Monarch's moves

BEHAVIOUR

 A pair of equivalent navigation apparatus in the monarch butterfly ensures that the loss of one set during its long migratory flight does not make it go off course. S Ananthanarayanan tracks the butterfly’s movement.

The monarch butterfly, danaus plexippus, performs each year the impressive feat of flight from Canada to Mexico, for the winter, and return in the spring. In fact, the monarch can carry out a trans-Atlantic crossing, and in Australia, where it is also found, it is known as the ‘wanderer’. Steven Reppert and colleagues at the University of Massachusetts at Worcester report their work on the navigation apparatus of this remarkable insect.
Who’s the monarch?

The monarch is orange and black, and has a wingspan of 3.5 to 4 inches. It is the only butterfly that regularly migrates seasonally, both south and north, like birds. But unlike birds, the monarch has a normal life span of just two months and cannot complete the round trip within a single generation. 

Butterflies born in late summer enter a non-reproducing phase and enjoy a longer life span of seven months and they first make the flight down to the south for ‘overwintering’. When the winter is over, in February or March, a new generation is born and these butterflies start to move northward. It is this second, or even the third or fourth generations, that actually make it to the northern locations, later in the spring. How the tendency to move consistently south or north is monitored and passed on has been a matter of wonder and research.

Initial work has shown that the migratory movement is controlled with the help of the butterflies’ antennae. The antennae contain a circadian – or 24-hour-cycle – mechanism, which helps the monarch fly true, due south or north, with the help of the sun. The clock action inside the antennae provides compensation for the changes in the sun’s position during the course of the day.

It has been noted that monarchs whose antennae have been removed or painted black, to cut out the illumination signal, cannot orient themselves with respect to the direction of light. Study of the action, in the antennae, of genes that react to light, shows that these genes do not express, through causing synthesis of proteins, in the regulated, 24- hour cycle when antennae are blacked out. 

It is clear that the clock mechanism lies in the antennae. However, a question that arises, as there are two antennae, is whether there is a relationship between the signals from the two antennae. It has been found that surgically removing either antenna does not affect the ability of the monarch to orient – both antennae are thus not necessary, one will do. And further, that each antenna is equally good – there is no asymmetry, unlike in the case of scent sensitivity of the honeybee or the bumblebee.

Bee & bumblebee

In the case of bees, the detection of odours, for food location and foraging, is through the pair of antennae. The antennae of bees have structures sensitive to touch, taste and smell.

Thus they can make out wind direction or force, vibrations, sweetness of nectar or, most sensitively, presence of odours, with the help of antennae. The bee, in fact, is highly trainable, and a number of experiments have been carried out, using odours and the proboscis extension reflex (PER), or the extension of a feeding organ when odours are associated with sweetened water.

But the interesting thing in the case of bees is the laterality - it has been seen that the learning response of bees is positively better with odours detected by the right antenna than the left antenna. In fact, even in the circling flight around a flower, before descent and feeding, it is seen that there is laterality, or a preferred direction of circling. The same tendency to prefer one side is seen in a number of other, small animals.

That there is no similar preference in the case of light sensing by the antennae of the monarch butterfly seems to be connected with the difference of the environmental feature being sensed – in the case of the honeybee, there are smells all around and different smells of preferred feeding at different times of the day.

The smells then need to be remembered – there is processing and storage of the smell information in the brain. Where long-term memories are involved, lateralisation of neural paths seems to be the way to go in many invertebrate species. In the case of the monarch butterfly, there is genetic programming for flight in a particular direction – there is no learning by repeated response and reward – and hence no reason for the signal of one antenna being separate from that of the other.

Blacking one antenna

But there has been a peculiar observation: when one antenna was not removed, but only blackened, the monarch butterfly was disoriented, just like when both antennae were blackened or removed. Which antenna was blackened, the right one or the left one, did not make a difference – there was no laterality – but it did seem that the signals from both antennae were processed together, and blackening one antenna caused disruption. And then, surgical removal of that blackened antenna brings directional orientation right back!

The finding seems to indicate that both antennae have separate, but similar functions of calibrating the sun’s directional guide with reference to the time of day, but how the data from the two antennae is integrated is not clear. The desynchronising of information from the blackened antenna seems to disrupt the processing of the data from the other antenna, leading to disorientation. 

Steven Reppert and colleagues followed through with analyses of the gene-protein generating activity in the antennae and the brain, with reference to the timing of the light signals at the antennae. It was found that the molecular-level activity was closely related to the light signal data, showing peaks and lows.

But when the antenna was blackened the activity was ‘flat’, with no variation with the timing. The blackening of one or other antenna also had no significant effect on the molecular-level activity of the other.

Comparison with the circadian information from the eyes, as in the case of the cockroach or cricket or sea slugs, does not clarify the nature of the integration of the olfactory signals from the antennae by the brain. It does appear, however, that the provision of a pair of equivalent navigation apparatus, in the case of the monarch butterfly, is to make sure that the loss of one set during the long flight does not make the migrant go off course.