From so simple a beginning

Evolution and Biodiversity

Page 11 of 20

White bellbird is the noisiest

Female runs a risk of hearing damage

White bellbird sings the loudest call

To seduce a female, a male white bellbird calls out to her so loudly at close range, that she may suffer hearing damage, Jeffrey Podos and Mario Cohn-Haft think. Still, she has to expose herself to the deafening noise.

Not all songbirds have a pleasant song. There are also squeakers, males that call as loudly as possible. Their call definitively is impressive. Up to now, the South American screaming piha, which emits an ear-splitting lashing sound that is characteristic for South-American rainforest, held the record for the loudest bird call.

But now, it turns out not to be the noisiest; it is surpassed by the white bellbird from the northeast of the Amazon. Its call can be three times as loud as that of the screaming piha, Jeffrey Podos and Mario Cohn-Haft discovered. The song consists of two tones and sounds like a horn.

Males of screaming piha and white bellbird do not invest time in raising their young; breeding and feeding are females’ tasks. Males are free and try to mate as many females as possible. To outdo each other in attractiveness, they scream, often in loose groups.

The screaming piha relies completely on its vocalization, as it has a dull appearance. But in the white bell bird, the eye also is to be satisfied. The males are white and have a long black fleshy wattle on their forehead, which dangles along their beak.

Extremely loud

The louder the screaming piha and white bellbird scream, the shorter their call will last, as investigation by Podos and Cohn-Haft showed. Apparently, it is demanding to make such a loud noise. So, females can deduce what a male’s quality is from the volume it produces. Females aim to mate a high-quality male, because that will yield healthy, strong offspring. Moreover, sons of such father will also be able to scream loudly, and so be attractive.

To assess the males’ quality on base of their sound volume, females have to come close to them. For bellbird females, which approach a male up to a meter distance, that is no fun, the biologists think. The males have two versions of their song: they usually shout roughly at the level of the screaming piha. But they are able to call even more loudly, like a pneumatic drill, no less than three times as loud as a screaming piha. A bellbird male is able to produce this sound because of its sturdy muscular body.

Risk

When a female approaches a male closely, he will choose the extremely loud version. He sings the first tone in a crouched position, head and tail bent downwards, his back towards her. Then he swivels around in a split second to blast the second, loudest tone right in her face.

She anticipates,  and flutters away when he is about to erupt, but still she is so close that she might suffer hearing damage.

Despite that risk, a female will still join different males, in order to be able to make a choice. It is in his interest to shout as loudly as possible to present himself favourably; it is in her interest to expose herself to that deafening noise, so that she is able to assess his quality.

Willy van Strien

Photo: White bellbird, singing male. ©Anselmo d’Affonseca

Watch and listen to a screaming white bellbird

Compare the sound of screaming piha and white bellbird

Source:
Podos, J. & M. Cohn-Haft, 2019. Extremely loud mating songs at close range in white bellbirds. Current Biology 29: R1055–R1069. Doi: 10.1016/j.cub.2019.09.028

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

Hidden eggs

Blue tit covers her clutch in case of danger

When a predator is around, female blue tits will hide their eggs

Are there any signs indicating that a predator is nearby? In that case, it is more likely that blue tit females will conceal the eggs, Irene Saavedra and colleagues show.

During the egg-laying period, blue tit females add a new egg to their clutch every day, and it was known that they sometimes deposit nest material on the eggs. When the clutch is completed, they start incubating. From that moment on, they no longer will cover the eggs, but are sitting on them continuously. Their male partners will bring them food.

Why do some females take the trouble to cover their clutch during the egg-laying period? One of the reasons, Irene Saavedra and colleagues hypothesized, may be to hide the eggs from predators. Blue tits breed in tree cavities, and also use nest boxes. A closed nest is safer than an open nest, such as that of a blackbird: larger predators cannot enter. But perhaps blue tit females take extra protective measures if needed.

Pungent

Experiments confirmed the hypothesis. During the egg-laying period, the biologists placed a piece of absorbent paper soaked with the urine and the anal gland fluid of a ferret, a marten-like predator, in a number of nest boxes; they pushed it between the floor and the nest. Such paper emits a strong scent. They already knew that blue tits recognize that scent and realize that it indicates danger. As a control, they placed a piece of paper with lemon scent or odourless wet paper in other nest boxes.

The blue tit mothers responded to the pungent predator’s smell. If a next box contained the scent, the chance that the occupant covered her clutch was higher than if a lemon odour was present or no odour at all. So, covering the eggs appears to be a measure to protect them if a predator is nearby; the tits may however have additional reasons to cover their clutch.

Whether the concealment helps in practice has not yet been investigated. It will not always do, because if a predator searches the nest thoroughly, he may find the hidden eggs.

Willy van Strien

Photo: N.P. Holmes (Wikimedia Commons, Creative Commons CC BY-SA 3.0)

Sources:
Saavedra, I. & L. Amo, 2019. Egg concealment is an antipredatory strategy in a cavity-nesting bird. Ethology, 5 augustus online. Doi: 10.1111/eth.12932
Amo, L., I. Galván, G. Tomás & J.J. Sanz, 2008. Predator odour recognition and avoidance in a songbird. Functional Ecology 22: 289-293. Doi: 10.1111/j.1365-2435.2007.01361.x

Higher quality nectar

Evening primrose responds to sound of insects’ wing beats

beach evening primrose detects a bee approaching

When a flying moth or bee is close to the evening primrose Oenothera drummondii, the flowers detect their buzz. Within minutes, they will produce nectar that is more rich in sugars, Marine Veits and colleagues discovered.

Plants have no ears and therefore they are unable hear. Yet, as it turns out, they perceive sound. The wing beats of a passing moth or bee produce sound waves that are detected by the beach evening primrose Oenothera drummondii, Marine Veits and colleagues show. Rapidly, the plant will change the quality of its nectar  by increasing the sugar content. The researchers suspect that, by doing so, the plant increases its reproductive success.

The beach evening primrose, which grows on beaches in Israel, relies on insects for the pollination of its flowers, to be able to set seed. It blooms at night and attracts hawk moths. Flying from flower to flower, they pick up pollen from one flower and deliver it on the pistil of the next one. At dusk, bees visit the flowers.

Energy drink

To keep the pollinators busy, plants must maintain a supply of nectar as a reward for their services. Preferably no soft stuff, but an energy drink: nectar with a high sugar content. But it takes the plant energy to synthesize it, and there is a risk that the precious nectar will be degraded by microorganisms or robbed by ants if it is not picked up by pollinators soon enough.

So it would be nice if a plant would produce high-quality nectar only if there were pollinators nearby. But how can it know?

The researchers hypothesized that plants might be able to detect the sound waves produced by the wing beats of flying insects and respond to it. An unusual idea, but with a series of experiments they showed this to really happen.

When they played back the recorded sound of flying bees to a beach evening primrose plant, the yellow petals of the flowers started vibrating. Soon after, within three minutes, the sugar content of the nectar had increased; before the sound, the flowers produced nectar with a sugar concentration of 16 percent, after the buzz it was 20 percent. Artificial sound at frequencies similar to the sound of flying moths and bees had the same effect, but sound with much higher frequency did not. Nothing happened in silence either.

Soundproof

The nicest test perhaps was with flowers that were contained in soundproof glass jars padded with acoustically isolating foam. These flowers did not respond when the sound of a bee or moth was play backed.

An increased sugar content is an extra reward for flower visitors. They probably will stay longer or go on to visit another flower of the same species. That increases the chance that they pick up or deliver pollen, augmenting the plant’s reproductive success.

If an insect passes by, it does not necessarily make sense for a plant to rapidly increase the sugar content of its nectar. That is only useful if this insect will remain in the area for a while or if it is not alone, because in that case, pollinators will taste the sweet nectar. Video recordings in the field showed that when one insect passes by, there usually are others around. If the weather is fine, many bees or moths are active simultaneously.

Now, more fieldwork is needed to assess whether the evening primrose’s response to insect buzz actually results in more offspring.

Willy van Strien

Photo: © Lilach Hadany

Source:
Veits, M., I. Khait, U. Obolski, E. Zinger, A. Boonman, A. Goldshtein, K. Saban, R. Seltzer, U. Ben-Dor, P. Estlein, A. Kabat, D. Peretz, I. Ratzersdorfer, S. Krylov, D. Chamovitz, Y. Sapir, Y. Yovel & L. Hadany, 2019. Flowers respond to pollinator sound within minutes by increasing nectar sugar concentration. Ecology Letters, online, July 8. Doi: 10.1111/ele.13331

The art of pest control

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

Stripe suit or mohawk

Jumping spider males have two ways to approach cannibalistic females

Striped male Maevia inclemens reduces female aggression

The jumping spider Maevia inclemens is peculiar by having two types of males. They look different and they behave differently. Why would that be? The morphs have developed alternative strategies to reproduce safely, Laurel Lietzenmayer and colleagues think.

Tufted male Maevia inclemens signals its qualityIn the North American jumping spider Maevia inclemens, two types of males exist that differ so much, that they seem to be different species. Some males are black with pale legs and have three tufts of setae on their head, a bit like a cross-positioned mohawk. Other males have black-and-white striped legs and orange pedipalps (the ‘boxing gloves’).

So, females have the opportunity to choose between a punker and a male in a stripe suit. But the ladies are not choosy at all: they respond to the first male they happen to see.

The difference in appearance is linked to a different courtship behaviour. According to Laurel Lietzenmayer and colleagues, alternative strategies to reproduce are behind the differences, each male type being successful in its own way.

Signaling quality

The males face a difficult problem. To be able to reproduce, they must attract the attention of a female. But Maevia inclemens is a predatory species, and males are potential prey for females. Therefore, a male must manage to elicit a female’s mating behaviour – and not her appetite.

The tufted male will stay at a safe distance if he aims to mate a female, about 9 centimetres; the males are only half an inch in length, females are slightly larger. He makes himself as tall as possible by standing on three leg pairs and lifting himself tall, raising and clapping his front legs rhythmically; he also moves his pedipalps and abdomen.

The larger a male is, the higher his quality, the researchers assume. A female will probably prefer to copulate with a large male, because his offspring will inherit his superior qualities. The mohawk may give the female an extra clue about his size, because, as measurements show, the larger the male, the longer his tufts.

Avoiding cannibalism

A striped male has to come closer to a female to attract her attention, because she is not able to discern him easily at a great distance. He courts at only 3 centimetres from her, running the risk of being cannibalized. He makes himself as small as possible by crouching and he slides in semicircles, while holding his front legs in a triangle-like configuration.

Experiments with prey (termites) in different capes of coloured paper show that potential prey with a black-and-white stripe pattern is more conspicuous. Still, it is not attacked more frequently than prey with a solid gray or orange colour. Apparently, the stripes suppress the aggression of female Maevia inclemens, perhaps because many striped prey species are venomous.

Two solutions

Both types of males seem to have a different solution for the problem of approaching a cannibalistic female, the researchers write, which is reflected in their dimorphic appearance and behaviour. The tufted male signals his quality at a far distance, while the striped male attracts her attention while reducing her aggression from nearby. In other words: the tufted male tries to stimulate her mating behaviour, the striped male to temper her appetite.

If a female is willing, the encounter follows the same pattern for both male types. They behave the same, have the same chance of mating successfully and on average sire the same number of offspring. After mating, they again run the risk of being consumed, but in almost all instances they are able to escape.

Genetic determined?

The story about the alternative strategies of Maevia inclemens males is not yet complete, Lietzenmayer indicates. Many questions are still open, for example: is a female actually able to estimate the size of a tufted male from his tufts’ length? Are courting males with striped legs really more visible from close distance than solid coloured males?

In addition, it is not yet known whether the difference between the male types is genetically determined and how it originated.

Few animal species are known with different male types. This remarkable jumping spider is one of them, and it will be fascinating to find out why.

Willy van Strien

Photos:
Large: Maevia inclemens, striped male. Opoterser (Wikimedia Commons, Creative Commons CC BY 3.0)
Small: Maevia inclemens, tufted male. Tibor Nagy (via Flickr, CC BY-NC-ND 2.0)

Watch both male types courting

Sources:
Lietzenmayer, L.B., D.L. Clark & L.A. Taylor, 2019. The role of male coloration and ornamentation in potential alternative mating strategies of the dimorphic jumping spider, Maevia inclemens. Behavioral Ecology and Sociobiology 73: 83. Doi: 10.1007/s00265-019-2691-y
Clark, D.L. & B. Biesiadecki, 2002. Mating success and alternative reproductive strategies of the dimorphic jumping spider, Maevia inclemens (Araneae, Salticidae). The Journal of Arachnology 30: 511-518. Doi: 10.1636/0161-8202(2002)030[0511:MSAARS]2.0.CO;2
Clark, D.L., 1994. Sequence analysis of courtship behavior in the dimorphic jumping spider Maevia inclemens (Araneae, Salticidae). The Journal of Arachnology 22 : 94-107.

Pair bonds in bats

Female Egyptian fruit bat selects male that shared its food

In Egyptian fruit bat, a fruit-eating mammal, males take the initiative to mate, but females determine whether mating occurs. They strongly prefer a friend that often offered them food, Lee Harten and colleagues write.

Bats are social animals, and so is the Egyptian fruit bat (Rousettus aegyptiacus), which occurs in Africa and the Middle East. The fruit-eating mammals live in large colonies of up to thousands of specimens. Individuals within a group maintain friendship bonds with a few others, meaning that they share food.

Lee Harten and colleagues previously reported that the animals have two ways to obtain food. A risky way is to get fruit from a tree on their own. When a bat lands in a tree to collect food, it runs the risk of being caught by a predator, such as a snake or a cat. Therefore, the bats forage high in the trees. And when a fruit tree has thin foliage, they fly with their catch to a safe place to consume it.

There is also a funky method that the bats often use. If a colony mate holds a fruit in its mouth, they approach it and try to steal it. The bat that has obtained the fruit may respond aggressively, but sometimes it will have its catch scrounged.

Faint-hearted

Individuals differ in their strategy. Some usually pick their own fruit, while others are more likely to try to scrounge it. The scroungers are more anxious. They are afraid to land on a place with food, and if they do, they are so vigilant that most times, they will not be able to pick any fruit. For faint-hearted bats, scrounging from others is the better option.

Often scroungers don’t approach any arbitrary colony member, but they have one or two partners that they regularly approach, and that tolerate it. So, a network of affiliations exists.

Overall, Egyptian fruit bat males and females use different strategies. Males are more likely to collect fruit on their own than to scrounge, while for females it is the other way around. Only during lactation – a female produces one pup once or twice a year – they shift to collecting food on their own; they then need extra energy. Outside that period, they prefer to scrounge, each from its own set of favorite males.

Reciprocity

Now, Harten shows that those relationships have big consequences. In his lab, he kept a colony of wild-born Egyptian fruit bats, fifteen males, ten females and the young that were born in the lab. Genetic paternity analysis of the pups showed that in most cases, the father was one of the males that the mother preferred to get food from. The transfer of food from father to mother had been most intensive in the period just before pregnancy.

It is not a direct exchange of food for sex, because not all food-sharing bonds result in a descendant. But by tolerating a few females to prig food, a male has a chance to sire offspring later. Although a male takes the initiative to mate, a female decides whether or not to accept it. If she does, the male gets something in return for its generosity. Such delayed reciprocity is probably an explanation, but maybe not the only one, that the animals share food with some others.

Each male has a number of regular scroungers and a chance to produce a young with one of them. The relationships persist during a breeding season, but when a new period starts, females select another male to sire their young.

Willy van Strien

Photo: Egyptian fruit bat with fig. Artemy Voikhansky (Wikimedia Commons, Creative Commons CC BY-SA 3.0)

Sources:
Harten, L., Y. Prat, S.B. Cohen, R. Dor & Y. Yovel, 2019. Food for sex in bats revealed as producer males reproduce with scrounging females. Current Biology, online May 23. Doi: 10.1016/j.cub.2019.04.066
Harten, L., Y. Matalon, N. Galli, H. Navon, R. Dor & Y. Yovel, 2018. Persistent producer-scrounger relationships in bats. Science Advances 4: e1603293. Doi: 10.1126/sciadv.1603293

Vine avoids spider mites

Tendrils curl away from herbivore-infested plants

Vine Cayratia japonica prevents spider mites from invading

When the Asian climbing plant Cayratia japonica stretches its tendrils to other plants, it is careful. The tendrils withdraw as soon as they detect the presence of spider mite, as Tomoya Nakai & Shuichi Yano observed.

The Asian vine Cayratia japonica is an excellent climber: in America, where it was introduced, it is known as bushkiller. Tendrils of the plant coil around stems of neighboring plants, enabling the vine to grow towards the light. The tendrils grab onto everything they can.

Well, not everything really. The tendrils withdraw when they touch upon a plant that is infested with two-spotted spider mite, Tomoya Nakai & Shuichi Yano show. Two-spotted spider mite or red spider mite (Tetranychus urticae) is a small arachnid hat sucks up plant sap from leaves, which often don’t survive it. The mites occur on hundreds of plant species. If their number at some place is too high, they will walk to another place. As they follow each other’s trails, a group will soon aggregate at this new site.

Spider mite web

Because of its physical contact with other plants, a vine could easily get infested by these harmful critters. But Cayratia japonica appears to have an effective way to prevent mites from invading. As soon as a tendril touches a plant that is occupied by mites, it withdraws and curls away from the infested plant. The researchers could show this in the lab, by placing a number of vines each next to a bean plant that was either clean or bearing many mites. They filmed the movement of the vine’s tendrils using time-lapse photography, making one film frame per minute.

The next question was: what cue does a tendril use to detect the presence of spider mite? Does it pick up the volatile compounds that a bean plant releases into the air when infested? Or does it feel the web with which the mites cover the plant surface to be safe underneath from predators?

Experiments showed that the volatile compounds released by infested bean plants have no effect on the stretching tendrils. But mite silk does: after contact with a spider mite web, the tendrils immediately withdraw. Nakai and Yano also tried spider silk, but the tendrils did not respond to it. The vine thus responds directly and specifically to the presence of spider mite.

This reduces the chance that mites disperse in groups from support plants to the climbing plant. A few of them will cross over during the short contact, but they are not save without the web and will disappear.

Willy van Strien

Poto: 石川 Shihchuan (via Flickr. Creative Commons CC BY-NC-SA 2.0)

Source:
Nakai, T. & S. Yano, 2019. Vines avoid coiling around neighbouring plants infested by polyphagous mites. Scientific Reports 9: 6589. Doi: 10.1038/s41598-019-43101-0

Suicidal repair team

Young aphids die when closing a hole in their nest

Soldier nymphs in Nipponaphis monzeni repair their nest with their body fluid

Japanese aphids, Nipponaphis monzeni, inhabit galls on hazel. A hole in the gall wall would mean the end of the colony living there, were it not for aphid soldiers that give their lives to close it. Mayako Kutsukake and colleagues show how.

The Japanese aphid Nipponaphis monzeni is a social species, living in colonies. Juveniles, called nymphs, serve as soldiers for a period before they become adults and reproduce. It is their task to defend the nest, which is located in galls on the branches of evergreen witch hazel (Distylium racemosum), and to repair it in case of damage.

To close a hole, they show a spectacular and unique behaviour. In a self-destructive action, they discharge their body fluid to plug the gap. The liquid solidifies, forming a scab. Mayako Kutsukake and colleagues were curious about the mechanism.

Vulnerable nest

Colonies of Nipponaphis monzeni are founded by females that reproduce parthenogenetically. A colony of sisters is formed that are genetically identical and produce identical daughters.

gall on hazel in which Nipponaphis monzeni livesThe aphids induce the hazel on which they live to form a closed, hollow tumour, a gall. The animals inhabit this gall, sucking plant sap from the inner wall; in this phase, they are wingless. The gall remains small for a long time, but after three to five years it begins to grow rapidly during spring months and the following summer, it is fully grown – up to eight centimetres long – and home to thousands of aphids.

Winged aphids then appear in autumn. They make an opening in the wall and fly away to a second host tree, an oak, where they mate and produce a new generation of colony foundresses.

A full-grown gall has a lignified, hard wall, offering safety. But during growth, the wall consists of soft plant tissue and the nest is vulnerable. Moth caterpillars consuming hazel tree leaves easily tunnel into such gall, ingesting aphids as well. The soldiers will not tolerate this and attack the enemy: they climb onto it and sting it to death with their mouth parts.

But the hole that the caterpillar gnawed in the gall wall still remains. It has to be closed, otherwise enemies or pathogens may invade, or the nest may desiccate.

Skilful plastering

Japanese researchers had already shown how the soldier nymphs repair the hole with a self-sacrificing behaviour. Dozens or hundreds of them gather around the hole and eject large amounts of white body fluid (hemolymph, which is comparable to our blood) through two tubes on the abdomen. They mix the secretion with their legs and skilfully plaster it over the hole. Some soldiers are buried, others are locked out in the process. And all shrivel after losing their body fluid and will die.

Any way, the hole is fixed; the plug hardens and turns black. As a result, the colony is likely to survive the damage. After the sealing, the gall wall is healed, as the soldiers trigger the tree to cover the plasterwork on the inside by regenerating plant tissue.

Coagulation

Now, Kutsukake investigated the substances with which the soldiers repair a hole. The body fluid, she shows, contains many peculiar large cells of a hitherto unknown type that are packed with fat droplets and the enzyme phenoloxidase; the fluid contains long proteins and tyrosine, an amino acid.

When the soldiers discharge their body fluid, the cells rupture and the fat globules are released; the soldiers plug the gap immediately with a soft lipidic clot. At the same time, the other components come into contact with each other, and a coagulation process starts in which the proteins are linked to form a network that reinforces the lipid plug so that it becomes a scab.

The researchers assume that the process is derived from the process by which wounds heal. But in soldier nymphs’ hemolymph, the components are accumulated in extremely large quantities, far beyond what is necessary for wound healing.

With their unique repair behaviour, the soldier nymphs of Nipponaphis monzeni exhibit extreme altruism to defend the colony: they give their lives. Thanks to this sacrifice, a large part of their family survives. Otherwise the entire colony would have been lost.

Willy van Strien

Photos : ©Mayako Kutsukake
Large: Nipponaphis monzeni soldier nymphs plastering their hemolymphe over a hole
Small: gall in which Nipponaphis monzeni lives

On YouTube, the researchers show how soldiers fix a hole in the gall wall

Sources:
Kutsukake, M., M. Moriyama, S. Shigenobu, X-Y. Meng, N. Nikoh, C. Noda, S. Kobayashi & T. Fukatsu, 2019. Exaggeration and cooption of innate immunity for social defense. PNAS, 15 april online. Doi: 10.1073/pnas.1900917116
Kutsukake, M., H. Shibao, K. Uematsu & T. Fukatsu, 2009. Scab formation and wound healing of plant tissue by soldier aphid. Proceedings of the Royal Society B 276: 1555-1563. Doi: 10.1098/rspb.2008.1628
Kurosu, U., S. Aoki & T. Fukatsu, 2003. Self-sacrificing gall repair by aphid nymphs. Proceedings of the Royal Society London B (Suppl.) 270: S12-S14. Doi: 10.1098/rsbl.2003.0026

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