From so simple a beginning

Evolution and Biodiversity

Page 9 of 21

Males parasitizing on females

The immune system of deep-sea anglerfishes is strongly modified

In deep-sea anglerfish, some species have parasitic males and an aberrant immune system

To the well-known peculiarities of deep-sea anglerfish, Jeremy Swann and colleagues add a new one: some species lack an important part of the immune system. This is associated with a unique parasitic lifestyle of males.

There are strange, very strange and extremely weird animals. We can safely include deep-sea anglerfish in the latter group.

Within the anglerfish (Lophiiformes), they form a separate group of over 160 species, the Ceratioidea, which, as the name indicates, have specialized in living in the utter darkness of the deep sea. Food and partners are extremely scarce down there. Hence, as was known, these fish exhibit some peculiarities. Now, it turns out that they also have a very aberrant immune system, Jeremy Swann and colleagues report.

Angling pole with glowing bulb

Deep sea anglerfish start their lives in a quite normal way, eggs and larvae dwelling in surface waters. But once they developed into young fish, things change. Females grow to a considerable size, males stay tiny.

The bigger a female gets, the more eggs she can produce. And so a young female starts growing. She has to eat much, several prey animals are on her menu. To capture prey, she uses a fishing rod growing from her back; it is a modified anterior dorsal fin. At the end it has a lure: a bulb in which bacteria live that produce light by carrying out a chemical reaction. It is a form of mutualism; the bacteria get a place to live in and food in exchange for light production.

An anglerfish’s light can flash and dance, resembling a moving animal. Living animals discern a tasty snack which they will approach. The anglerfish then ingests a large amount of water, including prey. With some luck, the catch will provide sufficient nutrients to sustain her for quite a while.

The females, plump and with large heads and mouths full of sharp teeth, are not the prettiest of all. They are bad swimmers, drifting around, just waiting for prey to come by.

Strong attachment

After completing the larval stage, males’ development takes a completely different direction. Males no longer grow and are unable to eat. Their only goal is to find a female in the empty deep sea. So, they swim constantly. In addition to the light bulb of their angling rod, young females also have two luminous organs on their backs. Maybe the dwarfed males, which have big eyes, are able to detect those organs. If they are lucky, they will meet a partner before they have used up all their reserves.

Upon meeting, he attaches himself to her body with sharp teeth. When, later on, she is ready to release eggs, he is ready to fertilize them. Males and females only become sexually mature when they’ve acquired a partner. Given the scarcity of conspecifics, this makes sense: only after pair formation it is guaranteed that eggs and sperm can come into contact.

Sperm bulge

In some deep-sea anglerfish, the attachment between female and male is temporary; after a while, he lets go.

But in other species, males attach themselves permanently to a female. These are most bizarre types, because the two partners fuse with each other, enabling the male to survive. Their skin tissues meld, the circulatory systems become connected. He now is a ‘sexual parasite’, little more than a sperm-producing bulge that feeds on nutrients that he derives from her. This sexual parasitism is a unique mode of reproduction, occurring only in deep-sea anglerfish.

It is called parasitism, but it may be considered a form of mutualism as well, as the male delivers sperm in return for nutrients.

The best known species is Ceratias holboelli; it is also the largest one and it has the most extreme sexual dimorphism. A female can grow more than a meter long (including tail), sixty times the size of a free-living male. Physical pair formation is permanent. Once attached to her belly, he grows to a maximum of 20 centimetres. A female carries no more than one parasitic male.

Another species with permanent attachment is Cryptopsaras couesii; in this species, up to eight males can be attached to a single female. A female can be 30 centimetres long, a free-living male only three centimetres.

Ancient immune system

It is remarkable that the female immune system doesn’t attack permanently attached, parasitic males, Swann and colleagues realized. You would expect the immune system to recognize and reject such males, as they are not-own tissue. But that does not happen.

Apparently, the immune system tolerates the very intimate mode of reproduction. To find out how, the biologists examined a number of genes that underpin various parts of immune defence. They investigated four deep-sea anglerfish species with temporarily attached males and six species with permanently attached parasitic males, including Cryptopsaras couesii. They compared these species to a number of anglerfish species outside the deep-sea group, where males don’t attach to females.

Fishes have the same immune system as other vertebrates; the system is 500 million years old. It consists of innate, general immune responses on the one hand and specific immune responses that build up against specific intruders that the system has to deal with on the other hand. The researchers focused on the adaptive, specific immune system.

Lethal

The results were surprising: deep sea anglerfish species in which males live as parasites on females lack essential immune genes. Their specific immune system is severely blunted.

In two of the species studied, species in which females can have more than one male attached, virtually no specific immune facilities are functional. This is highly remarkable, because such complete lack of specific immune defence is lethal for other animals. The first infection would kill them. Microbial pathogens occur in the deep sea too, so deep-sea anglerfish must be able to defend themselves. Most likely, they reorganized their innate immune defence, the researchers assume.

From their own and other research, they conclude that the common ancestor of deep-sea anglerfish had tiny, non-parasitic males that temporarily attached themselves to females. On a few occasions, species descending from that ancestor made the switch to permanent attachment and their specific immune defence has been largely dismantled.

It is unclear yet what happened first. Did males become parasitic, making it necessary to turn off the specific immune system? Or did the specific immune system lose important parts, making permanent attachment of males possible?

The deep sea anglerfish remain really puzzling creatures.

Willy van Strien

Drawing: northern giant seadevil, Cryptopsaras couesii (not included in this research); female with male attached. Tony Ayling (Wikimedia Commons, Creative Commons CC BY-SA 1.0)

Watch the fanfin angler, Caulophryne jordani (not included in the research) on YouTube; female with permanently attached male

Sources:
Swann, J.B., S.J. Holland, M. Petersen, T.W. Pietsch, T. Boehm, 2020.  The immunogenetics of sexual parasitism. Science, online July 30. Doi: 10.1126/science.aaz9445
Fairbairn, D.J., 2013. Odd couples. Extraordinary differences between the sexes in the animal kingdom.  Princeton University Press, Princeton and Oxford, VS. ISBN 978-0-691-14196-1

Resemblance is striking

Parasitic Vidua nestlings trick host parents with near-perfect mimicry

Vidua nestlings mimic the young of their host parents

In order not to stand out in the nest in which they grow up clandestinely, Vidua nestlings mimic the young of the host parents. They perform very well, Gabriel Jamie and colleagues report. But some slight discrepancies exist.

African whydahs and indigobirds, Vidua species, are brood parasites like the cuckoo. They lay their eggs in the nest of other bird species, in this case grassfinches, and have the host parents raise their young. Vidua finches are unable to provide parental care. But these brood parasites do much less harm to the host families than a cuckoo, because young Viduas don’t eject other nestlings from the nest. The host parents take care for their own offspring, but have some extra, foreign young.

The foreign nestlings should not stand out, otherwise the tricked parents will notice the deception. It was already known that Vidua young resemble their host parents’ young. With special computer software, Gabriel Jamie and colleagues now show how successful the mimicry is.

Ornamented mouths

pin-tailed whydah is brood parasiteThe Vidua genus contains nineteen species. In the breeding period, the males are real beauties, while the females are inconspicuous and difficult to recognize. Jamie took a closer look at three species: pin-tailed whydah (Vidua macroura), broad-tailed paradise whydah (Vidua obtusa) and purple indigobird (Vidua purpurascens). They are host-specific, each Vidua species has a single host species. Jamie compared the Vidua nestlings to that of their respective host parents and of a number of other grassfinch species.

Young grassfinches (Estrildidae) have ornamental mouth markings that become fully visible when they open their beaks; this ornamentation in unusual among birds. Each grassfinch species has its characteristic pattern, colour and structure.

Nestlings of the breeding parasites accurately mimic those characteristic markings, is the conclusion of the research. An analysis with pattern recognition software shows that the pattern is similar to that of their host parent species. The colours match well too. Vidua nestlings also cleverly imitate the begging calls and postures of their foster siblings.

Imprinting

Previous research, by Michael Sorenson, had shown that the nineteen species of whydahs and indigobirds are much younger than their hosts in an evolutionary sense. The idea is that their common ancestor switched to a brood parasitic lifestyle with a grassfinch as host parent.

Speciation could then occur quickly. Whenever a Vidua female happens to lay eggs in the nest of another host, a separate group associated to that new host arises, because Vidua nestlings imprint on the song of their host father. Each grassfinch species has its own characteristic song. When grown up, Vidua males will mimic the song of their host, and females are attracted to this song. Also, females select a nest of the host species they were raised by to lay their eggs in. The group turns into a new species.

The nestlings then become more and more similar to the nestlings of the new host through an evolutionary adaptation process. Because the more a Vidua nestling resembles the young of its host parents, the more likely they are to accept it and care for it, increasing its survival chance.

Exaggerated

And as a matter of fact, the resemblance between foreign and own young in a parasitized grassfinch’s nest turned out to be striking. But it is not entirely perfect. Small but consistent differences exist. Perhaps the foreign nestlings are (yet) unable to fully mimic their nest mates. And apparently, they are doing well enough: the host parents accept them.

But there may be another explanation for the discrepancies, the researchers write. Nestlings of pin-tailed whydah, for example, have spots in the beak that are slightly larger than those of their foster parents’ young, common waxbill (Estrilda astrild), and their begging calls are slightly extended. Unlike a waxbill nestling, they wave a wing under their open mouth while begging.

So, these Vidua nestlings are slightly exaggerating their host’s begging signals. And perhaps the host parents favour them as a consequence. An intriguing thought.

Willy van Strien

Photos:
Large: pin-tailed whydah nestling, the outside of the mouth markings visible. ©Gabriel A. Jamie
Small: pin-tailed whydah, breeding male. Alan Manson (Wikimedia Commons, Creative Commons CC BY-SA 2.0)

Sources:
Jamie, G.A., S.M. Van Belleghem, B.G. Hogan, S. Hamama, C. Moya, J. Troscianko, M.C. Stoddard, R.M. Kilner & C.N. Spottiswoode, 2020. Multimodal mimicry of hosts in a radiation of parasitic finches. Evolution, online July 21. Doi: 10.1111/evo.14057
Sorenson, M.D., K.M. Sefc & R.B. Payne, 2003. Speciation by host switch in brood parasitic indigobirds. Nature 424: 928-931. Doi: 10.1038/nature01863

Tap dance

Courting blue-capped cordon-bleu stamps its feet while bobbing

Blue-capped cordon-bleu performs tap dance

In blue-capped cordon-bleu, male and female show their commitment with song and movement. With a high-speed camera, Nao Ota revealed the tap dance that is hidden within.

The complex courtship displays of the blue-capped cordon-bleu, an estrildid finch species from East Africa, are nice to observe. Holding a piece of nesting material in the beak, the bird is singing and bobbing up and down. What we don’t see is that it rapidly stamps its feet several times during bobbing. Nao Ota made that ‘tap dance’ visible by recording the courtship with a high-speed camera. Earlier, she had filmed birds in the lab, now she also has footage from the field.

The birds live in monogamous pairs. Male and female look similar, but the male has more blue plumage than the female. Both sexes give song and dance performances.

Commitment

Blue-capped cordon-bleus perform most intensively when their mate is present on the same perch, but they don’t perform a duet. In contrast to humans, they may be able to see the fast tapping. Feet stamping produces sound, as Ota had already shown, and the birds probably feel the vibrations it causes in the perch on which they are sitting.

In presence of a conspecific bird besides the couple, they sing and dance more frequently. The performing bird then points its tail towards its mate. This seems to mean that the display is directed to the partner and to express commitment.

Willy van Strien

Photo: Blue-capped cordon-bleu, Uraeginthus cyanocephalus, male. Peter Steward (via Flickr. Creative Commons CC BY-NC 2.0)

Hear the song and watch the tap dance on YouTube

Sources:
Ota, N., 2020. Tap dancers in the wild: field observations of multimodal courtship displays in socially monogamous songbirds. The Science of Nature 107: 30. Doi: 10.1007/s00114-020-01686-x
Ota. N., M. Gahr & M. Soma, 2018. Couples showing off: Audience promotes both male and female multimodal courtship display in a songbird. Science Advances 4: eaat4779. Doi: 10.1126/sciadv.aat4779
Ota. N., M. Gahr & M. Soma, 2017. Songbird tap dancing produces non-vocal sounds. Bioacoustics 26: 161-168. Doi: 10.1080/09524622.2016.1231080
Ota. N., M. Gahr & M. Soma, 2015. Tap dancing birds: the multimodal mutual courtship display of males and females in a socially monogamous songbird. Scientific Reports 5: 16614. Doi: 10.1038/srep16614

Saved by decoration

Bird doesn’t attack the spider, but its web decoration instead

Cyclosa monticola and its web decoration

Thanks to a striking web decoration, the spider Cyclosa monticola escapes from hungry birds, as Nina Ma and colleagues show. The birds’ attacks fail.

The spider Cyclosa monticola, which is common in East Asia, constructs an elaborate web. Not only does it consist of sticky threads, but it also carries a striking, linear band of trash, containing moults, prey remains, and pieces of leaves and stems. According to Nina Ma and colleagues, this detritus decoration diverts attacks of predators, especially birds, away from the spider.

The spider is in the centre of its web, hardly visible in the decoration band, which extends in both directions. The animal’s colour is similar to the colour of the decoration. Birds cannot distinguish the colours of the spider from that of decorating trash.

Fine scissors

The researchers wondered whether Cyclosa monticola, a tasty snack for many birds, is safer as a result. In order to find out, they exposed spider webs to domestic chickens chicks, one web per chick. Some chicks were given a web with the resident spider present in it; from half of these webs, the researchers had removed the decoration with fine scissors without damaging the web. For comparison, other chicks were given either an empty web or a web with decoration only. Most chicks quickly pecked at whatever (spider and/or decoration) they saw. The researchers were interested in their first target.

Spiders that had been robbed of their web decoration were grabbed by the chick in almost all cases. Spiders that had kept their decoration survived much more frequently. In this situation, the chick usually did not peck at the spider, but at the trash, and the spider dropped down quickly to escape. Obviously, the decoration did confer safety.

More attractive

Although the spider is hardly detectable among the decoration trash, the protection was not only due to camouflage, as the researchers argue. Because in that case, attacks would be random and the risk for the spider to get captured would be equal to its size relative to the size of the decoration. However, the chance of being captured was lower and independent of the size of the decoration band. Apparently, the detritus decoration is more attractive to birds to peck at and diverts their attention away from the spider.

So, web decoration is an effective defence strategy.

The question now is whether insect prey will not avoid the structure. After all, the trick of a spider web is that insects don’t discern the threads and get caught in the web. But research on another spider species that adorns its web shows that insects are attracted to the decoration – and get stuck in the web. The web decoration of Cyclosa monticola may also have this effect; if so, it would have a double function.

Willy van Strien

Photo: web with Cyclosa monticola and detritus decoration. ©Shichang Zhang

Sources:
Ma, N., L. Yu, D. Gong, Z. Hua, H. Zeng, L. Chen, A. Mao, Z. Chen, R. Cai, Y. Ma, Z. Zhang, D. Li, J. Luo & S. Zhang, 2020. Detritus decorations as the extended phenotype deflect avian predator attack increasing fitness in an orb‐web spider. Functional Ecology, online July 16. Doi: 10.1111/1365-2435.13636
Tan. E.J., S.W.H. Seah, L-M.Y.L. Yap, P.M. Goh, W. Gan, F. Liu & D. Li, 2010. Why do orb-weaving spiders (Cyclosa ginnaga) decorate their webs with silk spirals and plant detritus? Animal Behaviour 79: 179-186. Doi: 10.1016/j.anbehav.2009.10.025

Antibacterial treatment

When the eggs are brown-coloured, hoopoe male is more helpful

Hoopoe male will feed its partner when she paints the eggs brown

A brooding hoopoe female repeatedly smears a dark substance from her preen gland onto the eggs. The browner the eggs, the more helpful her partner will be. That is because the colour has meaning to him, Silvia Díaz Lora and colleagues think.

During incubation, a dark-coloured, foul-smelling substance is produced in the preen gland (uropygial gland) of hoopoe females, which is greatly enlarged during this period. It was already known that a female smears the material onto the eggs with her beak. The colour that the eggshells get as a result determines how frequently the male will feed her, Silvia Díaz Lora and colleagues now report.

This has to do with the hatching success of the clutch that is to be expected. If prospects are good, he will invest a lot. If not, he will save energy for the next breeding event. The egg colour is an indication of the expected success.

In the breeding season, hoopoes establish a territory, form pairs and breed in tree cavities. Both parents take care of the nestlings until they fledge. But before nestlings appear, the clutch has to be incubated, which is the females’ task. They don’t leave the nest during this period, and they also stay with the young during the first week. Their partners provide them with food.

Symbiotic bacteria

The preen gland secretion that the females spread onto their eggs protects the embryos, thanks to bacteria that live in the gland during the breeding period and produce compounds that inhibit pathogenic bacteria. When an egg is covered with gland secretion, pathogens are prevented from penetrating the egg shell. This increases the chance the eggs will hatch, and the higher the density of beneficial bacteria, the better the result.

The mother smears the antimicrobial substance onto each egg soon after laying and repeats the procedure until the young hatch. Microscopic cavities on the eggshell enhance adhesion of the substance. Newly laid eggs are light bluish-gray, but they turn dark and greenish-brown by the treatment.

Embryos of other bird species are protected by an extra layer in the egg. But the hoopoe has its own, unique way.

Later on, also the nestlings’ preen gland will produce the brown secretion. The substance has another function: the stench deters predatory enemies. Outside the breeding season, the preen gland of females and fledged young, like that of males, is small. The bacteria are disappeared and the gland produces a white, colourless fat, which the birds use to preen their plumage.

Colour difference

Among hoopoe females, there is a difference in the colour of the substance they paint the eggs with. And what is important for this story: that difference is related to the amount of bacteria that are present in the preen gland. Without bacteria, the substance is red, with bacteria it is brown. The browner the colour, the higher the bacterial density – and the stronger the antimicrobial activity.

That means: the browner the eggs, the better the embryos are protected against infections.

When bringing food to their mate, males see the colour of the eggs. The researchers wanted to know whether they adjust their feeding effort to this colour. On the basis of video recordings at a number of nests, they investigated at what frequency the male came to the nest and what prey he carried. With a spectrometer, they measured the colour of the clutch and they sampled the female’s preen gland contents to assess the density of bacteria.

Willingness

Results are appealing. If the eggs were brown-coloured, the male frequently fed his partner while she was incubating. If the eggs were more reddish, he only worked this hard if her body condition was good. Apparently, hoopoe males are willing to invest a lot in a clutch if it is promising because the mother colours the eggs with a potent antibacterial material or because she is healthy.

Once the eggs had hatched, father’s behaviour no longer depended on the egg colour. There are probably other factors that determine his diligence at that stage, such as the begging behaviour of the young.

Wealth

But there is no proof yet that this story – if eggs are brown, a hoopoe male will work harder – is really true. An alternative possibility is that a father who brings in more food for its partner simply has a richer territory than a father who brings less. Thanks to lots of available food, the mother is in better condition and able to maintain a larger population of bacteria in her preen gland, which colours the secretion brown and gives the eggs good protection. So: the quality of the territory may determine both how much food the male brings in and the colour of the eggs.

To find out what is true, the researchers would have to do experiments in which they paint hoopoe eggs darker and see whether males respond by working harder. For now, it looks like they adjust their effort to the chance that the eggs will hatch successfully. But only if such experiments corroborate this, we can be sure.

Willy van Strien

Photo: Eurasian hoopoe, Upupa epops. Imran Shah (Wikimedia Commons, Creative Commons CC BY-SA 2.0)

Sources:
Díaz Lora, S., T. Pérez-Contreras, M. Azcárate-García, M. Martínez-Bueno, J.J. Soler & M. Martín-Vivaldi, 2020.  Hoopoe Upupa epops male feeding effort is related to female cosmetic egg colouration. Journal of Avian Biology, online June 20. Doi: 10.1111/jav.02433
Martín-Vivaldi, M., J.J. Soler, J.M. Peralta-Sánchez, L. Arco, A.M. Martín-Platero, M. Marínez-Bueno, M. Ruiz-Rodríguez & E. Valdivia, 2014. Special structures of hoopoe eggshells enhance the adhesion of symbiont-carrying uropygial secretion that increase hatching success. Journal of Animal Ecology 83: 1289-130. Doi: 10.1111/1365-2656.12243
Soler, J.J., M. Martín-Vivaldi, J. M. Peralta-Sánchez, L. Arco & N. Juárez-García-Pelayo, 2014. Hoopoes color their eggs with antimicrobial uropygial secretions. Naturwissenschaften 101: 697-705. Doi: 10.1007/s00114-014-1201-3

Attractive dark eyes

Thanks to black irises, female guppy escapes from predator

Guppy female blackens eyes when in danger

By drawing the attention of a predatory fish to the eyes and turning the head away as soon as it strikes, a guppy female manages to evade. Robert Heathcote and colleagues report this hitherto unknown escape strategy.

When Trinidadian guppies detect a predatory fish, they will approach and inspect it to find out if it is hungry and dangerous. The colour of their irises may change when they do; normally the irises are silver, but then they often turn black, making the eyes more salient. It doesn’t seem profitable to draw an enemies attention to the head, so Robert Heathcote and colleagues wondered why guppies blacken their eyes. Is it to deter the enemy? Or is it to divert its attack? But then, how does it work?

By conducting a series of experiments, they found the answer: the colour change is part of a successful escape strategy.

Wild Trinidadian guppies, Poecilia reticulata, live in northeastern South America. One of their enemies is the cichlid Crenicichla alta, a predatory fish that ambushes its victims.

First, the researchers exposed wild guppies to a visually-realistic model of this predatory fish in a tank, and observed whether they blackened their eyes. As it turned out, large individuals do. These are mostly females, which are larger than males on average.

Attack

The predatory fish is not deterred by those dark eyes, as became evident from the next series of experiments, this time with live predatory fish and models of guppies with either black or silver irises. The cichlid attacks guppies with black eyes as often as those with silver-coloured irises. So, the first possible explanation fails.

The researchers also investigated at what target the predator lunges when attacking its prey. When irises are silver-coloured, the predator aims at the broadest part of the body, they discovered. In dark-eyed fish, the attack is diverted to the front. So, colour change of the irises appears to be a diversion strategy. But the predatory fish grasps both types of models, with black and silver irises, just as easily, so a guppy doesn’t benefit from a dark eye colour in itself.

Matador

However, colour change does help when combined with a critically timed evasive manoeuvre, as the last tests showed. In these tests, living guppies were placed in a tank with a living cichlid, but were separated from it by a transparent acetate screen, keeping them from danger. From the movements of the fish, filmed with a high-speed camera, the researchers were able to calculate, for each attack, the probability that the predator would have caught the victim in real conditions, without screen.

The moment the predatory fish strikes, a guppy quickly pivots around an imaginary vertical axis, accelerates and swims away. The imaginary axis runs through the broadest part of the body (more precisely, through the centre of mass), roughly the point that the cichlid aims for in a victim with silvery, less conspicuous irises. This part of the body hardly moves during the rotation. If the predatory fish directs its attack at that point, its chances to succeed are high, as the analysis showed.

The head, on the other hand, immediately leaves its position during the rotational movement. If the predatory fish charges at that part of the victim – like it does in a prey with black irises – it usually misses out.

By blackening its eyes, a guppy thus increases its chance to escape with a quick manoeuvre. The researchers compare this escape strategy – drawing the enemy’s attention to a particular point and then moving it quickly away – with the behaviour of a bullfighter, the matador with his red cape. Such escape strategy was previously unknown in animals.

Only females

For the strategy to be successful, the distance between the eye and the broadest part of the body must be sufficiently large. Males are too small. Males also have a striking eye-sized black spot on their body, which makes it more difficult to draw the predator’s attention to the head. So it makes no sense for males to blacken their irises in presence of a predatory fish, just increasing the detection risk. Accordingly, they don’t.

But females can trick their enemies by making their eyes stand out. The predator aims for her attractive eyes. And they’re gone.

Willy van Strien

Photo: Guppy, Poecilia reticulata, female with silver iris. H. Krisp (Wikimedia Commons, Creative Commons, CC BY 3.0)

Source:
Heathcote, R.J.P., J. Troscianko, S.K. Darden, L.C. Naisbett-Jones, P.R. Laker, A.M. Brown, I.W. Ramnarine, J. Walker & D.P., 2020. A matador-like predator diversion strategy driven by conspicuous coloration in guppies. Current Biology, online June 11. Doi: 10.1016/j.cub.2020.05.017

Expensive defence

Ladybird cannot deal with all enemies at once

Harlequin ladybird cannot resist all enemies at once

When a ladybird has to defer predators regularly, it is less able to resist pathogens and parasites, Michal Knapp and colleagues write.

When threatened, ladybird beetles try to avoid being eaten by excreting a yellow, smelly and bitter-tasting liquid from their legs. This reduces the appetite of hungry insects, lizards, birds or small mammals. The liquid is haemolymph, the insect variant of blood. You can see the phenomenon by provoking a ladybird.

But you shouldn’t do that, because ‘reflex bleeding’ decreases the ability to fight pathogens and parasites, as Michal Knapp and colleagues report.

They conducted experiments with the harlequin ladybird, Harmonia axyridis. The species originally lived in East Asia, was introduced in Europe and North America and nowadays also occurs in South America and Africa.

Precious blood

Haemolymph is an expensive means to scare away enemies. It contains nutrients, as well as blood cells, proteins and other compounds that ladybirds need to eliminate pathogens and parasites. The harlequin ladybird uses, among other compounds, the substance harmonine, which has a strong antimicrobial effect. Each bleeding causes a loss of these valuable components.

To measure the effect of this loss, Knapp triggered reflex bleeding in ladybirds twice a week, during three weeks. Contrary to his expectations, the treatment did not affect the survival of the beetles, and they did not lose weight.

He also, during a month, triggered newly hatched females daily to bleed, and found that their reproductive capacity was unaffected. In their first month of life, they produced as many eggs as females that were untreated. They started laying eggs a few days later, though, especially after losing a high volume of haemolymph. That may be of little importance, however, as the beetles live for months.

Costs

But bleeding, the defence mechanism against predators, comes at the expense of the resistance to other enemies, as it turned out. The concentration of blood cells and proteins in haemolymph had decreased. The concentration of harmonine and similar compounds has not been measured, but other research indicates that it also will have decreased.

Indeed, haemolymph of ladybirds that bled was found to inhibit bacteria less strongly. Probably, these ladybirds are less resistant to parasites as well, as blood cells take part in defence, but this has not been investigated.

Ladybirds successfully deploy constituents of haemolymph against all types of enemies – but they cannot fight them all at once at full power. If they have to deal with hungry predators frequently, their resistance to pathogens and parasites is reduced.

Willy van Strien

Photo: Harlequin ladybird, Harmonia axyridis. Timku (via Flickr, Creative Commons CC BY-NC-SA 2.0)

Source:
Knapp. M., M. Řeřicha & D. Židlická, 2020. Physiological costs of chemical defence: repeated reflex bleeding weakens the immune system and postpones reproduction in a ladybird beetle. Scientific Reports 10: 9266. Doi: 10.1038/s41598-020-66157-9

Game of patience

Snake and frog wait for each other to initiate action

snake should not strike too early

When snake and frog meet, an endurance game begins. The one that moves first takes a risk, as Nozomi Nishiumi and Akira Mori show. If the snake attacks, it will see its prey escape. If the frog jumps, it will be captured.

frog should not jump too earlyAs the snake slowly slides closer, the frog remains motionless. Doesn’t that frog perceive the danger? Or can’t it flee, because it is frozen with fear? Neither, Nozomi Nishiumi and Akira Mori write. The best strategy is to remain motionless as long as possible.
In Japan, the biologists investigated interactions between the Japanese striped snake Elaphe quadrivirgata and one of its prey species, the black-spotted pond frog Pelophylax nigromaculatus. Tension is mounting, as staged encounter experiments showed, because neither animal will take action. And with good reason.

Intercepted

Of course, the frog could initiate flight by jumping away if the snake approaches. But then it is at a disadvantage. Because after take-off kicking, it can’t change his speed and direction. The snake will respond immediately and try to intercept the frog in mid-air, with a good chance of success. So, it is best for the frog to remain motionless.

Also, the approaching snake should refrain from initiating strike behaviour at the frog. Once it has started projecting its head, it can no longer adjust the direction. The frog can evade the strike by jumping away, and chances are high that it will succeed. The snake can make another attempt to capture the frog, but it looses some time because it has to assume the correct posture.

So, the opponents wait for the other to initiate action. The one that gives up first, takes a risk. Sometimes it is the frog that takes pre-emptive action and jumps – with a high chance of being caught. Other times, the snake launches into a strike – and the frog is likely to escape.

No chance

But if both predator and prey persevere, something must happen in the end. At some point they have to switch from waiting to taking action. When the snake has approached the frog to a distance of about six centimetres, the prey has no chance to escape anymore; the snake can successfully grab it. The frog should not wait that long: just before the snake is dangerously close and about to strike, it must jump. That can go wrong, but at least, escape is not yet excluded.

It is a game of patience, but also a game of life and death. In that sense, the tests in which snake and frog are forced to face each other are somewhat cruel, as some frogs were eaten. In nature however, as the researchers state in an ethical note, this is daily practice.

Willy van Strien

Photos:
Large: Japanese striped snake, Elaphe quadrivirgata. Ʃ64 (Wikimedia Commons, Creative Commons CC BY 3.0)
Small: black-spotted pond frog, Pelophylax nigromaculatus. Alpsdake (Wikimedia Commons, Creative Commons, CC BY-SA 3.0; flipped)

Source:
Nishiumi, N. & A. Mori, 2020. A game of patience between predator and prey: waiting for opponent’s action determines successful capture or escape. Canadian Journal of Zoology 98: 351-357. Doi: 10.1139/cjz-2019-0164

Scattering sand

Sea turtle creates decoy nests on the beach

sea turtle creates decoy nests

Sea turtle eggs, buried in a sandy beach, are an attractive meal for some animals. Turtle mothers confuse these enemies with a series of decoy nests, Thomas Burns and colleagues think.

For a sea turtle female, it is physically demanding to lay her eggs. She crawls from the sea onto a sandy beach, selects a suitable place, digs a hole, lays dozens of eggs in it and refills the nest cavity. You would expect her to return to the sea as soon as possible, where she can move more easily and is safer.

But she doesn’t, as Thomas Burns and colleagues report. She first scatters sand around the refilled egg chamber. And then she starts to travel a convoluted path over a large area, further and further away from the nest, stopping periodically to scatter sand again. Only after having done this at several scattering stations, she will leave the beach. What is this extra effort good for?

Tasty

Sea turtles lay their eggs on tropical and subtropical beaches worldwide; afterwards, they don’t look after their clutches any more. The eggs develop in the warm sand, and the young turtles dig through the sand and crawl to the sea. All a mother can do for her offspring is to make sure not to betray the location of the nest, where she has dug in the sand, to predators. The tasty eggs are liked by various animals, including gulls, foxes, raccoons and wild pigs.

Biologists presumed that sea turtles scatter sand around their nests to disguise or camouflage them, so they won’t be noticed. But that can’t be the reason, Burns and colleagues argue after thoroughly studying the behaviour of leatherback sea turtle (Dermochelys coriacea) and hawksbill sea turtle (Eretmochelys imbricata). Because why, in that case, would sea turtles scatter sand also in places that are at considerable distance from the nest?

Big effort

The researchers, who worked on the islands of Trinidad and Tobago, point out that female sea turtles behave according to a fixed pattern until they have finished the nest. Thereafter, their movements become unpredictable. They take a random route on the beach, changing direction at each station.

Research also shows that scattering sand is a time-consuming and exhausting activity. The hawksbill sea turtle puts in as much energy as it does in excavating a nest hole and refilling it, and for the leatherback it is even the most strenuous activity. The hawksbill often scatters sand at more than ten stations, the leatherback may stop more than twenty times. Despite the great effort, the turtles persist: at the last stop they are as active as at the first.

The researchers’ conclusion: the sea turtles create a series of decoy nests. An natural enemy looking for eggs will mostly dig in vain and lose a lot of time. As a consequence, real nests are less easily found and therefore safer.

Willy van Strien

Photo: Eretmochelys imbricata. Gerwin Sturm (Wikimedia Commons, Creative Commons CC BY-SA 2.0)

Sources:
Burns, T.J., R.R. Thomson, R.A. McLaren, J. Rawlinson, E. McMillan, H. Davidson & M.W. Kennedy, 2020. Buried treasure—marine turtles do not ‘disguise’ or ‘camouflage’ their nests but avoid them and create a decoy trail. Royal Society Open Science 7: 200327. Doi: 10.1098/rsos.200327
Burns, T.J., H. Davidson & M.W. Kennedy, 2016. Large-scale investment in the excavation and ‘camouflaging’ phases by nesting leatherback turtles (Dermochelys coriacea). Canadian Journal of Zoology. Doi: 10.1139/cjz-2015-0240

Synchronous calling for safety reasons

Pug-nosed tree frog male refrains from calling first

pug-nosed tree frog males call almost synchronously

As soon as a pug-nosed tree frog male starts calling, other males in the neighbourhood follow suit. After a short time of noise, it is quiet again for a long period. Henry Legett and colleagues found an explanation for this pattern.

In pug-nosed tree frog, aka Panama cross-banded tree frog (Smilisca sila), males face a difficult dilemma. The frog lives in Central America. In order to reproduce, males have to attract a female by calling, which they do in the evening from a location along or above a water stream. But their calls reveal their presence not only to females, but also to their natural enemies, the fringe-lipped bat (Trachops cirrhosus) and midges. The enemies use sound to localise their victims.

According to Henry Legett and colleagues, the frog males reduce the risk by creating an auditory illusion in their enemies.

That illusion arises by the way in which animals, including humans, process sound. If, with a short interval (milliseconds), two or more identical sounds are produced by sources that are close to each other, we will perceive this as one sound, which originated at the source that uttered it first. So, we ignore reflections that occur in a furnished room or a forest, hearing sounds clearly as a consequence. The priority given to the first sound is called the precedence effect.

Followers

fringe-lipped bat is susceptible for auditory illusionBecause of this effect, pug-nosed tree frog males that call nearly synchronously with another male, can hide from their enemies’ ears. And, according to playback experiments by the researchers, this works out pretty well. They used two speakers that almost simultaneously produced the call of a male; alternately, one or the other speaker was leading. The response of bats, midges and female frogs was observed.

As results suggest, a male that closely follows another male calling runs a smaller risk of being captured by a bat and attracts less mosquitoes than the predecessor.

So following pays off – at least as far as safety is concerned. But what about reproduction? If females also have more difficulty finding followers, males won’t benefit from auditory hiding.

But as it turns out, chances are not too bad. The precedence effect is strong in other frog species, such as the túngara frog (Engystomops pustulosus), which inhabits the same region and whose males also call at night, but not synchronously. Compared to túngara frog females, the effect is weak in pug-nosed tree frog females. They chose following males less often than predecessors, but the difference is small. Also followers are approached by females.

Silence

The question remains why any tree frog male is the first to start the synchronous calling. After all, being the predecessor, its attractive power to females is only a bit stronger, while it is more likely to be eaten and bitten.

On the other hand, someone has to do it. If all males would remain silent, nothing happens. But the restraint of males to be the first explains the long periods of silence, interspersed with short, sporadic bouts of calls.

Willy van Strien

Photos:
Large: Pug-nosed tree frog Smilisca sila. Brian Gratwicke (Wikimedia Commons, Creative Commons CC BY 2.0)
Samll: fringe-lipped bat. Karin Schneeberger alias Felineora (Wikimedia Commons, Creative Commons CC BY 3.0)

Sources:
Legett, H.D., C.T. Hemingway & X.E. Bernal, 2020. Prey exploits the auditory illusions of eavesdropping predators. The American Naturalist 195: 927-933. Doi: 10.1086/707719
Tuttle, M.D. & M.J. Ryan, 1982. The role of synchronized calling, ambient light, and ambient noise, in anti-bat-predator behavior of a treefrog. Behavioral Ecology and Sociobiology 11: 125-131. Doi: 10.1007/BF00300101

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