By Douglas Fox
It’s a warm May morning in Amboseli National Park in Kenya. Kilimanjaro’s frosted peaks dominate the south, and to the north, rolling plains of grass and stooped acacia gradually sink into swamps.
Slowly wading through is a tagalong troupe of 17 elephants (Loxodonta Africana) — a large matriarch with aged tusks, six more adults, and ten young. The family is on its way to swamps where it will spend most of the day feeding.
On such mornings it’s not unusual to hear the social calls of other elephant families as they too approach the swamps, and in fact, this is what happens: a reverberating burrrrr signals the presence of another family a kilometer away. Normally, the elephants would fan out their ears to listen but otherwise ignore the call and continue walking while munching tussocks of grass; after all, scores of families inhabit this area, and their calls are familiar. But this time something is amiss. The call is from an unfamiliar, possibly threatening group — and hearing it temporarily shatters the slow-mo routine of an elephant morning.
Within seconds, the family has bunched defensively around its matriarch. The elephants will remain bunched for ten minutes, no longer munching but instead listening with their ears stiffly spread, sniffing the air nervously with their trunks.
On the surface, this ritual of caution seems like simple cause and effect. But if you watched more closely, it would become apparent that something more was going on. Somewhere within the ten odd seconds during which these elephants decided to bunch for protection is an important social interaction that is relevant to conservation. Yet it could easily go unnoticed by park rangers charged with overseeing the population — or by the conservation community as a whole.
We have long managed wild populations with hunting or culling programs that remove older, larger individuals — all the while assuming these individuals play little role in the overall success of groups. But when you examine the elephants’ behavior, this rationale falls flat on its face. Just ask Karen McComb, a psychologist studying animal behavior at the University of Sussex in the U.K. For seven years, she meticulously studied the Amboseli elephants, 800 animals in all, replaying recordings of familiar and unfamiliar calls to them and watching their reactions. Her findings raised plenty of eyebrows.
It turned out that it was the family’s matriarch, its oldest female, that was running the show — deciding which calls were familiar and whether to bunch. A family’s ability to distinguish calls depended more than anything on the age of its matriarch. But what was even more thought provoking was McComb’s finding that the family’s overall reproductive success also correlated with the age of its matriarch: families with older matriarchs simply did better. This increased success probably arose from multiple factors, including improved knowledge of social calls, food sources, and parenting skills.
“What our results really have to say,” concludes McComb, “is that removing these older individuals is potentially very damaging for the social welfare and reproductive success of groups.” This is information a park administrator can use. It means that protecting tusk-heavy matriarchs from ivory poachers should be a top priority. And this principal of key individuals also applies to other species with oral culture and influential matriarchs, such as primates and cetaceans.
What’s more, this convergence of behavior and conservation is no isolated case. For decades, behavioral ecology and conservation biology have advanced along parallel paths, the former focusing on individuals and the latter looking at whole populations. But from captive breeding to species reintroductions to population modeling, the time may finally be ripe for the walls between behavior and conservation to come tumbling down.
This article describes several areas where conservation and behavioral ecology are already merging to produce powerful results — with powerful implications for policy makers, planners, and conservation workers managing populations on the front line.
Letting Down Defenses
Widespread loss of large carnivores during the past century plunged temperate North America into a massive ecological experiment. The return of carnivores to some areas 50 years later is now bringing that experiment full circle.
Joel Berger, a behavioral ecologist with the Wildlife Conservation Society in New York City, has had a front-row view as wolves and grizzly bears return to the Grand Tetons in Wyoming to feed on its bloated populations of moose (Alces alces) and elk (Cervus Canadensis). What makes this spectacle especially interesting is that these prey lost most of their predator-avoiding behaviors during their half-century hiatus from predation.
Surprisingly, Berger’s observations suggest that the return of carnivores can prompt prey to resume some obvious anti-predator habits within less than a year. This is good news for predator reintroductions; it means that prey are unlikely to be wiped out. But it’s too early to tell whether this rapid rehabituation signals a complete return to ecological normalcy. Prey have a collection of more subtle protective responses, and it’s not yet known whether these are also resumed. The question of whether they are has significant implications for the broader ecosystem.
I caught up with Berger for a chat in the middle of his busy moose calving field season as he crouched 2,100 meters up on a mobile phone-accessible mountain ridge in the Tetons, spying on a pregnant moose.
Berger has probed the predator-preparedness of moose using playback experiments: playing wolf howls or the calls of scavengers such as ravens, which signal the presence of carnivores, or else planting predator urine at browsing sites. At first, Teton moose showed no response to wolf howls, wolf urine, or raven calls; in contrast, moose from the predator-rich Talkeetna Mountains and Denali National Park of Alaska significantly increased their vigilance in response to all three stimuli. But the Teton moose’s naivety to predators that they previously coexisted with for thousands of years is most starkly illustrated by nature itself. “We’ve had several 150-kilogram moose calves,” said Berger, “that wolves approached to within five meters and then just took them down without them responding they way they should have. They may have thought these wolves were just large coyotes.”
Yet despite the occasional National Geographic-style predator-prey massacre, the Teton moose are actually regaining their astuteness with surprising speed. It appears, based on playback experiments, that losing a single calf to predation is sufficient to evoke increased vigilance in mothers in response to wolf howls (but not to wolf urine) — where previously there was none. Vigilance in response to raven calls seems to be returning more slowly.
Despite the dire predictions by hunting groups, these results suggest that prey can weather the reintroduction of predators without population crashes. That’s relatively straightforward. But there’s more. Behavioral changes that occur when prey lose their fear of predators can be deceptively subtle, including changes in habitat use. Following the disappearance of predators, moose and elk in the Tetons fed more frequently in riverine zones where once they were easy targets for predators. The ecological effects are significant. Increased riverine browsing reduces the secondary foliage that provides habitat for some insects and birds. As a result, numbers of several neotropical migrant warblers have declined. And now that grizzlies and wolves are returning, pregnant moose are choosing to give birth closer to roads — areas that carnivores avoid.
These subtle anti-predator responses may matter greatly. In predator reintroductions, behavioral responses provide a more sensitive measure than do simple carnivore and prey population surveys for determining whether reintroduction has worked. “If people are claiming that systems are restored with predators back in,” says Berger, “then prey should be responding. And if they’re failing to, then I don’t think we can claim that we really have ecosystems restored to a level such as they once existed.”
Invisible Thresholds
Population models can be powerful tools for making policy decisions. But these tools can also dangerously oversimplify reality, as a result overestimating how much exploitation a population can sustain — or failing to predict the point where population decline crosses the invisible threshold into an accelerating downward spiral.
“The opportunity we’re really missing,” says William Sutherland, a population biologist at the University of East Anglia in the U.K., “is to create population models from an understanding of behavior. The reason that’s incredibly important is we want to predict what will happen under novel conditions” such as exploitation or habitat alteration.
The African wild dog (Lycaon pictus) provides an excellent illustration of the power of behavioral modeling. Although this carnivore once ranged widely over 34 countries, only six countries now harbor populations of more than 100 animals. If current trends continue, the dogs could vanish within three decades.
The exact reasons for the decline have long puzzled observers. After all, hyenas, which inhabit overlapping locales and suffer similar levels of persecution, fare far better. But now it appears that the African wild dog’s cooperative hunting and breeding behaviors are at the center of its spectacular crash and burn.
Group hunting allows the African wild dog to tackle larger prey and guard fresh carcasses from hyenas. At the same time, cooperative breeding allows them to leave a baby-sitter home to protect pups while hunting parties are out.
But according to Franck Courchamp, a theoretical ecologist at the University of Paris XI in France, cooperation is buckling under pressure. “Because humans have decreased the pack size,” he says, “[the dogs] have become very sensitive to predation, to competition, to all kinds of things that they are well enough adapted to fight against when they are in sufficient number.” In Zimbabwe, Courchamp’s collaborator, Gregory Rasmussen of the University of Oxford in the U.K., found that once packs became too small, they no longer had enough dogs to leave a baby-sitter behind while still mustering a viable hunting party. Cour-champ devised a behavior-based model that incorporated the trade-off between hunting and pup guarding, and this model predicted that once a pack fell below a threshold of five adult animals, the pack was then apt to melt away. This prediction was borne out by several years of field observations.
The African wild dog’s penchant for Titanic-scale implosion illustrates a widespread behavioral phenomenon. The so-called Allee effect predicts that members of a species will live in groups or in close proximity to one another and that species that do this in the extreme owe a significant amount of their overall fitness to their group living. Allee effects are rooted in behavior — cooperative hunting or breeding (African wild dogs), cooperative predator avoidance (elk, rabbits, and schooling fish), and cooperative burrow construction (hairy nosed wombats), for example.
Incorporating Allee effects is crucial for creating models that can assess a species’ vulnerability as its population changes. But these effects are completely missed by traditional population models — with potentially disastrous results.
Consider the alpine marmot (Marmota marmota). This bucktoothed fur ball inhabits above-timberline meadows throughout the Alps, spending the winter hibernating in huddled groups in burrows beneath the snow. Group warming is critical for winter survival of juveniles: they’re kept at the center of the huddled mass, and group size determines just how warm they’re kept and, therefore, their survival rate.
The alpine marmot is widely hunted. Philip Stephens, of the University of East Anglia, U.K., and his colleagues (Walter Arnold, of the University of Veterinary Medicine in Vienna, Austria, and Sutherland) compared the ability of several models to determine sustainable hunting levels. On the one hand, they tried two frequently used “bush meat trade” constant yield models, which use population size, sex ratio, annual probability of reproduction, and average litter size to determine the maximum annual production of young. They then simply assumed that 20 percent of annual production could be safely removed by hunting.
On the other hand, they also developed a behavioral model with randomly determined litter sizes based on field observations and, most importantly, winter survival rates that depended on marmot group size. This model produced population trends and group sizes that matched field observations and revealed that even low levels of hunting (annual harvests as low as 5 percent of the adult population) would cause extinction. In contrast, the bush meat trade models overestimated sustainable hunting levels — in one case suggesting that annual harvests of 9 percent of the adult population were sustainable.
The alpine marmot isn’t currently threatened; this model simply provides proof of concept. But in the management of more heavily exploited species, Allee-based behavioral modeling could prove to be a lifesaver.
Yet despite the potential benefits, the puzzling truth is that behavior-based population models have yet to gain wide use in conservation. “There’s a few of us trying to do it,” says Sutherland, “but I think lots of people haven’t really appreciated the strength of that approach.”
Matchmaking
Captive breeding and some interventions in wild populations such as fish hatcheries can thrust conservation workers into the unlikely role of matchmaker. The potential for shaping populations is unprecedented, but a word of caution is warranted. Species themselves are much better at selecting their mates than humans are at selecting mates for them — and if we ignore this fact in our conservation efforts, then we risk undermining our best laid plans. The story of the Baltic Sea salmon hatcheries provides a stark reminder.
In the spring of 1974, the Atlantic salmon (Salmo salar) of the Baltic Sea were struck by a mysterious blight, and in hatcheries across the region, newly hatched salmon fry foundered in the water and died. It was fish hatched from poorly pigmented, pale-colored roe that died; fish hatched from dark red roe escaped unscathed. This pale egg blight became known as early mortality syndrome. Over the following years, the syndrome waxed and waned, occasionally striking up to 95 percent of the juvenile salmon in some hatcheries.
When early mortality syndrome struck, the Baltic salmon fishery had already been supported for over 50 years by hatcheries, which accounted for up to 90 percent of the Atlantic salmon living in the fishery. These hatcheries had always randomly mated fish to avoid artificially altering their allelic frequencies.
Yet some researchers speculate that random mating, together with increasing pollution in the Baltic Sea, has contributed to early mortality syndrome. The reason, says Torbjörn von Schantz, an evolutionary biologist at Lund University in Sweden, is that the fish themselves have never chosen their mates randomly; instead, females preferentially select mates according to several criteria including, he believes, red coloration. By doing so, they’re selecting mates with the largest reserves of carotenoids (antioxidant compounds producing red coloration in both fish and roe and important for fighting the effects of pollution). In contrast, random mating prevents selection of carotenoid-rich fish, gradually decreasing the population’s pigmentation and its resistance to ever-increasing pollution. To keep early mortality syndrome at bay, hatcheries have taken to treating fry with vitamin B-1, which doesn’t solve the underlying problem but for unknown reasons seems to prevent death.
The poor mate choice/pale egg theory of early mortality syndrome has yet to be conclusively shown. But even as an unproven hypothesis, it provides a potent reminder that conservation efforts should incorporate natural mate selection whenever possible. For the salmon of the Baltic Sea, “one should collect the breeding fish and analyze their carotenoid pigmentation,” says von Schantz, “and select those fish that have the highest concentration of carotenoids in their flesh.” For now, he’s simply suggesting that this technique be tried in a few hatcheries to see if it regenerates a salmon population that is capable of breeding without vitamin B-1 treatment.
In addition to fish hatcheries and replanted forests, where humans directly influence the genetic makeup of wild populations, this lesson also has implications for captive breeding.
Substantial effort is often made to match captive animals so that genetic variation is preserved. But once the homework is done, the star-crossed animal pair — a perfect match on paper — often shows no interest in mating. This problem occurs especially in solitary species such as pandas, gorillas, and some large cats.
The problem is being solved in cheetahs by mimicking natural mate selection. At the De Wildt Cheetah and Wildlife Centre in De Wildt, South Africa, cheetahs are housed separately to simulate their natural solitary exist-ence, but males are then introduced to large numbers of females one by one. Essentially, male cheetahs wander down a corridor (nicknamed “Lovers’ Lane”) that’s lined by enclosures containing solitary females. The males’ behavior (especially their notorious hot and bothered stutter barks) makes no mystery of which females interest them, and this is used to pair animals.
Fitness-determining genes are likely to be one criterion that cheetahs use to select mates. Although it’s not known which genes are important, one possibility is that cheetahs (and plenty of other picky species) choose mates based partly on their major histocompatibility complex (MHC) genotype. These immune markers are known to be involved in human and mouse mate selection and seem to be determined by scent. Females prefer mates whose MHC genotypes don’t match their own, and offspring from mixed-MHC matings are more resistant to disease and more successful at producing young. With credentials like that, MHC has been contemplated as an easily screenable marker that could be used to evaluate captive breeding pairings. But for the moment, it remains a matter of speculation; more research is needed before MHC’s true usefulness is known.
In the meantime, moderation should be the watchword. Whereas allowing free mate choice in captive populations may maintain high frequencies of “good genes,” the flip side is that individuals lacking such genes will reproduce less — and this speeds the loss of genetic variation, just the opposite of what’s needed in small, fragile populations. “We need to find an optimum between promoting good genes and maintaining genetic variation,” counsels Claus Wedekind, an evolutionary biologist at the Swiss Federal Institute for Environmental Science and Technology in Duebendorf, Switzerland. “Both are very good things to have, but you can’t get both at the same time.”
Animal Culture
But what if protecting the cultural diversity of animals were just as important as protecting their genetic diversity? The growing realization that some animals possess cultural traits that are passed from generation to generation has pushed this controversial question into the forefront.
The culture conundrum is nowhere more apparent than in cetaceans. Hal Whitehead and Luke Rendell, marine biologists at Dalhousie University in Halifax, Nova Scotia, have found that the sperm whales (Physeter macrocephalus) of the South Pacific can be subdivided into at least five separate clans, each with its own distinct culture including different vocal calls and different patterns of movement and habitat use. These clans range over broad, overlapping swaths of ocean and were only discovered through extensive data collection.
The problem is that whale harvesting has typically been managed by species or by region — a manner which totally overlooks the cultural subdivisions and therefore raises the possibility that what appears on a whole-population basis to be a reasonable harvest quota could actually decimate one entire clan while hardly touching another.
This could occur because clans’ individual behaviors (such as movement patterns, habitat use, and evasion strategies) may affect their vulnerability to whaling. The Galapagos Islands region, for example, hosts two major clans, one that stays close to shore and swims meandering routes, and another that remains further from shore and travels in straight lines.
Extinguishing entire clans is risky because their cultural behaviors are exquisitely adapted to specific environmental conditions. And so, erasing one set of behaviors from existence could harm the species’ ability to adapt or use its full range of habitats. During El Niño years, for example, one Galapagos clan has greater feeding success than the other clan does; whereas in other years, it’s the other way around. Observations like this are prompting some researchers to rethink the idea of biodiversity. “Culture is vital to how humans make a living and survive,” says Whitehead, “and we’re beginning to recognize that we’re not the only species in this regard.”
It’s a radical idea. But already there have been stories of success where novel, behaviorally sound conservation strategies also proved to be beautifully simple. In the end, drawing that much-needed connection between conservation and behavior may just be a matter of learning to look a little more closely.
Box: Learning from experience
Canada’s Grand Bank cod fishery — once the world’s lushest — collapsed in 1992, forcing thousands of fishermen from work. What was especially troubling was that catches had been consistently high from year to year — before suddenly plummeting in one season. Researchers now believe the crash stemmed from a failure to understand the fishes’ behavior, resulting in unsustainable harvesting.
Recent analyses reveal that cod numbers had been declining the whole time. But fishermen and regulators missed that salient fact because they were unaware that cod overwhelmingly preferred a few choice slices of habitat. And so even as overall populations fell, those spots were still bustling with cod. Fishermen casting their nets there continued to haul good catches, and population estimates remained over-optimistic.
But in the less-preferred zones inhabited by overflow cod populations, things were different. The density of cod was steadily declining because a steady stream of fish was emigrating to the popular spots to replace the huge numbers of fish being netted there. By 1993, there were none left to emigrate. If the peripheral decline had been heeded — and the fishes’ behavior understood — then fishermen might still be plying those waters today.
Tanagers are often hesitant to breed in captivity; you can put them together, but they may behave more like Ozzie and Harriet than Romeo and Juliet. But much of that disinterest may come down to poor lighting. It turns out that the birds are judging the sexiness of prospective mates, among other ways, by a visual cue in their plumage. And not just any cue — rather, one that’s visible only in the UV spectrum (which many tanagers, unlike humans, can see).
The problem is, many aviaries don’t provide natural, UV-containing light. But Patty McGill, an ornithologist at Brookfield Zoo, Illinois, found that simply providing some UV light increased pairs’ interest in courtship and nest building.
Nest boxes intended to help revive wood duck populations may actually have hindered the cause — all because the way they were placed failed to account for the ducks’ peculiar egg laying habits.
Nesting boxes are often placed in tight, highly visible clusters. And when this is done, the ducks lay extra eggs in each other’s nests.
Such parasitism comes naturally to wood ducks. The tree hollows where the wood ducks usually nest are limited in number, so a hen that doesn’t find one can at least squeak out a few young by laying eggs in someone else’s nest. Normally parasitism is limited, however, because tree hollows are dispersed and concealed.
But those nest boxes clustered like condos positively invite runaway parasitism. The number of eggs per nest soars, sometimes tripling. As a result, eggs are less likely to hatch due to inefficient incubation of abnormally large clutches, breaking of eggs leading to fungal infections in other eggs, and nest abandonment. A seven-year study of wood duck nest boxes at Montezuma National Wildlife Refuge in New York State found that with high parasitism, egg hatching success plummeted from 79 percent to 22 percent.
Fortunately, the solution is simple. Dispersing and hiding the nest boxes should increase production of young and possibly even reduce the number of nest boxes that are needed.
Suggested Reading:
Berger, J. et al. 2003. Through the eyes of prey: How the extinction and conservation of North America’s large carnivores alter prey systems and biodiversity. In Festa-Bianchet, M. and Apollonio, M. eds. Animal Behavior and Wildlife Conservation. Island Press, Washington, DC.
Courchamp, F., G.S.A. Rasmussen, and D.W. Macdonald. 2002. Small pack size imposes a trade-off between hunting and pup-guarding in the painted hunting dog Lycaon pictus. Behavioral Ecology 13(1):20-27.
Eadie, J., P. Sherman, and B. Semel. 1998. Conspecific brood parasitism, population dynamics, and the conservation of cavity-nesting birds. In Caro, T. ed. Behavioral Ecology and Conservation Biology. Oxford University Press, New York.
Grahn, M., Å. Langefors, and T. von Schantz. 1998. The importance of mate choice in improving viability of captive populations. In Caro, T. ed. Behavioral Ecology and Conservation Biology. Oxford University Press, New York.
Hutchings, J.A. 1996. Spatial and temporal variation in the density of northern cod and a review of hypotheses for the stock’s collapse. Canadian Journal of Fisheries and Aquatic Sciences 53:943-962.
McComb, K. et al. 2001. Matriarchs as repositories of social knowledge in African elephants. Science 292 (5516):491-494.
Rendell, L.E. and H. Whitehead. 2003. Vocal clans in sperm whales (Physeter macrocephalus). Proceedings of the Royal Society of London Series B-Biological Sciences 270(1512):225-231.
Stephens, P.A. and W.J. Sutherland. 1999. Consequences of the Allee effect for behavior, ecology and conservation. Trends in Ecology and Evolution 14:401-405.
Stephens, P.A. et al. 2002. Model complexity and population predictions. The alpine marmot as a case study. Journal of Animal Ecology 71:343-361.
Wedekind, C. 2002. Sexual selection and life-history decisions: Implications for supportive breeding and the management of captive populations. Conservation Biology 16:1204-1211.
About the Author:
Douglas Fox is a freelance science writer who splits his time between Australia and California.
