Honeydew with dopamine

Japanese mugwort aphid forces ants to provide extra protection

Japanese mugwort aphid manipulates attending ants

A Japanese mugwort aphid colony makes ants more aggressive, as Tatsumi Kudo and colleagues show. As a result, enemies have less opportunity to feed on the aphids.

The cooperation between aphids and ants is one of the best-known examples of cooperation or mutualism. Aphids, which feed on the plant saps, excrete excess sugars in a sticky substance, the honeydew. This is a great food source for ants. They collect the honeydew: they milk the lice. To secure the harvest, they protect the aphids from predators, as if it were their livestock. The parties thus exchange food for protection, and both sides benefit from this cooperation.

Such mutualism exists between the Japanese mugwort aphid (Macrosiphoniella yomogicola), which feeds on mugwort (Artemisia montana), and several ant species, of which Lasius japonicus is the most important one. This aphid manipulates the ants that protect it into becoming more aggressive against predators by excreting dopamine in their honeydew, Tatsumi Kudo and colleagues discovered. In other words: the aphids manipulate the behaviour of the ants.


Earlier, the Japanese research group had shown how the ant manipulates the aphids. Two colour morphs of the Japanese mugwort aphids exist, and the ants favour the morph that reproduces slower, but produces a better-quality honeydew. Now the team shows that, the other way round, the Japanese mugwort aphids do not quite behave like obedient livestock.

The researchers detected dopamine in the honeydew of the aphids, a substance that acts on the nervous system. The crop of ants that harvested the honeydew also contained dopamine.

And that affected the behaviour of the ants. The researchers conducted experiments to find out how aggressive ants were towards the Asian ladybird (Harmonia axyridis), a major predator of the aphids. Shortly after visiting an aphid colony, ants were more aggressive than ants that had not visited aphids. As other experiments show, this is due to the dopamine. In these experiments, administration of dopamine made the ants more aggressive than normal, whereas artificial honeydew without dopamine did not.

Extra benefit

So, both the Japanese mugwort aphid and the ant Lasius japonicus that protects it benefit from their mutualistic relationship. The aphid forces the ant to provide better protection, the ant manipulates the aphid colony so that an extra amount of high-quality food is produced.

The relationship with ants is especially important for the aphid. A colony wouldn’t survive without its ant bodyguards.

Willy van Strien

Photo: Japanese mugwort aphid. ©Ryota Kawauchiya

On YouTube: ladybird larva consuming aphids is bitten by an ant

See how the ant manipulates the aphid colony

Kudo, T., H. Aonuma & E. Hasegawa, 2021. A symbiotic aphid selfishly manipulates attending ants via dopamine in honeydew. Scientific Reports 11: 18569. Doi: 10.1038/s41598-021-97666-w

False alarm

Superb lyrebird male tries to prolong a female’s visit

a male superb lyrebirds show is also used to manipulate females

A male superb lyrebird can deceive a female into believing that danger is imminent, Anastasia Dalziell and colleagues think. This increases the chance that she will stay for a while and copulation ensues.

Superb lyrebirds are masters of imitating all possible sounds, and males make clever use of that talent. When a female pays a visit, a male imitates the sound of a flock of alarmed songbirds, creating the illusion that a predator is nearby, Anastasia Dalziell and colleagues write. Then she might stay a little longer than she really wanted.

The superb lyrebird (Menura novaehollandiae), one of the largest passerine species, lives in the forests of South East Australia. Males and females do not form breeding pairs; each bird lives in its own territory. Females have one young per year, which they raise on their own.

Just watching

During the breeding season, males make themselves as attractive as possible. They construct mounds in their territory, where they sing their songs. Sometimes they sing a special song accompanied by a dance according to fixed rules, as Dalziell described earlier, throwing their decorative tail feathers over their body and head.

The purpose of a male’s show, of course, is to attract females and get them to copulate, because every mating can result in a young that he sires. Females visit several males before making their choice. As a result, a female may come to watch a displaying male, but refrain from mating with him in the end.

That is not what he intended.

Illusion of danger

When she is about to leave without copulating, he adds a new element to his song, which is remarkably similar to the sound of a flock of aroused songbirds.

Small songbirds get aroused when they detect a predator, such as a snake, large lizard, roosting owl, or perched hawk. They utter alarm calls to recruit others and harass the enemy together. The researchers show how accurately a male lyrebird mimics such mobbing flock of multiple simultaneously calling birds. Even the noise of beating wings is incorporated into his song. It is so accurate, that small songbirds are misled and approach to join.

The predators that arouse the small birds are dangerous for lyrebirds too. Therefore, the researchers hypothesize, the song creates the illusion that danger is imminent; the female is inclined to stay, and there is a chance that a copulation will happen.


A male superb lyrebird also utters this cacophony during mating. This job is not done in a few seconds, as it is other birds. Only after havng sat on her for more than half a minute, does he transfer his sperm. From the moment he mounts her until the end, he mimics the sound of a mobbing flock to prevent her from leaving too soon. During mating, he beats his wings in front of him, obscuring her view. She is unable then to assess whether it is safe to go, the authors suggest.

In conclusion, the superb lyrebird male uses his song not only to advertise his good health and condition, as is usual, but also to get a female to stay by giving a false signal of danger. That is deception.

Whether a female will stay longer because of the false alarm, the researchers don’t know. To find out, they would have to do experiments, which would be difficult for this species.

Willy van Strien

Photo: Courting male, covered with his tail. Kim Edol (via Flickr, CC BY-NC-ND 2.0)

Anastasia Dalziell about her research on YouTube

Dalziell, A.H., A.C. Maisey, R.D. Magrath & J.A. Welbergen, 2021. Male lyrebirds create a complex acoustic illusion of a mobbing flock during courtship and copulation. Current Biology, online February 25. Doi: 10.1016/j.cub.2021.02.003
Dalziell, A.H., R. A. Peters, A. Cockburn, A.D. Dorland, A.C. Maisey & R.D. Magrath, 2013. Dance choreography is coordinated with song repertoire in a complex avian display. Current Biology 23, 17 juni online. Doi: 10.1016/j.cub.2013.05.018

Exit through head plug

Dead host helps parasitoid wasp escape from crypt

Parasitoid wasp Euderus set manipulates its host into performing a nasty task

The parasitoid wasp Euderus set lays its eggs near oak gall wasps that develop within their gall. The parasitoid larva will consume its host. But first, the larva manipulates it into performing a nasty task. Otherwise the parasitoid would be buried alive in the oak gall.

The North American parasitoid Euderus set is a natural enemy of gall wasps that develop within galls on oak trees.  It does not attack all oak gall wasps species; hundreds of oak gall wasp species live in North America. But at least seven species fall victim, as Anna Ward and colleagues report.

The researchers discovered the wasp several years ago and named this ‘crypt-keeper wasp’ after Seth, the Egyptian god of darkness and chaos. According to some sources, Seth killed his brother Osiris by trapping him in a tailor-made sarcophagus and throwing him into the Nile. The behaviour of the parasitoid  wasp is as naughty. One of the victims is the oak gall wasp Bassettia pallida, and the researchers described what happens to the galler when Euderus set appears on the scene.

Head stuck

The gall wasp female lays her eggs under the bark of young oak branches. A branch then is induced by the gall wasp to form a separate crypt for each egg, in which the wasp will develop into a larva, pupa and adult. A gall develops in the branch. The adult gall wasp has to chew its way out through woody tissue and bark.

The researchers found holes in oak branches through which an adult gall wasp had emerged. But they also discovered holes in which the head of a gall wasp was stuck. It was a mystery: why did the gall wasp sometimes get stuck?

On inspection, they found a stranger in the chamber behind stuck gall wasp heads: a larva or pupa of a parasitoid, which had consumed the gall wasp partially or completely. That parasitoid was Euderus set. In some cases, the stuck gall wasp head was pierced; the chamber behind such head was empty, except for the remains of the gall wasp.

Nasty task

Here is what happens, according to the authors: a female parasitoid lays an egg in the chamber of a developing gall wasp; after hatching, the parasitoid larva will eat its gall wasp host when it has reached adult stage. But first, it makes the host do some work. The parasitoid induces the young gall wasp to excavate an emergence hole that is narrower than normal. As a result, the gall wasp gets stuck as soon as its head reaches the surface; the head plugs the exit hole. The parasitoid then consumes its host entirely, pupates, emerges as adult parasitoid and leaves the chamber via the empty body and stuck head of the gall wasp.


How the parasitic wasp manipulates the behaviour of its host, is still unknown. But it is to its advantage, because there is little chance that it can chew its own way out through woody plant tissue and bark, as experiments showed. Without a passage in the form of the empty gall-wasp body and head, the parasitoid wasp would be buried alive.

Now, Ward showed that not only Bassettia pallida, but at least six other oak gall wasp species can be attacked by Euderus set. They live in similar galls that are integrated with an oak branch or leaf and that have no structures to keep enemies out, such as spines. This makes makes them vulnerable to Seth.

Willy van Strien

Photo: Andrew Forbes

On YouTube, the research group explains how parasitoid Euderus set manipulates its host

Ward, A.K.G., O.S. Khodor, S.P. Egan, K.L. Weinersmith & A.A. Forbes, 2019. A keeper of many crypts: a behaviour-manipulating parasite attacks a taxonomically diverse array of oak gall wasp species. Biology Letters 15: 20190428. Doi: 10.1098/rsbl.2019.0428
Weinersmith, K.L., S.M. Liu, A.A. Forbes & S.P. Egan, 2017. Tales from the crypt: a parasitoid manipulates the behaviour of its parasite host. Proc. R. Soc. B 284: 20162365. Doi: 10.1098/rspb.2016.2365

Smart offer

How parasitic thorny-headed worm reaches the right host

On parasitized Gammarus shrimp, an orange dot is visible

When fresh water shrimp is parasitized by thorny-headed worm, the parasite is visible from the outside as an orange dot. Thanks to this striking spot, fish will easily detect the shrimp and ingest it, whereupon the parasite completes its development in the fish. According to Timo Thünken and colleagues, only fish that are suitable as hosts preferentially swallow infected shrimp.

The thorny-headed worm Pomphorhynchus laevis is a parasite with a complex life cycle, which takes place in fresh water. During the first part of that cycle, it develops within fresh water shrimp Gammarus pulex, after the shrimp ingested parasite eggs from the water. The parasite develops to a certain stage, the cystacanth.

thorny-headed wormWhen the parasite has reached that stage, Gammarus no longer can serve as a host. The parasite has to switch to fish to be able to complete its life cycle. In the new host, the parasite hooks onto the intestinal wall, matures and reproduces. Female parasites produce eggs that are released together with fish faeces, completing the cycle.

The switch from shrimp to fish can happen in only one way: fish must ingest parasitized shrimp. Timo Thünken and colleagues show how the parasite manages this process.

Manipulation by thorny-headed worm

Normally, Gammarus pulex, no more than 2 centimetres in length, try to avoid being swallowed by fish. The shrimp hide in darkness, avoid areas with fish odour and have an inconspicuous colour.

But a parasitic thorny-headed worm that reached the cystacanth stage will intervene. It changes the behaviour of the host that it no longer needs; the shrimp leave darkness and show a preference for water with fish odour. Moreover, the mature cystacanth turns orange, being visible from the outside as an orange dot on the host.

Parasitized Gammarus seem to offer themselves as prey to fish: fish will easily encounter them and detect them. And indeed, they consume many parasitized shrimp, as was shown earlier in three-spined stickleback. For Gammarus, this is the end of the story, but for the parasite the future is opened.

At least …. if it has ended up in a suitable host. Not all fish species that prey upon Gammarus are a suitable host for the parasite. It will not survive in fish that exhibit an effective immune response. Manipulating Gammarus confers a lower net benefit if it also increases the chance of the parasite to end up in the wrong host.

Barbel suitable, brown trout not

Now, Thünken shows that the manipulation is effective: only suitable host fish ingest a relatively large amount of parasitized Gammarus.

He discovered this in experiments in which he painted an orange dot on unparasitized shrimp, so that they looked like shrimp carrying a ripe cystacanth. He then offered these shrimp, together with unpainted conspecifics, to a number of fish species. The painted shrimp were not really parasitized, and so they behaved the same as the unpainted ones. In this way, Thünken was able to check whether all fish species, just like stickleback in the earlier experiments, preferentially eat coloured prey.

In another experiment, he fed parasitized Gammarus to fish. Four months later, he checked if the fish were carrying living parasites, in order to assess which fish species are suitable hosts.

One of the fish species used, barbel, mainly consumes Gammarus with an orange dot, as it turned out, so this fish will easily get infected with the parasitic thorny-headed worm. This is beneficial for the parasite, because barbel turned out to be a very suitable host.

Brown trout, on the other hand, was as likely to swallow painted Gammarus as unpainted shrimp; the colour change had no effect on this fish. That’s also beneficial, because brown trout turned out not to be a host in which the parasite can survive. The same findings – indifferent to the colour change, poor host – applied to two other fish species, perch and ruffe.


Conclusion: an orange dot on Gammarus has an effect on fish that can serve as host of the horny-headed worm, barbel as well as stickleback in the earlier tests. These fish consumed colour Gammarus relatively often. But for unsuitable fish – brown trout, perch and ruffe – it makes no difference whether their prey has an orange spot or not. So, the dot increases the chance that the parasite will switch to a suitable host without increasing the risk that it will end up in the wrong fish.

How the link between the fish’s sensibility to the prey colour and its suitability to act as host might have arisen, is another question which has not yet been answered.


Stickleback are suitable hosts, but they do not fully meet the pattern. In the new experiments, not all stickleback seem to preferentially consume Gammarus with an orange dot; some even avoided them. With regards to this fish species, the colour alteration of Gammarus can be counterproductive.

According to the researchers, this is because this small fish suffers more from parasitic infection than the other species, which are considerably larger. Stickleback living in an environment in which thorny-headed worm is abundant are likely to avoid infection by skipping coloured Gammarus prey from their diet, warned by the orange colour. For larger fish species, on the other hand, avoiding parasitic infection is not important enough to let prey go.

Willy van Strien

Photo’s: © Nicole Bersau/Uni Bonn
Large: fresh water shrimp Gammarus pulex with thorny-headed worm Pomphorhynchus laevis visible as orange dot
Small: adult thorny-headed worm

Thünken, T.,  S.A. Baldauf , N. Bersau , J.G. Frommen & T.C.M. Bakker, 2019. Parasite-induced colour alteration of intermediate hosts increases ingestion by suitable final host species. Behaviour, online July 19. Doi: 10.1163/1568539X-00003568
Kaldonski, N., M.J. Perrot-Minnot, R. Dodet, G. Martinaud & F. Cézilly, 2009. Carotenoid-based colour of acanthocephalan cystacanths plays no role in host manipulation. Proceedings of the Royal Society B: 276: 169-176. Doi: 10.1098/rspb.2008.0798
Baldauf, S.A., T. Thünken, J.G. Frommen, T.C.M. Bakker, O. Heupel & H. Kullmann, 2007. Infection with an acanthocephalan manipulates an amphipod’s reaction to a fish predator’s odours. International Journal for Parasitology 37: 61-65. Doi: 10.1016/j.ijpara.2006.09.003
Bakker, T.C.M., D. Mazzi & S. Zala, 1997. Parasite-induced changes in behavior and color make Gammarus pulex more prone to fish predation. Ecology 78: 1098-1104. Doi: 10.1890/0012-9658(1997)078[1098:PICIBA]2.0.CO;2

Unopened flower

Moth larva enforces self-pollination in Canada Frostweed

Canada Frostweed may be enforced to self-pollination by a moth larva

The larva of the moth Mompha capella inhabits a flower bud of Canada Frostweed and prevents it from opening, as Neil Kirk Hillier and fellow researchers show. Pollinators cannot visit the flower, which has to pollinate itself instead.

Canada Frostweed (Crocanthemum canadense), a perennial plant of Northern America, is attractive to the moth Mompha capella, which lays its eggs on it. Then something unusual happens: the plant loses control over its reproduction.

The plant produces yellow flowers that normally open just after sunrise, revealing the female pistil and male stamens. Bees and flies visit the flowers, transferring the pollen from one to the next, so that the flowers are cross-pollinated. Multiple stamens lay against the five yellow petals, retracted from around the pistil to prevent self-pollination. Within a few hours, a flower’s own pollen has disappeared and the pistil is covered with pollen from other flowers. The petals fall off, the green sepals close over the pistil and protect the developing fruit with seeds within.

But when a moth has left its eggs on the plant, the larvae that hatch from these eggs crawl into a flower bud, one larva per bud. And then things are very different, Neil Kirk Hillier and colleagues discovered.


The larvae start to eat. And they don’t do it randomly, but first feed on the bases of the still folded petals. The severed petals no longer grow and don’t unfold when the flower should open, but remain folded like a cap over stamens, pistil and developing fruit, keeping the flower closed. Pollinators cannot enter. Because the stamens are compacted around the top of the pistil, the pollen is in contact with the pistil and seeds develop through self-pollination. Almost all of them will be consumed by the larva in the end.

Frostweed duped

As a consequence, the Canada Frostweed plant produces less offspring. A yellow flower produces on average about forty seeds, and a larva saves only one or two of them. Reproduction, however, is not in immediate danger. This is because the plant not only produces a small number of yellow flowers that open, unless caterpillar disturbs the process, but also a large number of flowers without yellow petals and only four or five stamens, which appear later in the year. These flowers never open and produce seeds through self-pollination. While they make less seeds than yellow, open flowers (only six or seven seeds per flower), there are much more of them. So seeds are produced anyway.

But seeds of open flowers that develop after cross-pollination are necessary for the exchange of hereditary material. In plant populations with a high infestation rate, such exchange is limited, and genetic variation is low.

Larva safer?

The researchers don’t mention what benefit a larva gains by intervening in the flowering process. If the flower opened and had been pollinated normally, seeds to be consumed would have appeared as well. Perhaps in a closed flower, the larva is safer from predators and parasites.

Willy van Strien

Photo: Homer D. House, 1918 (Wikimedia Commons)

Hillier, N.K., E. Evans & R.C. Evans, 2018. Novel insect florivory strategy initiates autogamy in unopened allogamous flowers. Scientific Reports 8: 17077. Doi:10.1038/s41598-018-35191-z

Role pattern erased

Twisted-wing parasites change the behaviour of host wasps

The paper wasp Polistes dominula is host to a manipulating parasite, Xenos vesparum

The life cycle of the parasite Xenos vesparum is closely linked to that of the wasps in which it lives. It modifies their behaviour in such a way that it meets its needs, as Laura Beani and colleagues demonstrate.

It is often creepy as well as fascinating to see how parasites control their host. A nice example is Xenos vesparum, parasite of the European paper wasp (Polistes dominula). Its manipulation skills are being unravelled by Laura Beani and her colleagues.

The parasite, which belongs to the insect group of twisted-wing parasites, has a bizarre life cycle, with a striking difference between males and females. In the larval stage, the parasite lives within a wasp host. Males pupate in their host; the front part of the pupae extrudes trough the cuticle between the plates of the host’s abdomen. When adult males emerge, they leave their host to live freely; within a day, they die.

Females live much longer. They remain in their host and don’t pupate, but turn into a ‘bag’ filled with egg cells and a fat supply. Only their cephalothorax, into which head and thorax are fused together, is tough and visible between the plates of the host’s abdomen. Usually only one parasite, either male or female, will mature in a parasitized wasp.

Male and female parasite must mate on the wasp in which the female lives. They do it fast.

Wasp colony

Xenos parasites effectively exploit the annual cycle of their host. In March, fertilized wasp queens, which have spent the winter in groups, awaken. Every queen occupies a place to establish a colony. She builds an open nest and lays the first eggs, which will produce workers. Before these eggs have developed into adults, the queen also has to collect food and take care of the brood. But later, from May, she is just laying eggs, while the workers, who don’t reproduce themselves, do the rest of the work.

In summer, the colony is flourishing with a maximum of fifty wasps, and it is time for the next step. The queen now starts laying eggs that will develop into males and sexual females, future queens. Males and sexual females (gynes) appear in July-August.


Then the queen has finished her task. She stops and the colony collapses. The gynes leave the nest and in early autumn, they aggregate in groups that attract males. Mating follows. As winter approaches, the fertilized gynes search for a sheltered place, again aggregating; they often cluster in buildings, for example under roof tiles. There they hibernate and wait for the spring. Males and worker wasps die before winter. In March, the new queens awaken from winter diapause and the cycle starts again.

The European paper wasp is a common species, and it is not as annoying as the common wasp, Vespula vulgaris.

Trumpet creeper

The parasite disturbs the role pattern of its host. But not immediately. In May, tiny parasite larvae penetrate into worker wasp larvae, which appear to be little affected by the presence of the parasite. Only when the hosts have developed into a pupa, the parasite larvae undergo a growth spurt and mature.

And then the manipulation starts: parasitized workers do not stick to their role. They are lazy and at the age of one week, they will leave the nest.

Beani, doing research in Tuscany, describes how in early summer the parasitized worker wasps are mainly to be found on trumpet creeper bushes; the trumpet creeper, originating from North America, has naturalized in Europe. It produces a lot of nectar, which the parasitized wasps enjoy. Healthy, non-parasitized wasps spend much less time on this plant. Because the hosts deserted the nest and moved to trumpet creeper, the parasites easily find a partner with which they can mate. In the wasp nest, mating would be impossible, as parasite males would immediately be chased off by healthy workers.

Castration by Xenos

Parasite embryos develop within the fertilized parasite females in a wasp’s body and new parasite larvae emerge at the end of July. A female parasite releases more than three thousand larvae which all need a host to develop. When healthy foraging wasps pass by, larvae cling to them, are transported to the wasps’ nest and start searching for wasp larvae. Among infected wasp larvae, there will now be putative males and sexual females, which were destined to reproduce. But they will never do the job, as the parasite castrates them.


From mid-July on, parasitized wasps (workers, males and gynes) form groups outside the nests, just like healthy young sexual females will do later in the season: the role pattern is erased. They gather on high plants and later on buildings, usually places where healthy males gather every year or where future queens use to overwinter. The parasitized wasps are inactive, the parasites have much opportunity to mate.

When healthy sexual wasp females fly out and aggregate, they often join these groups of parasitized wasps.

At the end of the season, when the gynes have been fertilized and gather at places to hibernate, wasps that contain a fertilized parasite female will join them. Parasite females safely spend the winter in a wasp body, in a group of wasps on a sheltered place. Wasps that carried a parasite male have no function anymore; they die in autumn.


When healthy young queens leave to establish a colony in spring, parasitized wasps are left behind. A few weeks later, when the first wasp larvae have hatched in wasp nests, the parasites release their larvae. They then apply a last manipulative trick: they induce their host wasp to deliver the mature larvae in several young wasp nests. There are still no adult workers to defend these nests and the queen is often gone to collect food. From within her host, the parasite female drops larvae in the nests. She also drops some larvae on plants, as a foraging wasp may come along and take them with it.

And so the Xenos parasite completes the circle – with enforced cooperation of the host.

Willy van Strien

Photo: European paper wasp. ©Hans Hillewaert (Wikimedia Commons, Creative Commons BY-SA 4.0)

Xenos peckii mating on YouTube

Beani, L., F. Cappa, F. Manfredini & M. Zaccaroni, 2018. Preference of Polistes dominula wasps for trumpet creepers when infected by Xenos vesparum: A novel example of co-evolved traits between host and parasite. PLoS ONE 13:e0205201. Doi: 10.1371/journal.pone.0205201
Beani, L., R. Dallai, D. Mercati, F. Cappa, F. Giusti & F. Manfredini, 2011. When a parasite breaks all the rules of a colony: morphology and fate of wasps infected by a strepsipteran endoparasite. Animal Behaviour 82: 1305e1312. Doi: 10.1016/j.anbehav.2011.09.012
Beani, L., 2006. Crazy wasps: when parasites manipulate the Polistes phenotype. Annales Zoologici Fennici 43: 564-574.
Hughes, D.P., J. Kathirithamby, S. Turillazzi & L. Beani, 2004. Social wasps desert the colony and aggregate outside if parasitized: parasite manipulation? Behavioral Ecology 15: 1037-1043. Doi: 10.1093/beheco/arh111

Gruesome boost

Damaged cicadas spread fungal spores via sexual behaviour

Magicicada species are manipulated by the fungus Massospora

Massospora fungi produce substances that we know as recreational drugs, Greg Boyce and colleagues write. By doing so, they manipulate the behaviour of cicadas in which they proliferate. The insects face a horrible fate.

The fungus Massospora cicadina infects periodical cicadas of the genus Magicicada and manipulates the behaviour of infested insects in such a way that they will transmit the fungal spores to conspecifics. Horribly enough, they do so by sexual activities, while their rear part has already been largely destroyed and turned into a fungal mass. Greg Boyce and colleagues try to find out how the fungus exerts its dismal influence.

Magicicada species, which live in the east of North America, are almost never to be seen. They spend most of their life underground as nymphs, the immature form. Only once in many years – some species take thirteen years, other species take seventeen years – mature nymphs emerge from the soil, synchronously and massively per species and per area. They moult into mature cicadas that live only for four to six weeks. In this period, they mate and the females lay their eggs on tree branches. Young nymphs fall down and disappear in the soil.

This unusual life cycle makes it very difficult for natural enemies such as birds to specialize on adult cicadas, because they would not be able to find prey for many years while occasionally, once in thirteen or seventeen years, there is an overwhelming amount.

But the fungus Massospora cicadina can deal with the life cycle of these cicadas.

Copulation attempts

Fungal spores rest in the soil until nymphs emerge and then infect them. After moult, the fungus proliferates in the abdomen of adult insects. Eventually, their rear part, genitals included, falls off and a fungal spore mass becomes visible.

The heavily damaged cicadas try to mate, even more vigorously than normal. Of course, this is useless to them, but the fungus benefits: during the copulation attempts, the unfortunate cicadas transmit spores to conspecifics.

In these insects, the fungus forms a second infection stage. Because now time runs out for the adult cicadas, a third infection is not feasible. Therefore, instead of infective spores, the fungus produces resting spores, which fall down and wait in the soil until the next generation of cicadas appears.

Bisexual males

Earlier this year, John Cooley and colleagues described deviant behaviour in males with a first stage infection. Normally, males sing in chorus to lure females. When a female shows interest in a male, she makes a flicking wing movement that is tuned to his song. He then utters more complex song, she answers with a tightly timed wing-flick, and a ‘duet’ is created while the two approach each other.

First stage infected males try to acquire a female mate in the normal way. But they also respond to the song of other males with female-like wing-flicks. As a result, not only females, but also males are attracted – and become infected. The fungal infection spreads extra fast.

It is striking that only males with a first stage infection assume a female role besides a male role. Males with a second stage infection, which does not produce infective spores, don’t exhibit wing-flicks.

Stimulating drug

Now, Greg Boyce shows how the fungus manages to affect the behaviour of the cicadas. Among the substances that it produces in the cicadas’ abdomen is cathinone. This is known as the active substance in khat, which is released when chewing leaves of the Khat plant, Catha edulis. It is surprising that a plant and a fungus share this substance. Cathinone is closely related to amphetamine, or speed, a stimulating drug, and just like the drug, it interferes with the communication between nerve cells. Apparently, this results in abnormal behaviour in male cicadas.

In a first stage infection, in which the cicadas transmit the fungus spores to conspecifics, the fungus produces more of this stimulating substance than in a second stage infection, which shows how accurately it manipulates its host.

Another Massospora fungal species, which infects cicadas with an annual cycle (Platypedia species), also manipulates the sexual behaviour of its victims, Boyce and colleagues discovered. It produces psilocybin, a hallucinogenic substance known from certain mushrooms, most importantly Psilocybe species. Again a remarkable finding, as the fungus is not closely related to these mushroom species.

Willy van Strien

Photo: Magicicada septendecim. Judy Gallagher( Wikimedia Commons, Creative Commons CC BY 2.0)

Boyce, G.R., E. Gluck-Thaler, J.C. Slot, J.E. Stajich, W.J. Davis, T.Y. James, J.R. Cooley, D.G. Panaccione, J. Eilenberg, H.H. De Fine Licht, A.M. Macias, M.C. Berger, K.L. Wickert, C.M. Stauder, E.J. Spahr, M.D. Maust, A.M. Metheny, C. Simon, G. Kritsky, K.T. Hodge, R.A. Humber, T. Gullion, D.P.G. Short, T. Kijimoto, D. Mozgai, N. Arguedas & M.T. Kasson, 2018. Discovery of psychoactive plant and mushroom alkaloids in ancient fungal cicada pathogens. BioRxiv preprint, July 24. Doi: 10.1101/375105
Cooley, J.R., D.C. Marshall & K.B.R. Hill, 2018. A specialized fungal parasite (Massospora cicadina) hijacks the sexual signals of periodical cicadas (Hemiptera: Cicadidae: Magicicada). Scientific Reports 8: 1432. Doi: 10.1038/s41598-018-19813-0
Cooley, J.R. & D.C. Marshall, 2001. Sexual signaling in periodical cicadas, Magicicada spp. (Hemiptera: Cicadidae). Behaviour 138, 827-855. Doi: 10.1163/156853901753172674

Multi-coloured livestock

Thanks to tending ants, mixed aphid colonies persist

Lasius japonicus tending its two-coloured livestock

The aphid milking ant Lasius japonicus ensures long-lasting coexistence of two colour morphs of the mugwort aphid, from which it harvests honeydew, Saori Watanabe and colleagues write. Without intervention, its favourite colour would be displaced.

Like many other ants, the Asian ant Lasius japonicus has a mutualistic relationship with aphids. The aphids suck sap from their host plant and excrete excess sugars, dissolved in a liquid: honeydew. The ant fights off their natural enemies and harvests (‘milks’) the sugary honeydew. One of its mutualistic partners is the Japanese mugwort aphid, Macrosiphoniella yomogicola, which lives on mugwort, a common plant of Europe and Asia. The protection by the ant is of crucial importance to the aphids; each colony will fall victim to its enemies if not protected.


The mugwort aphid occurs in different colours, with red and green as the most common types; large green specimens will turn black. The ant has a preference for the green morph, Saori Watanabe and colleagues show, because it excretes a higher quality honeydew. But as a consequence, the red morph, which retains a larger proportion of the sugars that it obtains from the host plant, can reproduce at a higher rate. All aphids are females that reproduce parthenogenetically, their young being clones of their mother. Red aphids produce red daughters, green aphids green daughters. The green morph runs a risk to be displaced by the red one, which multiplies faster.

But, as it turns out, the ants prevent this from happening. The researchers show that the red aphids indeed are able to multiply faster than the green ones. As a consequence, in laboratory experiments, the proportion of green aphids in a mixed colony decreased, but only if the researchers withheld attending ants. If, however, ants were allowed to join the aphids, the reproduction rate of the green morph increased, and the green aphids now reproduced as fast as the red aphids. Thus, in the presence of ants, the proportion between green and red morphs was stable.

It is not clear how the ants improve the reproduction rate of the green aphids, but it saves the green morph from local extinction.


In the field, almost all colonies are mixed. It is understandable that no pure red colonies are to be found. No ant would be interested in such colony, which produces only low quality honeydew, so it would be lost. But why don’t green colonies exist? Why wouldn’t the ants remove the red aphids from a mixed colony by eating them, so that only high quality honeydew would be produced?

Apparently, the presence of red aphids is advantageous for some reason. That has to do with the winter period, the researchers suggest. At the end of the season, the aphids give birth to daughters and sons, which mate and produce fertilized eggs that can overwinter if the host plant survives. However, after flowering in autumn, mugwort dies off. The researchers hypothesize that red aphids may suppress flowering, so that the plant persists. They are now going to test that idea.

Need each other

It would mean that the ant needs both aphid morphs, the green one for high quality honeydew, the red one to maintain the colony to the next season. It would also mean that the two types of aphids need each other. The red morph cannot do without the green one, which attracts attending ants, and the green morph cannot do without the red one, which prevents the host plant from dying off in winter.

But as dependent the aphid morphs may be on each other, they cannot live together for a long time without the ant interfering.

Willy van Strien

Photo: aphid tending ant Lasius japonicus and two colour morphs of Macrosiphoniella yomogicola. ©Ryota Kawauchiya

Watanabe, S., J. Yoshimura & E. Hasegawa, 2018. Ants improve the reproduction of inferior morphs to maintain a polymorphism in symbiont aphids. Scientific Reports 8: 2313. Doi: 10.1038/s41598-018-20159-w
Watanabe, S., T. Murakami, J. Yoshimura & E. Hasegawa, 2016. Color polymorphism in an aphid is maintained by attending ants. Science Advances 2: e1600606. Doi: 10.1126/sciadv.1600606