Your place or mine?

When a hermit crab needs a new home, it often tries to snatch one off a neighbour's back. By studying what makes a winner in these clashes, we can learn much wider lessons about dominant behaviour, says Simon Hadlington

Ah, the joys of moving home. Finding an affordable house in a decent location, learning how to translate estate agent-speak, arranging surveys and mortgages, praying that the neighbours haven't got a 15-year-old with a drum kit.

For the rest of the animal kingdom, things are usually somewhat more straightforward: locate a suitable hole in a tree, or space under a rock, and Bob's your uncle. But, for at least one animal, things are not quite so simple.

In the watery world of the hermit crab, there is something of a housing shortage. Hermit crabs have soft, vulnerable abdomens, so, to protect themselves, they occupy the empty shells of sea snails, such as winkles or whelks. When a crab outgrows its home, or if the shell is getting a bit tatty, it looks for another. If no suitable empty shells are available, it will forcibly evict another crab and steal its house. This process of eviction entails a bizarre ritual in which the attacking crab grabs hold of the hapless householder and rapidly clacks their shells together in a series of short bursts.

Researchers at Queen's University, Belfast, led by Dr Mark Briffa and Professor Bob Elwood, have been scrutinising this behaviour and believe that it offers a unique perspective into how animals signal aggression to one another, and could provide a model of aggressive signalling between animals generally.

When a crab gets too big for its shell, or when the shell's condition starts to deteriorate, it must find a new one. The crab has three main options for upgrading. It can find a suitable shell that is empty; it can find a shell that is still inhabited by its native snail, kill the snail and remove it; or it can find a shell that is already occupied by a hermit crab and evict it.

"Empty shells are in relatively short supply, and it is rare that a crab will kill and remove a snail," says Dr Briffa. "So eviction of a resident crab is common."

What happens is this. The house-hunting crab spots a potential new home and approaches it. Each crab displays its two "chelipeds", or claws. This allows each crab to receive information about the other. If the aggressor judges its potential victim to be too big, it will retreat. But if it thinks it has got a chance of eviction, it lunges at the other shell, clasping it with its four walking legs. At this point, the defending crab withdraws into its shell. The attacker then begins a detailed survey of the shell, turning it over, running its legs over the surface, inserting a claw into the entrance.

If it decides to go ahead and attempt the eviction, it turns the shell so that the two entrances are facing and extends a claw to grab the claw of the defending crab. Then a curious series of events occurs. By using its legs and abdominal muscles, the aggressor knocks the two shells together in a series of short bursts. Each burst – or bout – might be for six or 10 raps.

There are two possible outcomes of a fight – which might last a couple of bouts or many scores of bouts. The aggressor can give up and retreat, or the defender can release its grip on the inside of the shell and allow itself to be hauled out. The attacker then moves into the new home, and the evicted crab normally takes up residence in the attacker's now empty shell.

For scientists, the nice thing about this behaviour is that it is relatively easy to measure: the frequency of the raps, their intensity, the length of each bout and the pauses between them. These measurements can then be analysed with respect to the outcome of the fight – whether the eviction is successful or not.

But what exactly is the purpose of the rapping? "We believe that knocking the shells together is a form of communication between the animals, with the attacker giving the defender information about its fighting ability," says Dr Briffa. Shell rapping is therefore equivalent to muscle flexing, an elaborate form of posturing. It is saying to the defender "look at how powerful I am – resistance is futile".

The Queen's University researchers, who are funded by the Biotechnology and Biological Sciences Research Council, are now beginning to understand how this information is conveyed. "We know that attackers that put a higher effort into the first few bouts are much more likely to succeed," says Dr Briffa. "We have also observed consistently that the aggressor increases its effort just before the eviction – it seems that a sudden rise in effort is a signal that eviction is about to occur. It is possible that the defender somehow lets the attacker know that it is about to surrender."

Precisely why the defender throws in the towel is not understood. It might be that the force of the knocks causes the defender to grip the shell more tightly, draining its energy resources. But if the defender is expending energy, the attacker certainly is.

"Repeated signalling must be energetically costly," says Dr Briffa. "In all such contests between animals, it is reasonable to assume that the participants are constantly carrying out a cost-benefit analysis – appraising how much energy it is worth expending on achieving their goal. In this case, either succeeding in evicting the defender, or successfully resisting eviction."

To look into this, the scientists have been analysing key metabolic indicators in the blood and tissues of both attacking and defending hermit crabs. First, they looked at levels of lactic acid, a typical by-product of muscle activity; as lactic acid accumulates, the muscles tire. So the lower the lactic acid in the blood after a given level of exertion, the greater the stamina of the animal. "We have found that unsuccessful attackers have much more lactic acid in their blood than successful ones," says Dr Briffa. "It could be that the attacker bases its decision to withdraw on a threshold level of lactic acid." In the defenders, there appeared to be no difference in lactic-acid levels in successful or unsuccessful defences of the home.

The researchers also examined the levels of glucose in the animals' blood. Glucose is needed for energy and is a measure of how prepared an animal is to expend effort. There was no measurable difference in blood glucose levels in successful or unsuccessful attackers. However, in defenders there was an unexpected finding.

"Defenders that were evicted had lower levels of glucose than those that successfully resisted," says Dr Briffa. "This is surprising, because you would think that a defender that had spent a lot of energy in successfully resisting eviction would have depleted glucose, whereas those that surrendered early on wouldn't have wasted a lot of energy so would have higher glucose."

The explanation might be that successful defenders have mobilised their reserves of the storage carbohydrate glycogen, converting it into glucose in preparation for the struggle. Unsuccessful defenders have not bothered to do this, hanging on to their energy reserves but giving up their home.

If this is what happens, it looks as though the defender makes a decision quite early on about how much energy it will apportion to the defence of its home. If a defender fancies its chances, it will elevate its glucose and prepare for a long struggle. If it thinks it only has a slim chance of resisting eviction, it will hang on until its existing glucose levels become depleted, and will then throw in the towel.

"We think that by being able to correlate the signalling behaviour with the animal's physiology, we can begin to answer some general questions about this type of communication in the animal kingdom," says Dr Briffa.

In particular, the crabs demonstrate that even though the signalling behaviour falls short of full-blown violent aggression, it does still have an energetic cost to the aggressor. If the aggressor was not fit and strong, it would not be able to knock shells together with such vigour. In other words, it could not call the defender's bluff. "Some biology theorists maintain that for signalling to be effective, it must handicap the sender in some way for the concept to work – the signalling must represent an honest picture of the sender," says Dr Briffa. "Our work with the hermit crabs would appear to bear that out."