Emergency leap after mating

Spider male escapes from cannibalism

Philoponella prominens male jumps away to safety after mating

With a catapult mechanism, a male of the spider Philoponella prominens manages to escape his hungry partner after copulation. Shichang Zhang and colleagues recorded it on video.

For many male spiders, mating is life-threatening. Because to a female, a male not only is a supplier of sperm that she can use to fertilize her eggs, but also a tasty snack. And when he has given his sperm, he is just a meal. Dying without siring offspring is no option. So, he has to proceed with caution, and leave immediately after finishing copulation.

A Philoponella prominens male, a spider species from woods of central China, is very accomplished. After mating, he swiftly leaps away, out of her reach, Shichang Zhang and colleagues show. They recorded mating and leaping with a high-speed camera.

High pressure

During mating, which lasts half a minute, he folds his two front legs against her, the researchers observed. By suddenly stretching them afterwards, he pushes off and shoots away. He had already secured himself before with a safety line of silk, which he had tied to the edge of her web. After leaping, he crawls back via that line to mate with her again. He is able to repeat the action up to six times.

Spiders move their legs not only with muscles, but also use hydraulics. They bend the legs by contracting flexor muscles but lack extensor muscles. Instead, they fill the joints with body fluid at high pressure, so that the legs stretch by released hydraulic power as the flexor muscles are relaxed. In this way, a male Philoponella prominens jumps from his partner. He reaches a speed of about seventy centimeters per second, spinning around at high speed. A female is unable to grasp him.

The leap is lifesaving, as the researchers showed. If they prevented a male from leaping with a fine brush, he was grabbed by his partner and eaten. As if he were just prey.

Willy van Strien

Photo: Philoponella prominens, mala above female. © Shichang Zhang

Emergency leap on video

Another spider male that has to be careful: Maevia inclemens

Source:
Zhang, S., Y. Liu, Y. Ma, H. Wang, Y. Zhao, M. Kuntner & D. Li, 2022. Male spiders avoid sexual cannibalism with a catapult mechanism. Current Biology 32: R341-R359. Doi: 10.1016/j.cub.2022.03.051

First migration trip in Caspian tern

Father teaches young bird how to travel

Caspian tern father accompanies young during first autumn migration

Young Caspian terns learn from their father how to migrate to the wintering grounds. When, in following years, they make that autumn trip independently, they remember their fathers’ lesson, Patrik Byholm and colleagues show.

A young Caspian tern that is born at the end of May along the coast of Finland or Sweden, will migrate to West Africa at the end of summer to hibernate there. Its father’s job is to guide it on that first journey, Patrik Byholm and colleagues noted.

The researchers wanted to know how information about autumn migration – route and stopover sites – is passed on from one generation to the next. To find out, they equipped birds with GPS tracking devices.

The Caspian tern, Hydroprogne caspia, is found in many places in the world. In Europe, it also breeds along the Black Sea and the Caspian Sea, and in North America along ocean coasts and the great lakes. Some birds from Finland and Sweden make a stop in the Netherlands during their migration to Africa. They travel singly or in small family groups, which are single-parent families.

Reduced tempo

The collected travel data shows that couples that started a nest with two or three eggs in spring and raised their young together, leave each other after the breeding season. They travel separately, sometimes weeks apart, to the wintering area.

Young birds travel with one of the parents, and mostly, that is the father. They cannot travel safely on their own: young terns that for one reason or another lose contact with parents, are captured by birds of prey. So, they stay close to their father during the trip. He teaches them the route and knows good stopover sites, where the birds can roost and forage during the migration. The lesson is learned: the young birds will follow the same route southwards in the years that follow, using the same stopover sites.

Fathers that accompany one or a few young, will adjust their tempo a bit. They progress less quickly than adult birds traveling alone. This is mainly because young birds take more time to rest.

After arrival, the bond between father and young loosens and parental care finishes. They gradually spend less time without each other, and after a month or two they stop seeing each other at all. Sometimes, a young travels a little further south, in the company of another congener.

Willy van Strien

Photo: Colony of Caspian tern. Dmitry Mikhirev (Wikimedia Commons, Creative Commons CC BY-SA 3.0)

Source:
Byholm, P., M. Beal, N. Isaksson, U. Lötberg & S. Åkesson, 2022. Paternal transmission of migration knowledge in a long-distance bird migrant. Nature Communications 13: 1566. Doi: 10.1038/s41467-022-29300-w

Increasing efficiency in brood parasite

Cuckoo catfish improves its timing

Cuckoo catfish, Synodontis multipunctatus, improves efficiency by practizing

It is not easy for a cuckoo catfish to get its eggs adopted by intended host parents, because these are wary. But it learns the trick by experience, as Holger Zimmermann and colleagues show.

Cuckoo catfish dump their eggs at host parents to let them take care of their offspring: they are brood parasites. That seems easy and, in a way, it is, because the eggs can develop safely without the real parents having to worry. But they do have to bring them to the host parents, and that is not so easy. In that sense, cuckoo catfish spend more effort for their offspring than most fish, which simply lay eggs and leave them behind.

They have to practice the art of parasitism, Holger Zimmermann and colleagues write. The cuckoo catfish (Synodontis multipunctatus) is, as far as we know, the only fish species that, like a cuckoo, relegates the raising of its offspring to others. It lives in Lake Tanganyika in Africa.

Abuse

It takes advantage of species of cichlids that have the most extensive form of parental care, the so-called mouthbrooders. In these species, mothers take the fertilized eggs in the mouth and keep them there until they hatch, after a few weeks.

During spawning, such mouthbrooding cichlids circle around each other and release eggs and sperm; in between acts, they defend the spawning site against intruders.

But a group of cuckoo catfish may intrude. They consume some cichlid eggs before the mother has been able to collect them and drop a few eggs themselves and fertilize them. The cichlid mother panics and collects her eggs as fast as she can; in her haste, she also takes up catfish eggs.

The catfish must interfere at exactly the right time, when the female cichlid is busy laying eggs; it’s a matter of seconds. By experience, they learn to improve the timing of egg laying and fertilization, Zimmermann shows with experiments in tanks, in which he exposed cichlids (4 males and 12 females) to three cuckoo catfish pairs.

Sharper timing

The researchers searched for host parents that have no resistance against the underwater cuckoo. With resilient host parents, the learning process of the parasite would not show up. They selected the mouthbrooder Astatotilapia burtoni, which lives in Lake Tanganyika and is known to the catfish. But they took a population from a neighbouring river, where the cuckoo catfish does not occur. The chosen host parents have no innate defences against cuckoo catfish, nor do they learn to avoid it, but they do behave aggressively towards any fish that disturb the spawning to predate on eggs.

Unexperienced cuckoo catfish almost never managed to get their eggs taken up by these host parents. Only 3 percent of their attempts succeeded. But after some time – in the experiments after four months, about 30 attempts – things got much better: more than 25 percent of the attempts now was successful. That success rate did not increase further. Experienced catfish also managed to consume more eggs of the host parents in the brief time available.

The improvement was possible because the parasites learn to lay and fertilize their eggs at precisely the right time, as behavioural observations showed. In addition, groups of catfish improve the coordination of their intrusive act.

Host parent is loser

Most attempts fail, though, even in experienced cuckoo catfish, because the vigilant cichlids outsmart their enemy. But that does not matter, because the profits for the parasite are large if the action does succeed. A host mother then carries on average five parasite eggs. The catfish will hatch sooner than the cichlids, and the young catfish devour some cichlid embryos.

The host mother is the loser. She is abused and produces fewer young of her own.

Willy van Strien

Photo: Cuckoo catfish. Calwhiz. (Via Flickr, CC BY-NC-ND 2.0)

Cichlids from Lake Tanganyika have learned to coexist with cuckoo catfish

Source:
Zimmermann, H., R. Blažek, M. Polačik & M. Reichard, 2022. Individual experience as a key to success for the cuckoo catfish brood parasitism. Nature Communications 13: 1723. Doi: 10.1038/s41467-022-29417-y

Flower opener

Without flying fox no fruits on Dillenia tree

Flowers of Dillenia biflora have to be openend by a flying fox

The flowers of the tree Dillenia biflora cannot open on their own. That means that the pollinator, a flying fox, has an extra job to do, Sophie Petit and colleagues write.

The relationship between a plant and its pollinators can be special, and the tree Dillenia biflora may have one of the most remarkable. Its peculiar flowers cannot open. Their petals are fused and form a globose corolla, a lid that covers the anthers and stigma.

Dozens of Dillenia species exist that are pollinated by bees that come to collect pollen; these species do not offer them nectar. So, it was a mystery what happens in Dillenia biflora with its permanently closed flowers and inaccessible anthers. There must be pollinators, because the tree produces fruits with seeds and the flowers cannot self-pollinate. Sophie Petit and colleagues wondered: who are the pollinators, and how do they do it?

Long teeth

Flower of Dillenia biflora is tightly closedThe flowers produce scent, are pale-coloured, large and stout and last only one night. People had noticed large bats, or flying foxes, near the trees at night, and pollen was found in flying fox droppings. These findings suggested that these animals play a role in pollination. On the floor, corollas can be found with four tiny holes.

To find out what happens, the researchers placed video cameras near trees at night, when flying foxes are active. They conducted their research on Fiji’s two largest islands, Vanua Levu and Viti Levu, where Dillenia biflora grows in rainforests.

The footage was clear. Trees are visited at night by the Fijian blossom bat Notopteris macdonaldi, which roosts during the day in large groups in caves. The animals grasp the lid of a flower with their four long canines, pull it away and drop it. Hundreds of anthers and a stigma then are accessible.

Mutual dependence

A flying fox has good reason to do the job: unlike those of related species, the flowers of Dillenia biflora turn out to contain a copious amount of nectar. While the animal is drinking, its snout gets covered with pollen, part of which ends up on the stigma of the next flower it visits. That flower is then pollinated and will form seeds.

It is beneficial for a flower to remain closed. The contents then are safe from rain, from insects that feed on them, and from moths and geckos that sip nectar without pollinating the flowers.

The researchers suspect that more Dillenia species have a similar exclusive relationship with flying foxes, because more species exist with flowers that do not open. They also think there are more bat species that open the flowers and enjoy the hidden food source, such as the Pacific flying fox, Pteropus tonganus.

These trees are completely reliant on nectar-feeding bats that remove the corollas: without their visit, the flowers are aborted and don’t reproduce. Conversely, nectar is the main food source for these flying foxes. That has implications for nature conservation. Many Dillenia species are threatened, and to conserve them, it is necessary that the bats do well. In turn, the flying fox Notopteris macdonaldi is a vulnerable species, and its conservation requires that the trees do not disappear.

Willy van Strien

Photos:
Large: The Pacific flying fox Pteropus tonganus also possibly opens Dillenia flowers; it feeds on fruits, pollen and nectar. Paul Asman, Jill Lenoble (Wikimedia Commons, Creative Commons, CC BY 2.0)
Small: Labeled flower of Dillenia biflora. © Sophie Petit

Source:
Sophie Petit, S., A.T. Scanlon, A. Naikatini, T. Pukala & R. Schumann, 2022. A novel bat pollination system involving obligate flower corolla removal has implications for global Dillenia conservation. PLoS ONE 17: e0262985. Doi: 10.1371/journal.pone.0262985

Valves closed

Blue mussels learn to avoid parasites

blue mussels close their shells when parasites are around

Blue mussels adapt their behaviour when parasitic larvae are nearby, according to research by Christian Selbach and colleagues.

During food intake, blue mussels, Mytilus edulis, run a risk. The bivalve molluscs feed by filtering water. It enters through an inlet and flows over gills, which not only take oxygen from the water, but also food particles, mainly plankton. These particles get stuck on a mucous layer and are transported to the stomach. The water exits through an outflow opening.

With the inflow of water, mussels may ingest larvae of a harmful parasite.

Mussels that encountered the parasite before, have learned to be more careful. If they notice the presence of parasites in the water, they close their valves and stop filtering to avoid further infection, Christian Selbach and colleagues show.

Intermediate host

The parasite, the fluke (or trematode) Himasthla elongata, has a complicated life cycle in which mussels are indispensable. The cycle starts in a bird that lives near or at sea, such as an oystercatcher, common eider, or scoter; in these animals, adult parasites thrive. They mate and produce eggs that end up in the water with the bird’s faeces. The eggs hatch and the larvae, so-called miracidia, are eaten by common periwinkles; the small snails are the first intermediate host.

In the snails, the parasites develop into the next larval stage, the cercariae, which also end up in the seawater. These are the larvae that infect filtering mussels, which are the second intermediate host. Mussels live in the tidal zone, near the coast, where they can form large shell reefs.

After ingestion by mussels, the parasitic larvae form cysts, a resting stage. Infected mussels grow poorly and are vulnerable to predation by oystercatcher, eider or scoter. And that completes the circle: those birds are the primary host. Once a bird has eaten infected mussels, the parasites mature, and the story starts all over again.

Shut off

If infective larvae are present in the water, mussels cannot help ingesting them when filtering. The only thing they can do to avoid infection is to stop taking in water. But that has a price, because it also means that they cannot take in oxygen and food.

Yet they stop, according to Selbach’s experiments in which he exposed mussels to infective larvae. But they have to learn it.

Mussels that have no previous experience with the parasites go on filtering when they are exposed to larvae. But mussels that met the parasite before and got infected, now shut themselves off. They reduce filtration activity and close the valves with the adductor muscles, which costs energy. But apparently, it would be worse to ingest another dose of parasitic larvae.

Now, it would be interesting to find out how the mussels notice that there are infective larvae around; that is still unclear.

Willy van Strien

Photo: blue mussel. Inductiveload (Wikimedia Commons, public domain)

Source:
Selbach, C., L. Marchant & K.N. Mouritsen, 2022. Mussel memory: can bivalves learn to fear parasites? Royal Society Open Science 9: 211774. Doi: 10.1098/rsos.211774

Flying saucers

Dance fly female advertises quality by inflating her body

Feamle long-tailed dance fly advertises quality by making herself bigger

Shaped like flying saucers, long-tailed dance fly females seek the attention of males. Their wide shape indicates their quality, Jessica Browne and colleagues write.

Females of the long-tailed dance fly (Rhamphomyia longicauda), which lives in North America, possess ornaments that make them attractive to males. They have sacs on either side of their abdomen and feathery black scales on their legs. By inflating the sacs and wrapping the legs along them while flying, they become laterally expanded. In this way, they show their quality, Jessica Browne and colleagues argue.

Sex roles reversed

In most animal species, females are choosy and males try to impress them by showing off. But in long-tailed dance flies, it is just the other way around: the males are choosy, the females try to seduce them to mate.

The reason is that females are unable to gather their food on their own. They need food to produce eggs, but cannot hunt for the smaller insects on which they live. That is why they have to to be provisioned by males. A male intending to mate brings a prey as a nuptial gift. Females mate frequently, because every mating yields a meal. But males have to catch prey first. That is hard for them, and a male that has gone to all that trouble will offer his gift only to a female that deserves it.

Silhouette

In order to seduce males, females gather in a lek. At dawn or dusk they form a swarm of dozens of flies in a clearing in the forest and ‘dance’ about half a meter above ground level. Males that have captured a prey will approach such swarm from below and see the females silhouetted against the dimly lit sky. Upon detection of an attractive female, a male will hover just below her. She doesn’t miss the chance and immediately drops on him. Together they leave the swarm to mate. She stores his sperm to fertilize eggs with later.

Males prefer large females. To be attractive, females inflate their sacs, lift their legs and wrap them along the laterally expanded sacs, so that their silhouette becomes much wider. They look like flying saucers. The wider a female is, the greater her chance of being chosen.

But what exactly does a large silhouette signify? Why is it beneficial for males to choose such inflated female?

Magnified difference

The higher the quality of a long-tailed dance fly female is, the wider she can make herself, as Browne and colleagues show. A dance fly begins its life as a larva. After pupation, an adult fly emerges with dimensions that are fixed; also the size of the sacs and the scales on the legs of females is fixed. Probably, the size of an adult fly is an indication of quality and a result of how good conditions were during its larval stage. Now, it turns out that the larger a female is, the larger her expandable sacs and leg scales are in proportion. Because large females can make themselves relatively wider, the differences in quality that exist between females are magnified.

Males preferring inflated females are choosing quality.

Paternity not guaranteed

Their choice is a good one, because a wide female potentially produces many eggs. And because she is attractive, she will be chosen frequently and fed many meals, so she will be able to indeed develop those eggs. She also has a good chance of surviving long enough.

But a male that chooses an attractive female can only hope that he will sire some of that progeny. If he is the first to mate her, she will use his nuptial gift to initiate egg development, but by the time she is going to lay them, she has stored sperm from many more males and his chances are small. A male probably has the best chance to sire much offspring if he is the last to mate with her before she starts laying eggs, when they are almost mature.

But in what state of development the eggs of an attractive female are, a male cannot infer from her size. He must be choosy, but he must also be lucky.

Willy van Strien

Photo: Female Rhamphomyia longicauda with inflated sacs. ©Heather Proctor

Sources:
Browne, J.H. & D.T. Gwynne, 2022. Deceived, but not betrayed: static allometry suggests female ornaments in the long‑tailed dance fly (Rhamphomyia longicauda) exaggerate condition to males. Evolutionary Ecology, online Jan. 7. Doi: 10.1007/s10682-021-10148-3
Murray, R.L., J. Wheeler, D.T. Gwynne & L.F. Bussière, 2018. Sexual selection on multiple female ornaments in dance flies. Proceedings of the Royal Society. B 285: 20181525. Doi: 10.1098/rspb.2018.1525
Funk, D.H. & D.W. Tallamy, 2000. Courtship role reversal and deceptive signals in the long-tailed dance fly, Rhamphomyia longicauda. Animal Behaviour 59: 411-421. Doi: 10.1006/anbe.1999.1310

Content with second place

European pied flycatcher may prefer to be a concubine

Female pied flycatcher may become secondary mate of a male

A high quality male is so desirable that a female pied flycatcher may be willing to become his secondary mate – as long as it is not too hard to take care of the young without his assistance, Simone Santoro and colleagues write.

Like most passerine birds, the European pied flycatcher (Fidecula hypoleuca) is mainly socially monogamous. But some males have a secondary female. This concubine gets little help from him when raising the young, but in good years, when food is abundant, that may not be a major problem, Simone Santoro and colleagues argue.

Short breeding season

The males are the first to return from the wintering area in Africa, mid-April. They look for a suitable nest hole, which can be a tree cavity or nest box, and defend a small territory around it. Once a male occupies a good place, he tries to attract a female to breed with. Females visit a number of males before making their choice.

A couple is then busy for about five weeks. She lays five or six eggs and starts breeding when the clutch is complete. Both parents feed the young until they fledge, and dad defends the family. The breeding season covers the months of May and June; only one clutch can be raised in this period. But some males want more.

Good genetic quality

To get more, an ambitious male will have to occupy a second nest site and attract another mate. If successful, he will have to divide his paternal efforts over two nests. The research group, which works in Spain, had already shown how things go.

Males that succeed in starting a second nest are birds that have arrived and started breeding early, and that are able to defend two nests against rivals. These are strong males: of high genetic quality and in good condition. Such male stays with his first mate during the week that she is laying eggs. When she starts incubating, he tries to seduce to a second female. Usually, a second nest is located close to the first one.

When the young hatch in the first nest, he goes there to help feeding them. The primary female gets his full attention. Only when that first nest has fledged does he offer his services to the second nest.

So, the secondary female is worse off, as she has to feed the kids on her own for a while: that is hard work and she will see fewer young fledge. But, on the other hand, these young inherit a good genetic quality from their father. That is why a female may prefer to be the secondary mate of a high quality male rather than the only mate of a low quality male.

Fat and lean years

Particularly later in the season – when desirable single males are not available anymore -the choice to become a secondary female can turn out fairly well, because the time interval between father’s first and second brood will be larger and he will start helping on the second nest earlier.

Now, the researchers show that the availability of food also matters.

Because secondary females have to work harder than females in a monogamous relationship, their chance of survival is lower. (That is also true for primary females. Apparently, the situation is not ideal for them either, but it isn’t their choice.)

However, the lower survival rate of secondary females is an average over years; the researchers followed the birds for 26 seasons. The survival rate varies from one year to the next. In good years, a secondary female has less difficulty raising her young and her chance to survive is almost as high as that of a female in a monogamous relationship. To assess whether a year was good or bad, the researchers considerd the percentage of young that survived and fledged. A good year probably is a year in which food is abundant. In such year, a female can more easily accept a secondary position.

And sometimes. she does, as it turns out: in fat years it is more common for a male to have two families than in lean years. But even then, monogamous relationships remain the majority.

Willy van Strien

Photo: Caroline Legg (Wikimedia Commons, Creative Commons CC BY 2.0)

Sources:
Santoro, S., P. Fernández‑Díaz, D. Canal, C. Camacho, L.Z. Garamszegi, J, Martínez‑Padilla & J. Potti, 2022. High frequency of social polygyny reveals little costs for females in a songbird. Scientific Reports 12: 277. Doi: 10.1038/s41598-021-04423-0
Canal, D., L. Schlicht, J. Manzano, C. Camacho & J. Potti, 2020. Socio-ecological factors shape the opportunity for polygyny in a migratory songbird. Behavioral Ecology 31: 598–609. Doi: 10.1093/beheco/arz220

Hurry up please

Spikethumb frog males transfer messages to females by biting

Spikethumb frog males bite partner during mating

Males of three spikethumb frog species give their mate a chemical message during mating, using their upper teeth, as Lisa Schulte and colleagues show.

During mating, males of some species of spikethumb frogs (Plectrohyla) press their upper lip onto their mate’s head or back. That’s not exactly a caress, on the contrary: they scrape their teeth over it, Lisa Schulte and colleagues found. The scratches are clearly visible afterwards. Why would they do this?

Swollen lips

In three species, females are found that have scratches on their head or back: Hartweg’s spikethumb frog (Plectrohyla hartwegi), Matuda’s spikethumb frog (Plectrohyla matudai), and arcane spikethumb frog (Plectrohyla sagorum). The distance between the scratches is similar to the distance between the upper teeth of the males, which are elongated and protruding. These frogs live in the South American tropics.

In addition to elongated teeth, the males have swollen upper lips during the breeding season. They turn out to contain specialized, large glands. These produce mucus and excrete it on the inside and outside of the lips. The researchers found several proteins in the mucus, including proteins known from salamanders as messenger molecules with which the animals communicate with each other.

Direct message

The conclusion is that during mating, the males transfer the mucus of the glands into their partner’s skin with teeth and lips. These proteins are probably taken up by the blood and delivered elsewhere. As a consequence, eggs are laid more quickly, the researchers think.

That would  be advantageous. When mating, a frog male clings to a female with a mating embrace or amplexus. The two stay like this for hours or even days, until she lays her eggs, and he can fertilize them. And all the while, such a joined pair is less agile than a single frog, and thus an easy prey for predators. The sooner a mating is completed, the shorter that unsafe state lasts.

The males are not very gentle. But if the mating is finished earlier because of the biting behaviour, both partners benefit. It is not yet known whether mating indeed is faster.

Anyway, the males of these frogs give off a chemical message during mating and are sure that it is received.

Willy van Strien

Photo: Plectrohyla sagorum. Ruth Percino Daniel (Wikimedia Commons, Creative Commons CC BY-SA 3.0)

Source:
Schulte, L.M., A. Martel, R. Cruz‑Elizalde, A. Ramirez‑Bautista & F. Bossuyt, 2021. Love bites: male frogs (Plectrohyla, Hylidae) use teeth scratching to deliver sodefrin precursor‑like factors to females during amplexus. Frontiers in Zoology 18: 59. Doi: 10.1186/s12983-021-00445-6

Cleaner wrasse cheats client secretly

Female knows if partner observes her behaviour

in a bluestreak wrasse pair, a conflict may arise

A bluestreak cleaner wrasse female sometimes scares a customer away by biting off a bit of its mucus layer. But if she knows that her partner can see what she’s doing, she behaves somewhat better, Katherine McAuliffe and colleagues report.

Bluestreak cleaner wrasses (Labroides dimidiatus) often work in pairs. Male and female jointly inspect their clients, fish that want to be cleaned. With their pointed snout, the cleaners pick up ectoparasites and dead skin cells. It is a textbook example of cooperation between species, called mutualism: clients get rid of their parasites, cleaners have a meal.

In cleaner wrasses that operate as a couple, a conflict sometimes arises because the female bites a client; that client then will leave, causing the male to miss his meal. A female cleaner is more likely to misbehave if she knows that her partner can’t see what she’s up to, Katherine McAuliffe and colleagues found.

Punishment

When a female cleaner bites, it is for good reason. She takes a mouthful out of a client’s protective mucus layer. This is tempting, especially during breeding season, because she needs a lot of energy and mucus is more nutritious than the parasites she should be eating. But upon being bitten, a client leaves, and the male, that serves the client properly, is the victim: because she cheats, he also loses the client – without the benefit of ingesting a bit of mucus like she has done.

There is also a risk that he will lose his territory, in which several females live. This is because these fishes change sex during their lifetime. Young cleaner wrasses are always females which, after reaching a certain size, become males. A female that eats nutritious mucus grows well. If she is almost the same size as her partner, she can change sex any moment and compete with him; maybe she’ll manage to chase him off and take over his territory.

It is therefore logical for a male not to tolerate that his partner bites a client. When she does, he punishes her by chasing or biting her. It was known from previous research that he punishes more severely when the client is larger, presenting more food. The punishment is also more severe if his partner is about the same size as himself and a risk of takeover exists.

After punishment, the female delivers good service to the clients and the partners cooperate well.

Model clients

McAuliffe already knew that cleaners treat their clients better when other fishes, potential clients, are watching. That is because bystanders leave when they see clients being hurt. Now, she wanted to know whether a bluestraek cleaner wrasse female is less likely to cheat a client when she knows that her partner can see her.

The cleaner fish live on coral reefs, where they occupy a ‘cleaning station’, as single or as a couple. It is difficult to observe exactly what is happening between cleaners and their clients. That is why the researchers did experiments in the lab, where they brought cleaner pairs into contact with artificial clients: plexiglass plates with food items stuck on them. Mashed prawn, which cleaner fish like, served as a model for a client’s mucus; a mixture of fish flakes and prawn, which the cleaners like less, did for parasites.

First, the cleaner fish learned to deal with the model clients. If they ate fish flake mixture, against their preference, that was seen as good cleaning service. But if they took a bite of mashed prawn, it was considered cheating, and the researchers removed the model client.

After training, the researchers first investigated how females behave when their partner was separated from them by either a transparent or an opaque barrier. As soon as a female took a bite of mashed prawn, the model client was removed, and her partner was given access.

Bad service

When their partner was visible and could see them, cleaner females ate a little more fish flake items on average before taking a bite of mashed prawn and chasing off the model client. So, in that case, the females provided a better service. If the partners were invisible to each other, females took less fish flake items. In other words, they cheated more in secret.

Males, that could punish their partner after she had eaten mashed prawn, punished less severely the more fish flake items she had consumed before. Surprisingly, it made no difference whether males had seen their partner’s behaviour or not. Apparently, they still noticed somehow how much their partner had cheated.

Choosing two times

So, it seems that females are aware whether their partner is or is not able to observe what they are doing, and that they are more inclined to cheat a client when the partner cannot see it.

A next, somewhat more complicated test affirmed this finding. In this set-up, the male was again behind a transparent or opaque partition, but now, two model clients were offered behind additional partitions. One of them was visible to the male – if the male himself was behind a transparent partition- behind a transparent partition; the other was hidden from him behind an opaque screen. The female was allowed to choose which model client to serve. She was given the choice twice; in between the male was admitted, having the opportunity to punish her.

The first time, females were more likely to choose the model client behind the opaque partition if their partner could watch them than if he couldn’t. But the second time, they went more often to the model client behind the transparent partition. This was probably because males were more likely to punish their partner after the first time if she had visited the hidden client. And, in accordance with the first experiment, they punished her whether they had been able to see that she went there or not. Apparently, she betrayed herself somehow.

Clever fish

The researchers’ main conclusion: a bluestreak cleaner wrasse female is more likely to cheat a client if she knows that her partner, who punishes bad behaviour, cannot see what she is doing. In the first trial, females more quickly took a mashed prawn item, which equated to the protective mucus layer of a client fish. In the second trial, they initially preferred to visit a model client hidden from the partner to a visible one.

That she realizes what he can see indicates impressive cognitive capacities. Such capacities were already known: the cleaners recognize themselves in a mirror.

But the question is why a female should care about whether her partner can see her bad behaviour or not, because that did not affect the punishment.

So, the story still does not have an end. But it probably will continue, as the research group has been conducting thorough research on these cleaner fish for years.

Willy van Strien

Photo: Bluestreak cleaner wrasse cleaning a blue angelfish (Pomcanthus semicirculatus). Longdongdiver (Vincent C. Chen) (Wikimedia Commons, Creative Commons CC BY-SA 4.0)

More about the behaviour of bluestreak cleaner wrasse

Sources:
McAuliffe, K., L.A. Drayton, A. Royka, M. Aellen, L.R. Santos & R. Bshary, 2021. Cleaner fish are sensitive to what their partners can and cannot see. Communications Biology 4: 1127. Doi: 10.1038/s42003-021-02584-2
Kohda, M., T. Hotta, T. Takeyama, S. Awata, H. Tanaka, J-y. Asai & A.L. Jordan, 2019. If a fish can pass the mark test, what are the implications for consciousness and selfawareness testing in animals? PLoS Biol 17: e3000021. Doi: 10.1371/journal.pbio.3000021
Raihani, N.J., A.I. Pinto, A.S. Grutter, S. Wismer & R. Bshary, 2012. Male cleaner wrasses adjust punishment of female partners according to the stakes. Proceedings of the Royal Society B 279: 365-370. Doi: 10.1098/rspb.2011.0690

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.

Dopamine

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

Source:
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

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