parasitism Archieven - From so simple a beginning

15 March 2023

Fairy lantern rediscovered

Unexpectedly, the cheating plant Thismia kobensis still exists

It was discovered in 1992 and believed to be extinct because the site where it had been found was destroyed in 1999. But now, it is rediscovered elsewhere: the Kobe fairy lantern. Kenji Suetsugu and colleagues describe the beautiful but cheating tiny plant.

You would hardly recognize them as plants, the small, splendid ‘fairy lanterns’ on the forest floor, often hidden under fallen tree leaves. Fairy lanterns, Thismia species, are indeed remarkable plants. What you see are the flowers, less than a centimeter in size. The plants have no green leaves, only some scales on the very short stem. Most of the plants lives underground.

There are about 90 species, one of which is Thismia kobensis, the Kobe fairy lantern. Small and inconspicuous as it is, it was only discovered in 1992, in an oak forest near the Japanese city of Kobe. The find was small: it consisted of no more than one specimen. The site was destroyed in 1999 when an industrial complex was constructed, and the newly discovered species went extinct. That was what people thought. But fairy tales exist: in 2021 biologists unexpectedly rediscovered the plant on a conifer plantation in the town of Sanda, 30 kilometers from the original site. And this time the find was larger: almost 20 individuals. Now, Kenji Suetsugu and colleagues provide a scientific description of the species.

The loveliness of its flower is deceptive: Thismia kobensis belongs to a group of cheating plants.

Energy requirement

The cheating has to do with the lack of green leaves.

The green leaves of normal plants contain many chloroplasts. In these cellular organelles, photosynthesis takes place: plants extract carbon dioxide from the atmosphere and with the help of sunlight they fix the carbon in carbohydrates such as sugars and starch. From these carbohydrates, they derive energy. Plants without green leaves cannot make carbohydrates, but they do need energy.

Many of these plants solve this problem by extracting sugars with their roots from fungi in the soil. The scientific term for this is mycoheterotrophy.

Fairy lantern is sugar thief

Most mycoheterotrophic plants target fungi that live in a mutualistic relationship with green plants. The fungi get sugars from these plants. In return, the fungi help the green plants to absorb water and nutrients such as nitrogen and phosphorus from the soil. This collaboration, called mycorrhiza, is mutually beneficial and both parties are honest.

However, when mycoheterotrophic plants such as Thismia make contact with mycorrhizal fungi, they don’t cooperate in this way. They do receive water and nutrients, but they do not return sugars. They can’t. Instead, they take up sugars from the fungus in addition to water and nutrients. In other words: they steal. The fungus had received those sugars from green plants, so mycoheterotrophic plants indirectly parasitize on green plants via mycorrhizal fungi.

Difficult alternative

There are about 500 species of mycoheterotrophic plants. They live on nutrient-poor soils in forests, where little sunlight reaches the soil and the ability for photosynthesis, i.e., sugar production, is limited. Sugar theft is the alternative that these plants developed.

But it’s not as easy as it seems. It is difficult for a mycoheterotrophic plant to form a relationship with a mycorrhizal fungus. Where a green plant interacts with many mycorrhizal fungi species simultaneously, a mycoheterotrophic plant can make contact with only one or a few fungal species. That’s probably because most fungi detect the cheaters and hold off on the relationship. Therefore, mycoheterotrophic plants are always rare and never widely distributed.

Mycoheterotrophic species often target a fungus that has many different green partners. With so many suppliers, the sugar supply is always guaranteed.

Dust seeds

The vast majority of land plants live in association with mycorrhizal fungi. The mycoheterotrophic mode of life -which abuses this mutualism – has developed dozens of times. In the case of fairy lanterns, this happened many millions of years ago. That is why they have little resemblance to ordinary plants. Other mycoheterotrophic plants emerged much more recently and have a more normal appearance.

Some plants are mycoheterotrophic shortly after germination only; this applies to all orchid species. The seeds are as fine as dust and contain no food. After germination, these plants get their sugars from fungi until they have leaves and can make their own sugars. This could be a first step towards a fully mycoheterotrophic lifestyle. There are also orchid species that stay mycoheterotrophic during their whole life, for example the bird’s nest, Neottia nidus-avis.

Broomrape species (Orobanche) look similar to some mycoheterotrophic plants, but are different: with their roots, they parasitize directly on other plants.

Willy van Strien

Photos:
Large:
Fairy lantern of Kobe, Thismia kobensis ©Kenji Suetsugu
Small:
Snow plant, Sarcodes sanguinea, a mycoheterotrophic plant from North-west America. David῀O (Wikimedia Commons, Creative Commons CC BY 2.0)
Bird’s nest orchid, Neottia nidus-avis. BerndH (Wikimedia Commons, Creative Commons CC BY-SA 3.0)

Sources:
Suetsugu, K., K. Yamana & H. Okada, 2023. Rediscovery of the presumably extinct fairy lantern Thismia kobensis (Thismiaceae) in Hyogo Prefecture, Japan, with discussions on its taxonomy, evolutionary history, and conservation. Phytotaxa 585: 102-112. Doi: 10.11646/phytotaxa.585.2.2
Gomes, S.I.F., M.A. Fortuna, J. Bascompte & V.S.F.T. Merckx, 2022. Mycoheterotrophic plants preferentially target arbuscular mycorrhizal fungi that are highly connected to autotrophic plants. New Phytologist 235: 2034-2045. Doi: 10.1111/nph.18310
Jacquemyn, H. & V.S.F.T. Merckx, 2019. Mycorrhizal symbioses and the evolution of trophic modes in plants. Journal of Ecology 107: 1567-1581. Doi: 10.1111/1365-2745.13165
Gomes, S.I.F., J. Aguirre-Gutiérrez, M.I. Bidartondo & V.S.F.T. Merckx, 2017. Arbuscular mycorrhizal interactions of mycoheterotrophic Thismia are more specialized than in autotrophic plants. New Phytologist 213: 1418-1427. Doi: 10.1111/nph.14249

10 October 2022

Cuckoo duck seeks defence

Foster family protects duck eggs against birds of prey

Young cuckoo ducks do not need any care: they are independent upon hatching. Then why does the duck burden other birds with its eggs, Bruce Lyon and colleagues wondered.

In South America a duck species occurs that, like a cuckoo, lays its eggs in nests of other bird species. The hosts then unintentionally take care of them. This is the black-headed duck, Heteronetta atricapilla, with the appropriate nickname cuckoo duck; it is a so-called brood parasite.

Bruce Lyon and colleagues wondered why the cuckoo duck dumps its eggs in other birds’ nests. They don’t require much care, apart from brooding. After hatching, the young are immediately independent. That is a big difference with all other brood parasites, such as the common cuckoo. These species have young that have to be fed and protected for weeks, so it is very profitable for parents to outsource the care. But how does the cuckoo duck profit?

Easy prey

The shedding of parental duties may have to do with the danger of predation, Lyon hypothesized. If the cuckoo duck were to make its own nest, it would be close to water. And in such nest, eggs are easy prey for avian predators, especially the chimango caracara. This was shown in experiments in which the researchers placed chicken eggs in a self-made, unguarded nest. Within a few days, all eggs were gone.

Unless they placed the nest in a colony of brown-headed gulls. In that case, hardly any egg was stolen.

This gull is one of the hosts in whose nests the cuckoo duck dumps its eggs. In Argentina, where the study was conducted, two other important hosts occur, the red-fronted coot and the red-gartered coot. Like the brown-headed gull, they are aggressive birds that are capable to defend their nests fiercely. Is that the reason why the cuckoo duck chooses them to care for its offspring?

Safe

It seems to be. The duck eggs are indeed quite safe with these fierce foster parents, the researchers noted. Admittedly, it may happen that foster parents recognize a foreign egg and throw it out of the nest. But if they accept the egg, it almost always remains undisturbed and hatches. This very high chance of survival upon acceptance far outweighs the risk of rejection.

The researchers do not know exactly how much the cuckoo duck gains. They could not determine how many eggs would survive in a self-defended nest, because it never builds a nest. But related duck species that do incubate and guard their own eggs lose quite a lot to birds of prey.

Willy van Strien

Photo: black-headed duck couple. Cláudio Dias Timm (Wikimedia Commons, Creative Commons BY-SA 2.0).

Source:
Lyon, B.E., A. Carminati, G. Goggin & J.M. Eadie, 2022. Did extreme nest predation favor the evolution of obligate brood parasitism in a duck? Ecology and Evolution 12: e9251. Doi: 10.1002/ece3.9251

12 April 2022

Increasing efficiency in brood parasite

Cuckoo catfish improves its timing

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

17 March 202121 March 2021

New body

Loose head regenerates a complete Elysia sea slug

Sea slugs Elysia marginata en Elysia atroviridis can decapitate themselves and regrow a new body from the loose head, Sayaka Mitoh en Yoichi Yusa show. A bizarre phenomenon. Why do they do it, and how do they survive?

Sayaka Mitoh and Yoichi Yusa must have been dumbfounded when seeing sea slugs that they kept in their lab, species Elysia marginata, sever their heads from their bodies. The loose heads moved around, as they report. After a day, the wounds were closed. In some cases, especially in young sea slugs, things got even crazier: the head began to feed; after a week, a new body started to grow and in three weeks it was complete.

The loose bodies also moved for a while, sometimes even months, but eventually they decomposed. No new head appeared on any loose body.

Parasite

There are more animals that can regrow a missing body part, such as a lizard that shed its tail or a fiddle crab that lost a claw. But this – regenerating almost an entire body – is very extreme. These sea slugs even have a groove behind the head as a predetermined breakage plane for self-decapitation. Why do they do it?

In any case, it is not to escape from a predator, like a lizard sheds its tail when a predator grasps it. The sea slugs take hours to separate body from head; that is not effective to avoid predation. And when the researchers simulated an attack by teasing them, nothing happened. The animals have a different defence mechanism against predators: they are poisonous.

The reason for self-decapitation became clear by observations on wild-caught specimens of a related species, Elysia atroviridis. Once in the lab, some of them shed the whole body, and these specimens turned out to contain a parasite, a copepod of the genus Arthurius. It is a large parasite that occupies almost the entire body of its host. In fact, a parasitized sea slug has already lost its body. If it sheds it, it will get rid of the parasite while losing almost nothing more.

Chloroplasts

But how does it survive without organs such as heart and kidneys? This has to do with a special property of sacoglossan sea slugs, to which Elysia belongs, the researchers suppose. They extract chloroplasts from algal food and incorporate them in special cells that line their highly branched digestive gland. The head also contains chloroplasts. Thanks to the chloroplasts, which they need to survive, these sea slugs can endure a period without food, it was known.

It is a mystery how exactly they utilise the chloroplasts. The chloroplasts continue to do what they do in plants: they convert carbon dioxide into carbohydrates with the help of sunlight, a process called photosynthesis. Whether the sea slugs can survive on sunlight as a result, just like plants, is a matter of debate.

Regardless, it may well be thanks to the chloroplasts that a loose head of Elysia marginata and Elysia atroviridis survives.

No eternal life

Parasitized Elysia sea slugs shed their worthless bodies. But they only manage to grow a new one from the head when they are young. The loose head of an older specimen does not feed and does not grow, but will die within ten days. Shedding and regrowing a body is not a recipe for eternal life.

Willy van Strien

Photo: Elysia marginata. Budak (via Flickr, CC BY-NC-ND 2.0)

The research explained on YouTube

Sources:
Mitoh, S. & Y. Yusa, 2021. Extreme autotomy and whole-body regeneration in photosynthetic sea slugs. Current Biology 31: R233-R234. Doi: 10.1016/j.cub.2021.01.014
Wägele, H., 2015. Photosynthesis and the role of plastids (kleptoplastids) in Sacoglossa (Heterobranchia, Gastropoda): a short review. Aquatic Science & Management 3: 1-7. Doi: 10.35800/jasm.3.1.2015.12431

10 September 2020

Well-timed flowering

Dodder eavesdrops on host plant’s signal

Dodder, a plant that parasitizes other plants, flowers almost simultaneously with its host. The parasite takes up the host’s signal that activates flower development, Guojing Shen and colleagues show.

A plant may be covered with a tangle of thin, sticking threads. That is a bad condition for the plant, because those threads are stems of a parasitic plant: dodder (Cuscuta), of which about two hundred species exist worldwide. Most of them thrive on several host plant species. And whether a host flowers sooner or later in the season, dodder joins in and develops its flowers simultaneously. Guojing Shen and colleagues discovered how Australian dodder (Cuscuta australis) manages to synchronize its flowering time with that of its various hosts.

Once young dodder plants get hold of a host plant after germination, their roots disappear, so they cannot take up water and nutrients from the soil anymore. Also, they don’t have green leaves that take carbon dioxide from the air and convert it into carbohydrates with the help of sunlight, like other plants. Everything they need, they extract from the host, round the stems of which they wind extensively.

Maximum benefit

To exploit its host, the parasite forms numerous haustoria that penetrate into the host’s stems and connect with phloem, the tissue that transports organic compounds, and xylem, the tissue that transports water. The haustoria enable the parasite to extract nutrients and water from its victim.

Annual dodder species, like Cuscuta australis, first grow, then flower and eventually die. The parasite benefits most from its host when it flowers simultaneously. Because if it blooms earlier, it will not reach the size it could have reached by growing longer, and as a consequence it will produce fewer flowers and fewer seeds than it could have produced. But if it postpones flower development for too long, it will be short of nutrients during flowering. Because the host then channels as much nutrients as possible to its own flowers and seeds, leaving less to circulate in phloem and xylem from which dodder taps.

So, dodder has to adjust its flowering time to that of its host.

Dodder is eavesdropping

Most plants regulate their flowering time by tracking changes in day length. When it is about time for flowers to appear, the leaves produce the protein FT (flowering locus T), which moves through the phloem. This protein switches on flower development; it is, in other words, a mobile flowering signal.

Dodder would not benefit from having a flowering signal of its own. As it has to synchronize with its host, it must be flexible. It is therefore not surprising that it does not appear to have functional FT protein. There is a dodder variant of the protein, but it does not activate flowering. How then does the parasite regulate its flowering time?

By eavesdropping on the host’s flowering signal, Shen writes. He investigated flowering in Australian dodder, but the story will apply to other dodder species as well. To European dodder (Cuscuta europaea), for example, which can be found in Western Europe growing on nettle and hops; or to lesser dodder (Cuscuta epithymum), or hellweed, that grows on heather, broom, gorse, thyme and other plants.

It was already known that the parasite not only extracts water and nutrients from the host plant via haustoria, but that also several biologically active substances are exchanged.

Including the FT protein.

Perfect mechanism

As the host starts flower development and the plant produces FT protein, this is transferred to dodder. The researchers show that the host’s protein retains it activity in the parasite, initiating flower development there too.

And so the flowering time of the parasite will coincide nicely with that of its host. Eavesdropping is a perfect method for alignment.

Willy van Strien

Photo: Australian dodder, Cuscuta australis. Harry Rose (Wikimedia Commons, Creative Commons CC BY 2.0)

Watch the growth of fiveangled dodder (Cuscuta pentagona, from North America) on video

Sources:
Shen, G., N. Liu, J. Zhang, Y. Xu, I.T. Baldwin & J. Wu, 2020. Cuscuta australis (dodder) parasite eavesdrops on the host plants’ FT signals to flower. Proceedings of the National Academy of Sciences, online August 31. Doi: 10.1073/pnas.2009445117
Liu, N., G. Shen, Y. Xu, H. Liu, J. Zhang, S. Li, J. Li, C. Zhang, J. Qi, L. Wang & J. Wu, 2020. Extensive inter-plant protein transfer between Cuscuta parasites and their host plants. Molecular Plant 13, 573-585. Doi: 10.1016/j.molp.2019.12.002

13 August 2020

Males parasitizing on females

The immune system of deep-sea anglerfishes is strongly modified

To the well-known peculiarities of deep-sea anglerfish, Jeremy Swann and colleagues add a new one: some species lack an important part of the immune system. This is associated with a unique parasitic lifestyle of males.

There are strange, very strange and extremely weird animals. We can safely include deep-sea anglerfish in the latter group.

Within the anglerfish or seadevils, they form a separate group of over 160 species, the Ceratioidea, which, as the name indicates, have specialized in living in the utter darkness of the deep sea. Food and partners are extremely scarce down there. Hence, as was known, these fish exhibit some peculiarities. Now, it turns out that they also have a very aberrant immune system, Jeremy Swann and colleagues report.

Angling pole with glowing bulb

Deep sea anglerfish start their lives in a quite normal way, eggs and larvae dwelling in surface waters. But once they developed into young fish, things change. Females grow to a considerable size, males stay tiny.

The bigger a female gets, the more eggs she can produce. And so a young female starts growing. She has to eat much, several prey animals are on her menu. To capture prey, she uses a fishing rod growing from her back; it is a modified anterior dorsal fin. At the end it has a lure: a bulb in which bacteria live that produce light by carrying out a chemical reaction. It is a form of mutualism; the bacteria get a place to live in and food in exchange for light production.

An anglerfish’s light can flash and dance, resembling a moving animal. Living animals discern a tasty snack which they will approach. The anglerfish then ingests a large amount of water, including prey. With some luck, the catch will provide sufficient nutrients to sustain her for quite a while.

The females, plump and with large heads and mouths full of sharp teeth, are not the prettiest of all. They are called seadevils for good reason. They are bad swimmers, drifting around, just waiting for prey to come by.

Strong attachment

After completing the larval stage, males’ development takes a completely different direction. Males no longer grow and are unable to eat. Their only goal is to find a female in the empty deep sea. So, they swim constantly. In addition to the light bulb of their angling rod, young females also have two luminous organs on their backs. Maybe the dwarfed males, which have big eyes, are able to detect those organs. If they are lucky, they will meet a partner before they have used up all their reserves.

Upon meeting, he attaches himself to her body with sharp teeth. When, later on, she is ready to release eggs, he is ready to fertilize them. Males and females only become sexually mature when they’ve acquired a partner. Given the scarcity of conspecifics, this makes sense: only after pair formation it is guaranteed that eggs and sperm can come into contact.

Sperm bulge

In some deep-sea anglerfish, the attachment between female and male is temporary; after a while, he lets go.

But in other species, males attach themselves permanently to a female. These are most bizarre types, because the two partners fuse with each other, enabling the male to survive. Their skin tissues meld, the circulatory systems become connected. He now is a ‘sexual parasite’, little more than a sperm-producing bulge that feeds on nutrients that he derives from her. This sexual parasitism is a unique mode of reproduction, occurring only in deep-sea anglerfish.

It is called parasitism, but it may be considered a form of mutualism as well, as the male delivers sperm in return for nutrients.

The best known species is Ceratias holboelli; it is also the largest one and it has the most extreme sexual dimorphism. A female can grow more than a meter long (including tail), sixty times the size of a free-living male. Physical pair formation is permanent. Once attached to her belly, he grows to a maximum of 20 centimetres. A female carries no more than one parasitic male.

Another species with permanent attachment is Cryptopsaras couesii; in this species, up to eight males can be attached to a single female. A female can be 30 centimetres long, a free-living male only three centimetres.

Ancient immune system

It is remarkable that the female immune system doesn’t attack permanently attached, parasitic males, Swann and colleagues realized. You would expect the immune system to recognize and reject such males, as they are not-own tissue. But that does not happen.

Apparently, the immune system tolerates the very intimate mode of reproduction. To find out how, the biologists examined a number of genes that underpin various parts of immune defence. They investigated four deep-sea anglerfish species with temporarily attached males and six species with permanently attached parasitic males, including Cryptopsaras couesii. They compared these species to a number of anglerfish species outside the deep-sea group, where males don’t attach to females.

Fishes have the same immune system as other vertebrates; the system is 500 million years old. It consists of innate, general immune responses on the one hand and specific immune responses that build up against specific intruders that the system has to deal with on the other hand. The researchers focused on the adaptive, specific immune system.

Lethal

The results were surprising: deep sea anglerfish species in which males live as parasites on females lack essential immune genes. Their specific immune system is severely blunted.

In two of the species studied, species in which females can have more than one male attached, virtually no specific immune facilities are functional. This is highly remarkable, because such complete lack of specific immune defence is lethal for other animals. The first infection would kill them. Microbial pathogens occur in the deep sea too, so deep-sea anglerfish must be able to defend themselves. Most likely, they reorganized their innate immune defence, the researchers assume.

From their own and other research, they conclude that the common ancestor of deep-sea anglerfish had tiny, non-parasitic males that temporarily attached themselves to females. On a few occasions, species descending from that ancestor made the switch to permanent attachment and their specific immune defence has been largely dismantled.

It is unclear yet what happened first. Did males become parasitic, making it necessary to turn off the specific immune system? Or did the specific immune system lose important parts, making permanent attachment of males possible?

The deep sea anglerfish remain really puzzling creatures.

Willy van Strien

Drawing: northern giant seadevil, Cryptopsaras couesii (not included in this research); female with male attached. Tony Ayling (Wikimedia Commons, Creative Commons CC BY-SA 1.0)

Watch the fanfin angler, Caulophryne jordani (not included in the research) on YouTube; female with permanently attached male

Sources:
Swann, J.B., S.J. Holland, M. Petersen, T.W. Pietsch, T. Boehm, 2020. The immunogenetics of sexual parasitism. Science, online July 30. Doi: 10.1126/science.aaz9445
Fairbairn, D.J., 2013. Odd couples. Extraordinary differences between the sexes in the animal kingdom. Princeton University Press, Princeton and Oxford, VS. ISBN 978-0-691-14196-1

5 August 202027 November 2020

Resemblance is striking

Parasitic Vidua nestlings trick host parents with near-perfect mimicry

In order not to stand out in the nest in which they grow up clandestinely, Vidua nestlings mimic the young of the host parents. They perform very well, Gabriel Jamie and colleagues report. But some slight discrepancies exist.

African whydahs and indigobirds, Vidua species, are brood parasites like the cuckoo. They lay their eggs in the nest of other bird species, in this case grassfinches, and have the host parents raise their young. Vidua finches are unable to provide parental care. But these brood parasites do much less harm to the host families than a cuckoo, because young Viduas don’t eject other nestlings from the nest. The host parents take care for their own offspring, but have some extra, foreign young.

The foreign nestlings should not stand out, otherwise the tricked parents will notice the deception. It was already known that Vidua young resemble their host parents’ young. With special computer software, Gabriel Jamie and colleagues now show how successful the mimicry is.

Ornamented mouths

The Vidua genus contains nineteen species. In the breeding period, the males are real beauties, while the females are inconspicuous and difficult to recognize. Jamie took a closer look at three species: pin-tailed whydah (Vidua macroura), broad-tailed paradise whydah (Vidua obtusa) and purple indigobird (Vidua purpurascens). They are host-specific, each Vidua species has a single host species. Jamie compared the Vidua nestlings to that of their respective host parents and of a number of other grassfinch species.

Young grassfinches (Estrildidae) have ornamental mouth markings that become fully visible when they open their beaks; this ornamentation in unusual among birds. Each grassfinch species has its characteristic pattern, colour and structure.

Nestlings of the breeding parasites accurately mimic those characteristic markings, is the conclusion of the research. An analysis with pattern recognition software shows that the pattern is similar to that of their host parent species. The colours match well too. Vidua nestlings also cleverly imitate the begging calls and postures of their foster siblings.

Imprinting

Previous research, by Michael Sorenson, had shown that the nineteen species of whydahs and indigobirds are much younger than their hosts in an evolutionary sense. The idea is that their common ancestor switched to a brood parasitic lifestyle with a grassfinch as host parent.

Speciation could then occur quickly. Whenever a Vidua female happens to lay eggs in the nest of another host, a separate group associated to that new host arises, because Vidua nestlings imprint on the song of their host father. Each grassfinch species has its own characteristic song. When grown up, Vidua males will mimic the song of their host, and females are attracted to this song. Also, females select a nest of the host species they were raised by to lay their eggs in. The group turns into a new species.

The nestlings then become more and more similar to the nestlings of the new host through an evolutionary adaptation process. Because the more a Vidua nestling resembles the young of its host parents, the more likely they are to accept it and care for it, increasing its survival chance.

Exaggerated

And as a matter of fact, the resemblance between foreign and own young in a parasitized grassfinch’s nest turned out to be striking. But it is not entirely perfect. Small but consistent differences exist. Perhaps the foreign nestlings are (yet) unable to fully mimic their nest mates. And apparently, they are doing well enough: the host parents accept them.

But there may be another explanation for the discrepancies, the researchers write. Nestlings of pin-tailed whydah, for example, have spots in the beak that are slightly larger than those of their foster parents’ young, common waxbill (Estrilda astrild), and their begging calls are slightly extended. Unlike a waxbill nestling, they wave a wing under their open mouth while begging.

So, these Vidua nestlings are slightly exaggerating their host’s begging signals. And perhaps the host parents favour them as a consequence. An intriguing thought.

Willy van Strien

Photos:
Large: pin-tailed whydah nestling, the outside of the mouth markings visible. ©Gabriel A. Jamie
Small: pin-tailed whydah, breeding male. Alan Manson (Wikimedia Commons, Creative Commons CC BY-SA 2.0)

Sources:
Jamie, G.A., S.M. Van Belleghem, B.G. Hogan, S. Hamama, C. Moya, J. Troscianko, M.C. Stoddard, R.M. Kilner & C.N. Spottiswoode, 2020. Multimodal mimicry of hosts in a radiation of parasitic finches. Evolution, online July 21. Doi: 10.1111/evo.14057
Sorenson, M.D., K.M. Sefc & R.B. Payne, 2003. Speciation by host switch in brood parasitic indigobirds. Nature 424: 928-931. Doi: 10.1038/nature01863

4 October 201927 November 2020

Exit through head plug

Dead host helps parasitoid wasp escape from crypt

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.

Rescue

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

Sources:
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

11 September 2019

Smart offer

How parasitic thorny-headed worm reaches the right host

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.

When 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.

Beneficial

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

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

Sources:
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

1 November 201820 September 2021

Role pattern erased

Twisted-wing parasites change the behaviour of host wasps

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.

Overwintering

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.

Safe

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.

Delivery

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

Xenos peckii mating on YouTube

Sources:
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