, a large number of males is produced to increase the chances of a successful mating event. The compound male gall of A. pharetrata contains between 300-350 individual galls, housing for plenty of breeding stock.

5. When things go wrong

Male bug nymphs succumb to attack by parasitic wasps

Developing male gall bugs are vulnerable to attack, as their gall chamber is clearly open to the outside world. In some galls, I found that a bug nymph was missing from almost all the tubular chambers. The space was instead occupied by a parasitic wasp.

It is likely that a female wasp thrusts her ovipositor into the opening of the male gall and lays an egg within its cavity. The wasp larvae themselves were not sighted, but pupae and adult wasps were found in abundance. The adult wasps would sometimes eclose immediately after I cut their gall open. There appear to be two (or even three) different species of adult wasps in these galls.

The wasp larva probably devours the resident bug nymph completely, as there was no sign of it in these parasitised galls.

Parasites of parasites of parasites - mites on wasps on bugs

Justice seems to have been served on some of these parasitic wasps. Dead pupae or adults were found in some galls with strange spherical creatures attached to them.

These were identified as a parasitic mite Pyemotes sp. by Owen Seeman, collection manager at the Queensland Museum - iNaturalist observation here. He described the specimen in the last image above as a “delightfully disgusting gravid female”.

The first video below shows that female moving her legs while her abdomen was pressed down under a coverslip - effectively immobilising her. The second video shows another female moving over the carcass of a wasp she has killed.

These mites are known to inject a toxin into their host (the wasp in this case), killing it immediately and then sucking up the fluids in its body. The mite’s abdomen swells up to a sphere the size of a small pinhead as her ovaries grow massively, supplied by this sudden nutrient source (p.369, Gruner et al., 1993).

Embryos develop within the mother mite’s body and the resulting young are born alive, emerging from the birth canal at the end of her abdomen. They remain on her body, tap into her abdomen and suck up her body juices. So they’re parasites too.

Lovely!

Adult female bugs are vulnerable to fly larvae

While the adult female bug is well protected from predators within her gall, this is not a sealed chamber. Its pore provides an exit route for her crawlers and an opening to eject her honeydew. It also presents an open door for parasites.

In 6 of 8 female galls I examined, the female bug inside had been killed by fly larvae. Both live larvae and pupae were found in the gall cavity, along with the corpse of the female.

I collected several of these fly pupae and adult flies eclosed from them 9 days later. These were identified as frit flies, subfamily Oscinellinae - see iNaturalist observation.

The small adult females have an elongate ovipositor with a narrow tip. This would readily fit into the pore of the gall, enabling the fly to deposit eggs or larvae inside its cavity. It’s small wonder many female bugs fall prey to this parasite.

The pore of the gall is pretty small - around 0.4mm wide - but this is presumably large enough for the adult flies that develop inside to get out.

This has been just one gall story from a southern forest. There are many more out there waiting to be discovered!

Postcript:

The events I described above - the development of male and female galls and the insects inside them- took place in late summer. At that time, all of the female galls had compound male galls attached to them and the females inside were producing crawlers.

It’s now early October, mid spring and we’ve discovered galls of the same species - Apiomorpha pharetrata - in the forest again. These were presumably made from by last summer’s crawlers which settled down, induced galls of their own and have continued to develop.

While these galls look similar to the female galls we saw back in January, most are much smaller and have a tubular rather than globular shape. None of them carries the plate of compound male galls which we saw in summer.

Almost all have an accumulation of wax around the apical pore and ants were often seen searching for honeydew there. So it seems that each houses a living bug.

So what’s going on here? I opened up a few to get some answers.

The largest galls each housed a large female bug - identical to those seen last summer.

Some of these females were clearly already reproducing. Many crawlers were seen inside the gall.

These will soon move out of their natal gall and establish new galls elsewhere - the females dispersing to new locations, the males crawling onto the surface of their mother’s gall to make their own gall.

So what is in the smaller galls?

Opening the smallest galls revealed that they housed bugs which are about twice as large as crawlers - presumably 2nd instar nymphs. These already show development of anal lobes, a structure found only in females.

Somewhat larger galls contained larger nymphs - about 3mm long, about half the length of mature females. I presume these are 3rd instar nymphs.

These 3rd instar nymphs will grow and moult once more to become adult females.

But where are the male bugs? These will develop from crawlers produced by adult females. We’ll be keeping our eyes open for male galls on the surface of the largest female galls.

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, P.J. (2008) Insect, not plant, determines gall morphology in the Apiomorpha species-group (Hemiptera: Coccoidea) Aust.J.Entomol. 47: 51-57

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.

Gruner, H-E, M. Moritz, W. Dunger (1993) Lehrbuch der Speziellen Zoologie. Band I: Wirbellose Tiere 4. Teil: Arthropoda (ohne Insecta) Gustav Fischer Verlag Jena.

Gullan, P.J. (1984) A revision of the gall-forming coccoid genus Apiomorpha Rübsaamen (Homoptera: Eriococcidae: Apiomorphinae) Aust. J. Zool. Suppl. Ser. 97: 1-203.