Parrots Climb Using Three Limbs, Thereby Violating The ‘Forbidden Phenotype’

Parrots are unique because they use their beak and legs when climbing, which makes them the only animal with three functional limbs

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Humans have had an extraordinarily long fascination with the triskelion motif, whose name is derived from the Greek and translates as “three-legged”. Three-legged creatures feature in ancient Chinese mythology, a triskelion featuring three human legs joined at the hip and flexed at the knees adorns the coat of arms for the Isle of Man, and much more recently, author H. G. Wells described Martian invaders attacking Earth with massive, three-legged war machines called tripods that they modelled after their own three-legged body plan in his extraordinarily popular and influential 1898 science-fiction novel, War of the Worlds.

Despite this surfeit of imagination, there are no three-legged animals alive today, and nor have any such fossils ever been unearthed. Considering the immense length of geologic time during which life has evolved, and the many riotous forms life has taken, it makes one wonder why a three-legged animal never once appeared.

Studies indicate there is a developmental constraint against an animal possessing an odd number of limbs because the bilaterally symmetrical body plan only gives rise to even numbers of limbs, and this became the established body plan very early in evolutionary history. Thus, tripedalism is known to scientists as a “forbidden phenotype” even though locomotion studies suggest that a three-legged phenotype would be functional and possibly advantageous over some of these other, more familiar, body plans.

In spite of this evolutionary constraint, tripedal and pentapedal gaits have emerged in multiple lineages, including mammals (ref & ref) and birds (ref & ref). Further, despite the lack of three limbs, the tripedal stance does exist and is widely used throughout the animal kingdom. For example, kangaroos use their tail as a brace when pummelling a rival as well as when grazing (ooo, pentapedalism!?). Woodpeckers use their tail as a support whilst hammering holes into a tree. And perhaps most familiar to those of us who live with modern dinosaurs, we often see our parrot friends use their beaks as a third limb when climbing up a steep incline or perpendicular surface (ref & ref). Hey, now that looks like tripedalism.

But are parrots using their beaks simply to stabilize themselves or are they using their beaks to actually propel and power themselves as they cycle through their left leg-right leg-beak sequence whilst climbing? How much locomotive force do their beaks provide compared to their legs? How does this force compare to that generated by other animals, particularly rock-climbing humans?

To better understand these questions and to assess the contribution of a parrot’s beak and head to climbing, Melody Young, a graduate student who is also pursuing her medical degree in Osteopathic Medicine at the New York Institute of Technology (NYIT), teamed up with several colleagues, including her mentor, evolutionary biomechanist Michael Granatosky, an Assistant Professor at NYIT, who is one of the leading experts in the analysis of animal motion data.

“At the time I joined the lab, the parrot experiments had just begun so this was a project Dr. Granatosky was interested in way before I even came into the picture”, Ms Young told me in email. “With a parrot of his own at home, he’d also observed this beak forward locomotion and wanted to quantify this beak use in some form.”

Ms Young and her collaborators purchased six young healthy rosy-faced lovebirds, Agapornis roseicollis, and trained them to participate in two separate experiments. But because Ms Young had no previous experience working with parrots, this project was a bit of a challenge.

“I have so many fun memories of chasing parrots around the lab with my lab mates as they hid under tables, sinks, carts (and gave us all the cardio we needed)”, Ms Young said. “However, I was really surprised at how easy they were to work with once they understood the task. In a way they were a perfect experimental animal because they were intelligent enough to grasp the task quickly, yet not so much so as to cause any huge setbacks or issues during data collection. Overall, they were super cooperative and fun to work with”.

To carry out these experiments, Ms Young and her collaborators designed a flat runway that rotated at the base so its angle of ascent could be modified. Lovebirds were filmed from the side and from the back with two high-speed cameras as they moved across the runways at their own pace. Watching these films, Ms Young and her collaborators scored and calculated the frequency of each parrot’s beak-, tail- and wing-use across each of the substrate conditions (Figure 1).

Ms Young and her collaborators used a sensor to quantify how much force was exerted and in which directions by the climbing lovebirds. The team found that the climbing lovebirds’ beaks generated as much propulsive force as their legs. They concluded that the head and beak of parrots had been co-opted to function biomechanically as a third limb, conferring both the stability and the propulsive force necessary to power bipedal gait. Further, the team found that the parrots’ beak and head match or exceed peak force magnitudes measured in rock-climbing humans (ref) and in climbing monkeys (Figure 3).

“We found the lovebird beaks to exert comparable propulsive (moving the animal up/down the vertical substrate) and tangential (pushing or pulling in/out of the substrate) forces to their hindlimbs and thus coined the term ‘propulsive’ limb to describe the beak’s contribution to locomotion”, Ms Young explained in email. “Essentially, the head/neck/beak structure form the necessary third limb that lovebirds require to ascend a vertical substrate”.

Parrots are truly unique because they managed to evolutionarily shift the function their beaks and faces to perform an additional role, a specific locomotor role, effectively transforming their heads into a third propulsive limb used during climbing. This is an evolutionary novelty known only in parrots.

“For them to take their faces and integrate it into their stride cycle is pretty incredible”, Ms Young said. She pointed out that the birds’ nervous systems would have had to change to fit beak movement into the normal rhythm of walking, and that parrots would have had to repurpose the muscles in their necks and heads so they can effectively climb on their beaks, using them the way rock climbers use their arms.

Studies that investigate violations of the forbidden phenotype force us to confront previously hidden gaps in our understanding of evolution. Basically, the facts appear to suggest that animals with three legs do not exist simply because animals spring from an evolutionary constraint imposed by the adoption of a bilateral body plan extremely early in evolution. This made it unlikely that any animal might evolve an odd number of legs, although there are a few extremely rare exceptions of ancient animals with unusual body plans — echinoderms and some Ediacaran organisms, for example. But even amongst these exceptions, a triskelion animal with three locomotory limbs, has never appeared. The fact that parrots have been able to co-opt their feeding apparatus and neck neuromusculature so they can use their beaks to propel themselves upwards while climbing is an evolutionary novelty not observed in any other taxa.

Source:

Melody W. Young, Edwin Dickinson, Nicholas D. Flaim and Michael C. Granatosky (2022). Overcoming a ‘forbidden phenotype’: the parrot’s head supports, propels and powers tripedal locomotion, Proceedings of the Royal Society B: Biological Sciences, 20220245 | doi:10.1098/rspb.2022.0245

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