Evolution and Biodiversity

Category: seeing, hearing

Eyeshadow

In bright sunlight, a peregrine falcon can see well thank to malar stripes

Peregrine falcon can see well in bright sunlight thanks to dark malar stripes

Solar glare can impede vision. Michelle Vrettos and colleagues make it plausible that the black malar stripes of a peregrine falcon are helpful during hunt.

With an impressive high-speed dive, a hunting peregrine falcon descends to capture a prey in mid-air. It is the fastest flier among the birds – it can reach about 350 kilometres per hour in a hunting stoop – and it hunts other birds and bats while flying. Its striking black stripes below the eyes help it to track its fast-moving, agile prey, Michelle Vrettos and colleagues write.

Glare

The idea that those black stripes, the so-called malar stripes, are important for sharp vision already existed. Light feathers would reflect sunlight from the cheeks into the eyes, blurring the image, but dark feathers absorb the light. As a consequence, a hunting peregrine falcon would suffer less from solar glare. Other falcon species and some songbirds and hunting mammals have similar dark stripes or an eye mask. And some American athletes blacken their cheeks with eye black to reduce glare and better track fast balls. Does it help?

Apparently, it does, at least in peregrine falcons. Vrettos used photos that were posted on internet of a few thousand peregrines from all over the world; except in Antarctica, the bird is found everywhere. She measured the malar stripes on each photo. And she found that the malar stripes are larger and darker as the average annual solar radiation in the area where a photo was taken is higher. Even though, in sunny areas, dark feathers have the disadvantage that they absorb heat.

Experiments are required to proof that the malar stripes really help vision by reducing solar glare. But the findings are at least striking.

Willy van Strien

Photo: A peregrine falcon with prominent malar stripes. Kevin Cole (Wikimedia Commons, Creative Commons CC BY 2.0)

Source:
Vrettos, M., C. Reynolds & A. Amar, 2021. Malar stripe size and prominence in peregrine falcons vary positively with solar radiation: support for the solar glare hypothesis. Biology Letters 17: 20210116. Doi: 10.1098/rsbl.2021.0116

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

White bellbird is the noisiest

Female runs a risk of hearing damage

White bellbird sings the loudest call

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

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

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

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

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

Extremely loud

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

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

Risk

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

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

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

Willy van Strien

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

Watch and listen to a screaming white bellbird

Compare the sound of screaming piha and white bellbird

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

Idea of lenses abandoned

Brittle star senses light with network of photosensitive cells

Ophiocoma wendtii possesses network of light-sensitive cells

A network of thousands of photosensitive cells allows brittle stars to detect dark places where they can hide from predators, Lauren Sumner-Rooney and colleagues write. No lenses are involved, as has been hypothesized.

The brittle star Ophiocoma wendtii, which lives on coral reefs in the Caribbean, has a strong aversion to light and during the day it retreats into dark crevices, where it is safe from predators. So, it perceives a difference between dark and light places, and this is possible thanks to an impressive network of thousands of light-sensitive cells across the entire body surface, Lauren Sumner-Rooney and colleagues discovered.

Microlenses

At the same time, they reject the existing idea that the dorsal side of the arms is covered with microlenses, as described by for instance Joanna Aizenberg and colleagues. These lenses were thought to focus incident light onto light-sensitive cells beneath; these cells would then transmit a signal to nerve fibres and from these signals neural centres would construct an image of the environment. In fact, the whole animal would act as one compound eye.

Those lenses don’t appear to exist.

Where did the idea come from? Brittle stars have an internal skeleton consisting of a spongy, porous form of calcite (calcium carbonate). The calcite plates of the arms extend into many bumps at the surface, which are hemispherical and transparent. They look just like tiny lenses – and so they were assumed to be tiny lenses.

But now, Sumner-Rooney succeeded in locating cells with light-sensitive pigments. She found many such cells, but not beneath the proposed microlenses, where the focal points should be. Instead, the light-sensitive cells occur at the surface in between the putative lenses, embedded in the skin; they are regularly arranged across the entire body. She also found bundles of nerve fibres that project towards these cells, and no nerve fibres that terminate beneath the ‘lenses’.

Safe place

In conclusion: the brittle star Ophiocoma wendtii possesses thousands of light-sensitive cells at the surface, but the transparent crystal bumps (the putative lenses) are not associated with them. The bumps are completely covered with skin, which is also in contradiction with an optical role. Also, no neural centres are found that could process the signals. With the extensive network of photosensitive cells the animals can distinguish light from dark very coarsely and find a safe place.

Willy van Strien

Photo: Ophiocoma wendtii. © Lauren Sumner-Rooney

Sources:
Sumner-Rooney, L., I.A. Rahman, J.D. Sigwart & E. Ullrich-Lüter, 2018. Whole-body photoreceptor networks are independent of ‘lenses’ in brittle stars. Proceedings of the Royal Society B 285: 20172590. Doi: 10.1098/rspb.2017.2590
Aizenberg, J., A. Tkachenko, S. Weiner, L. Addadi & G. Hendler, 2001. Calcitic microlenses as part of the photoreceptor system in brittlestars. Nature 412: 819-822. Doi: 10.1038/35090573

Alternative imaging

Scallops see thanks to hundreds of tiny mirrors

scallop eyes are similar to reflecting telescopes

If a potential predator is in sight, a scallop moves away. It sees the danger with special eyes, which don’t use a lens for image formation, but a concave mirror instead. Benjamin Palmer and colleagues visualized the scallops’ eyes.

great scallop has many blue eyes

With many bright blue eyes along the edge of their mantles, scallops scan their environment continuously. The eyes are peculiar. They do not use a lens to form an image of the outside world, like almost all other eyes do (including ours), but a concave mirror; the eyes are similar to reflecting telescopes. As a second oddness, each eye contains not one retina, but two.

Using various microscopic imaging techniques, Benjamin Palmer and colleagues took a detailed look at the eyes of the great scallop, Pecten maximus, an inhabitant of the Atlantic Ocean which is appreciated in the kitchen. It has about two hundred eyes, each about one millimetre in size.

Tiles

At the back, the eyes appear to be ’tiled’ with a mosaic of thin, square guanine plates, that are neatly placed next to each other. There are twenty to thirty layers of tiles, and the system reflects almost all incoming light: it is a highly reflective mirror. The fact that the crystals are thin square plates is prove that the scallops have strong control over the crystallisation process, because guanine crystals would take a different form when growing in the lab.

Guanine is also known as the nucleobase G, one of the four letters of the genetic material, the DNA; but it has quite a different application here.

Danger

The mirror is curved, it is concave, so that reflected light is focused in front of it. It has no regular shape, but is flattened in the middle. As a result, light that falls in obliquely, that is, from the periphery of the field of view, is focused slightly closer to the mirror than the light falling in perpendicular, from the centre of the field of view. Each eye has two retinas in front of the mirror which absorb the reflected and focused light: closest to the mirror a retina on which an image is formed of the peripheral field of view, in front of it a retina for the central field of view (incoming light has to pass through the retinas before it hits the mirror).

On the outside of the retinas, the eyes also have a lens, but this lens is weakly refracting and it hardly contributes to the imaging.

Thanks to the many eyes, a scallop can see if a predator is approaching. In case of danger, it makes sure to get away: scallops can move by opening and closing their valves quickly. Though it is not quite like swimming, they can escape if they have to.

Willy van Strien

Photos:
Large: eyes of a scallop. Matthew Krummins (Wikimedia Commons, Creative Commons CC BY 2.0)
Small: great scallop. ©Ceri Jones (Haven Diving Services)

Watch a scallop moving in its habitat

Source:
Palmer, B.A., G.J. Taylor, V. Brumfeld, D. Gur, M. Shemesh, N. Elad, A. Osherov, D. Oron, S. Weiner & L. Addadi, 2017. The image-forming mirror in the eye of the scallop. Science 358: 1172-1175. Doi: 10.1126/science.aam9506

Cleansing hair

Honey bee rubs her eyes after visiting a flower

honey bee quickly cleans herself after visiting a flower

A busy bee gets dirty: she gets covered with the pollen of flowers. But within minutes she has cleaned herself after visiting a flower, as Guillermo Amador and colleagues report, thanks to the hairs on her body.

A bee that has visited a flower to collect nectar or pollen may be completely covered with yellow pollen grains. When the eyes and antennae are dirty, she is not able to see or smell well. But the discomfort lasts only a few minutes, because during flight she manages to quickly remove the pollen, as Guillermo Amador and colleagues show. She puts it in the baskets on her hind legs to it take to the nest as food for the young, or she drops it.

Using high speed cameras, the researchers recorded the cleaning process in a number of honeybees that they had coated in pollen of dandelion or other plants. To keep the bees in front of the cameras, they tethered them temporarily to a thin wire. As the footage showed upon analysis, the bee hairs are essential for the rapid cleaning process.

Brushes

A honeybee that is covered in pollen starts grooming her eyes. The hairs on the eyes are spaced so that the sticky pollen grains are suspended near the tips, where they can be easily wiped away by the pollen brushes on the forelegs. As the hairs of these brushes are closer spaced than those of the eyes, the pollen grains attach to the brushes.

With a fast movement, the bees swipe a foreleg across an eye, from dorsal to ventral, removing almost all the particles that are touched by the brush. As the researchers calculate, about twelve swipes are needed to clean the entire surface of an eye. In reality, the bees rub each eye ten to twenty times. After each swipe, they spend a few seconds to clean the pollen brush with the other legs or the mouth.

Pollination

The hair on the eyes (and on the rest of the body) and the bristle brushes on the forelegs facilitate quick removal of sticky pollen after a flower visit, the conclusion is.

Still, some of the accumulated pollen must be left ungroomed, so that the bee can deliver it on the pistil of the next flower she visits. Otherwise, bees would not pollinate any flowers.

Willy van Strien

Photo: Honey bee collecting pollen. Jon Sullivan (Wikimedia Commons, Public Domain)

On this video, a pollen-covered honey bee rubs her eyes

Source:
Amador, G.J., M. Matherne, D. Waller, M. Mathews, S.N. Gorb & D.L. Hu, 2017. Honey bee hairs and pollenkitt are essential for pollen capture and removal. Bioinspiration & Biomimetics 12:  026015. Doi: 10.1088/1748-3190/aa5c6e

Cockeyed

Strawberry squid looks upwards with a bulging eye

Light is scarce in the mesopelagic region of the deep sea, which asks for special adaptations of the eyes of the animals that live there. Squids of the family Histioteuthidae addressed this challenge by developing two different eyes, Katie Thomas and colleagues report.

If symmetry is a characteristic of beauty, then adult deep sea squids of the family Histioteuthidae are really ugly, because in addition to a normal right eye, they have a protruding left eye which is twice as large and usually yellow coloured. They are cockeyed. And, while not very nice, this is functional, as Katie Thomas and colleagues report.

As early as 1975 Richard Young proposed an idea of why these squids, which hunt prey like fish, shrimp and smaller squid, possess dimorphic eyes.

The squids live at a depth of several hundred meters in the oceans where it is dark apart from dim, downwelling sunlight. How do the animals manage to find their food in this nearly complete darkness? When prey animals are swimming above the squids, they may perceive their contrasting silhouette against the almost dark background, provided that their eyes are very sensitive to light. Below, they can only detect prey that produces bright flashes of light, as many deep sea animal species do for various reasons. To be able to localise such prey, the squids need eyes that produce images with high spatial resolution.

Video recordings

The enlarged left eye of cockeyed squids, Young stated, is light sensitive and more apt to detect silhouettes upwards, whereas the small right eye produces images of higher resolution which enable the squids to localise bioluminescent prey below. But as the animals live at great depths, he was not able to access and observe them to determine whether they actually turn their bulging left eye upwards.

Nowadays, this is possible. For 25 years now, the Monterey Bay Aquarium Research Institute (California) has been sending remotely operated underwater vehicles into depth to make video recordings. Thomas used the video footage to observe the strawberry squid Histioteuthis heteropsis and Stigmatoteuthis dofleini and to find out how these squids behave.

She ascertained that adult cockeyed squids almost always oriented the head downwards in an oblique body position, with the ten arms stretched straight ahead. And, as expected, the animals twist their heads so that the large left eye is directed upwards and the small right eye slighty downwards. So, what Young had supposed proved to be right: the animals have two different eyes that are adapted to two different sources of light, dim downwelling sunlight from above and light flashes in the dark below.

Yellow

Then, why has the left eye a yellow colour in most of these squids?

Many prey prevent detection by predators that approach from below by producing a ventral glow that matches the weak downwelling sunlight, so their silhouette is camouflaged against the background (counter illumination). A predator’s yellow eye filters out ultraviolet light, and this probably results in different colours of the ventrally emitted light of prey and the background light, breaking the camouflage and rendering the prey visible.

Willy van Strien

Photo: Young strawberry squid Histioteuthis heteropsis (not in its normal swimming posture) © Katie Thomas

View the strawberry squid Histioteuthis heteropsis on video

Sources:
Thomas, K.N., B.H. Robison & S. Johnsen, 2017. Two eyes for two purposes: in situ evidence for asymmetric vision in the cockeyed squids Histioteuthis heteropsis and Stigmatoteuthis dofleini. Phil. Trans. R. Soc. B 372: 20160069. Doi: 10.1098/rstb.2016.0069
Young, R.E., 1975. Function of the dimorphic eyes in the midwater squid Histioteuthis dofleini. Pacific Science 29: 211-218.