WALLACE CRAIG cupped the lifeless feathery bundle in his hands and sighed. Glancing at his watch he noted the time: 1.00 pm. The date was 1 September 1914, and Martha the passenger pigeon had just expired. With her went an entire species.
It was the most unlikely extinction. In the early 18th century flocks of migrating passenger pigeons had darkened the skies above eastern North America, taking three days to pass by. Hunters simply pointed a gun upwards, fired, and then got out the way as the pigeons tumbled to Earth. When the birds stopped to roost, trees broke under their combined weight. With an estimated population of somewhere between 3 and 5 billion, the passenger pigeon was the most abundant bird that ever lived. Yet by the late 1890s the species was almost extinct. A few birds found their way to zoos, but they languished in captivity and refused to breed.
It was a result that perplexed Craig and his contemporaries, and today’s conservationists often face a similar problem. It isn’t just that living in a zoo can ruin an animal’s sex life. When wild species experience a population crash they too can go into free fall, even though you would think that by removing the pressure of overcrowding, the survivors would flourish. Now conservationists are beginning to realise that under-crowding itself can help drive species to extinction. It’s a counterintuitive idea, but it’s not a new one: the consequences of low population density were first studied more than half a century ago by American biologist Warder Allee.
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For decades his ideas were largely forgotten, but now an awareness of these “Allee effects” looks set to transform conservation practices. “They alter our perception about the risks facing populations that have declined markedly, even if they are not numerically tiny,” says Georgina Mace from the Institute of Zoology in London.
“Allee effects centre on the observation that some species find it very difficult to breed successfully once the population falls below a certain number or density,” says Franck Courchamp of the University of Paris-Sud. “It used to be thought that such populations would simply rebound, but clearly this isn’t always the case,” adds Philip Stephens from the University of East Anglia. And as Allee pointed out, there are various reasons why.
For some species, such as blue whales, it is simply that with only a few, solitary individuals remaining, finding a mate can prove extremely difficult. It’s a little more complicated for New Zealand’s giant flightless parrot, the kakapo, where dwindling numbers mean insufficient males coming together at breeding time. Male kakapos gather at leks and the females are attracted by their multiple calls-a bit of a problem when the world population is down to 54 dispersed individuals. A similar fate could await other species that use leks, such as the European black grouse and South America’s cock-of-the-rock.
Perhaps the commonest Allee effect occurs in species that congregate to protect themselves against predators. Animals such as flamingos and penguins just won’t get into breeding mood unless they are surrounded by many other mating individuals. In such species, natural selection favours animals that synchronise their breeding because their offspring are more likely to survive the vulnerable early weeks if there are plenty of other young animals around for potential predators to pick off. “This may not be a problem for a species that is usually abundant,” says Bill Sutherland from the University of East Anglia, “but can become important once it becomes rare or once people are trying to breed it in captivity.” In some species, a behaviour that probably evolved as a way of swamping potential predators, seems to have developed into a near-unbreakable psychological dependence.
“But Allee effects can be more subtle and complex in group-living species,” says Courchamp, who was until recently, part of a team from Cambridge University studying the African hunting dog, Lycaon pictus. Once numerous and widespread, the hunting dog is now Africa’s most endangered large carnivore. “Declines of up to 30 per cent occurred even in protected areas where other previously persecuted species like spotted hyena were increasing,” says David Macdonald, director of the Wildlife Conservation Research Unit at Oxford University. The reason for this was a real puzzle.
The Cambridge team was led by Tim Clutton-Brock who had previously studied Kalahari meerkats. Meerkats are cooperative breeders, which rely on helpers to raise their pups, and Clutton-Brock had found that small groups were far more likely to die out than large ones. Could the peculiar social system of Lycaon make it similarly vulnerable? Digging around in the literature, Courchamp found a treasure trove of studies showing how reduced population density could adversely affect the rate of population growth of many species. “It was all being totally ignored,” he says. The team started to suspect that Allee effects might be to blame for the hunting dog’s failure to flourish.
African hunting dogs have a rather odd social life. When the young reach reproductive age they leave the pack with a group of up to six other individuals of the same sex. A new pack is formed when they meet a group of the opposite sex. One pair becomes dominant and they alone breed, while the rest hunt and look after the puppies. The researchers wondered whether there was a minimum pack size, below which survival was difficult. Using a mathematical model and the field observations of other researchers including Scott Creel from the University of Montana and Greg Rasmussen from Oxford University, they found there was-three or four adults plus the breeding pair. “Smaller packs find it hard because helpers are needed for cooperative hunting and to defend kills from lions and hyenas,” says Courchamp. The problem is that these same adults must also care for the pups. “And smaller packs will send off smaller cohorts to colonise new areas,” says Clutton-Brock, so the problem continues to the next generation.
“The Lycaon study was the first time an Allee effect has been fully demonstrated, and it could have major implications for the conservation of other cooperative breeders,” says Clutton-Brock. Animals that have no alternative but to rely on one another for breeding success are most at risk from this particular form of under-crowding. The effect will be strongest in species such as the naked mole-rat, white-winged chough and social insects, predicts Clutton-Brock. Less at risk are animals that help each other to raise young but do not rely so heavily on such cooperation, including wolves, lions and marmosets. Even so, this effect may explain the slow recovery of the Ethiopian wolf following a rabies epidemic that wiped out much of the population between 1988 and 1992.
Allee effects are not confined to purely social species or, indeed, animals. Those that simply aggregate may also be vulnerable. For example, hemlock trees outcompete other species by producing acids which they pump into the surrounding soil to raise its water content and drown out competitors. The more hemlocks in any patch of forest, the more dramatic the effect. So despite the fact that the densely packed trees are competing for sunlight and nutrients, hemlocks grow faster in a crowd than when they are thinly spread.
Indeed, researchers including Clutton-Brock have come to the conclusion that Allee effects are widespread. “Many species may show Allee effects when populations reach extremely low densities,” he says. “However, they probably occur at a wide range of densities in cooperative species where breeding success and survival increase with group size.” And the implications are far from academic.
Take the strongly schooling fish that make up many of the world’s most important commercial fisheries (91av, 27 January, p 16). North Atlantic herring stocks, for example, have failed to recover despite a 25-year fishing ban, and the annual haul of Peruvian anchovies has plummeted from 11 million tonnes in the late 1960s to less than 100,000 tonnes today. Many fisheries biologists believe that once numbers of these sorts of fish fall below a certain point, predators become a significant force. Where in the past they would have merely nibbled at the edges of vast shoals, they may now be doing enough damage to check the population’s expansion.
The effects of under-crowding can also threaten attempts to reintroduce endangered species into the wild. Australian biologists trying to establish a wild population of rare marsupials called bush-tailed phascogales,Phascogale tapoatafa, for example, first tried releasing the males and females together. But this strategy failed because the animals dispersed and then the males couldn’t find the females. Once the team realised what was happening they were able to minimise this effect by simply releasing the females first and allowing them to establish and mark their territories before introducing the males, who could then track them down.
Allee effects could also have major implications for the success of biological controls. Some 65 per cent of attempts to control insects and 41 per cent of agents freed to destroy weeds never became effectively established. “Most such releases flop,” says Rob Freckleton from Oxford University. He believes there’s good evidence that Allee effects underlie many of these failures, and points to the gorse thrip as an example. The effectiveness of this tiny insect against invading gorse plants increases in proportion to the number of thrips initially released. “Numbers used in releases are often simply too small for populations to breed,” says Freckleton. “This not only wastes a lot of money and effort, it also turns people away from control agents that might have been successful if only the right release procedure had been used.”
If Allee effects are so far-reaching, why did the idea languish for 50 years? “I honestly don’t know,” says Courchamp, pointing out that there have always been scattered papers on the subject. Stephens points out that Allee was way ahead of his time. “The major population dynamic debates in Allee’s day were about top-end regulation of populations-what prevented them from growing indefinitely, or cycling irregularly,” says Stephens. “There was little concern about extinction back then, or the problems of small populations. Interest in low-end population dynamics was very limited. So the Allee effect simply never caught on at the time.”
Today concern about the biodiversity crisis has changed all that, putting Allee effects at the cutting edge of conservation concepts. Their revival also reflects the trend for thinking about conservation in behavioural biology terms. “This work on Allee effects is another illustration of the importance of individual behaviour- especially social behaviour-in population processes,” Macdonald says. “This is vital for conservation planning. Too often people treat populations as if individuals were merely numbers, whereas the reality is that they are behaviourally complex, and management must take account of that.”
But bringing this approach to mainstream conservation isn’t going to be plain sailing. So far, there have been very few field studies done with Allee effects in mind, and some conservation biologists feel the approach is irrelevant to their work. “There is, for example, a lingering perception that the Allee effect is a phenomenon only of very small populations and thus of limited importance to conservationists,” says Stephens. He believes that Allee effects can determine the growth and dynamics of any population, small or large.
To most people who have embraced the study of Allee effects, it is the potential impact on practical conservation that fuels their research. Their only regret is that the importance of Allee’s work was not recognised from the start. “The threats of over-exploitation, habitat fragmentation and so on might have been focused on sooner,” says Stephens. “Conservation science might have developed earlier, with a fully developed, unifying theory to hand.”
Even if that had happened it would have been too late for Martha and the last few passenger pigeons.