New body

Loose head regenerates a complete Elysia sea slug

Elysia sea slug can grow new body from head

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

Well-timed flowering

Dodder eavesdrops on host plant’s signal

dodder manages to flower simultaneously with its host

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

Males parasitizing on females

The immune system of deep-sea anglerfishes is strongly modified

In deep-sea anglerfish, some species have parasitic males and an aberrant immune system

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

Resemblance is striking

Parasitic Vidua nestlings trick host parents with near-perfect mimicry

Vidua nestlings mimic the young of their host parents

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

pin-tailed whydah is brood parasiteThe 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

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.

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

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.

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

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.

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

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

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

Cuckoo catfish in search of foster parents

Cichlid mothers see through the deceit, but pay a high price

cuckoo catfish parasitizes on cichlid species

The cuckoo catfish tries to dump its eggs among those of fish of the cichlid family. Cichlids usually avoid being used as foster parents, Radim Blažek and colleagues report, but by becoming too cautious, they often reject their own eggs as well.

Just as the cuckoo lays its eggs in the nests of songbirds, manipulating them into raising their young, the cuckoo catfish transfers the care for its offspring to other fish. Several species of the cichlid family are the involuntary foster parents of this ‘underwater cuckoo’. Cichlid mothers breed their eggs in the buccal cavity to protect them from predators. They also carry the newly hatched young in their mouths, and when the fry are able to swim around freely, they continue to pick them up in case of danger during the first few weeks.

Bad ending

The cuckoo catfish (Synodontis multipunctatus) exploits the dedicated behaviour of these mouthbreeders and approaches them while they are spawning. The female of a mating couple repeatedly lays a few eggs and collects them quickly in her mouth. She then picks up sperm from the male to fertilize the eggs in her mouth.

When a group of cuckoo catfish disturbs such spawning pair, the cichlids will chase off the invaders. Still, the catfish often manage to eat some cichlid eggs and place a number of fertilized eggs of their own among the cichlid eggs. The cichlid mother will gather also the catfish eggs in her mouth.

Then, things can go wrong for her own brood. The eggs of the cuckoo catfish are smaller than the eggs of the cichlid mother and hatch earlier, and the young catfish will devour their stepsiblings. Later, when the young parasites are released, the host mother will continue to protect them as if they were her own offspring.

Defence

Now, Radim Blažek and colleagues show that the cichlids are not entirely defenceless against the brood parasite. The cuckoo catfish only occurs in Lake Tanganyika in Central Africa, and the many cichlid species that inhabit the lake have been dealing with this enemy for millions of years. The researchers investigated how one of them, Simochromis diagramma, responds to the behaviour of the cuckoo catfish. They compared its response with the behaviour of cichlids from other African lakes, which have never been in contact with the underwater cuckoo.

They maintained different cichlid species separately in aquariums with a group of catfish and first assessed how often the catfish succeeds in imposing its eggs to the cichlids.

When housed with Simochromis diagramma, the cichlid from Lake Tanganyika, the cuckoo catfish was much less successful than with cichlids from other lakes. Only 5 percent of the Tanganyika females were found to have parasite’s eggs in their mouths 12 hours after spawning. Apparently, because of the shared evolutionary history, this cichlid species has learned to resist the brood parasite.

Rejection

To find out how Tanganyika cichlids deal with the cuckoo catfish in more detail, the biologists then artificially infected breeding cichlid females with parasites by injecting six fertilized eggs of the cuckoo catfish into their mouths. They used two cichlid species: Simochromis diagramma from Lake Tanganyika and Haplochromis aeneocolor from Lake George in Uganda. Next day, they determined whether the females had retained the foreign eggs. Also, in additional experiments, they assessed how often artificially parasitized females eventually released young cuckoo catfish and / or their own young.

The cichlid from Lake George was easily misled: only 7 percent of the females rejected the introduced parasite’s eggs instead of retaining them. As a consequence, the eggs of cuckoo catfish had a high survival chance: 86 percent developed successfully.

The Tanganyika cichlid, however, was not fooled into raising foreign young: nearly all females (90 percent) rejected foreign eggs and only 13 percent of the cuckoo catfish eggs survived. In those cases where the cuckoo catfish eggs hatched, individual experience reduced the damage. Cichlid females that had already given birth to young catfish earlier now managed to save some of their own young.

High price

The cichlids from Lake Tanganyika have learned to cope with the parasite and to see through their deceit. They rarely pick up foreign eggs. Nevertheless, the presence of the cuckoo catfish lowers their reproductive success because, if these cichlids detect foreign eggs, they become so choosy that they also reject some of their own eggs, as the experiments showed. So, they pay a high price to keep the parasite out.

There are about one hundred species of brood parasites among birds. In fish, the cuckoo catfish is the only one known to display cuckoo behaviour.

Willy van Strien

Photo: Cuckoo catfish Synodontis multipunctatus. ©Institute of Vertebrate Biology, Brno (Czech Republic)

See a short video documentary of National Geographic on cuckoo catfish

Source:
Blažek, R., M, Polačik, C. Smith, M. Honza, A. Meyer & M. Reichard, 2018. Success of cuckoo catfish brood parasitism reflects coevolutionary history and individual experience of their cichlid hosts. Science Advances 4: eaar4380. Doi: 10.1126/sciadv.aar4380

Unrewarded services

Orchid utilizes fungi and fruit flies without paying

Drosophila fly on flower of the deceptive orchid Gastrodia pubilabiata

The orchid Gastrodia pubilabiata lives at the expense of other species. It steals sugars from fungi, which also attract fruit flies that provide pollination service, as Kenji Suetsugu shows, without receiving any reward in return.

While most plants produce sugars from carbon dioxide using energy from sunlight in a process called photosynthesis, the orchid Gastrodia pubilabiata leaves the job to others. The small and inconspicuous plant, which grows in Japan and Taiwan, does not have green leaves, as it lacks chloroplasts, the cell organelles that conduct photosynthesis. With its roots, it steals sugars from the underground hyphae of a number of mushroom forming fungi species; the fungi obtained these sugars from dead organic material. The fungi get nothing in return.

And while most plants produce nectar as a food resource for insects (or other animals) that pollinate the flowers in return, this orchid doesn’t. To be pollinated, it exploits fruit flies (Drosophila species) without rewarding them.

Deceived

The flies need fermenting fruit or decaying mushrooms to lay their eggs in, and their larvae will consume that stuff. Apparently, the brown-coloured flowers of Gastrodia pubilabiata smell like fermenting and decaying substrates, as the flies are deceived into laying their eggs on the flowers. Consequently, the larvae will find no suitable food and die. But the orchid has been served. While visiting a flower, the flies pick up pollinia, masses of pollen grains, which they deliver to the next flower they visit, thereby pollinating that flower.

Service

The orchid thus takes nutrients from mushrooms and is pollinated by fruit flies, and neither of these partners receives any reward for its services. Both are victims of a parasitic and deceptive plant.

Now Kenji Suetsugu shows that mushroom-forming fungi still provide another service. Old mushrooms attract fruit flies that have to lay their eggs, and upon arrival, they will also visit the orchid flowers that mimic fermenting and decaying material. Suetsugu conducted experiments in which he removed decaying Mycena mushrooms from the orchids’ proximity or added extra specimens; Mycena species are the main victims of theft by the plant. He found that the more decaying mushrooms are around, the more pollen is removed from and delivered to orchid flowers by flies that are misled, and the more seeds are produced.

So, the fungi not only function as food providers, but also as magnets that attract pollinators – without reward.

Willy van Strien

Photo: Gastrodia pubilabiata, flower and fruit fly bearing pollinia. © Kenji Suetsugu

Source:
Suetsugu, K., 2018. Achlorophyllous orchid can utilize fungi not only for nutritional demands but also pollinator attraction. Ecology, online March 25. Doi: 10.1002/ecy.2170

Useful cigarette butts

House finch has to accept harmful side effects

House finches add cigarette butts to their nests to repel parasites

Smoked-trough cigarette filters are noxious, still some bird species add them to their nest lining, where the nicotine will repel blood-sucking parasites. They do so only when they need to, as Monserrat Suárez-Rodríguez and Constantino Macías Garcia show.

Spent cigarette filters are popular among some bird species, for instance the house finch. The birds weave cellulose fibres from discarded butts into the lining of their nests, together with more conventional soft materials such as feathers, fur or cotton. Monserrat Suárez-Rodríguez en Constantino Macías Garcia wondered whether the birds collect cellulose from butts accidently, or whether they do it to protect their young against blood-sucking parasites: lice and ticks. From earlier research, they knew that ectoparasites are repelled by nicotine, and the more smoked-through cigarette butts could be found in a nest, the smaller the amount of parasites was. Weight gain and fledging success of young increased with the proportion of cellulose from butts in the nest lining.

But they also knew that the butts are harmful to adult birds and their offspring. Next to nicotine, the butts contain more than 400 different substances such as heavy metals and insecticides, many of which are toxic. The substances may enter the birds’ bodies through the skin or the lungs.

Damage

The research team had analysed blood samples of parents and young and found nuclear abnormalities in many red blood cells (in contrast to human red blood cells, those of birds contain a nucleus with dna). The larger the proportion of butts in the nest lining, the more genotoxic damage was seen. Red blood cells live for only two to four weeks, so the damage may have no serious consequences. But other cells types likely are damaged too. The question is whether the benefits of adding cigarette butts to the nest lining – less parasites, resulting in better growth – are large enough to outweigh these costs.

The answer will depend on how much the butts are needed to fight off parasites.

Ticks

Now, experiments reveal that house finches act accordingly: they bring more smoked-through cellulose fibres from cigarette butts to their nests if parasites are present than if they’re not. The researchers removed the nest lining from a number of nests shortly after the young hatched, and added a piece of felt instead; by doing so, they removed the bulk of the tick population from the nest as well. They measured the amount of butts in the original lining. They added living ticks to some of the artificial felt nest linings, dead ticks to other linings and nothing to the remaining linings. After the young fledged, they collected the artificial linings to investigate how much butts the parents had added.

It appeared that the birds collected more butts if the researchers had added living ticks to their nest, so when it was useful to bring butts. Also birds that had brought a large amount of butts into their original nest lining, collected many butts now as well; apparently, they had experienced a high parasitic load during incubation.

The birds don’t collect cigarette butts randomly, the conclusion is, but in response to the presence of ectoparasites; so, it is a form of self-medication.

Willy van Strien

Photo: house finch male feeding young. Susan Rachlin (Wikimedia Commons, Creative Commons CC BY 2.0)

Sources:
Suárez-Rodríguez, M. & C. Macías Garcia, 2017. An experimental demonstration that house finches add cigarette butts in response to ectoparasites. Journal of Avian Biology, online September 1. Doi: 10.1111/jav.01324
Suárez-Rodríguez, M., R.D. Montero-Montoya & C. Macías Garcia, 2017. Anthropogenic nest materials may increase breeding costs for urban birds. Frontiers in Ecology and Evolution 5: 4. Doi: 10.3389/fevo.2017.00004
Suárez-Rodríguez, M. & C. Macías Garcia, 2014. There is no such a thing as a free cigarette; lining nests with discarded butts brings short-term benefits, but causes toxic damage. Journal of Evolutionary Biology 27: 2719–2726. Doi: 10.1111/jeb.12531
Suárez-Rodríguez, M., I. López-Rull & C. Macías Garcia, 2013. Incorporation of cigarette butts into nests reduces nest ectoparasite load in urban birds: new ingredients for an old recipe? Biology Letters 9: 20120931. Doi: 10.1098/rsbl.2012.0931