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Page last updated at 13:13 GMT, Thursday, 28 October 2010 14:13 UK
The Twilight Zone: where animals battle for dominion

By Ella Davies
Earth News reporter

Owl
As night falls, battle commences

As nature draws the velvet curtain of night across the animal kingdom, a battle for survival begins.

In the murky half light, bats and owls go head to head with the scuttling, slithering, squeaking creatures of the undergrowth.

Each uses a different strategy to come out on top, relying on either sight, smell or sound to seek dominion of the Twilight Zone, the period of time between daylight and absolute night at both dawn and dusk.

Many species use these murky hours as a frantic, fleeting window of time for feeding, mating and communicating.

Yet despite his bustle of activity, scientists do not yet fully understand how creatures behave in the twilight zone, or even why they choose to emerge within it.

The eyes have it

Animals are known as "crepuscular" if they are active at this peculiar time of day.

The most quoted theory for crepuscular activity is that it offers an optimal balance: there is just enough light to see, but it is dark enough to lower of the odds of being caught and eaten.

Many predators active in the day are let down by their eyesight as the light fades.

For example, even the incredible eyes of the kestrel diminish with the departing sunlight.

An eagle owl's eye (c) woodwalker
Owls trade high resolution for high sensitivity with their night vision

The reason is that diurnal birds of prey rely on their sophisticated vision during the day to identify small prey from long distances.

Analyses of the eye structure of these birds show their retinas are densely packed with cones: light processing cells that allow high resolution, detailed sight in bright light.

But crucially, birds with a greater number of cones have fewer rods: the cells needed to process low light intensities or "see in the dark".

Lynn M Stone / Naturepl.com
Barn owls' flat faces channel sound to their ears
The eyesight of American kestrels diminishes rapidly once the sun sets

Avian vision expert Professor Graham Martin from the University of Birmingham explains that diurnal birds of prey sacrifice twilight sight for their exceptional daytime vision.

"There is a trade-off between high resolution and high sensitivity," Prof Martin explains.

"From this we would predict that as light levels [fall] during twilight the ability of birds to detect details will decrease rapidly."

That gives small mammals, lizards and amphibians a short window of "safety" from most birds.

But not all.

Owls are well known for their large eyes. Less known is that their eyes' retinas contain abundant rods but few cones.

That means their vision becomes blurry at higher light intensities, but it makes them experts at hunting out prey in extremely low light.

Colour is key

As well as detailed sight in bright light, cone cells or "photo receptors" allow for colour vision.

So as daylight fades, so does the colour perception of daytime predators. Equally, with their higher proportion of rods, many nocturnal specialists are rendered colour blind, offering crepuscular species another chance to capitalise.

For some creatures, twilight is a time for colourful mating and feeding frenzies.

A Jamaican turquoise anole displaying at dusk (c) Terry J. Ord/Harvard University and University of California, Davis
Jamaican turquoise anole lizards perform colourful displays at dusk

Last year, researchers found that Jamaican turquoise anole lizards (Anolis grahami) performed unique visual displays during dusk.

Their complex routine of "push ups" and brightly coloured throat flap extensions suggested that the lizards must have excellent sight and colour vision during this murky time if the displays were to attract any attention from fellow lizards.

Reptiles aren't the only twilight-active animals found to recognise colours at low light levels.

Horned scarab beetles (Coprophanaeus lancifer) in the Amazon basin are only active during dusk.

By analysing the beetles' appearance "through beetle eyes", researchers from France found that their deep violet-blue bodies were far more visible to potential mates during dusk than daytime.

Also, fellow invertebrates, elephant hawkmoths (Deilephila elpenor), are able to discern colours at all light intensities, according to research published in the Journal of Experimental Biology.

Scientists found that the moths could recognise the colour of their favourite flowers regardless of the light conditions. This effectively means moths can pick their mealtimes to avoid diurnal birds and nocturnal bats with a taste for insects.

Close up of the open mouth of a Noctule bat (Nyctalus noctula)
Noctule bats feast during twilight

Smell 'o' vision

Further tactics employed by twilight specialists focus on senses that do not rely on light levels at all.

Moths are known to use olfactory or "smell" clues to find their preferred food sources.

A study into flying insects found those with a taste for decaying food also let their noses lead the way in dim light. The researchers attributed this to dusk temperatures and air conditions that make smells easier to trace as the air is still and moist.

A brown long-eared bat close up
Long-eared bats can "smell out" their prey

With their diminished sense of smell, many avian predators again lose out in the twilight war of the senses, but mammals such as bats are at no such disadvantage.

Bats are known to identify their young in large colonies by scent alone and the lesser short-tailed bat (Mystacina tuberculata) and long-eared bat (Plecotus auritus) are two species known to use their sense of smell to hunt.

Bats' mammalian eyes are better suited to twilight too, as their retinas are composed of both rods and cones, according to research by scientists in Germany.

This balance suggests they can see in colour, even UV, and at a variety of light intensities including the changing light of dusk.

The only thing keeping bats in their roost until dark is the risk of predation.

Although perfect for night hunting, their dark camouflage casts a conspicuous silhouette in lighter skies.

The bats which are often seen flying in twilight are usually fast flying species such as the noctule - these are best able to avoid predatory birds
Professor Gareth Jones

"Daylight flying is largely avoided, and the most favoured hypothesis is that bats don't fly then because they would be captured and eaten by diurnal birds of prey," says Professor Gareth Jones, who runs the Bat Ecology and Bioacoustics lab at the University of the Bristol, UK.

"Others argue that avoidance of competition with aerial insectivorous birds, and threats of overheating may stop bats flying by day," he adds.

Studies into bats' foraging behaviour suggest that twilight emergence is more likely amongst bats with stronger defences in the shape of more protective tree cover or physical strengths.

"The bats that emerge earliest in the evening and hence which are often seen flying in twilight are usually fast flying species such as the noctule - these are best able to avoid predatory birds," says Prof Jones.

Savour the sounds

Pipistrelle bat hunts by twilight
A pipistrelle bat hunts by twilight

Bats are well-known for their ability to echolocate: pinpointing prey by bouncing sound signals off them and listening for the echo.

This unique skill effectively means they can hunt regardless of light levels.

Owls too employ excellent hearing to catch their prey. The barn owl in particular has a large flat face that channels sound to its asymmetrically positioned ears.

Recent research has found that the birds can pick up not just high but also low frequencies as they search for a meal.

However, it is not only the hunter that is listening carefully in post-sunset struggles, as researchers studying moths have found.

Certain species are now known to hear and understand bat calls so that they can take defensive measures. A study of Choerocampine hawkmoths found that they can hear with their mouthparts and respond to bat calls with evasive manoeuvres.

SOURCES

Large yellow underwings (Noctua pronuba) meanwhile can tell whether they have been "spotted" by bats and American researchers last year found that tiger moths (Eptesicus fuscus) use their own ultrasound clicks to jam predators' echolocation signals.

Scientists point to this evidence as proof of a "co-evolutionary arms race" between bats and moths with each species developing counter-measures to maintain their survival.

The thing about arms races, however, is that they are rarely won.

So it seems likely that the battle for dominion of the twilight zone will continue. Just as night follows day, and day follows night.



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