Category: reproductive behaviour (Page 3 of 4)

Arabian babbler leads partner to hidden place

Unlike other animals, the Arabian babbler keeps its sex life private. It has a subtle way to invite another bird for a concealed copulation, as Yitzchak Ben Mocha and colleagues observed.

Animals do not seek to conceal their sexual behaviour. But the Arabian babbler, Argya squamiceps, is an exception. The birds, which live in stable kin groups of two to twenty individuals, do not want to be detected when copulating. A couple that is going to mate will take care to be out of sight of their group mates: at a certain distance or behind thick vegetation.

Yitzchak Ben Mocha and colleagues describe how the birds take a partner to such hidden place without revealing their intention to the other birds.

Arabian babblers live in open, dry landscapes across the Arabian Peninsula and Israel, where each group defends a territory. Within a group, only one pair, the dominant pair, will breed. They are the parents of nearly all young in the group. The other adult group members are subordinates and help raise the young. After hatching, the young stay in the nest for two weeks. And after fledging, it takes another eight weeks until they reach independency. During this period, they need care: protection and food.

Unobtrusive

Observing a population, the researchers witnessed that the birds have a subtle way to invite another bird to copulate. They place themselves in a location that is visible to that specific bird only while holding an object in the beak; often they slightly shake their head. The object can be anything, such as a twig, leaf, fruit, small animal or eggshell. The signalling behaviour is unobtrusive, but the partner grasps the message. When he or she accepts the invitation and approaches, the initiator moves away or hides behind the vegetation and the partner will follow. If they lose contact, the initiator comes back, places itself within the other’s visual field and repeats the invitation.

Usually, a copulation follows. But when another group member appears, the  signaller drops the object and stops the mating behaviour.

The object presented is nothing special, just something that happens to be abundant. So, it is not intended to impress. Neither is it a gift; although it may be edible, that does not affect the partner’s response. The presentation is just a subtle way to invite a mate for a concealed copulation.

Crucial help

Even dominant birds, which don’t have to fear that subordinates will dare to disturb a copulation, take great care to hide their mating behaviour. Why is that? The authors offer an explanation. The care of subordinate group members is crucial for raising the offspring. Without that care, the young have a smaller chance to reach adulthood. Moreover, they gain less weight and will be less capable to acquire food once they are independent.

The dominant pair does not want to lose that precious help. With overt mating behaviour, the researchers suggest, they would cause social tension in the group and increase the chance that subordinates leave or fight, which would be undesirable. So, the parents prefer to keep peace by keeping their love life private.

Willy van Strien

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

See invitation for concealed copulation on YouTube

Sources:
Ben Mocha, Y. & S. Pika, 2019. Intentional presentation of objects in cooperatively breeding Arabian babblers (Turdoides squamiceps). Frontiers in Ecology and Evolution 7: 87. Doi: 10.3389/fevo.2019.00087
Ben Mocha, Y., R. Mundry & S. Pika, 2018. Why hide? Concealed sex in dominant Arabian babblers (Turdoides squamiceps) in the wild. Evolution and Human Behavior 39: 575-582. Doi: 10.1016/j.evolhumbehav.2018.05.009
Ridley, A.R., 2007. Factors affecting offspring survival and development in a cooperative bird: social, maternal and environmental effects. Journal of AnimalEcology 76: 750-760. Doi: 10.1111/j.1365-2656.2007.01248.x

Sperm to both 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

Hummingbird male shines for a split second

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

Maker simply digs ditches, following a few rules

Thousands 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.

In 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

Females apply more colourful make-up than males

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

Squid male changes its mating tactic when growing larger

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