Costs before benefits

By guarding stepkids, bee male may get the mother

In bee Ceratina nigrolabiata, the male takes care of other males' offspring

Ceratina nigrolabiata bee males guard the nest of their female partner. This seems surprising, as the brood consists mainly of other males’ offspring, as Michael Mikás and colleagues show. Still, the males have good reason.

Bee males don’t do much. Okay, they mate with females and of course that is important, but that’s it. The females construct a nest and take care of the offspring. In solitary species, such as the species that visit a bee hotel, each female makes her own nest; social species, such as the honeybee, live in groups in which queens produce eggs and workers do the work.

There is one exception, Michael Mikát and colleagues report: in the solitary bee species Ceratina nigrolabiata, males do participate in care – but, surprisingly, mainly by protecting other males’ offspring.

Guard

A Ceratina nigrolabiata female makes her nest in the hollow stem of a plant. She goes inside, lays an egg, brings food for the larva that will hatch, closes the space by building a wall and lays another egg in the next part of the stem. Ultimately, a nest consists of six to seven cells in a row, with young in a descending stage of development when viewed from the inside out. The mother leaves when the nest is completely provisioned.

In the majority of nests in which a female is active, a male is present, as the researchers observed during their studies in the Czech Republic. When the female performs foraging trips, the male stays inside the nest to protect it from predators such as ants, driving them away when they come near. He is sitting near the entrance with the head facing inwards. When she returns, she will scratch his abdomen and he will let her pass.

The benefit for her is clear: thanks to this guard, she can leave to forage without having her nest unattended.

For him, it is different. DNA analyzes show that in most cases the brood that he protects does not contain any offspring that he fathers. So he takes care of other males’ offspring, and in general, that is not a good strategy from an evolutionary point of view.

Male switches

In fact, the bee males have no interest in the brood at all; it is the mother that captivates them. A male only has a chance to mate if he finds a female and stays with her until she is willing; in Ceratina nigrolabiata, a female will mate several times in her life. So he has to stay at her nest. While he certainly participates in care by actively protecting the brood, this stepfather care is a by-product of monopolizing a female, according to the researchers.

And indeed, if they removed a female from her nest, the male abandoned the brood.

So, every female is assured of a helpful lover. If a male disappears, his place is usually taken by another.

These stepfathers are not ideal helpers, because they stay on average for only seven days, while a female needs about forty days to complete her nest. As a consequence, the male inhabitant of most nests changes one or more times, and in fatherless periods the female spends less time collecting food, staying on the nest instead. The more changes, the fewer offspring she therefore can produce. But at least she gets help, which is unique among solitary bees.

Willy van Strien

Photo: Ceratina nigrolabiata, female returns at her nest in a hollow plant stem and scratches the guarding male. ©Lukáš Janošík

Source:
Mikát, M., L. Janošík, K. Cerná, E. Matoušková, J. Hadrava, V. Bureš & J. Straka, 2019. Polyandrous bee provides extended offspring care biparentally as an alternative to monandry based eusociality. PNAS: 116: 6238-6243. Doi: 10.1073/pnas.1810092116

Humboldt squid doesn’t discriminate

Sperm to both male and female partners

Humboldt squid male mates male and female partners

Males of the humboldt squid are generous with their sperm cells; male-to-male mating is as common as male-to-female mating, Henk-Jan Hoving and colleagues discovered.

The mating of the humboldt squid or jumbo squid, Dosidicus gigas, is peculiar. Males produce spermatophores, long narrow capsules in which sperm cells are packed, and deposit them around a partner’s beak, which is between the eight arms and two tentacles. Each spermatophore then turns itself inside out to form a so-called spermatangium, which attaches itself to the skin.

If the partner is a female, the sperm cells will be needed. When she is spawning, she will use the sperm cells to fertilize the eggs. But the males transfer their sperm packets not only to females, but also to other males, according to Henk-Jan Hoving and colleagues. And males can’t use them.

It is not possible for researchers to directly observe the mating behaviour of the squid, which occurs in the eastern Pacific Ocean, because the animals live at a depth of several hundred meters. Instead, in order to learn something about that behaviour, the team examined the buccal area of captive specimens, both males and females, and counted the implanted spermatangia. They found sperm packets attached to both females’ and males’ buccal tissues, the same number in both sexes. The motto of mating males seems to be: ‘deposit your spermatophores anywhere you can’.

The question is why they don’t distinguish between male and female partners, as sperm cells transferred to a male are wasted.

Sharp teeth

The authors offer an explanation. The animals live in large mixed schools, in which they encounter many females and males. External morphological differences between the sexes are small, and a male that is about to mate has little time to check whether the individual in front of him is female. If he doesn’t manage to deliver his spermatophores quickly between the other squid’s arms and tentacles, he is in danger to be attacked. The humboldt squid is a predator; the suckers on its tentacles are lined with sharp teeth and its mouth has sharp edges. Cannibalism occurs.

That is why a male prefers a partner that is not larger, but of similar size. Because males are on average smaller than females, he will often deposit his spermatophores on a female that is not yet sexually mature. That is okay; she will store it until she needs it. But there is a chance that he accidentally transfers his sperm to a male.

Because of this strategy – be fast and stay safe – a humboldt squid male admittedly will waste sperm. But that is not a serious drawback. A male has hundreds of spermatophores available, and no more than 80 are transferred per mating. Even if he often mistakenly chooses a same-sex partner, he can still mate many females.

Storage

A female has dozens of sperm-storage organs in the buccal membrane, the seminal receptacles. Sperm cells leave the spermatangium after mating and migrate over the female skin to those storage organs, which apparently secrete an attractant.

When spawning, a female releases millions of eggs, held together in a gelatinous spherical mass. When that mass of eggs passes her mouth, the sperm cells will leave the storage organs, swim to the egg mass and fertilize the eggs.

Willy van Strien

Photo: Foto: Humboldt squid. Rick Starr. Credit: NOAA/CBNMS (Wikimedia Commons, Creative Commons CC BY 2.0)

Sources:
Hoving, H-J.T. Fernández‑Álvarez, F.Á., E.J. Portner & W.F. Gilly, 2019. Same‑sex sexual behaviour in an oceanic ommastrephid squid, Dosidicus gigas (Humboldt squid). Marine Biology 166: 33. Doi: 10.1007/s00227-019-3476-6
Fernández-Álvarez, F.Á., R. Villanueva, H-J.T. Hoving & W.F. Gilly, 2018. The journey of squid sperm. Reviews in Fish Biology and Fisheries 28: 191-199. Doi: 10.1007/s11160-017-9498-6

Romantic sea

Fairytale light shows of Cypridinid ostracods

ostracod produces light to escape from predator

With an amazing show of light pulses, male cypridinid ostracods try to attract a mate. Each species has its own specific show program, with either very short lasting flashes or bulbs that glow for several seconds. Nicholai Hensley and colleagues examined the chemistry behind.

It looks like a fairytale scene: dozens of blue lights dancing in the dark waters of the Caribbean Sea. The spectacle is visible to those who dive or snorkel at the beginning of the night. The light artists are ostracods of the Cypridinidae family, tiny crustaceans (less than two millimeters long) with a carapax consisting of two valves, like a clam shell.

They are also known as sea fireflies. Nicholai Hensley and colleagues study their behaviour and the chemistry behind their light.

Slimeballs

Ostracods produce light by expelling mucus containing a reactant, vargulin, and the enzyme c-luciferase, which react with oxygen in seawater emitting blue light. The ostracods use their light mainly to avoid predation. If a fish picks up an ostracod, the prey will produce a cloud of blue mucus that is pumped into the water via the gills of the fish. It makes the fish visible to its own predators. Startled, it will spit out the bite.

In ostracods of the family Cypridinidae that live in the Caribbean Sea, males use the same light reaction in a much more subtle way with a completely different purpose: they place luminescent slimeballs in the water in order to seduce a female into a mating. This courtship behaviour produces the fairytale scenes.

Train of lights

The light artist best known is Photeros annecohenae, one of the most abundant species off the coast of Belize. In the first dark hour of the night, when the sun is down and the moon is not shining, groups of males display above seagrass beds. They have to perform well, because competition is high. While there are as many females as males, most are unavailable. This is because they incubate fertilized eggs in a brood pouch, and during this period, they will not mate.

American biologists examined male courtship behaviour in the lab, using infrared light. A displaying male will first swim in a looping pattern just above the tips of the seagrass blades and place about three bright flashes of light, probably to draw attention. Then, while spirally swimming upward, it places weaker light pulses at regular intervals. It swims at high speed, slowing down when it releases a luminescent slime ball.

By doing so, it creates a train of about twelve consecutively flashing lights that can be 60 centimetres long. When finished, it descends to start a new series. Often other males join and start displaying in synchrony.

Interception

To choose a mate, females assess the light pulses that the males produce. If a female is attracted to a particular male, she will swim to him without producing any light herself. Thanks to his regular flashing pattern, she manages to meet him just above his last light pulse. Mission accomplished.

Sometimes males try to obtain a mate without producing light themselves. Instead, they intercept a female that is on her way to a performing male.

Starting a show, following another male’s show or sneaking to get a female are different tactics to acquire a mate and a male can easily switch among them.

Species-specific shows

In the Caribbean Sea, many other species of Cypridinidae also occur, and about ten species commonly live at the same place. Because they all have their own characteristic light show, a female has no difficulty finding a conspecific partner. The shows vary in the trajectory a courting male swims, the number of light pulses, the brightness of the light, the interpulse distance and time interval and the time that a pulse remains visible.

Romantic

Hensley investigated the cause of the variation in light pulse length. For although all species perform the same chemical reaction to make light pulses, the duration of the pulses varies greatly: some species, such as Photeros annecohenae, show flashes that last only a fraction of a second, others make light bulbs that continue to glow for 15 seconds.

The structure of the enzyme c-luciferase appears to vary between species, resulting in the light reaction to proceed faster in one species than in another. This determines how soon the light extinguishes. In addition, the reaction rate depends on the amount of vargulin compared to the amount of enzyme: the more vargulin, the longer it takes before it is all converted and the light disappears.

Courting males produce far less light than an animal that avoids predation. Romantic lights don’t have to be that big and bright.

Willy van Strien

Photo: Luminous cloud around a fish that intended to consume an ostracod. It will spit it out. © Trevor Rivers & Nicholai Hensley

Fifteen-scaled worm emits light to defend itself in another way

Sources:
Hensley, N.M., E.A. Ellis, G.A. Gerrish, E. Torres, J.P. Frawley, T.H. Oakley & T.J. Rivers, 2019. Phenotypic evolution shaped by current enzyme function in the bioluminescent courtship signals of sea fireflies. Proceedings of the Royal Society B 286: 20182621. Doi: 10.1098/rspb.2018.2621
Rivers, T.J. & J.G. Morin, 2013. Female ostracods respond to and intercept artificial conspecific male luminescent courtship displays. Behavioral Ecology 24: 877–887. Doi: 10.1093/beheco/art022
Rivers, T.J. & J.G. Morin, 2012. The relative cost of using luminescence for sex and defense: light budgets in cypridinid ostracods. The Journal of Experimental Biology 215, 2860-2868. Doi: 10.1242/jeb.072017
Morin, J.G. & A.C. Cohen, 2010. It’s all about sex: bioluminescent courtship displays, morphological variation and sexual selection in two new genera of Caribbean ostracodes. Journal of Crustacean Biology 30: 56-67. Doi: 10.1651/09-3170.1
Rivers, T.J. & J.G. Morin, 2009. Plasticity of male mating behaviour in a marine bioluminescent ostracod in both time and space. Animal Behaviour 78: 723-734. Doi: 10.1016/j.anbehav.2009.06.020
Rivers, T.J. & J.G. Morin, 2008. Complex sexual courtship displays by luminescent male marine ostracods. The Journal of Experimental Biology 211: 2252-2262. Doi: 10.1242/jeb.011130

Giving everything he’s got

Hummingbird male shines for a split second

broad-tailed hummingbird male performs spectacular dive

In order to seduce as many females as possible, a broad-tailed hummingbird male performs tight diving courtship flights. He combines movement, colour and sound into a spectacular whole, Ben Hogan and Cassie Stoddard show.

With a striking display, a broad-tailed hummingbird male (Selasphorus platycercus) tries to gain a female’s interest. He performs a number of U-shaped dives, getting down from great height (up to 30 meters!) while his wings are trilling. The lowest point of the dive is close to the targeted female, which is perched. At that point, he will give everything he’s got: he rushes past her with a top speed of more than 20 meters per second while his tail feathers produce buzzing sounds. The female perceives his iridescent gorget rapidly shifting from bright red to dark green. Then he climbs up to enable a new dive.

The show is so fast that we can’t see what exactly happens. But Ben Hogan and Cassie Stoddard made video and audio recordings of a large number of shows and analyzed them.

Blink of an eye

An entire dive takes about 6.5 seconds. At the lowest point, the small bird appears to tightly synchronize the components of the show, as the analysis revealed. As a result, top speed, buzzing sounds and colour change almost coincide, all occurring within 300 milliseconds, a human blink of the eye. When he rapidly rises again from the lowest point, the pitch of wing- and tail-generated sounds drops sharply, as when a car with a siren is passing by (the Doppler effect).

The whole is meant to make an overwhelming impression on her. But she is used to see shows like his, because all males perform them. The hummingbird males do not contribute to nest construction or care for the young, leaving all of the work to the females. They try to sire young with as many females as possible. With their tightly synchronized dive, they advertise their genetic quality, promising healthy and attractive offspring.

But is he able to seduce a female? The researchers have not yet figured out what exactly makes a show appealing and how it is performed perfectly in her eyes.

Willy van Strien

Photo: Greg Schechter (Flickr/Wikimedia Commons, Creative Commons CC BY 2.0)

Source:
Hogan, B.G. & M.C. Stoddard, 2018. Synchronization of speed, sound and iridescent color in a hummingbird aerial courtship dive. Nature Communications 9: 5260. Doi: 10.1038/s41467-018-07562-7

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

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

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

Males in transition

Squid male changes its mating tactic when growing larger

Males in the squid Doryteuthis pleii adopt alternative mating tactics, depending on their age

When becoming sexually active, male squids are little successful at first. Only later they perform better, increasing their chances to sire offspring. This development includes major changes, Lígia Apostólico and José Marian discovered.

In squid like Doryteuthis pleii, a species living off the coast of Brazil, small males are able to mate, but they have to do it at an inappropriate time and in a little successful way, as sneakers. Large males act much more effectively as real partners or consorts, as Lígia Apostólico and José Marian report.

Shooting mechanism

When squid mate, s male delivers sperm packages to a female. With a special arm, a male takes the packages, spermatophores, from the spermatophoric sac, where they are produced, and places them on the body of a female with a rapid movement. Then he is done, the sperm packages themselves will do the rest of the work. With a shooting mechanism (ejaculatory apparatus), a package turns inside out, and when evaginated, it attaches onto the female’s body and the sperm cells swim out.

A large male delivers its sperm packages neatly. He approaches a female that is about to release her eggs, places himself next to her with his head pointing in the same direction as hers, moves his special arm behind her head under the mantle that surrounds her body and places his spermatophores near the opening of the oviduct from which the eggs will be released in capsules. The sperm cells have immediate access to the eggs. The male guards the female and tries to keep rivals at bay with flickering colour patterns, because if another male also mates with her, his sperm will have to compete with that other male’s sperm.

Aggregate

A small man does not stand a chance against a large one, so he can only mate at a less exciting time, when no eggs are to be released soon. He doesn’t put his arm under the female’s mantle, but he assumes a head-to-head position and places his sperm packages under her beak, that is between the arms. When she releases the eggs, she holds the capsules for a while near the beak before depositing them on the substrate, and then a sneaker’s sperm cells have a chance – as far as the eggs are not fertilized already by a consort’s sperm.

The sperm cells of sneakers are adapted to the unfortunate site where they are placed and the wide time interval between mating and fertilization chances, and their spermatophores differ from those of consorts. Sneakers have smaller and thinner spermatophores; after evagination, they are short and club-like shaped. The sperm cells come out slowly and aggregate at the exit, having nothing to do there for the time being. The spermatophores of consorts, in contrast, are larger and after evagination, they are long and hook-like shaped. The sperm is quickly discharged in a powerful flow and sperm cells immediately diffuse, so the eggs that are released will pass through a cloud of them.

Now in Doryteuthis pleii, Apostólico and Marian found some males, intermediate in size between sneaker and consort (about 17 centimetres mantle length), that produce sneaker-like spermatophores as well as consort-like spermatophores, and often also an intermediate form. The sneaker-like packages are oldest and stay in the anterior part of the spermatophoric sac, the consort packages are youngest and reside in the posterior part, and the intermediate packages are to be found in between.

Fast switch

This indicates that a male starts as a sneaker and, if he exceeds a certain size limit, he will go on as a consort, implementing all changes that are required by the transition. Age estimates show that sneakers are indeed younger than consorts; the estimates are based on the size of small particles in the organs that enable the animals to control their position and balance; every day these particles, statoliths, increase a little in size. The switch from sneaker to consort must take place very fast, as only few males are found that are in transition.

So, during their lives, which lasts less than a year, the males go through a major development. They are small when at summer the mating season starts, but still they mature sexually, so that they can begin to reproduce – although for the time being only as little successful sneakers.

But perhaps not all males follow that path, Apostólico and Marian think. Males that were born early, in late summer or autumn, have much time before the mating season starts. They can grow to a large size before they become sexually active, and then they can be consorts from the start.

Willy van Strien

Photo: Alvaro E. Migotto (Cifonauta. Creative Commons CC BY-NC SA 3.0)

Sources:
Apostólico, L.H. & J.E.A.R. Marian, 2018. From sneaky to bully: reappraisal of male squid dimorphism indicates ontogenetic mating tactics and striking ejaculate transition. Biological Journal of the Linnean Society 123: 603-614. Doi: 10.1093/biolinnean/bly006
Apostólico, L.H. & J.E.A.R. Marian, 2018. Dimorphic male squid show differential gonadal and ejaculate expenditure. Hydrobiologia 808: 5-22. Doi: 10.1007/s1075
Apostólico, L.H. &  J.E.A.R. Marian, 2017. Dimorphic ejaculates and sperm release strategies associated with alternative mating behaviors in the squid. Journal of Morphology. 278: 1490-1505. Doi: 10.1002/jmor.20726

Blacker than black

Almost no light escapes from of bird of paradise feathers

many birds of paradise have velvety super black feathers

Many birds of paradise have beautiful colours, the brightness of which partly is an illusion, created by dark feathers that surround coloured patches. These feathers are not normal black, but velvety super black, as Dakota McCoy and colleagues show.

Birds of paradise, which mainly occur in New Guinea, deserve their name. The bird family includes many species in which the males have brilliant colours, wear exuberant plumage ornaments and perform exciting dances. With their spectacular appearance, they try to seduce females.

Black feathers play an important role in their courtship, Dakota McCoy and colleagues write. The black feathers that these birds display are not normal black, but super black: they absorb almost all light – more than 99.5 percent – that falls on it. Against this velvety super black background, blue and yellow colours seem brighter than they really are; it looks as if the colours were luminescent. Such super black material is extremely rare in nature.

Ragged, curled edges

The researchers show that the deep black appearance is brought about by the special surface structure of the smallest components of the feathers. A feather consists of a shaft on which barbs are implanted, and the barbs are densely packed with barbules. Normally, these barbules are smooth and just bear hooks that interlock to make the feather stiff. The black feathers of crows and ravens have such normal barbules, as do the black feathers of birds of paradise that play no role in their show, such as back feathers.

But the barbules of super black feathers are highly modified. They have very ragged, curled edges with which deep, curved cavities in between, and this structure retains almost all light that falls on it. A normal black surface absorbs 95 to 97 percent of the incident light and reflects the remaining 3 to 5 percent. But in the micro jungle of spikes and cavities of super-black feathers, the light hits obstacles that scatter it again and again, and each time part of the light is transmitted into the material, where it is absorbed. Ultimately, less than half a percent of the incident light is reflected, so the feathers look super black for someone who faces the male – for instance a choosy female.

Photo: Victoria’s riflebid, Ptiloris victoriae, courting male. Francesco Veronesi (Wikimedia Commons, Creative Commons CC BY-SA 2.0)

Watch paradise birds in a video of BBC Earth, and another one of BBC Earth, and one of Cornell University featuring the magnificent riflebird.

Source:
McCoy, D.E., T. Feo, T.A. Harvey & R.O. Prum, 2018. Structural absorption by barbule microstructures of super black bird of paradise feathers. Nature Communications 9:1. Doi: 10.1038/s41467-017-02088-w

Disarmed, but not impotent

Disabled cactus bug produces more sperm

male Narnia femorata that dropped a leg grows larger testes

With their enlarged hind legs, male cactus bugs fight with each other to defend a territory or to achieve access to a female. What will become of a male that lost one of those weapons, Paul Joseph and colleagues wondered.

The leaf-footed cactus bug Narnia femorata can drop (autotomize) a leg when this leg is grasped by a predator, entrapped or damaged. Thanks to such self-amputation the bug survives the incident, but from now on it has only five legs left to stand on and to walk on; a leg that is lost is not regenerated. For a male, it is extra annoying if it has to sacrifice one of its two hind legs, because it uses them to fight with other males for the possession of a territory or the access to a female. However, if it loses a hind leg before it is fully grown, it can compensate for it, write Paul Joseph and colleagues.

cactus bug narnia femorata preferably feeds on cactus fruitsIn the southwest of the United States, Mexico and parts of Central America, the bugs live on cacti, for instance on the prickly pear cactus Opuntia mesacantha. They feed on the plants, preferably on the ripe fruits, and females lay their eggs on them, selecting parts with ripe fruits.

Fierce fight

Males try to defend a territory on a cactus. If an intruder shows up, both males position themselves rear to rear to display, kick and wrestle with their hind legs until one of them gives up. In the presence of a female – when there is a lot at stake – the fight is fiercer, and the male with the largest hind legs will be the winner. The hind legs of males are real weapons, they are enlarged and serrated.

A male that loses one of its hind legs is in problems. It cannot defeat an intact rival and the chance that it will mate a female has decreased considerably. But it may compensate for its disability, Joseph hypothesized, by growing larger testes. This would be possible if the leg is lost before the male is full-grown; bugs don’t go through a complete metamorphosis with a pupal stage, but they grow gradually.

In order to find out whether juvenile males grow larger testes after losing a hind leg, Joseph experimentally induced juvenile bugs to drop a leg by grasping the leg with a pair of forceps and tickling with a small paintbrush, mimicking what can happen in the wild. As expected, after such treatment the testes grew extra large, while everything else developed as it normally does.

More sperm

And is it useful to have enlarged testes? The researchers paired disabled and untreated males each with a female for 24 hours. Afterwards, they counted how many eggs the females laid and how many of them hatched, meaning that they had been fertilized. They noticed that most females produced about twenty eggs, independent of whether or not they had mated. Clutches of females that had been paired with an untreated male were more likely to contain eggs that hatched than clutches of females with a disabled partner. Apparently, males that dropped a hind leg less often succeeded in mating.

But if disarmed males managed to mate, they fertilized a larger proportion of the eggs. Their enlarged testes produced more sperm, and so they sired more offspring than intact males.

In conclusion, males can compensate for the loss of a weapon by investing more in testes growth – but only if they lose it when still young. Otherwise, it is just bad luck.

Willy van Strien

Photos
Large: leaf-footed cactus bug Narnia femorata; male that dropped a hind leg. ©Christine Miller
Small: leaf-footed cactus bug male on cactus fruit. Cotinis (via Flickr; Creative Commons CC BY-NC-SA 2.0)

Sources:
Joseph, P.N., Z. Emberts, D.A. Sasson & C.W. Miller, 2017. Males that drop a sexually selected weapon grow larger testes. Evolution, 20 november online. Doi: 10.1111/evo.13387
Procter, D.S., A.J. Moore & C.W. Miller, 2012. The form of sexual selection arising from male-male competition depends on the presence of females in the social environment. Journal of Evolutionary Biology 25: 803–812. Doi: 10.1111/j.1420-9101.2012.02485.x