Sensory Exploitation of a Prey's Motion Habituation Mechanisms
Sensory Exploitation by Male Frogs and Eavesdropping Bats
Aposematic Coloration and Mimicry Complexes
Many prey have evolved to be cryptic and the challenge for many predators is locating unmoving and concealed prey. Development of a search image greatly aids in locating cryptic prey during a birds active foraging flight. Other organisms that forage actively use olfactory cues to locate concealed prey.
However, the challenge for many predators is not so difficult. Many predators are sit-and-wait rather than actively foraging. Sit-and-wait predators remain motionless for long periods of time. When a prey item moves in their receptive field, the predator lunges with great speed (relative to the prey) and snaps it up. We will consider the visual system of a classic sit-and-wait predator, the toad.
The key to the toads motion-based prey detector is the receptive field, the fundamental unit of its perception machinery. Each of the thousands of receptive fields in the toad eye consists of the following components:
This is the smallest neural unit of stimulus filtering found in the visual system. Other stimulus filtering is found at the level of the specific photoreceptors in that individual neurons on pay attention to certain signals (e.g., rods vs cones, and if cones, then the kind of photopigment found in the cone). The stimulus filtering found in receptor sensitivity is hard-wired by evolution. However, receptive field has special cellular interactions built into it that result in certain information being ignored and other information being acted upon. The receptive field is also the smallest unit of the toads motion detector. The excitatory and inhibitory cells act in unison to either filter or detect objects from higher centers such as the optic tectum. The stimulus filtering in the receptive field is also capable of being modified by the animals internal state -- food satiated or hungry.
If a large object casts an image over the visual field, the light intensity changes on the photoreceptors. Both excitatory and inhibitory cells from many receptive fields are triggered. Because the ganglion receives impulses from both the excitatory and inhibitory cells (through their respective bipolar cells) the effect inhibitory cells cancels out the effect of excitatory cells. No impulse is sent from the ganglion cell to the optic tectum.
However, if a small image passes over the visual fiel, the small image tends to trigger fewer receptive fields per se. The small image will also tend to excite some of these fields because the image hits many of the central excitatory cells, but only a few peripheral inhibitory cells. The ganglion cell receives impulses from the excitory cells (through their bipolar cells), but with little inhibitory feedback, the action potential is relayed on to the optic tectum for further integration.
The optic tectum receives inputs from all ganglion cells. Several clutsters of ganglion cells form a higher-order receptive field at the level of the optic tectum that integrates information form the clusters of receptive fields.
Consider objects of different shapes that might strike receptive fields. Receptive fields come in a variety of "flavors". Some are used for detecting long thin objects, others large objects, etc. One of the toads favorite foods consists of worms -- long thin objects. There are receptive fields that are tuned to fire when long thin objects pass across them. When several "long-thin" receptive field detectors have the image of a bar pass over the receptors, their ganglion cells will relay the information to the optic tectum. The grasp reflex then takes hold, and the toad orients with both eyes. Once both eyes are locked on, other motor neurons cause the toad to lean forward, open its mouth and eat the worm.
Recall that the motion detectors of Anolis lizards rapidly become habituated to the sinusoidal frequencies of branches swaying in the wind. In contrast, Anolis lizards are extremely sensitive to the square-wave like patterns that are found in signature displays and challenge displays. In fact receptive female lizards move towards the square-wave displays of males. Thus, males use the displays to attract females to their territory and also repel other males. The dual function signal also has a sinister third side to it.
Consider the vine snake, Oxybellis aeneus, which is a voracious predator on Anolis lizards. Fleishman (1989) has done careful laboratory studies where the wind conditions and swaying of plant vegetation were manipulated and their patterns recorded on video and analyzed for their spectral properties.
First, vine snakes prefer to move when the wind is blowing. Moreover, when the snake moves, it not only slithers in a forward direction, but it also sways its head back and forth. In addition, the frequency of the snakes swaying body seems to correspond to the natural resonance frequencies of swaying branches and vines. The vine snake appears to exploit a weakness of the Anolis motion detector system. Anolis must habituate to swaying branches in order to see conspecific displays. Vine snakes have evolved a motion that slithers into the "habituation zone" of motion detectors that Anolis uses.
Even though the signaller may receive some benefit, many animals can receive the signal. A receiver could in fact be a predatory species. Sexual ornaments are intended for the female. However, the ornaments also make the male more obvious to a predator and thus they entail costs. Advertising calls make males of many species vulnerable to a predator's prey-detection mechanisms. There may be costs to signals that arise from predators that can also intercept the signals. As we will discover below, the bat has exquisite acoustical transmission and receptive organs. However, there are bats that do not have to echolocate to find their prey in the dark -- they need only listen to calling males.
Species of tungara frogs produce two kinds of sounds when they are trying to attract mates. The first is a whine which may or may not be followed by a chuck. Mike Ryan and his colleagues have shown that females of many species in this group strongly prefer males that produce a chuck.
Ryan and his colleagues determined that the ancestral species only produces a whine. Males of the ancestral species never produce a chuck. In contrast males of all of the derived species can produce chucks.
They used pairs of speakers in a female choice experiment to determine the preference of females from:
Females of the ancestral species strongly prefer males that produce the chuck even though their own males never produce such sounds. The lineage of tungara frogs had a preexisting sensory bias for chucks early in its evolutionary history, before the "invention of the male's chuck", and during the process of sexual selection and evolution, males of the new species began producing chucks to exploit the preexisting preferences of females.
A cladogram provides a phylognetic reconstruction of ancestor and descendant relationships. The pattern of chuck preference arising before chuck production on the clade for Tungarar frogs provides the evidence for sensory bias. Because preference for chucks in females predates the production of chucks by males, Ryan and his colleagues suggested that the sensory bias was important in shaping the subsequent sexual selection in male calling.
The fringe-lipped bat does not have to call to find its prey by echolocation, rather it listens for male Tungara Frogs calls. The bat then swoops down and captures a male. Bats also strongly prefer speakers that are projecting a chuck at the end of the whine in a 2 to 1 ratio compared to speakers with only the whine and no chucks. Thus, male Frogs are caught in the middle of their own sensory exploitation of females who prefer chucks, and the interception of such signals by their bat prey, who prefer males with chucks. When calling alone, male frogs only use the whine as there are no other males to compete with. The whine may be sufficient to attract a female under these conditions. When calling in a group, they are forced to use the chuck, and risk the chance of being taken by a fringe-lipped bat.
Nothing transcends the special effects capabilities of a Star Wars Tie Fighter like watching bats snarffle insects on a moon-dappled night. The ability of bats to locate prey in flight even in the face of the evasive Maneuvers of prey is simply amazing and their repetoire is as follows:
Bats with a nose leaf emit sound through their nose, but most bats emit sound through their mouths. Bats typically emit short chirps 0.5-10 milliseconds (thousandths of a second long) with a long period of time between chirps. The signals are frequency modulated in the 15-150 kHz range. Some species of bats drop the interval between chirps to smaller and smaller times as they target their prey. These bats use the information from the broad band of frequencies and the echo delay (time between emission and return), and form images of the prey by using the echo information from a broad range of frequencies.
To process these echo returns, bats rely on some elaborate neural circuits that are tuned to the information coming back from their ears. Bats possess special echo detector neurons that are sensitive to a sound (the bat making a chirp) followed by a second sound with a specified delay (its echo). The neurons are sensitized by the first sound and if the sensitized neurons are stimulated again within the specified time, the bat registers this information. Certain echo neurons are range tuned to long echo delays (e.g., far away), others are range tuned to shorter and shorter delays. This sequence of echo-detecting, range-tuned neurons are arranged in a linear sequence back into the brain, such that they form a brain map of the bats attack pattern at the prey. From such neural maps, the bat can compute other information on speed of prey.
To detect the shape of the object, other neurons decode the distortion of the echo. A small dimple in the returning echo describes the size of the head/thorax relative to wing placement of the insect. A bat with frequency modulated chirps has special frequency-tuned neurons that fire when they detect a specific frequency of its own voice. This is information is stored in the neurons for a given amount of time after the chirp and such neurons are referred to as having a long latency -- the neurons take a while before they decay from the "activated" or "excited" state. The bat is actually storing a neural template of its own frequency-modulated chirp with a each group of frequency-tuned neurons holding the information for their own unique frequency (each of which was emitted a slightly different time because the bat modulates the frequency of the chirp over time).
When the echo returns, short-latency neurons fire that are also frequency-tuned and a set of higher order integrating neurons compares the two populations of short and long latency neurons. Because the returning echo is distorted by the shape of the object, some of the original frequencies are so attentuated that they do not fire the short-latency neurons. The difference between the long and short latency neurons firing patterns leads to a crude "image" of object's shape being formed. Eventually the long and short-latency neurons return to ground state and the bat is ready to resolve more shape information on the next chirp and echo return set.
Rather than use a frequency modulated chirp, other bats use a compound signal which has a constant frequency (~80 kHz) component (100 milliseconds) that is longer and tacked onto the end of the frequency modulated component. Bats that use such compound signals can measure the wing beat frequencies of their prey. The motion of the wings of prey causes glints in the echo return that is used by the bats to compute wing frequency. Neurons sensitive to resolving such "glints" decode the wing frequency information by even more complex spectral analysis. Many bats strongly prefer the fluttering target that is presented by a flying insect.
Picture the echo hitting the flying target. At the instant that the first wave of sound hits the target, some of the surfaces of the target are moving away and others are moving towards the target (e.g., body vs wing beat). Such differences in body and wing motion cause the constant frequency signal to becoming "doppler shifted" in which the frequency is increased or decreased. A doppler shift in any waveform (e.g., light or sound) occurs when an object has apparent motion relative to the observer. In this case the insects wings and body are moving relative to the bat. As the pulse of the constant frequency chirp strikes the insect, parts of it are doppler shifted down in frequency, others are doppler shifted up in frequency. This distorts the pure constant frequency signal coming from the bat and creates higher and lower frequencies when they pulses are reflected back as an echo.
As the bat comes in for the attack, it drops the constant frequency signal by a few kHz, and it shortens the interval between signals. By dropping the frequency, it avoids any interference that might be coming from other signals as it gets closer and closer to the target. Interference can arise at the level of sound (e.g., overlap between its own voice and returning echos), as well as the neural circuitry, because of the very short time frames during the targeting phase of attack and capture. Neural circuits need time to return to ground state before they can be used.
The prey are by no means helpless in their encounters with bats. Moths, grasshoppers, mantids have all evolved neural circuitry that them aids in eluding the bats. The bat must send out a signal to echolocate, and the prey can receive this signal and begin evasive Maneuvers.
Moths receive the ultrasonic bat vocalizations with two ears on each side of the thorax. When pressure waves from the high energy bat vocalizations strike the ears and vibrate the membranes of the moth ears, two sensory receptors (A1 and A2) can fire but the firing depends on the energy of the sound.
The sensory neurons trigger an action potential in the sensory interneurons which conduct the electrical impulses to the next synapse. The next neuron in the chain after the first synapse is triggered by neurotransmitters which are released and cross the synaptic junction and trigger a new action potential. The impulse can travel to the brain in this manner, or to ganglia in the thorax. Neurons in the ganglia or brain can integrate the information and send an action potential on to motor neurons that cause muscles to fire. The differential senstivity of the A1 and A2 sensory neurons leads to a stimulus filtering of the bat sounds that gives the moth two options:
The A1 cell is sensitive to low energy sounds (e.g., distant bat calls), and the A2 is sensitive to high energy sounds (e.g., close bat calls), however, the frequency of the sounds for both neurons must be in the ultrasonic range of bat calls (>20 kHz).
When A1 is stimulated, the firing rate of the neuron is proportional to the intensity of sound, and the moth can detect whether the bat is approaching. A1 fires more and more rapidly as the sound gets louder and louder. By comparing the time delay between right and left ears, the moth can tell which direction the bat is coming from. The wings can also obscure the sound from above or reflect it from below, thus the moth can also assess the bats altitude. The moth can use all of this "long range information" to alter its flight path to avoid being detected (recall that the bats detection distance is < 5 m).
If all these evasive Maneuvers fail, and the bat is about to collide, the A2 neuron begins firing because of the high energy reaching the moth ear. The A2 cells send a message to the thoracic ganglia, and this seems to shut down wing beats or cause them to fire erratically. This leads to erratic flight which may be a last ditch attempt to elude the ranging and speed computing neurons of the bats brain.
The bats impulses are being integrated by the brain and thus they have long distances to travel, The moths neurons short-circuit the brain by looping from sensory neurons to ganglia to motor neurons. Thus, the moth can produce evasive Maneuvers a little faster than the bat might be able to respond.
A variety of mechanisms have evolved in the insects for evading bats. Crickets possess ultrasonic recpetors in the forelegs that have a low intensity threshold to sounds in the 40 kHz range -- bat sound. They also possess another low intensity threshold in the 5 kHz range -- cricket song. If the legs detect 40 kHz, this causes sensory interneurons to relay the information to thoracic ganglia, which sends an impulse out to the motor neurons of the opposite rear leg. The muscles in the leg raise the leg into the wing, which causes the wing to beat with less energy on that side and the cricket turns away from the bat. The reverse is true if it detects cricket song. It causes the rear leg on the same side to lift, and turn towards the song.
By virtue of their small size and availability for use in a laboratory, bat sonar has been very well studied. Dolphin sonar has also been studied for both reasons of pure science, as well as for the practical implications in commerce and warfare. The principles used in bat and dolphin sonar are very similar and the contrast between the two media, air versus water, is useful to highlight the constraints that the medium imposes on signal design and decoding.
As discussed above, the constant frequency signal of bats can be used to analyze the doppler shift of the prey. In constrast the frequency modulated signal of bats is Doppler Intolerant in that the signal is not significantly altered by the bat or the preys motion. Dolphins tend to produce frequency modulated signals and dolphins cannot decode the information that might be encoded in a doppler shift.
Whereas bats produce sound from the larynx and emit it from either the mouth or nose, dolphins produce sounds with their nasal sacs. Whereas bats receive sound in their ears, dolphins detect return echos through the lower jaw back into the stirrup and anvil of the inner ear. Despite these gross anatomical differences, bats and dolphins seem to resolve a similar range of sounds frequencies. In addition, bats have a special muscle response which locks down the ears and reduces the intensity of sound received at the level of the ear during signal transmission. This gain control prevents damage to the sensitive ears. It is unclear whether dolphins possess similar gain control.
Bats and dolphins differ in the target detection range owing to the properties of air versus water. Consider the ability of a bat or dolphin to resolve a ~one inch sphere. Bats can correctly target such a sphere 75% of the time at a distance of 5 m. Thereafter, their ability to target falls way off. Below this distance, targeting success rises slowly to 90%. Dolphins on the other hand can resolve the sphere at 75 m. The lower detection distances for bats arises because air absorbs a considerable amount of the acoustical energy in the ultrasonic frequencies that bats use. In contrast absorption of these frequencies in water is two orders of magnitude lower for dolphins. In addition, dolphins can simply produce much more energy in their signal compared to bats because of size.
Finally, water and air transmission differs in one important regard. The impedance in air is very high. Sound waves bounce back from relatively solid objects in the air and they are not distorted by travelling into the object because of the dramatic difference between the densities of the wave (air) and the object. In contrast, the density of a fluid filled body in water is very comparable to the density of waves travelling through the water, and this low impedance allows dolphins to potentially be able to resolve information regarding the structure of the object. Some of the energy of sonar is bouncing off the object, but other energy penetrates a little before being reflected back. Bats can resolve differences between plastic versus wood or metal objects when they are trained for target discrimination, but cannot resolve differences between metal types. Dolphins in constrast can resolve density differences between metal (e.g., iron versus brass).
Aposematic or warning signals are bright colors or loud distinctive signals associated with prey. These signals alert the predator that it should not attack or there will be negative consequences. Many aposematic species form Mullerian mimicry complexes in which unrelated species come to resemble one another in form, and they all possess some kind of toxin or deterrent. The predators do not have to learn to avoid a diversity of prey types, as the unrelated species all resemble one another.
Examples of aposematic signals include:
Each of the species listed above have a Batesian mimic associated with them. The Batesian mimics do not possess the noxious substances or dangerous venoms, but do benefit from the presence such deterrents in their toxic or deadly Doppelgangers.
Feeding trials of Monarchs to blue jays indicates that jays can rapidly learn to avoid vomit inducing forms. Such aversive stimuli are rapidly learned and require only a single trial in most cases. Moreover, the jays also then tend to avoid Mullerian mimics such as queen butterflies.
In other cases, the costs may be so high that an innate recognition is beneficial. For example, motmots (a south american king fisher) do not appear to require any conditioning. Laboratory reared motmots (no experience in the wild) avoid rods painted with yellow and red rings, more so than they avoid yellow and red stripes or green- and blue-ringed rods.
Butch Brodie III and his father Butch Brodie II tested whether milksnake batesian mimics are effective in nature against bird predators. Do batesian milksnake dummies receive fewer pecks in the wild?
Yes!
Ronald Fisher observed that many aposematic forms tend to also be quite gregarious and congregate in the same locale. Fisher speculated that kin selection may favor such aggregations. An individual may die during the learning required to teach a naive predator that the color also results in a bad experience. However, because the predator leaves the remaining kin alone, the inclusive fitness of the dead aposematling is positive because the cost of individual death is balanced by the surviving kin that are left alone. Gregariousness can easily result from kin groups (e.g., a localized clutch), and such kin groups greatly enhance the probability that aposematic coloration will spread even though brightly colored individuals attract attentions of naive predators.
It is difficult to address the origin of aposematic coloration and mullerian mimicry because predators may not be naive to the effects of prey (e.g., see innate responses of motmots). Reconstructing the intial conditions during the origin of the trait is nearly impossible. However, Alatalo and Mappes used an artificially constructed world of prey types to test a fundamental factor involved in the evolution of aposematic coloration -- the adaptive value of aggregation behavior. In creating their world they only used black and white markings to avoid any preexisting color biases in their naive predators, the Great Tit, Parus major.
In the first series of trials they created hollow fat-filled rye straws -- Tit treats. They put wings on the straws and used symbols on the wings (pluses or squares) to make the treats stand out (e.g., warning signals) or be cryptic (the background matched the wing markings).
Finally, they created two treatments comprised of the three treat creatures:
They let the naive Tits forage in amongst the treats and looked at the "death" rate of the three kinds of treat creatures.
The Tits took a lot longer to figure out that aposematic treats were unpalatable when aposematic treats were solitary compared to when they were aggregated. Thus, being aggregated is a definite advantage for aposematic forms compared to unpalatable cryptic and palatable cryptic forms. In fact being aposematic and solitary attracted the Tit's attention and the Tit's would continue to pick up and attempt to eat solitary aposematic forms that stand out by virtue of their warning signals relative to the cryptic palatable and unpalatable treats. However, the Tits learned that first aposematic treat in an aggregation were yucky in the first tasting and the avoided the remaining treats in the clump! Eventually, the predators did learn that solitary aposematlings were nasty but it took much longer.
The second test used the same birds, but altered the creatures -- almond sliver bodies rather than rye straws filled with fat. They used a different body, but similar wings on the new creatures. They wanted to see if the new creatures were protected because the experiences of their Tit predators had conditioned the predators to avoid aposematlings. Again they used solitary and clumped almond sliver creatures. This experiment tests whether clumping is still important in the evolution of a mullerian mimic.
They found that the new creatures were protected even though they were quite novel in appearance. In addition clumping had no further advantage.
Thus clumping and perhaps kin selection may be important in the early evolution of aposematic coloration. However, clumping is not essential for the refinement of mullerian mimicry complexes.
They also, conclude that kin selection per se is not essential, but aggregation or clumping is the essential trait that reduces the risk of survival.