From so simple a beginning

Evolution and Biodiversity

Category: mutualism (Page 1 of 2)

Shell with windows

10 December 2024 /

Heart cockle accommodates algae that require light

Shell of heart cockle Corculum cardissa has many tiny windows

The shells of heart cockles (Corculum cardissa) have many transparent windows on their sun-facing side for the benefit of resident algae. The windows have a special structure, Dakota McCoy and colleagues show.

Shells need to be hard and sturdy to protect the mollusk inside. It is a simple function and usually there is nothing special about a shell, apart from the diversity in shapes and colours. But the shells of heart cockles (Corculum cardissa and other species) are remarkable: they contain a large number of transparent windows, orderly arranged. They are there for a reason: they transmit sunlight to the unicellular algae that live within the mollusk. Dakota McCoy and colleagues investigated shape and function of the windows.

But why are algae living in shellfish in the first place?

Algae, like plants, are able to capture carbon dioxide from air to synthesize sugars with the use of sunlight in a process called photosynthesis; the sugars are the basis for energy and building materials. The nutrients that algae and plants need are chemical elements such as nitrogen, phosphorus, and calcium, which they incorporate into complex carbon compounds such as proteins and DNA, carrier of genetic information. Animals are dependent on photosynthesis; they must feed to obtain energy and building materials. Or…..

…. they can accommodate algae, so that they have sugars at their immediate disposal and do not have to feed.

Tiny windows

Some bivalves use this alternative opportunistically. And there are two groups that can only live with algae: the giant clams (Tridacninae, including the large Tridacna gigas) and many heart cockles (Fraginae). They house unicellular algae in fine branches of their intestinal tract. The algae provide sugars in exchange for a safe living place and probably also nutrients.

A prerequisite for successful cooperation is that the algae have access to sunlight. The hosts, which are partially buried, must ensure this. They live in shallow water, where sunlight penetrates to the bottom. Giant clams often keep their shells open, so that the animal is bathed in sunlight. Heart cockles have a different solution. Their shells remain closed, but the algae receive light through minuscule windows in the sun-facing side of the shells.

The researchers wanted to know more about the structure of these windows and examined those of the heart cockle Corculum cardissa.

Optic fibres

The shells of Corculum cardissa consist of aragonite, a calcium compound (calcium carbonate, CaCO3) that forms planar crystals that are crossed in orientation.

The windows have a different microstructure: here, the aragonite forms fibres instead of planar crystals. Each window is a bundle of cables consisting of parallel aragonite fibres that runs perpendicular to the shell surface. The cables transmit light, just like glass fibre cables. Fibre optic cables are exceedingly rare in nature, and cable bundles have never been found before.

Experiments show that the sun-facing shell sides – the windowed sides – transmit colours of sunlight that are important for photosynthesis; on average 31 percent of these colours passes through. In contrast, for ultraviolet light, which is harmful to animal tissue and algae, this percentage is only 14. The sand-facing shell sides transmit hardly any light.

Some individuals have a microlens beneath each window, also consisting of aragonite, which condenses the incoming light and focuses it deeper in the tissue, where the algae are. That completes the design.

You wouldn’t make it up: shells with windows. But it exists.

Willy van Strien

Photo: the sun-facing side of heart cockle Corculum cardissa. Ria Tan, Wildsingapore, via Flickr. Creative Commons: CC BY-NC-ND 2.0

Sources:
McCoy, D.E., D.H. Burns, E. Klopfer, L.K. Herndon, B. Ogunlade, J.A. Dionne & S. Johnsen, 2024. Heart cockle shells transmit sunlight to photosymbiotic algae using bundled fiber optic cables and condensing lenses. Nature Communications 15: 9445. Doi: 10.1038/s41467-024-53110-x
Kirkendale, L. & G. Paulay, 2024. Photosymbiosis in Bivalvia. Treatise Online no. 89: Part N, Revised, Volume 1, Chapter 9. Doi: 10.17161/to.v0i0.6568

Mutualism, no deception

14 September 2023 /

Smelly Gastrodia orchid provides food for fly larvae

Gastrodia foetida rewards its fly visitors for pollination

For its pollination, Gastrodia foetida, attracts female flies that normally visit mushrooms to lay their eggs on. The orchid seems deceptive, but it is not, Kenji Suetsugu discovered.

Many orchids are cheaters. Whereas most plants cooperate with insects and offer them nectar as a reward for pollination, such orchids have their flowers pollinated without offering a reward in return. They lure their pollinators with false pretences. For example, some orchids mimic female insects to abuse males who want to mate and, in their futile attempts, pick up pollen from one flower and deposit it on another.

Another type of deception is perpetrated by orchids of the genus Gastrodia. They attract fly females who want to lay eggs by mimicking the smell of material in which fly larvae grow up, such as fermenting fruits or decaying mushrooms. But the promise is false, as turns out when females visit these flowers. If they lay eggs on them, which they do occasionally, the larvae that hatch die of starvation.

Gastrodia foetida is an exception, Kenji Suetsugu discovered.

Entrapped

Gastrodia foetida is a rare plant from the forests of Japan and Taiwan. As do other Gastrodia species, the plants have no normal leaves, and the succulent flower does not look like much to us: it is inconspicuous and brown. But to females of some fly species the flower is attractive because of its musty smell; foetida means stinky. A common visitor is Drosophila bizonata, a species with larvae that develop in decaying mushrooms.

Drosophila bizonata carrying pollen

When a female fly enters the flower, the hollow lip in the flower bends up to the column that carries pistil and stamens. The female is stuck in the resulting channel between column and lip. To escape from that trap chamber, she has to crawl through a narrow opening along the stamens, and then the pollen, which is packed in two clumps, gets attached to her back (unless there had been another fly before, because then the clumps are already gone). If she then visits another flower in which she is locked up again, the pollen clumps end up on the pistil and this flower will produce many seeds. In other Gastrodia species, things go in the same way.

Decomposing flowers

But unlike those other species, the stinky orchid really is a suitable place to lay eggs on. Suetsugu frequently found eggs on flowers of Gastrodia foetida that had been visited by a female fly. And surprisingly, the eggs hatch and the larvae do not die, but grow well. Three or four days after pollination, the flowers fall off, leaving only the ovary behind. As the flowers decompose on the soil, the larvae feed on the floral tissue until they mature and pupate. Two weeks after pollination they emerge as adult flies.

Although the larvae of Drosophila bizonata are mushroom eaters, these flowers apparently meet their needs.

Mutual service

It is not clear why mushroom eating fly larvae can also grow well on these flowers. It may have to do with the fact that the orchid cannot make its own sugars through photosynthesis, like normal plants, because it does not have the green leaves necessary for this process. Instead, it steals sugars from fungi. Suetsugu suggests that, as a result, the plant tissue may have chemically similarities to that of mushrooms.

In any case, Gastrodia foetida appears to have gone from deception back to mutualism with pollinators, but with a reward other than nectar. Flies pollinate the flowers, and the succulent decomposing flowers then serve as food for their larvae. It is the first time that this form of ‘nursery pollination’ has been demonstrated.

The mutualism is indispensable for the plant, but not for the fly; it still can lay its eggs on mushrooms also.

Willy van Strien

Photos: ©Kenji Suetsugu
First: Gastrodia foetida
Second: Drosophila bizonata carrying pollen on its back in de flower; the trap chamber (the column above, the lip below) is open

See also:
Gastrodia pubilabiata smells like a brood site for fly larvae, but it is not

Source:
Suetsugu, K., 2023. A novel nursery pollination system between a mycoheterotrophic orchid and mushroom-feeding flies. Ecology, online 23 August. Doi: 10.1002/ecy.4152

Cleaner wrasse cheats client secretly

19 October 2021 /

Female knows if partner observes her behaviour

in a bluestreak wrasse pair, a conflict may arise

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

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

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

Punishment

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

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

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

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

Model clients

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

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

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

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

Bad service

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

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

Choosing two times

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

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

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

Clever fish

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

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

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

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

Willy van Strien

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

More about the behaviour of bluestreak cleaner wrasse

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

Honeydew with dopamine

8 October 2021 /

Japanese mugwort aphid forces ants to provide extra protection

Japanese mugwort aphid manipulates attending ants

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

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

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

Dopamine

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

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

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

Extra benefit

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

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

Willy van Strien

Photo: Japanese mugwort aphid. ©Ryota Kawauchiya

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

See how the ant manipulates the aphid colony

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

Hanging baskets

19 April 2021 /

Ants grow plants in tree nests

Well-maintained ant garden of Camponotus femoratus and Crematogaster levior

Some ants have ant gardens. In their nests, one or more plant species are flourishing. The ants are good gardeners, as a Brazilian research team shows: they select the plants carefully and protect them.

In the forests of the Amazon region, you can see hanging baskets, balls from which plants grow. They are the nests of ants that live in trees. These ant gardens  benefit both parties. The plants belong to species that do not root in the soil but grow on tree branches (or in an arboreal ant’s nest), so-called epiphytes. They benefit because the ants disperse the seeds and fertilize the plants that germinate. The ants benefit because the plant roots strengthen the nest and make it rainproof.

Most of the hanging gardens in the Amazon region belong to two ant species that live together: Camponotus femoratus and Crematogaster levior. They share nests and foraging trails but keep their broods separated. A Brazilian research group describes how well this ant duo takes care of their gardens.

Division of tasks

The two species have divided the tasks. Crematogaster levior goes out to get food. The researchers think that it also is the one that, within a colony, takes the initiative to create a new nest; a colony contains on average 17 nests. Crematogaster levior workers are in the majority, especially in young nests; in initial nests, they are even the only ones.

But Camponotus femoratus is the stronger and more aggressive of the two. He constructs and defends the nests.

This species is also the one that collects seeds of the desired plants and puts them in the cardboard nest wall. He is picky: of the many epiphyte species that grow in South America, the ants only use a handful. Only one or two species are grown per nest.

The most common garden plant is Peperomia macrostachya. Probably, the ants are fond of it because, in addition to nectar glands, flowers and fruits, it also has oil glands. Oil is a hard-to-find part of the diet, so these glands are valuable. Among other plants used are Philodendron species.

Maintenance of ant gardens

The ants take good care of the plants. If a leaf is damaged, experiments showed, workers of Camponotus femoratus will gather there; they are triggered by volatile substances that are released upon damage. So, they arrive at places where herbivore insects are gnawing and they can chase them away. Especially damage to the precious Peperomia macrostachya provokes a rapid influx of many workers.

In addition, the ants prune ‘weeds’. The walls of an ants’ nest are an attractive growing place for many epiphytes because they are rich in nutrients. But the ants prevent the growth of unwanted plants that would compete with the garden plants. If the wrong seeds stick to the wall, the ants will remove them, and if the wrong plants germinate, they will cut the stem or leaves.

No wonder that the garden plants flourish and the hanging baskets look good.

Willy van Strien

Photo: Garden with Philodendron of the ant duo Camponotus femoratus and Crematogaster levior. ©Ricardo Eduardo Vicente

More about gardening ants: mini garden

Sources:
Pereira, A.A., I.V. da Silva & R.E. Vicente, 2021. Interaction between epiphytic chemical allelopathy and ant‑pruning determining the composition of Amazonian ant‑garden epiphytes. Arthropod-Plant Interactions, online April 9. Doi: 10.1007/s11829-021-09825-5
Dacquin, P., F. Degueldre & R.E. Vicente, 2021. Relative colony size of parabiotic species demonstrates inversion with growth. Insectes Sociaux, online January 2. Doi: 10.1007/s00040-020-00798-x
Vicente, R.E., W. Dáttilo & T.J. Izzo, 2014. Differential recruitment of Camponotus femoratus (Fabricius) ants in response to ant garden herbivory. Neotropical Entomology 43: 519-525. Doi: 10.1007/s13744-014-0245-6

Shrimp keepers

24 February 2021 /

Longfin damselfish have their algal farms fertilized

Longfin damselfish grows algae with help of shrimp

Every intruder is chased away from the algal farm of the longfin damselfish, but a swarm of opossum shrimp is allowed stay and even receives protection. For good reason, Rohan Brooker and colleagues report.

The longfin damselfish (Stegastes diencaeus) is an aggressive, territorial fish that lives on coral reefs. It grows its own food by creating a farm of a few square meters where palatable algae grow. It tends its algae and defends its territory fiercely; all animals are chased off.

Or rather: almost all animals. Rohan Brooker and colleagues show that during the day, a swarm of opossum shrimp (Mysidium integrum) can be found in many algal farms. A farmer not only tolerates the shrimp’s presence, but it also protects them from their predators, although it takes some extra effort. Apparently, the tiny animals are worth it.

Flourishing farm

Why would an algae-farming longfin damselfish care about the shrimp, Brooker wondered. Although the fish supplements its algae diet with some small animals, it does not eat these shrimp. Perhaps, Brooker supposed, the shrimp are fertilizing the algae with their feces.

And that turned out to be the case. A farm with a swarm of shrimp does better than a farm without such swarm, thanks to nutrients excreted bythe shrimp. It hosts more large brown algae that form a structure on which turf-algae, which the damselfish prefers to eat, grow well. This translates into a better condition of the fish: damselfish with a shrimp swarm on their farm have a larger energy reserve than colleagues with a non-fertilized farm.

Brookers conducted his research on coral reefs off the coast of Belize, Central America.

Domesticated

Thus, the farming fish benefits for its flourishing crop, the shrimp for its guarded refuge. There are no shrimp swarms to be found outside farms during daytime. The shrimp leave the farm at night, when it is safe, to filter food from the water at the surface. Then they return to their permanent residence.

The fidelity to this place is so strong that young shrimp remain in their parents’ farm. Therefore, the authors consider the relationship between longfin damselfish and opossum shrimp as an early stage of domestication. The fish ‘keep’ the shrimp as livestock.

Willy van Strien

Photo: Longfin damselfish Stegastes diencaeus. Mark Rosenstein (Wikimedia Commons, Creative Commons CC BY-SA 4.0)

The research explained on YouTube

Source:
Brooker, R.M., J.M. Casey, Z-L. Cowan, T.L. Sih, D.L. Dixson, A. Manica & W.E. Feeney, 2020. Domestication via the commensal pathway in a fish-invertebrate mutualism. Nature Communications 11: 6253. Doi: 10.1038/s41467-020-19958-5

Males parasitizing on females

13 August 2020 /

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 (Lophiiformes), 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 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

Joint forces against brood parasite

7 April 2020 /

When yellow warbler is warning, red-winged blackbird will attack

Red-winged blackbird eavesdrops on yellow warbler's alarm call

The yellow warbler utters a specific alarm call when a brood parasite is nearby. The red-winged blackbird picks up the signal and attacks, as Shelby Lawson and colleagues write. Together, the birds protect their nests.

Brown-headed cowird parasites on nests of songbirdsA bird’s nest with eggs or young is vulnerable. One of the dangers is that a heterospecific bird will lay an egg in it and charge the parents with the care of a foster young, like the cuckoo does. The red-winged blackbird, which breeds in wet areas in North and Central America, runs such risk. Here the brown-headed cowbird is the ‘cuckoo’, the brood parasite.

Although a young cowbird, unlike a cuckoo chick, does not eject its foster brothers and sisters out of the nest, its presence is to their detriment. The foreign chick demands so much attention that the legitimate young will suffer and starve or fledge in a bad condition.

So, the red-winged blackbird must keep the cowbird out of its nest. It takes advantage of the vigilance of the yellow warbler, another passerine bird that is visited by the cowbird, Shelby Lawson and colleagues show. The yellow warbler, in turn, takes advantage of the aggression of the redwing.

Defense

Yellow warbler utters specific alarm call when brood parasite is presentWhen yellow warblers detect a brown-headed cowbird, they utter a specific alarm signal, a ‘seet’ call. Upon hearing that call, all females respond appropriately: they immediately return to their nest (if they were not already there), repeat the seet and sit tightly on their clutch. As a consequence, a cowbird has no access.

Yellow warblers utter the seet call only in response to the brood parasite and only during the breeding period. To warn of predators, they have a different signal, and upon hearing that call, females will change perches and remain alert, but they won’t return to the nest. The combination of the specific alarm signal for brood parasites and the appropriate response of females is unique.

The researchers wondered whether red-winged blackbirds eavesdrop on that specific signal and take advantage of it. They play backed different sounds nearby redwings’ nests and observed their responses.

Both redwing males and females became aggressive upon hearing the seet of yellow warblers and attacked the speaker. They reacted as heated as in response to the chatter of brown-headed cowbirds. Also the call of a blue jay, a nest predator, aroused their aggression. Apparently, the response to the seet call is a general defence against various dangers that threaten a nest. The birds neglected the song of an innocent songbird.

Chatter of other redwings elicited the strongest defence response; the birds seem to consider conspecifics that invade their territory to be the greatest risk.

Together

The yellow warblers’ signal to warn of brood parasites is picked up by red-winged blackbirds, which respond by approaching the danger. This is to the benefit of yellow warblers: previous research had shown that their nests suffer less from parasitism by cowbirds if they breed in the neighbourhood of red-winged blackbirds. Redwings and yellow warblers often nest in loose aggregations; together they are able to resist the brood parasite.

So far, the red-winged blackbird appears to be the only bird species that understands and responds to yellow warblers’ warning of brood parasites.

Willy van Strien

Photos:
Large: Red-winged blackbird. Brian Gratwicke. (Wikimedia Commons, Creative Commons CC BY 2.0)
Small, upper: Female brown-headed cowbird. Ryan Hodnett (Wikimedia Commons, Creative Commons CC BY-SA 4.0)
Small, lower: Male yellow warbler. Mykola Swarnyk (Wikimedia Commons, Creative Commons CC BY-SA 3.0)
https://commons.wikimedia.org/wiki/File:Yellow_Warbler_Setophaga_aestiva_m_Toronto1.jpg

Researchers tell about their work on YouTube

Sources:
Lawson, S.L., J.K. Enos, N.C. Mendes, S.A. Gill & M.E. Hauber, 2020. Heterospecific eavesdropping on an anti-parasitic referential alarm call. Communications Biology 3: 143 . Doi: 10.1038/s42003-020-0875-7
Gill, S.A. & S.G. Sealy, 2004. Functional reference in an alarm signal given during nest defence: seet calls of yellow warblers denote brood-parasitic brown-headed cowbirds. Behavioral Ecology and Sociobiology 5671-80. Doi: 10.1007/s00265-003-0736-7
Clark, K.L. & R.J Robertson, 1979. Spatial and temporal multi-species nesting aggregations in birds as anti-parasite and anti-predator defenses. Behavioral Ecology and Sociobiology 5: 359-371. Doi: 10.1007/BF00292524

Leaf cutters prevent traffic jams

16 December 2019 /

Take no heavy load when traffic flow is high

leaf cutter ants carry small leaf fragments on crowded trails

When the number of workers on foraging trails is high, leaf cutters maintain the flow by carrying only small pieces of leaf with them, Mariana Pereyra and Alejandro G. Farji-Brener show. Otherwise traffic jams would arise.

The fungus that leaf cutter ants grow in their gardens needs fresh plant material continuously to grow on. And so ant workers walk up and down trails that are cleared and maintained free of debris. They leave the nest to cut leaf fragments from plants and return with a piece in their jaws.

Sometimes ants carry extra-large leaf fragments, causing them to move slowly. That is cumbersome when the trail is crowded, because then a slow ant may hinder the flow. Accordingly, when many ants are walking on the path, they only take small loads with them, Mariana Pereyra and Alejandro Farji-Brener write.

Truck-driver effect

In earlier research, Farji-Brener and colleagues had shown that workers of the leaf cutter Atta cephalotes sometimes carry a strikingly large piece of leaf, up to twice the normal size, to deliver a large gain at the nest. But such extra large burden also has disadvantages; a heavily loaded ant runs slower and hinders the ants that come behind her carrying a normal load. Their walking speed may be reduced by up to 50 per cent. So, a traffic congestion may form behind a heavily loaded worker; the researchers call it the truck-driver effect. It slows down the entire column.

A slow ant on the trail is especially obstructive when it is busy, because in that case, ants walk close together and cannot overtake a slow colleague. At high ant flows, the biologists observed relatively few ants with a heavy load. Is that because the ants are so ‘wise’ not to enter a busy path with a heavy load?

Steady flow

Pereyra and Farji-Brener now answered that question in another species, Acromyrmex crassispinus. They offered workers pieces of ‘leaf’: filter paper soaked in orange juice. They presented pieces of normal size and of extra large size and observed what choice the ants made when different numbers of ants were walking on the trail. And indeed: only at low ant flows, workers selected extra large pieces of paper; when many ants were running, they only picked up the smaller pieces.

Various reasons are thinkable for avoiding large pieces; they make it more difficult to manoeuvre in case of obstacles, the chance of collisions is greater and a heavily loaded ant is more vulnerable to predators. But the fact that ants tend to ignore the large parts at high ant flows suggests that they also do so in order not to obstruct traffic. In this way, leaf cutters optimize colony performance. All going at the same speed: on a busy path, that is the best way to keep a steady flow.

Just like on highway.

Willy van Strien

Photo: Atta cephalotes ©Alejandro Farji-Brener

Sources:
Pereyra, M. & A.G. Farji-Brener, 2019. Traffic restrictions for heavy vehicles: Leaf-cutting ants avoid extra-large loads when the foraging flow is high. Behavioural Processes, online November 25. Doi: 10.1016/j.beproc.2019.104014
Farji-Brener, A.G., F.A. Chinchilla, S. Rifkin, A.M. Sánchez Cuervo, E. Triana, V. Quiroga & P. Giraldo, 2011. The ‘truck-driver’ effect in leaf-cutting ants: how individual load influences the walking speed of nest-mates. Physiological Entomology 36: 128-134. Doi: 10.1111/j.1365-3032.2010.00771.x

The art of pest control

9 July 2019 /

Fungus-growing termites keep their gardens clean

Termites that grow fungus for food manage to keep their crops free from pests, such as weeds, pathogens and fungus-eating nematodes, Saria Otani and Natsumi Kanzaki and their colleagues report. Bacteria in the termites’ gut play a role in pest control.

Some termites species practice agriculture by growing a fungus in their nests for food. And just like human farmers, they have to protect their crop against pests. As is known, they perform well. Saria Otani and colleagues show how a number of African termite species keep their fungal gardens free from non-edible, proliferating or pathogenic fungal species. And Natsumi Kanzaki and colleagues report that the Asian termite Odontotermes formosanus suppresses fungus-eating nematodes.

One way by which the termites control these pests, is by ingesting the plant material on which they grow the fungus crop, so that it passes through their gut. Gut bacteria produce substances that inhibit harmful fungi and nematodes, to ensure that the pre-digested stuff is pretty clean.

Agriculture in termites

Just like ants and some bee and wasp species, termites are eusocial. They live in large colonies that can exist for decades. Most residents are sterile: they are either workers that maintain the nest, take care of the brood and forage for food, or soldiers that defend the nest. Reproduction is a privilege of the royal couple, that has no other duties. The queen is nothing more than an egg laying machine, the king’s task is to mate with her.

Winged sexual individuals (alates) appear once a year. They make a nuptial flight, and couples form that may found a new colony.

More than three hundred species of termites from Africa and Asia have a special way of life: in indoor gardens, they grow fungi in highly productive monocultures. In these species, the workers have the additional task of taking care of the crop. They forage for tough plant-derived material on which they grow the fungus: dry grass, wood and leaf litter. The gardeners consume the stuff and deposit it with their faeces on top of the garden. They are unable to degrade the cellulose and lignin of plants, but the fungus grows well on the pre-digested and fertilized material. It forms nutritious buds, the nodules, which are consumed by the termites. The nodules contain asexual spores, which pass the termites’ gut undamaged; by dropping them on top of the fungal garden, the termites maintain the crop. They also consume older, lower garden parts that are whitish with fungal mycelia.

Cleaning process

Both termite and fungus profit from this agriculture: it is a mutualistic relationship. The fungus has a safe and comfortable living place, the termites have a food supply. But a problem is, that the well attended fungal gardens are suitable as a living place or food source also to other parties.

A garden, for instance, is attractive to fungi that are of no use to the termites, but are competitive with or pathogenic to the crop. The plant material that the workers bring in from the field is not free of such species. Yet, Otani could hardly find harmful fungi in the gardens of three African species, including Macrotermes natalensis. He shows that both the fungal crop and the garden contain substances that inhibit the growth of foreign fungi.

The termites do not synthesize such substances, but their gut bacteria do. By eating the plant material before provisioning the fungus crop, the gardeners probably subject it to a cleaning process. Gut bacteria are deposited on the garden with the faeces, and continue to produce fungicidal substances.

Grooming

Because the fungal crop is full of carbohydrates, proteins and fats, it is an attractive food source for other animals, such as fungus-eating nematodes. Their presence would reduce the harvest. Natsumi Kanzaki shows, in the Asian termite species Odontotermes formosanus, that workers that leave the nest to forage for plant material often carry such nematodes upon return, as does their load.

The fungal crop is not toxic to the nematodes. But they don’t get a chance to eat it, because the termites will groom returning colony mates to remove hitchhiking nematodes. Also, the foragers are not in direct contact with the garden. And when the gardeners consume the new plant material, gut bacteria will suppress nematodes that cling on it.

Obligate

Termite farming originated in Africa. The farming is obligate for both partners: fungi-growing termites and cultivated fungi no longer are capable to live on their own.

Although termites look a bit like ants, they are not related to them. On the evolutionary tree of life, they are close to cockroaches. That is why certain differences exist between termites and ants. Whereas male ants are not engaged in colonial life (all workers are females), sterile male termites help their nest mates as workers or soldiers. Juvenile termites do not go through larval and pupal stages, but are nymphs, small versions of adult animals.

Willy van Strien

Photos:
Large: Odontotermes formosanus, young alates and workers. ©Wei-Ren Liang
Small: Macrotermes natalensis: fungus garden with nodules, soldiers and nymphs. ©Saria Otani

Sources:
Kanzaki, N., W-R. Liang, C-I. Chiu, C-T. Yang, Y-P. Hsueh & H-F. Li, 2019. Nematode-free agricultural system of a fungus-growing termite. Scientific Reports 9: 8917. Doi: 10.1038/s41598-019-44993-8
Otani, S., V.L. Challinor, N.B. Kreuzenbeck, S. Kildgaard, S. Krath Christensen, L. Lee Munk Larsen, D.K. Aanen, S. Anselm Rasmussen, C. Beemelmanns & M. Poulsen, 2019. Disease-free monoculture farming by fungus-growing termites. Scientific Reports 9: 8819 . Doi: 10.1038/s41598-019-45364-z
Aanen, D.K. & J.J. Boomsma, 2006. Social-insect fungus farming. Current Biology 16: R1014-R1016. Doi: 10.1016/j.cub.2006.11.016
Aanen, D.K., P. Eggleton, C. Rouland-Lefèvre, T. Guldberg-Frøslev, S. Rosendahl & J.J. Boomsma, 2002. The evolution of fungus-growing termites and their mutualistic fungal symbionts. PNAS 99: 14887-14892. Doi: 10.1073/pnas.222313099

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