Evolution of the Enigmatic Eclectus

tags: researchblogging.org, dichromatism, mating system, plumage color, sex allocation, eclectus parrots, Eclectus roratus, ornithology, birds, avian, parrots

Some of you might recall the recent story about scientists learning to identify plumage coloration from fossilized feathers. This might seem a sort of esoteric pursuit meant to entertain scientists with access to big and expensive machines, but in fact, knowing the color of a bird's plumage is very important for learning something about their natural history. Let me explain.

Birds are highly visual animals, like humans and other apes, so their plumage color evolves because it serves as a signal to other birds, especially when choosing a mate. Plumage color and ornamentation also correspond to the birds' mating system: long-lived monogamous birds that mate for life are often sexually monochromatic, while polygynous birds where the males do not assist in parental care are very strongly dichromatic where males have brilliant feather coloring and often have elaborate plumage adornments while the females are usually smaller and drably colored. So, based on that information, what would you predict for the reverse situation where the females of the species are brilliantly colored while the males are cryptically colored?

This is precisely the situation that confronted early naturalists when they first discovered the eclectus parrot. Eclectus parrots are medium-sized parrots that are endemic to several islands in the south Pacific Ocean, including Australia. This parrot species is famous because it has such extreme sexual dichromatism that when the birds were originally discovered by white explorers, the emerald and royal blue males and scarlet and royal blue females were thought to be different species. In fact, males were first described in 1776 while females were not described until 61 years later.

The late Bill Hamilton, professor of evolutionary biology at Oxford University, was especially enamored by these parrots. One time when he gave a public talk about eclectus parrots, he concluded by proclaiming he would be ''ready to die'' when he finally understood the mystery underlying the evolution of the intensely colorful plumages of this species.

In fact, understanding the evolutionary reasons for eclectus parrots' plumage coloration is making a significant contribution to evolutionary theory. But because of the difficulty of studying parrots in the wild combined with an academic bias against parrots as valid research subjects (primarily based in their popularity as avicultural subjects and as pets), evolutionary and field biologists have been surprisingly slow to formally document these birds' natural history.

Fortunately, a scientific study has just been published that documents the life history of wild Australian eclectus parrots, Eclectus roratus macgillivrayi, also known as MacGillivray's (red-sided) eclectus parrots. Unlike my own Solomon Islands eclectus parrot, Elektra, which is the smallest of the eclectus, the Australian red-sided eclectus is the largest subspecies of this enigmatic parrot. Unlike most subspecies of eclectus, the Australian eclectus parrot is not widely bred nor kept as a companion pet outside of Australia. According to some reports, there is only one pair of this subspecies in the United States.

All parrots nest in cavities of one sort or another, although most of them nest in holes in trees. Like most parrots, Australian eclectus parrots live and nest between 20-30 meters (65-100 feet) above the ground in the canopies of forests in remote areas ranging from Australia's Iron Range National Park where this study took place, to the challenging terrains of New Guinea, the Moluccan Islands, and as far east as the Bismarck Archipelago and the Solomon Islands. As Robert Heinsohn, of the Australian National University and the sole author of this study observed, these birds are difficult to observe in the wild because they are notoriously shy and quickly disappear by escaping over the treetops when disturbed.

But Heinsohn persists even to this day. Throughout his research, he has observed three interrelated traits in these birds that provide special insights into the relationship between ecology and evolution and how they shape species. First, eclectus parrots show reversed sexual dichromatism where females are more brilliantly colored than males; second, wild eclectus have a cooperative breeding system that is unique among parrots; and third, the data suggest that females manipulate the sex of their offspring. Further, and this is unique among birds with reversed sexual dichromatism, eclectus parrots do not have reversed sex roles. Instead, it is thought that the evolutionary reason underlying the peculiar eclectus plumage coloring is based on the relative lack of appropriate tree holes for nesting, so both sexes engage in intense competition for those few holes that exist.

This has also caused the birds to develop tremendously different lifestyles, where male and female eclectus face different selection pressures, and this is reflected in their vastly different plumages. Males are primarily brilliant green because they range widely in search of fresh fruits for their mates and chicks, so they face strong predation pressures, particularly from peregrine falcons, Falco peregrinus, and rufus owls, Ninox rufa. These predators, whose eyes are atuned to movement, cannot distinguish green parrots against the green foliage of flowering trees, but eclectus parrots, whose eyes are designed to see UV as well as other colors, can easily spot each other, especially when they are in front of the contrastingly dark tree bark next to their nest hollow.

Female eclectus, on the other hand, almost never leave their nest tree once they have found a suitable hole to nest in, so they remain dependent their mates to forage for them while they remain with their tree, defending it against all challengers. Since there is fewer than one nest hollow per square kilometer of rainforest, female eclectus have sometimes been observed fighting to the death over this rare and precious resource. Thus, the female's brilliant scarlet coloring serves as a warning to potential interlopers that a particular tree is occupied. Predatory birds can also see the female's contrasting plumage, especially because she positions herself prominently on top of her nest tree, but she quickly retreats into the safety of her nest hollow when threatened.

Because of the rarity of nest hollows, eclectus parrots have evolved a fascinating mating system. Limited nesting opportunities prevents this species from having either a relatively common monogamous pairing, and it also prevents a classical polyandrous mating system where the female competes for and mates with several males who have their own nests. Instead, the rarity of nest hollows caused eclectus parrots to maximize their reproductive output by evolving cooperative polyandry. This is where the female mates with two or more males and all of them remain together to raise the chicks. The resident female, who cannot leave her nest tree for fear of losing possession of it, is dependent upon being fed by a number of males -- Heinsohn has observed as many as seven males at one nest tree. Are these "extra males" related to each other or to the resident female? Originally, it was thought they were related to each other or they might be offspring from previous nestings that had not yet dispersed. But molecular data reveal that neither situation was the case.

Curious as to why there are so many males hanging around each female when most of these males gain paternity only irregularly, Heinsohn wondered if the males were interacting with other females in addition to collecting food for the tree-owning female. He used radio-tracking to establish the size of the males' territories and found that they are truly huge and encompass nest trees for several female eclectus, all of whom they help feed. These males were apparently hedging their reproductive bets by caring for several tree-holding female eclectus, hoping to father chicks with more than one female. In fact, the author found that male eclectus do fathered chicks at several widely dispersed nest trees -- one male's chicks were identified at trees that were 7.2 kilometers apart.

So on the surface, this mating system appears to be cooperative polyandry, but careful observation and data analysis reveals that eclectus rely upon a very rare polygynandrous breeding system, where both males and females mate with more than one individual per nesting cycle. But the eclectus parrots' system is the most geographically dispersed polygynandrous system yet described.

Biased sex allocation among a female eclectus's chicks is something that was only apparent after aviculturists brought this to Heinsohn's attention. Birds, like mammals, have an equal chance of having either male or female offspring so, over time, the sex ratio of a female's offspring should be 50:50. However, aviculturists have noticed for quite some time that this is not the case, a finding that is statistically significant. For example, the author mentions one captive female eclectus that produced 20 male chicks before switching her output to females.

But it has been documented that other birds can and do choose the sex of their offspring based on the potential benefits to those offspring, such as earlier future breeding opportunities or increased survival. But why do female eclectus manipulate the sex of their offspring, and how is this related to nest cavity availability? That research is still ongoing, but because male offspring do not hang around the nest to help feed their mother and her chicks, it is clear that a breeding female would not increase her production of male chicks when she needs more help at the nest. But a likely clue can be found in body size: because eclectus parrots do not have a sex role reversal, males are slightly larger than females in of all the subspecies, so it is possible that female eclectus parrots choose to produce females when there are fewer males feeding her or when she has a poor quality nest hollow because male chicks are more energetically expensive to raise. Heinsohn's paper that examines this in detail will certainly be fascinating reading.

Eclectus parrots are making important contributions to our understanding of the complex and subtle relationships between resource allocation, ecology and evolution. Additionally, plumage color is a powerful way to gain a clearer insight into the natural history of bird species.

Source

Heinsohn, R. (2008). Ecology and Evolution of the Enigmatic Eclectus Parrot (Eclectus roratus). Journal of Avian Medicine and Surgery, 22(2), 146-150.