Barbets are a group of diverse and attractively coloured birds placed under the family Capitonidae. There are a total of 82 species, of which 25 are Asian. Malaysia is home to 14 species. Of these, Singapore used to have five species. Now only three: Coppersmith (Megalaima haemacephala) (above left), Lineated (M. lineata) (above right) and Red-crowned (M. rafflesii) (below left) are around. The other two, Brown (Calorhamphus fuliginosus) (below right) and Blue-eared (M. australis) have long disappeared from the scene.

Although colourful, these birds are surprisingly difficult to spot. In fact they are more often heard than seen. Their calls can be monotonous and ventriloqual, making it difficult to locate the bird.

The monotonous call of barbets is best represented by Coppersmith, often called “brain-fever” bird. It gives a series of “pook” notes incessantly. This sound is supposed to resemble the tapping of a coppersmith’s hammer.

All barbets excavate their own nesting cavities, some even their roosting cavities.

These are primarily fruit eaters, although they catch insects to feed their young. There are a few reports of barbets taking lizards, tree frogs, birds and their eggs. Our earlier posts document barbets taking a flowerpecker and a sparrow.

Photo credits: Coppersmith (Willis), Lineated (Mark Chua), Red-crowned (Johnny Wee) and Brown (Eric Tan).

According to the literature, the prominent black sac seen in the Blue-eared Barbet (Megalaima australis) is a gular sac, also called vocal sac. See earlier posts 1, 2 and 3.

Birds produce most of their sounds with their syrinx, the sound producing organ sited where the windpipe divides into two. What is less known is that there are secondary acoustic structures that modify the sounds produced by the syrinx – whether to spread, amplify or reverberate. One of these is the vocal sac, prominent and exaggerated in some species.

According to Dantzker & Bradbury (2006), the bare vocal or gular sacs seen in the North American grouse and the Neotropical cotingas are inflated only in acoustic display. As most of these sacs are brightly coloured, they are probably also involved in visual signaling. The pan-tropical frigatebirds (below left) and two storks, the Old World Marabou (Leptoptilos crumeniferus) (below right) and New World Jabiru (Jabiru mycteria), also inflate their necks and vocalise, but not always at the same time.

In the above species, the sacs are often held fully inflated for lengthy periods in a strictly visual display and only used occasionally in sound production.

Three other groups have vocal sacs that are equally impressive but not devoid of feathers. Perhaps the most striking is the kakapo (Strigops habroptilus), an endangered flightless parrot from New Zealand that seems to inflate its whole body when booming. Many medium to large bustards, like the Kori Bustard (Ardeotis kori) (below left) inflate sacs that are often covered in elaborate feathering; and some but not all inflating bustard species vocalise while inflated (Collar, 1996; Dantzker & Bradbury, 2006).

According to Johnsgard (1983), certain calls among yearling crowned cranes involve the inflation of the gular sac. This is thought to serve as a resonator that may provide increased carrying power. In the Australian Crane (Grus rubicundus), the gular sac of the male is inflated during display and possibly helps to resonate low-frequency sounds. The Grey Crowned Crane (Balearica gegulorum) of Africa is shown above (right).

Strangely, there is no mention of barbets having gular sacs, not even in the most recent monographs of these birds. It is now obvious that the Blue-eared Barbet’s black sac plays a role in vocalisation, possibly also in fruit storage. And according to Adrian, other species of barbets also have these sacs. Obviously, there is much to be learnt about gular sacs and barbets. Happily, bird photographers like Adrian are currently at the forefront of this investigation.

References:
1. Collar, N. J. (1996). Family Otididae (Bustards). Pp. 240-275 in: del Hoyo, J., Elliott, A. & Sargatal, J. eds. Handbook of the birds of the world. Vol. 3. Hoatzin to Auks. Barcelona: Lynx Editions.
2. Dantzker, M. S. & Bradbury, J. W. (2006). Vocal sacs and their role in avian acoustic display. Acta Zoologica Sinica (Suppl.) 52:486-488.
3. Johnsgard, P. J. (1983). The cranes of the world. Bloomington: Indiana University Press.
4. Short, L. L. & Horne, J. F. M. (2001). Toucans, barbets and honeyguides: Ramphastidaer, Capitonidae and Indicatoridae. Oxford University Press.
5. Short, L. L. & Horne, J. F. M. (2002). Family Capitonidae (Barbets). Pp. 140-219 in: del Hoyo, J., Elliott, A. & Sargatal, J. eds. Handbook of the birds of the world. Vol. 7. Jacamars to Woodpeckers. Barcelona: Lynx Editions.

Image of barbet by Adrian Lim, others by YC.

In the earlier post on the prominent black pouch of the Blue-eared Barbet (Megalaima australis) by Adrian Lim a.k.a wmw998, there was a discussion of the pouch being used as a possible storage for food.

Adrian was adamant in his belief that the pouch was for vocalisation and not for food storage. He wrote, “I had watched the birds for days, and I can safely tell you the pouch wasn’t used for the purpose of holding food, like a hamster! At all times, I had observed the food to be delivered directly from the male’s beak, not regurgitated food.

“I strongly believe that the pouch was for sound production to attract the female (soft note, sounds exactly like blowing a football referee’s whistle lightly, one note at a time ) and perhaps to warn other males of its presence (the chiok chiok sound). I had seen the bird perching on a branch, making both sounds, both using the pouch. The soft sound, as I had mentioned earlier, was made in between feeding the female, when the female happened to be away ‘temporarily’, eg. flown away from the feeding perch because of disturbance. And if you look carefully, the entire breast and belly of the male bird sunk in whenever it made such sound, to inflate the pouch.

“Please check into my posting in NaturePixel a couple of months back… I had some photos of the same male doing the blowing and puffing thing.“

The images above and below show the sequence of pouch inflation. In the absence of food in the bill and a female around, it would seem that the pouch is more involved in vocalisation.

Adrian added, ”This bird comes to the tree near my balcony and blows nonstop, a few times a day. No other bird joins it…

“…I think all barbets, except the Brown, and possibly the Lineated, do the same blow job. So far, I have also captured the Golden-throated doing the same thing. Funny though, they do not open the beak while blowing.”

According to Short & Horne (2001): “Most barbets.. sing to proclaim and maintain a territory; since these species largely occur in pairs or social groups, the female is usually near or with her mate. …the basic form of the song is not elaborate in most barbets, in which a series of low-pitched ‘hoot’ or ‘hoop’ or ‘ooo’ notes are uttered perhaps ad nauseum, seemingly, as in some tinkerbirds and the Coppersmith Barbet.”

In another communication, Short & Horne (2002) state that “most barbets give a relatively low-pitched ‘hoot’, ‘hoop’ or ‘pop’ notes that may be repeated in short to long series as a song, uttered with the bill closed or nearly so.

“…Aggressive calls generally are noisy, and commonly include fast, chattery, squawky, honking, rattling and grating sounds, usually repeated in short to long phrases and often compounded, as in a squeaky grating or squeaky chatter.

“…the more hooping, popping or hooting songs seem ventriloquial, and may vary in volume simply as a result of the barbet turning its head as it sings.”

We will discuss the role of the pouch, or gular sac, in another post.

All images by Adrian Lim.

References:
1. Short, L. L. & Horne, J. F. M. (2001). Toucans, barbets and honeyguides: Ramphastidaer, Capitonidae and Indicatoridae. Oxford University Press.
2. Short, L. L. & Horne, J. F. M. (2002). Family Capitonidae (Barbets). Pp. 140-219 in: del Hoyo, J., Elliott, A. & Sargatal, J. eds. Handbook of the birds of the world. Vol. 7. Jacamars to Woodpeckers. Barcelona: Lynx Editions.

This post is a cooperative effort between NaturePixels.org and BESG to bring the study of bird behaviour through photography to a wider audience.

In the earlier post on the courtship behaviour of the Blue-eared Barbet (Megalaima australis) by Adrian Lim a.k.a wmw998, there was a mention of a prominent black throat pouch that the male displayed when making its mating call (below).

The male was described as puffing and blowing to expand his throat pouch. As the pouch expanded, it pushed aside the black feathers that make up the black upper breast band, exposing a smooth, rounded, black sac.

Adrian is of the view that “the sac is only a tool for making the call, I doubt it is for attracting the female. If you look at the shots carefully, you will notice that the breast of the male bird sinks in whenever the sac inflates or puffs up.”

Dr Geoffrey Davison was consulted and responded: “The throat of most birds bulges a bit when they call, but this looks rather extreme. I would have guessed that its crop is stuffed with food, and then when it is calling as well the upper part of the breast would swell even more.

“I have watched other species of barbets calling, and have not seen such an extreme swelling. On the photo it looks as though part of the patch is bare skin, and black - or is this perhaps a patch of feathers that have got wet and sticky from its food? If it is bare black skin then this does imply a signal function. The bases of the feathers within this patch are black.“

On seeing an enlarged image of the pouch, Geoff added: “Quite dramatic, isn’t it? The black skin is very clear in your tweaked version of the photo. I’m not familiar with the literature on anatomy, but many fruit-eating birds are able to store quantities of food in a gular pouch, for later regurgitation. It’s the equivalent of the macaques’ cheek pouches, though a different part of the anatomy (lower down in the oesophagus). I would be inclined to avoid the word ’sac’ for such a structure.

“Presumably a female barbet would be able to distinguish at a glance a male who has a supply of fruit ready (bigger black pouch = more food), and more inclined to allow copulation. I remember seeing something recently… about male birds rewarding the female who allows copulation by giving her fruit after she has submitted, rather than using fruit to tempt her beforehand.

“The other possibility is that this is a hollow structure, part of the air sac system, used as a resonance chamber to enhance sound production as it calls. These are not mutually exclusive possibilities (there could be both a resonating chamber in the air sac system and a pouch in the oesophagus) but not quite so easy to visualise how the two would work together.”

Morten Strange had this to say: “Bizarre image… This bird is not calling, the gular pouch seems to be stuffed to the brim with fruits…” while Wang Luan Keng suggested a ventriloquism function.

Yes, the pouch stores fruits, plenty of fruits. This species of barbet apparently has to offer a fruit for each act of copulation and usually a series occur one after another.

According to the literature, the skin of the throat or the neck on many non-passerine birds is bare, loose and distensible. In many instances it forms a pouch, especially in fruit-eating birds like hornbills (Kinnarid & O’Brien, 2007). The pouch comes in useful in the transporation of fruits to the nest to feed the chcks and/or mate.

In pelicans the pouch is for catching and holding fish for the young birds. That of the male Great Bustard (Otis tarda) is inflated in display (Garrod, 1874). In male frigatebirds (Fregata spp.) (above left), Marabou Stork (Leptoptilus crumeniferus) (above right), among others, similar pouches are inflated and displayed in courtship or social displays.

In grouse and Painted-Snipe (Rostratula benghalensis), the pouches increase the vocalisations by enlarging the sound resonating chamber (Stettenheim, 2000). Morten also pointed out that the Chestnut-winged Babbler (Stachyris erythroptera) produces low-pitched notes by inflating its neck, barring two patches of skin. The puffed-out neck-skin is a conspicuous blue or violet. His image is published in Collar & Robson (2007).

Image of barbet by Adrian Lim, those of frigatebird and stork by YC.

References:
1. Collar, N. J. & Robson, C. (2007). Family Timaliidae (Babblers). Pp. 70-291 in: del Hoyo, J., Elliott, A. & Sargatal, J. eds. Handbook of the birds of the world. Vol. 12. Picathartes to Tits and Chikadees. Barcelona: Lynx Editions.
2. Garrod, A. H. (1874). On the “showing-off” of the Australian bustard (Eupodotis australis). Proc. Zool. Soc. London 1874, No. 31:471-473.
3. Kinnarid, M. F. & O’Brien, T. G. (2007). The ecology and conservation of Asian hornbills: Farmers of the forest. University of Chicago Press.
4. Short, L. L. & Horne, J. F. M. (2002). Family Capitonidae (Barbets). Pp. 140-219 in: del Hoyo, J., Elliott, A. & Sargatal, J. eds. Handbook of the birds of the world. Vol. 7. Jacamars to Woodpeckers. Barcelona: Lynx Editions.
5. Stettenheim, P. S. (2000). The Integumentary morphology of modern birds - An overview. Amer. Zoologist 40:461-477.

Adrian Lim a.k.a wmw998 documented a pair of courting Blue-eared Barbet (Megalaima australis) in Malaysia sometime in May 2008

The female was perching on a branch of a tree doing nothing in particular. Suddenly there was a loud call, made by a male nearby. He had food in his bill but this did not prevent him from making “such sweet music” as described by Adrian (left). The male was puffing and blowing to expand his throat pouch. As the pouch expanded, it pushed aside the black feathers that make up the black upper breast band, exposing a smooth, rounded, black sac.

The female was attracted to the male’s display but waited for him to come close and make his courtship offering of food. Only then was there copulation. Each act of copulation was preceded by an offer and actual transference of a succulent fig to the female (below). No fig, no sex! *

This courtship feeding of fruits followed by copulation went on for a number of times, as is typical of barbets (below).

In the image below the male is covering the female with his wings in another act of copulation.

The courtship feeding of the Blue-eared appears different from that of the Coppersmith (M. haemacephala). Whereas the former offered one fig per act of copulation, the latter often got away with less number of fruit as compared with number of copulations - often getting away with two for the price of one. Such behaviour was confirmed by another observation where the Coppersmith managed to copulate with the female, to only release the fruit after and not before. And then he mounted her a second time without offering a second fruit. Two for the price of one!

During mating, singing by the pair is incessant and simultaneous, with head bobbling, side to side tail movement, all these in an aggressively looking manner (Short & Horne, 2002).

Adrian confirms the above with his statement about the male: “Blue-eared Barbet seems to make very loud noise most of the time, when it is not having a female or attracting a female… Normally, it sounds like ‘CHIOK CHIOK’, and it can be doing that for minutes at a time. I have a feeling that it is trying to make its presence known to other males. This is a ‘territorial behaviour’ perhaps!

“However, when it is courting a female, or trying to attract a female to a certain perch or tree, the noise is much gentler and softer, and totally different from the ‘CHIOK CHIOK’. I can’t describe the sound to you in words, but in both cases, you can see the black sac.”

There seems to be no mention of the prominent black throat pouch in the literature. As such, this can be a first record in the Blue-eared Barbet, or any barbet for that matter. Discussion of this throat pouch will be posted in the next few days. So stay tuned!

Addenda:
“I have to clarify here that the courtship is a process that is likely to continue for a few days at the least, between the pair. It is not a case of a male going out to have a ‘good time’, spotted a female and making a lot of noise to attract it! In my opinion, the birds had already ‘accepted’ each other, and so the offer of food was like feeding a young, nothing spectacular, no noise making at all, even when the ACT was over. The only time that the gentle sound was made was when the female bird flew off for reason such as disturbance by other birds or animals, and the male wanted to call it back to the same tree.” Adrian, 1st June 2008

*Adrian has written in to clarify that there were occasions when “…the male bird would feed the female continuously, and only once in a while, got on top of her, though still with the food held in the beak and about to offer her.” 4th June 2008.

Reference:
Short, L. L. & Horne, J. F. M. (2002). Family Capitonidae (Barbets). Pp. 140-219 in: del Hoyo, J., Elliott, A. & Sargatal, J. eds. Handbook of the birds of the world. Vol. 7. Jacamars to Woodpeckers. Barcelona: Lynx Editions.

This post is a cooperative effort between NaturePixels.org and BESG to bring the study of bird behaviour through photography to a wider audience.

All images by Adrian Lim.