Friday, December 7, 2007
High tailing hypotheses
Here we are again at Point Reyes National Seashore looking at a brush rabbit high tailing it down the bunny trail. Yes, I am milking the camera trap results for all they are worth.
I always thought that the words "high tailing" originally came from the tobacco stained lips of a gun bearing American somewhere east of the Mississippi. There has never been any question in my mind that the white-tailed deer was the inspiration for this woodsy Americanism.
Apparently not everyone agrees. A competing theory attributes the term to cowboy talk, and the fact that horses also gallop with their tails up. It doesn't matter. A lot of mammals beat a hasty retreat with high tails.
What I want to dwell on here is the eye-catching flight of mammals that leap and bound while ostentatiously flashing white tails and rumps. The high-tailed pogostick gait is called pronking, which comes from the Africaans verb pronken -- to show off, strut or prance. Spronking and stotting mean the same thing, though their origins are vague.
This business of leaping and flashing the fanny became a controversy some years ago when a free-thinking graduate student named Nick Smythe proposed that it evolved in many mammals as "pursuit invitation signals". The conventional wisdom held that tail flagging and the like were alarm signals that aided visibility and cohesion among the fleeing groups. Smythe couldn't reconcile that idea with another observation. When animals like antilopes pronk, they broadcast their whereabouts to predators.
It's probably fair to say that the pursuit invitation idea came to Smythe while in the desert on a horse with no name. (We were office chums so he won't mind me saying that).
He was in Argentina, a student of caviomorph rodents, watching Patagonian cavies, which have been described as rodents trying to be antelopes. When he approached the fleet footed rodents at an oblique angle they would flee and stott at a critical distance of 30-40 meters. Then they would sit and watch him. "If I rode my horse directly at the animals they would gallop straight away. If I rode in such a way as to be in clear sight, but to remain well outside the flight distance. . . .they would freeze and let me pass."
Smythe reasoned that cursorial species like jackrabbits, antelopes, and Patagonian cavies play a game of catch-me-if-you-can with their predators. The predator often decides to give chase, lured by flagging white tails and rumps. His key assumption is that "a healthy prey animal once aware of the predator, stands a good chance of escaping if the predator initiates its attack from outside the flight distance." Unsuccessful chases waste time and energy, but by provoking the chase the quarry brings the threat of predation to closure, and enjoys a net saving of time and energy needed for foraging and other activities.
The publication of the idea apparently caused a stir, but it took 7 years before the other views started to circulate.
The first to object were David Hirth and Dale McCullough, then at the University of Michigan. Years of watching white-tails had given them a different impression, so they examined their data on tail-flagging and another alarm behavior called snorting. For much of the year, white-tails live in closely related female groups or relatively unrelated male groups. Male and female groups tailflagged more or less equally, but female groups snorted significantly more than male groups. Tailflagging, they concluded, is a normal response to predators when the threat is low, "and should be considered a low-cost form of altruism." Female groups snort significantly more often than male groups, which means it probably benefits relatives and is maintained by kin selection.
They felt that the presumption of predator gullibility was a major flaw. Are there no "prudent predators"? If there are no gains to be won by chasing tail-flaggers, wouldn't a crafty canid learn to pursue only non-flaggers? And if so, isn't that an example of a pursuit deterrent signal? And what about plains-dwelling ungulates whose rump patches are permanently switched 'on'? Are these species inviting pursuit all the time? Or do such patches have a different (species recognition) function?
Smythe wrote a rebuttal, but the debate wasn't over.
Bruce Coblentz's critique was titled, "On the improbability of pursuit invitation signals". Coblentz drew on new predator-prey findings from Africa to show that stotting Thomson gazelles gain no advantage when pursued by hunting dogs and spotted hyenas. As for Smythe's assumption about the prey's net energy savings, Coblentz pointed to new findings on the critical energy balance of white-tailed deer in winter, when the costs of strenuous exercise alone can be fatal. Under those conditions, eliciting a predator chase would mean death even if you escaped. It was pretty convincing evidence, but he conceded that the rival group cohesion hypothesis also needed better substantiation.
Next, ornithologist Keith Bildstein jumped into the fray. Like Hirth and McCullough, he also impersonated a predator, this time with white-tails in Virginia. He also used golf balls to mark the distance covered by fleeing deer. Bildstein drew attention to the fact that tail flagging is indeed directed to the predator, and that deer are more likely to flag when at greater distances (75m) from the predator. He did not concur that tail flagging was exclusively a cohesion signal, but didn't agree that it was an invitation to pursue. His take was that it most likely serves as a pursuit deterrent or predator detection signal.
At about this time came Tony Pitcher's antiambush hypothesis -- "that stotting evolved as a secondary defense to reduce the effectiveness of ambush attack by socially hunting predators". That's right, high-jumping helps the antelope see who's lurking in the bushes. Somehow the debate had missed this point.
Then a bird study from down under clarified the pursuit invitation issue further. Australia's eastern swamphen flashes its white tail feathers to potential predators just like tail-flagging mammals, but they don't do it while running or flying away. The tail flashing signal is covert to other swamphens, and overt to predators, and its frequency increases as ground predators (like people) get closer. It flashes whether alone or in groups. When cover is available, it just hides. When a predator appears within its flight distance, it flees without signaling. D. J. Woodland and coworkers concurred with Smythe that such signals are intended for potential predators, but argued that they dissuade rather than goad the predator to attack -- for swamphens, the pursuit deterrent hypothesis made the most sense.
Finally someone did an experiment, and while the example is peripheral to pursuit invitation, it still bears on the issue in the meandering way that science solves problems. Roger Powell examined the role of black tipped tails in weasels to predation by raptors. White winter coats make weasels hard to see in snow, but black-tipped tails would seem to give them away to predators, just as white tails and rump patches do in ungulates. Powell trained three red-tailed hawks to attack six models of weasels (2 sizes) scooting over a flat simulated snowfield. The models differed in the presence and location of the black spot. Guess what? Attacking hawks had trouble striking the pure white models, but clearly zeroed in on the black spots. They easily struck models with a black spot on the body, but missed models with the black tail tip. Powell didn't conclude that the tail markings of weasels evolved to invite attack, but thought they served to deflect the strike away from vital parts. Thus we have the predator deflection hypothesis.
Testing hypotheses is like trying on new shoes. You take the shoe that fits. The pursuit invitation hypothesis was rejected by some, while others cobbled its parts into new hypotheses that fit their data. Most hypotheses have short lives, but if they make it to print, they are likely to stimulate further investigation and get chewed up along the way.
That's how we learn new things, and find out that we've only scratched the surface.
Coblentz, B. 1980. On the improbability of pursuit invitation signals. American Naturalist, 115:438-442,
Hirth, D.H., and D.R. McCullough. 1977. Evolution of alarm signals in ungulates with special reference to white-tailed feer. American Naturalist, 111:31-42
Pitcher, T. 1979. He who hesitates, lives. Is stotting antiambush behavior? American Naturalist, 113:453-456.
Powell, R. 1982. Evolution of black-tipped tails in weasels: predator confusion. American Naturalist, 119:126-131.
Smythe, N. 1970. On the existence of "pursuit invitation" signals in mammals. American Naturalist, 104:491-494.
Smythe, N. 1977. The function of mammalian alarm advertising: social signals or pursuit invitation. American Naturalist, 111:191-194.
Woodland, D.J., Z. Jaafar, and M.-L. Knight. 1980. The pursuit deterrent function of alarm signals. American Naturalist, 119:748-753.