Stealthy moth

Bats receive attenuated echo of their calls

The moth Bunaea alcinoe applies acoustic camouflage

Scales and furry coat of the moth Bunaea alcinoe thwart the searching method of hunting bats, as Zhiyuan Shen and colleagues show. That is how it manages to make itself undetectable.

Moths, which fly around at night, have to deal with agile enemies: bats. These predators find their prey by emitting high (ultrasonic) calls and hearing the echo of their sound when it is reflected by a wall, a tree – or a moth. This ‘echolocation’ enables them to localize a moth and find out in which direction it goes, and then they can catch it.

Moths have developed different ways to escape from these enemies. Some hear the bats’ sounds and quickly change direction; others produce a sound by themselves with which they startle or confuse a hunting bat; still others have wings that distort the echo.

Another defence strategy is to absorb part of the bats’ sounds, preventing their reflection. That idea is applied by Bunaea alcinoe, the cabbage tree emperor moth which lives in Africa, as Zhiyuan Shen and colleagues show.

Vibrations

The numerous scales that cover the wings of this moth are responsible for the absorption. The scales, which look like leaves on a pedicel under a microscope, have a regular, very open nanostructure. Thanks to this structure, they can vibrate exactly at the frequencies of the bats’ sound, the researchers show. The sound waves are transferred to the scales, where they are extinguished by friction: acoustic camouflage against bat echolocation.

Butterflies, which are active during daytime and are not hunted by enemies that use echolocation, have scales on their wings with a different nanostructure, that do not vibrate at the frequency of bat calls.

Another feature is the striking hair growth on the backside of the moths. That furry coat also absorbs sound, in the way curtains and carpets do.

As a result, bats have difficulty finding this prey, Bunaea alcinoe, as only a part of the sound of their calls is reflected when it hits a moth.

Willy van Strien

Photo: Paul Wursten (via Flickr, Creative Commons CC BY-NC-SA 2.0)

Explanation by researchers on YouTube

Sources:
Shen, Z., T.R. Neil, D. Robert, B.W. Drinkwater & M.W. Holderied, 2018. Biomechanics of a moth scale at ultrasonic frequencies. PNAS, online Nov. 12. Doi: 10.1073/pnas.1810025115
Neil, T.R., Z. Shen, B.W. Drinkwater, D. Robert & M.W. Holderied, 2018. Stealthy moths avoid bats with acoustic camouflage. Journal of the Acoustical Society of America 144: 1742. Doi:  10.1121/1.5067725
Zeng, J., N. Xiang, L. Jiang, G. Jones, Y. Zheng, B. Liu & S. Zhang, 2011. Moth wing scales slightly increase the absorbance of bat echolocation calls. PLoS ONE 6(11): e27190. Doi:10.1371/journal.pone.0027190

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Complex cooperation

Weaver ant will rescue nestmate from spider web

a weaver ant on its nest

Floria Uy and colleagues show that workers of the weaver ant care about their nestmates: when an ant gets entangled in a spider’s web, others are willing to help it. The ants were already known for their ‘living sewing machine’.

The weaver ant or green tree ant, Oecophylla smaragdina, is common in the tropical parts of Asia and Australia. Its presence is clearly visible because of its nests, which stand out as balls of leaves in bushes and trees. The arboreal nests are the result of a special piece of group work, involving not only workers, but also larvae.

weaver ants building their nestTo construct a nest, the ants must glue the leaf edges together. Workers will line up, grasp the edges of two leaves (or two pieces of a long leaf) and draw them together. If the distance between the leaf edges is large, they grab each other and form living chains to bridge the gap. By then shortening the chain, they pull the leaf edges towards each other.

 

Living sewing machine

They then attach the edges firmly to each other with a ‘living moveable sewing machine’, as described by Ross Crozier. While many workers hold the leaf edges, others join with a mature larva between their jaws.weaver ants use larval silk to construct the nest The workers stimulate the larvae to spin a silk thread and move them zigzag between the leaf edges, stitching the leaves together.

In many ant species, larvae spin silk to make a cocoon in which they pupate. But in the weaver ant, their silk is used for nest construction.

A colony of weaver ants consists of multiple nests in several trees; many ants are running on trails between these nests. In peripheral nests of the colony, soldiers live that guard the boundaries of the territory and defend it against conspecific ants from foreign colonies. On average, a colony will live for eight years and can have as many as half a million inhabitants.

That is a lot, and you would be inclined to think that an ant’s life does not matter that much.

Yet, the ants are concerned when a nestmate that is in danger, Floria Uy and colleagues now show. They discovered a second example of complex cooperation within this species.

Ant in distress

If a weaver ant is trapped in a spider’s web, conspecifics may bite the threads of the web and free the victim, as Uy showed. But an alternative scenario is also possible: ants may attack a worker that is entangled in a spider’s web and kill it. When will the ants rescue a conspecific, and when will they kill it?

Uy, who conducted experiments on the Solomon Islands, put a number of ants next to an ant trail after having wrapped them in spider’s silk; in some cases, the victim was a nestmate of the ants on the trail, in other cases it was from a foreign colony.

She found that ants will always help a nestmate in distress. But for ants from a different colony, the outcome is uncertain: some are rescued, others are killed. That some of them are killed is to be expected: to the residents on the trail, they are intruders and accordingly, they are treated aggressively. The fact that some non-nestmates in distress are helped instead is surprising.

It may be a mistake, the researchers hypothesize. In the study area, ants from neighbouring colonies have a greater chance of being rescued than ants from distant colonies. Ants recognize nestmates and colony mates by smell, and neighbouring colonies may have a rather similar odour.

Willy van Strien

Photos:
Large: weaver ant on nest. Rushen (via Flickr, CC BY-SA 2.0)
Small, middle: workers building the nest. Sean.hoyland (Wikimedia Commons, Public Domain)
Small, below: nest with weaver ants. Bernard DUPONT (via Flickr, CC BY-SA 2.0)

Watch weaver ants building a nest

Sources:
Uy, F.M.K., J.D. Adcock, S.F. Jeffries & E. Pepere, 2018. Intercolony distance predicts the decision to rescue or attack conspecifics in weaver ants. Insectes Sociaux, online Nov. 3. Doi: 10.1007/s00040-018-0674-z
Crozier, R.H., P.S. Newey, E.A. Schlüns & S.K.A. Robson, 2010. A masterpiece of evolution – Oecophylla weaver ants (Hymenoptera: Formicidae). Myrmecological News 13: 57-71

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Role pattern erased

Twisted-wing parasites change the behaviour of host wasps

The paper wasp Polistes dominula is host to a manipulating parasite, Xenos vesparum

The life cycle of the parasite Xenos vesparum is closely linked to that of the wasps in which it lives. It modifies their behaviour in such a way that it meets its needs, as Laura Beani and colleagues demonstrate.

It is often creepy as well as fascinating to see how parasites control their host. A nice example is Xenos vesparum, parasite of the European paper wasp (Polistes dominula). Its manipulation skills are being unravelled by Laura Beani and her colleagues.

The parasite, which belongs to the insect group of twisted-wing parasites, has a bizarre life cycle, with a striking difference between males and females. In the larval stage, the parasite lives within a wasp host. Males pupate in their host; the front part of the pupae extrudes trough the cuticle between the plates of the host’s abdomen. When adult males emerge, they leave their host to live freely; within a day, they die.

Females live much longer. They remain in their host and don’t pupate, but turn into a ‘bag’ filled with egg cells and a fat supply. Only their cephalothorax, into which head and thorax are fused together, is tough and visible between the plates of the host’s abdomen. Usually only one parasite, either male or female, will mature in a parasitized wasp.

Male and female parasite must mate on the wasp in which the female lives. They do it fast.

Wasp colony

Xenos parasites effectively exploit the annual cycle of their host. In March, fertilized wasp queens, which have spent the winter in groups, awaken. Every queen occupies a place to establish a colony. She builds an open nest and lays the first eggs, which will produce workers. Before these eggs have developed into adults, the queen also has to collect food and take care of the brood. But later, from May, she is just laying eggs, while the workers, who don’t reproduce themselves, do the rest of the work.

In summer, the colony is flourishing with a maximum of fifty wasps, and it is time for the next step. The queen now starts laying eggs that will develop into males and sexual females, future queens. Males and sexual females (gynes) appear in July-August.

Overwintering

Then the queen has finished her task. She stops and the colony collapses. The gynes leave the nest and in early autumn, they aggregate in groups that attract males. Mating follows. As winter approaches, the fertilized gynes search for a sheltered place, again aggregating; they often cluster in buildings, for example under roof tiles. There they hibernate and wait for the spring. Males and worker wasps die before winter. In March, the new queens awaken from winter diapause and the cycle starts again.

The European paper wasp is a common species, and it is not as annoying as the common wasp, Vespula vulgaris.

Trumpet creeper

The parasite disturbs the role pattern of its host. But not immediately. In May, tiny parasite larvae penetrate into worker wasp larvae, which appear to be little affected by the presence of the parasite. Only when the hosts have developed into a pupa, the parasite larvae undergo a growth spurt and mature.

And then the manipulation starts: parasitized workers do not stick to their role. They are lazy and at the age of one week, they will leave the nest.

Beani, doing research in Tuscany, describes how in early summer the parasitized worker wasps are mainly to be found on trumpet creeper bushes; the trumpet creeper, originating from North America, has naturalized in Europe. It produces a lot of nectar, which the parasitized wasps enjoy. Healthy, non-parasitized wasps spend much less time on this plant. Because the hosts deserted the nest and moved to trumpet creeper, the parasites easily find a partner with which they can mate. In the wasp nest, mating would be impossible, as parasite males would immediately be chased off by healthy workers.

Castration by Xenos

Parasite embryos develop within the fertilized parasite females in a wasp’s body and new parasite larvae emerge at the end of July. A female parasite releases more than three thousand larvae which all need a host to develop. When healthy foraging wasps pass by, larvae cling to them, are transported to the wasps’ nest and start searching for wasp larvae. Among infected wasp larvae, there will now be putative males and sexual females, which were destined to reproduce. But they will never do the job, as the parasite castrates them.

Safe

From mid-July on, parasitized wasps (workers, males and gynes) form groups outside the nests, just like healthy young sexual females will do later in the season: the role pattern is erased. They gather on high plants and later on buildings, usually places where healthy males gather every year or where future queens use to overwinter. The parasitized wasps are inactive, the parasites have much opportunity to mate.

When healthy sexual wasp females fly out and aggregate, they often join these groups of parasitized wasps.

At the end of the season, when the gynes have been fertilized and gather at places to hibernate, wasps that contain a fertilized parasite female will join them. Parasite females safely spend the winter in a wasp body, in a group of wasps on a sheltered place. Wasps that carried a parasite male have no function anymore; they die in autumn.

Delivery

When healthy young queens leave to establish a colony in spring, parasitized wasps are left behind. A few weeks later, when the first wasp larvae have hatched in wasp nests, the parasites release their larvae. They then apply a last manipulative trick: they induce their host wasp to deliver the mature larvae in several young wasp nests. There are still no adult workers to defend these nests and the queen is often gone to collect food. From within her host, the parasite female drops larvae in the nests. She also drops some larvae on plants, as a foraging wasp may come along and take them with it.

And so the Xenos parasite completes the circle – with enforced cooperation of the host.

Willy van Strien

Photo: ©Hans Hillewaert (Wikimedia Commons, Creative Commons BY-SA 4.0)

Xenos peckii mating on YouTube

Sources:
Beani, L., F. Cappa, F. Manfredini & M. Zaccaroni, 2018. Preference of Polistes dominula wasps for trumpet creepers when infected by Xenos vesparum: A novel example of co-evolved traits between host and parasite. PLoS ONE 13:e0205201. Doi: 10.1371/journal.pone.0205201
Beani, L., R. Dallai, D. Mercati, F. Cappa, F. Giusti & F. Manfredini, 2011. When a parasite breaks all the rules of a colony: morphology and fate of wasps infected by a strepsipteran endoparasite. Animal Behaviour 82: 1305e1312. Doi:10.1016/j.anbehav.2011.09.012
Beani, L., 2006. Crazy wasps: when parasites manipulate the Polistes phenotype. Annales Zoologici Fennici 43: 564-574.
Hughes, D.P., J. Kathirithamby, S. Turillazzi & L. Beani, 2004. Social wasps desert the colony and aggregate outside if parasitized: parasite manipulation? Behavioral Ecology 15: 1037-1043. Doi:10.1093/beheco/arh111

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Airmobile brigade

Hovering guards of bee colony position themselves orderly

Hovering guards defend the nest of Tetragonisca angustula

It is difficult for a robber bee to stealthy approach a colony of the stingless bee Tetragonisca angustula, because hovering guards will detect it. These guards arrange themselves in an organized manner, Kyle Shackleton and colleagues show.

Workers of the stingless bee Tetragonisca angustula defend their colony extraordinary well against their enemies. Some workers are dedicated guards; they are heavier than other workers and have longer legs. Such specialised soldier caste is not known in other bee species. And while during the day always guards are standing in or near the nest entrance, there are often also some hovering in front of it to keep an eye on the access route, especially in the afternoon. Such an airmobile brigade is unique too.

Robbery

The most important enemy is the robber bee Lestrimelitta limao. Robber bee workers do not collect nectar and pollen from flowers themselves, but get it from colonies of other species. They also steal food that is prepared for the larvae and nest constructing material. Tetragonisca angustula, with its large colonies, is vulnerable. No wonder, then, that there are guards that keep an eye on what is near the nest. It is important to deal with an approaching single robber bee at once, because it is a scout. It will recruit hundreds of others for a raid that will last for hours or days.

As more hovering guards are active, such a flying intruder is detected earlier and intercepted at a greater distance from the nest. The guards recognize the robber bee from its odour and colour; it is black and smells like lemon. The guards wrestle it to the ground by clamping to an antenna or wing. They are not able to kill it, because it is three times heavier than a they are. But they may stop it.

Maximal field of view

Often only a few hovering guards are hanging in front of the nest. Kyle Shackleton and colleagues now show that these guards do not choose their position randomly, but in a coordinated way. If two guards  are hovering, there will usually be one on the left and one of the right side of the access route to the nest. In case of three guards, it rarely occurs that all of them hover at the same side. And four guards mostly are distributed evenly; sometimes sometimes three guards hover at the one side and one at the other side, and it hardly happens that all four guards are at the same side. Because of this coordinated distribution, the hovering guards have a maximal field of view and they will discover an approaching flying enemy as fast as possible.

In case of immediate danger, more guards will be hovering in front of the nest. An even distribution between left and right is less important in that case, because together they will have a good view anyway. There is no surveillance at night, for in the evening the bees close the nest entrance with wax.

Willy van Strien

Photo:
A Tetragonisca angustula hovering guard bee next to a nest-entrance. Bibafu (Wikimedia Commons, Creative Commons CC BY-SA 3.0)

Sources:
Shackleton, K., D.A. Alves & F.L.W. Ratnieks, 2018. Organization enhances collective vigilance in the hovering guards of Tetragonisca angustula bees. Behavioral Ecology 29: 1105-1112. Doi: 10.1093/beheco/ary086
Grüter, C., C. Menezes, V.L. Imperatriz-Fonseca & F.L.W. Ratnieks, 2012. A morphologically specialized soldier caste improves colony defense in a neotropical eusocial bee. PNAS 109: 1182-1186. Doi: 10.1073/pnas.1113398109
Grüter, C., M.H. Kärcher & F.L.W. Ratnieks, 2011. The natural history of nest defence in a stinngless bee, Tetragonisca angustula (Latreille) (Hymenoptera: Apidae), with two distinct types of entrance guards. Neotropical Entomology 40: 55-61. Doi: 10.1590/S1519-566X2011000100008
Van Zweden, J.S., C. Grüter, S.M. Jones & F.L.W. Ratnieks, 2011. Hovering guards of the stingless bee Tetragonisca angustula increase colony defensive perimeter as shown by intra- and inter-specific comparisons. Behavioral Ecology and Sociobiology 65: 1277-1282. Doi: 10.1007/s00265-011-1141-2

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Swirling lights

Scale worm deceives its enemy by detaching glowing scales

Scale worm emits light to escape from predator

If the fifteen-scaled worm is attacked by a lobster, green lights appear in the water. They are scales and tail segments that the worm released to escape, as Julia Livermore and colleagues show.

It is a cheerful sight: animals that emit light, such as fireflies. In marine habitats, this sight is much more common than on land, because most light artists live in dark water. They use their light to defend themselves against predators or to lure prey, or they perform a light show to seduce a partner.

The fifteen-scaled worm, Harmothoe imbricata, uses its light for defence, Julia Livermore and colleagues write. The worm, three to six centimetres in length, occurs everywhere on the northern hemisphere, from the inter-tidal zone to a depth of a few kilometres. On its back it carries fifteen pairs of disc-shaped scales for protection, which flash green light when the worm is irritated. It can also detach the scales, upon which they float through the water as little lights for some time. If it is in great danger, it also releases its posterior body segments, which then also emit light.

Deceived

The researchers show how this behaviour enables the worm to actually escape from its predators, crabs and lobsters. They brought worms into the lab and conducted experiments in which they exposed a worm to the American lobster, Homarus americanus, or the green shore crab, Carcinus maenas; a refuge for the worm to hide was provided.

If an enemy approaches, a worm sometimes tries to slowly swim away unseen. If that fails, its scales will flash and / or the worm detaches scales and sometimes also segments of its tail, which then emit light. Because of the movements of the animals, the parts will swirl in the water. The predator is deceived: it goes after the lights and grabs them – and it will eat the dropped scales and tail segments.

In the meantime, the worm gets a chance to safely escape, as it turns out. Especially when it drops tail segments, its chance of survival is high. The swirling lights therefore function as an effective defence, but also an expensive one: the worm sacrifices protective scales and sometimes also a piece of its tail. That will regenerate, but it takes a while: a few days for the scales, a few weeks for the tail. But the sacrifice may save its life.

Willy van Strien

Photo: Harmothoe impar, a scale worm that is closely related to Harmorhoe imbricata. Saxifraga-Eric Gibcus

The researchers filmed experiments with a crab predator

A flashlight fish uses light to lure prey

Sources:
Livermore, J., T. Perreault & T. Rivers, 2018. Luminescent defensive behaviors or polynoid polychaete worms to natural predators. Marine Biology 165: 149. Doi: 10.1007 / s00227-018-3403-2
Verdes, A. & D.F. Gruber, 2017. Glowing worms: biological, chemical, functional diversity or bioluminescent Annelids. Integrative and Comparative Biology 57: 18-32. Doi: 10.1093 / icb / icx017
Plyuscheva, M. & D. Martin, 2009. On the morphology of elytra as luminescent organs in scale worms (Polychaeta, Polynoidae). Zoosymposia 2: 379-389. Doi: 10.11646 / zoosymposia.2.1.26

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Curbed pregnancy

Pipefish father responds to sight of attractive female

male pipefish curb their pregnancy upon seeing an attractive female

A pipefish father with a filled brood pouch may see a female who produces better offspring than the mother of the embryos he currently carries. He will then curb his pregnancy, as Mário Cunha and colleagues show.

In pipefish, long thin fish species with a tubular snout, parental care is provided by the males. The fathers carry the fertilized eggs until the young hatch and swim away. In some species, including the black-striped pipefish (Syngnathus abaster), they even have a brood pouch, within which the water is of good quality and the eggs are protected and provided with oxygen and nutrients. Black-striped pipefish males carry eggs from three females per ‘pregnancy’ on average. They prefer to receive eggs of large partners, because then the pregnancy will result in more and larger offspring.

Now, a dilemma arises if a pregnant male encounters a female that is larger than the females whose eggs he is brooding, Mário Cunha and colleagues realized. A pregnancy that would yield more than the current one is within reach, but his pouch is already occupied. What would he do: just continue the pregnancy? Or would he break it off, end it earlier or invest less in it to save time and energy for a next brood?

Extremely attractive

To find out, the researchers brought pipefish into the lab and conducted experiments. They paired a number of males with one female of large size and waited until the embryos were developing. They then removed the mother and introduced a very large, extremely attractive female to some of the males. She was behind a transparant divider; the males could see and smell her, but physical contact was not possible.

The researchers checked how long the pregnancy lasted and measured the length of the young fish after birth. For comparison, other fathers were either allowed to remain in contact with the mother or exposed to another female that was equally sized.

embryo of pipefish Syngnathus abasterFathers who perceived a particularly large female were found to respond to this encounter. They curbed their pregnancy: its duration was shorter than that of other fathers, and the young fish that emerged were smaller. Another trial showed that it was more likely that some embryos died. So, when a male sees a very attractive partner, he will invest less in his current pregnancy.

Insensitive behaviour

In our view, that is insensitive behaviour. But it may occur if it increases the breeding success of pipefish fathers. In that case, a fast new pregnancy with high yield should compensate for the smaller number of offspring from the current pregnancy.

Willy van Strien

Photos:
Large: Syngnathus abaster. Giacomo Radi (Wikimedia Commons, GNU Free Documantation License 1.2)
Small: embryo of Syngnathus abaster near the end of the pregnancy. © Sara Mendes

Source:
Cunha, M., A. Berglund, S. Mendes & N. Monteiro, 2018. The ‘Woman in Red’ effect: pipefish males curb pregnancies at the sight of an attractive female. Proceedings of the Royal Society B 285: 20181335. Doi: 10.1098 / rspb.2018.1335

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The pufferfish’s wonderful nest

Maker simply digs ditches, following a few rules

White-spotted pufferfish creates wonderful nest by digging ditchesThousands of times the white-spotted pufferfish male digs a rectilinear ditch in the sand, following simple rules. Ryo Mizuuchi and colleagues explain how this process results in a huge and beautiful sand structure.

Geometrical nest of white-spotted pufferfishIn 1995, divers detected a circular structure with a nice regular pattern on the sandy bottom of the subtropical sea around the southern islands of Japan; its diameter was no less than two meters. Shortly after, more of these structures were found. People were wonder-struck. How did these mystery circles emerge?

The answer was just as surprising as the find itself: the builder turned out to be the male of an unknown pufferfish, an inconspicuous animal only ten centimetres long. It was named Torquigener albomaculosus, white-spotted pufferfish. The large structure is its nest. It consists of an inner circle filled with fine sand particles, surrounded by an outer ring with 25 to 30 radially arranged ditches and ridges; half way, the ring is flattened and the ditches are a bit wider.

Decoration

Hiroshi Kawase and colleagues described how the pufferfish creates this impressive structure, which takes seven to nine days to complete. First, it makes dozens of irregular depressions in the sand, probably to demarcate its building site. On the second day, a basic circular shape begins to emerge, with a flat inner circle and a vague pattern of ditches and ridges. The animal digs the ditches by swimming over the bottom and stirring up sand with its body and fins. The next few days, the inner circle grows and the pattern of ditches and ridges becomes increasingly clear. Moved by the fish’s bustle, the finest sand particles are deposited on the bottom of the ditches and then flow into the inner circle.

Eventually, the pufferfish creates an irregular pattern in the inner circle by flapping its anal fin on the bottom. On the ridges, it deposits some pieces of shell and coral for decoration. And then it is ready to receive females – because that is what it is all about.

Care

When a female shows up outside the ring, he invites her to enter the circle by stirring up a lot of fine sand particles. She likes that, because she prefers to lay her eggs on fine sand. When she is inside the nest, a game of approaching starts. He repeatedly rushes to her and retreats, she sometimes pretends to leave. Eventually she goes down to lay eggs, and while he bites her behind her mouth, he fertilises them with his sperm. They spawn repeatedly. Then she leaves, perhaps to come back again. On this day, the male will receive several females in his nest.

Then a new period starts: the care for the eggs is his task. He flaps his fins, keeps the eggs free from debris, and chases away fishes that come close to the nest. He now does not care about maintaining the structure anymore, so that the pattern fades and the gathered fine sand particles disperse. When the larvae are about to hatch after six days, he flaps his fins at a higher frequency. If the male starts a new breeding cycle, he will make a new nest instead of repairing the old one.

Repeat

The question remains as to how this pufferfish is able to accurately construct a large structure with such geometric design. It mainly stays near the bottom and therefore it has no overview.

It doesn’t need to, as Ryo Mizuuchi and colleagues now show. The structure emerges because the fish repeats a simple behaviour – digging a ditch – thousands of times, applying a few simple rules.

The researchers derived those rules from their observations. They saw how the male marks the centre of the circle by pressing its belly on the ground. Then it repeatedly digs a rectilinear ditch. Initially, the ditches have a random orientation, but later they are more and more directed to the centre of the area. To dig the ditches in the ring, the male always swims from the outside to the inside. The pattern is becoming clearer because it always starts at a low position, where a ditch is already visible. It also digs in the inner circle, but mostly from the inside out; that is probably to demarcate the circle.

When the researchers simulated the building process on the computer following these rules, the ring structure with ditches and ridges did emerge. They also discovered that the thicker or stronger the male is, the wider its ditches are. It is possible that females assess ditch width to select a suitable male, next to the amount of sand he is stirring up. The research on this fish is not finished yet.

Willy van Strien

Photos: Hiroshi Kawase (via Flickr, Creative Commons CC BY-NC 2.0)

A BBC-video shows how the pufferfish male builds its wonderful nest

Sources:
Mizuuchi, R., H. Kawase, H. Shin, D. Iwai & S. Kondo, 2018. Simple rules for construction of a geometric nest structure by pufferfish. Scientific Reports 8: 12366. Doi: 10.1038/s41598-018-30857-0
Kawase, H., R. Mizuuchi, H. Shin, Y. Kitajima, K. Hosoda, M. Shimizu, D. Iwai & S. Kondo, 2017. Discovery of an earliest-stage “mystery circle” and development of the structure constructed by pufferfish, Torquigener albomaculosus (Pisces: Tetraodontidae). Fishes 2: 14. Doi: 10.3390/fishes2030014
Kawase, H., Y. Okata, K. Ito & A. Ida, 2015. Spawning behavior and paternal egg care in a circular structure constructed by pufferfish, Torquigener albomaculosus (Pisces: Tetraodontidae). Bulletin of Marine Science 91: 33-43. Doi: 10.5343/bms.2014.1055
Kawase, H., Y. Okata & K. Ito, 2013. Role of huge geometric circular structures in the reproduction of a marine pufferfish. Scientific Reports 3 : 2106. Doi: 10.1038/srep02106

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Mode of transport

Ants select best carrier material for collecting fluid food

Ant Aphaenogaster subterranea uses tools to collect fluid food

The ant Aphaenogaster subterranea uses absorbent material to carry fluid food back to its nest. It selects the most easily portable material, or it takes material that is discovered first, as Gábor Lörinczi and colleagues observed.

Ants of many species possess a greatly distensible crop and a highly modified proventriculus, in which they transport large volumes of liquid food back home for their nest mates. But other species, among which Aphaenogaster subterranea, don’t possess such internal carrier sac. Still, they are able to collect fluid food. They drop debris in such food source, and grasp the food-soaked material with their mandibles to take it with them. Their choice of carrier material is flexible, Gábor Lörinczi and colleagues write.

Aphaenogaster subterranea occurs in forests in Central and Southern Europe. It lives in colonies, mostly in a nest in the soil, under a stone. Specialised workers collect fluid food for the colony: fruit pulp and body fluids of dead arthropods.

Aphaenogaster is flexible in its choice of toolsLörinczi held a number of nests in plastic boxes the laboratory and conducted experiments in which the nests were connected to a foraging arena via a plastic tube. In the foraging arena, he offered a drop of honey diluted in water or honey enriched with sugars as a liquid food source on a plastic disc; or he offered pure water as a control. Around the disc, he placed different piles of carrier material: small soil grains (1 millimetre in diameter), large soil grains (2 millimetre in diameter), pieces of pine needles (5 millimetre in length), pieces of plant leaves (5 millimetre in length) and pieces of sponge (5 millimetre in length). He then observed the foraging behaviour of the ants.

Flexible

If all piles of ‘carrier bags’ were close to the food bait (at a distance of 4 centimetres), the ants selected mainly small soil grains to transport to and drop into the food. These grains are most easily transportable.  If all piles were at greater distance  (12 centimetres), the ants were less selective. And if one type of material was close to the food bait while the other types were not, they used that material relatively more often. So, the choice of carrier material is not fixed. The ants prefer small soil grains, but if something else is discovered sooner or more readily accessible, they will use that, maximizing their efficiency.

Leave fragments were used only infrequently, even if it could be found close to the food bait. This material is difficult to handle.

Ants that retrieved food-soaked material from the food bait, mainly picked up small soil grains. From honey, they also collected many pieces of sponge. As the authors suggest, these may be easy to pick up because of their buoyancy. They also observed that after a while, the ants started to tear the pieces of sponge into smaller fragments before using them.

Into water, objects were dropped infrequently, and no objects were retrieved from it.

So, workers of Aphaenogaster subterranea show flexibility in foraging tool use, and they even modify some material, which is unique among insects as far as is known.

Willy van Strien

Photos:
Large: Aphaenogaster subterranea. Christophe Quintin (via Flickr, cropped; Creative Commons CC BY-NC 2.0)
Small: The ants covered a drop of food with absorbent material. ©Gábor Lörinczi

Sources:
Lőrinczi, G., G. Módra, O. Juhász & I. Maák, 2018. Which tools to use? Choice optimization in the tool-using ant, Aphaenogaster subterranea. Behavioral Ecology, online August 1. Doi: 10.1093/beheco/ary110
Maák, I., G. Lőrinczi, P. Le Quinquis, G. Módra, D. Bovet, J. Call & P. d’Ettore, 2017. Tool selection during foraging in two species of funnel ants. Animal Behaviour 123: 207-216. Doi: 10.1016/j.anbehav.2016.11.005

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Gruesome boost

Damaged cicadas spread fungal spores via sexual behaviour

Magicicada species are manipulated by the fungus Massospora

Massospora fungi produce substances that we know as recreational drugs, Greg Boyce and colleagues write. By doing so, they manipulate the behaviour of cicadas in which they proliferate. The insects face a horrible fate.

The fungus Massospora cicadina infects periodical cicadas of the genus Magicicada and manipulates the behaviour of infested insects in such a way that they will transmit the fungal spores to conspecifics. Horribly enough, they do so by sexual activities, while their rear part has already been largely destroyed and turned into a fungal mass. Greg Boyce and colleagues try to find out how the fungus exerts its dismal influence.

Magicicada species, which live in the east of North America, are almost never to be seen. They spend most of their life underground as nymphs, the immature form. Only once in many years – some species take thirteen years, other species take seventeen years – mature nymphs emerge from the soil, synchronously and massively per species and per area. They moult into mature cicadas that live only for four to six weeks. In this period, they mate and the females lay their eggs on tree branches. Young nymphs fall down and disappear in the soil.

This unusual life cycle makes it very difficult for natural enemies such as birds to specialize on adult cicadas, because they would not be able to find prey for many years while occasionally, once in thirteen or seventeen years, there is an overwhelming amount.

But the fungus Massospora cicadina can deal with the life cycle of these cicadas.

Copulation attempts

Fungal spores rest in the soil until nymphs emerge and then infect them. After moult, the fungus proliferates in the abdomen of adult insects. Eventually, their rear part, genitals included, falls off and a fungal spore mass becomes visible.

The heavily damaged cicadas try to mate, even more vigorously than normal. Of course, this is useless to them, but the fungus benefits: during the copulation attempts, the unfortunate cicadas transmit spores to conspecifics.

In these insects, the fungus forms a second infection stage. Because now time runs out for the adult cicadas, a third infection is not feasible. Therefore, instead of infective spores, the fungus produces resting spores, which fall down and wait in the soil until the next generation of cicadas appears.

Bisexual males

Earlier this year, John Cooley and colleagues described deviant behaviour in males with a first stage infection. Normally, males sing in chorus to lure females. When a female shows interest in a male, she makes a flicking wing movement that is tuned to his song. He then utters more complex song, she answers with a tightly timed wing-flick, and a ‘duet’ is created while the two approach each other.

First stage infected males try to acquire a female mate in the normal way. But they also respond to the song of other males with female-like wing-flicks. As a result, not only females, but also males are attracted – and become infected. The fungal infection spreads extra fast.

It is striking that only males with a first stage infection assume a female role besides a male role. Males with a second stage infection, which does not produce infective spores, don’t exhibit wing-flicks.

Stimulating drug

Now, Greg Boyce shows how the fungus manages to affect the behaviour of the cicadas. Among the substances that it produces in the cicadas’ abdomen is cathinone. This is known as the active substance in khat, which is released when chewing leaves of the Khat plant, Catha edulis. It is surprising that a plant and a fungus share this substance. Cathinone is closely related to amphetamine, or speed, a stimulating drug, and just like the drug, it interferes with the communication between nerve cells. Apparently, this results in abnormal behaviour in male cicadas.

In a first stage infection, in which the cicadas transmit the fungus spores to conspecifics, the fungus produces more of this stimulating substance than in a second stage infection, which shows how accurately it manipulates its host.

Another Massospora fungal species, which infects cicadas with an annual cycle (Platypedia species), also manipulates the sexual behaviour of its victims, Boyce and colleagues discovered. It produces psilocybin, a hallucinogenic substance known from certain mushrooms, most importantly Psilocybe species. Again a remarkable finding, as the fungus is not closely related to these mushroom species.

Willy van Strien

Photo: Magicicada septendecim. Judy Gallagher( Wikimedia Commons, Creative Commons CC BY 2.0)

Sources:
Boyce, G.R., E. Gluck-Thaler, J.C. Slot, J.E. Stajich, W.J. Davis, T.Y. James, J.R. Cooley, D.G. Panaccione, J. Eilenberg, H.H. De Fine Licht, A.M. Macias, M.C. Berger, K.L. Wickert, C.M. Stauder, E.J. Spahr, M.D. Maust, A.M. Metheny, C. Simon, G. Kritsky, K.T. Hodge, R.A. Humber, T. Gullion, D.P.G. Short, T. Kijimoto, D. Mozgai, N. Arguedas & M.T. Kasson, 2018. Discovery of psychoactive plant and mushroom alkaloids in ancient fungal cicada pathogens. BioRxiv preprint, July 24. Doi: 10.1101/375105
Cooley, J.R., D.C. Marshall & K.B.R. Hill, 2018. A specialized fungal parasite (Massospora cicadina) hijacks the sexual signals of periodical cicadas (Hemiptera: Cicadidae: Magicicada). Scientific Reports 8: 1432. Doi: 10.1038/s41598-018-19813-0
Cooley, J.R. & D.C. Marshall, 2001. Sexual signaling in periodical cicadas, Magicicada spp. (Hemiptera: Cicadidae). Behaviour 138, 827-855. Doi: 10.1163/156853901753172674

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Flamingos use cosmetics

Females apply more colourful make-up than males

Flamingos prefer colourful mates

To catch the attention of possible mates, flamingos use make-up. They produce a colourful oil which they apply over the feathers to reinforce their colour, signalling their quality. For females this is more important than for males, Juan Amat and colleagues write.

Flamingos, both males and females, are keen to find the best mate they can get. Mate selection is a cumbersome process. Months before breeding, the birds join large mixed groups to see each other and to be seen. They exhibit their plumage with outstretched necks and stuffed feathers. And when they selected a mate, the game is not finished yet. They stay alert, and if possible they exchange their mate for a better one. Mutual assessment and selection continue until they actually start breeding.

It is important to stand out with a beautiful pink plumage in such displaying group, because a colourful bird is preferred and will quickly acquire an equally attractive partner. Together they can occupy a good nesting place in the breeding colony, enjoying an advantage over less popular birds.

A beautiful colour is attractive for good reason. The feather colour arises during moult at the end of the summer, when the birds incorporate pigments (carotenoids) that they ingested with their food into their feathers. A beautiful colour is proof that the bird has been successful in obtaining food. It can afford to incorporate the pigments into the feathers, which means that it is not under pressure, because in that case it would have to use the pigments to prevent cell damage caused by stress. The substances are antioxidants, which eliminate harmful oxygen radicals that arise during stress. In short, a bird that has beautiful a colour after moult is healthy and in good condition.

However, a long time passes by between the periods of moult and mate choice during which the original colour fades, and in this time the condition of a bird may either improve or deteriorate. The original feather colour is no good indicator of condition during display. How is it possible to make a good choice?

Cosmetics

There is a solution to this problem. The birds are able to reinforce the colour of their feathers, Juan Amat and colleagues showed in 2011; the team studies a large colony of greater flamingos (Phoenicopterus roseus) that breeds on islands and dikes in the salty South Spanish lagoon Fuente de Piedra, a nature reserve.

Flamingos produce a preen oil in the uropygial gland with pigments that were ingested with their food. They apply the preen oil over the feathers by rubbing their cheeks first on the gland and then along neck, chest and back, using the oil as cosmetics. The feather colour now is an up-to-date indicator of health and condition, because only strong birds find sufficient food to obtain pigments and can use them to tinge their plumage. They also have the time to reinforce the colour of their feathers frequently, which is necessary as the applied pigments quickly bleach.

Amat showed that the more time the birds spend rubbing, the deeper pink the colour of their plumage is. They produce preen oil with highest pigment concentrations in the period of display, when they use their make-up extensively and are most colourful. Once they have started breeding – each pair produces one young -, they stop maintenance behaviour of plumage and the colours fade. The parents stay together until their young is independent, after about three months. They then split up – and in October the long-lasting game of display and mate choice starts again.

Effort

Now, Amat shows that on average females are more colourful than males. They exhibit the same rubbing behaviour, but their uropygial gland contains pigments in higher concentrations. Apparently, it is more important for females to signal their quality.

As the researchers explain, the care for the young is more demanding for the mothers than it is for the fathers. The wetlands where the birds forage are no less than 150 to 400 kilometres away from the breeding colony. So, provisioning the chicks is quite an effort. The female makes the trip more frequently than the male and as she is smaller, the journey is heavier for her. That is why, during pair formation, she has to convince males beforehand that she can handle this task by showing a beautiful pink colour.

After the chick hatched, the female’s colour fades faster than that of her mate because now she is under more pressure and needs the pigments to combat stress damage. She doesn’t need to be attractive anymore – until the next display period starts.

Willy van Strien

Photo: Bernard Dupont (Wikimedia Commons, CC BY-SA 2.0)

Watch flamingos parading their plumage

Sources:
Amat, J.A., A. Garrido, F. Portavia, M. Rendón-Martos, A. Pérez-Gálvez, J. Garrido-Fernández, J. Gómez, A. Béchet & M.A. Rendón, 2018. Dynamic signalling using cosmetics may explain the reversed sexual dichromatism in the monogamous greater flamingo. Behavioral Ecology and Sociobiology 72: 135. Doi: 10.1007/s00265-018-2551-1
Amat, J.A., M.A. Rendón, J. Garrido-Fernández, A. Garrido, M. Rendón-Martos & A. Pérez-Gálvez, 2011. Greater flamingos Phoenicopterus roseus use uropygial secretions as make-up. Behavioral Ecology and Sociobiology 65: 665-673. Doi: 10.1007/s00265-010-1068-z

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