Bulbuls

(Pycnonotidae)

Class: Aves

Order: Passeriformes

Suborder: Passeri (Oscines)

Family: Pycnonotidae

Thumbnail description
Medium sized, short-necked songbirds with short round, wings; fluffy plumage, many with crested heads

Size
3.6–11.5 in (9.3–29 cm); 0.5–2 oz (15–59 g)

Number of genera, species
15 genera; 123 species

Habitat
Forest, forest edge, open woodland, scrub, cultivated lands

Conservation status
Endangered: 2 species; Vulnerable: 5 species

Distribution
Africa, Indian subcontinent, Asia, Indonesia, northwestern Australia, Malagasy region, introduced populations in United States

Evolution and systematics

In the introduction to his 1945 revision of the family Pycnonotidae, Jean Delacour states that "The bulbuls constitute one of the most clearly defined groups of perching birds (Passeres). This means that the different genera and subgenera which belongs to the group are obviously related to one another, and rather far removed from any others." Recognition of the bulbuls as a "natural" group has not stood the test of time, however, and the placement of the Pycnonotidae within Passeriformes remains unresolved, as do the relationships of these songbirds to each other.

Depending on the characters examined, the Pycnonotidae have been allied with a number of families. Early authors placed them next to cuckoo-shrikes (Campephagidae) based on shared anatomical and plumage characters, such as abundant rump feathers. Egg-white protein analysis in the early 1970s suggested a relationship to drongos (Dicruridae) or starlings and orioles (Sturnidae, Oriolidae). Current DNA evidence suggests that bulbuls belong in the superfamily Sylvioidea, between kinglets (genus Regulus, sometimes treated as a family, Regulidae) and the African warblers (genus Cisticola, sometimes treated as a family, Cisticolidae). More controversial than the family placement however, are the relationships of various bulbuls to each other. Several species will probably eventually be shuffled to different genera and even other families as research continues. DNA analyses in 2001 suggest that the African and Asiatic genus Criniger, united chiefly by the conspicuously colored throat, is not a natural group. This study recommends that the Asian Criniger take the genus name Alophoixus, and the African species remain as Criniger. Other research examining the relationships of 13 birds endemic to Madagascar, including some of the African greenbuls (Phyllastrephus spp.) found that the Malagasy genera, normally distributed across three families, were actually all most closely related to each other. Some ancient relative of these birds probably arrived at the island at least nine million years ago, then evolved and diversified there rather than different birds of different lineages colonizing the island several times, as previously thought. This study recommends that the Malagasy bulbuls be removed from the genus.

Also controversial is the placement of two of the endemic African genera Neolestes and Nicator. The striking plumage of the black-collared bulbul (Neolestes torquatus) allies it with the shrikes (Malaconotidae, Laniidae, or Prionopidae), DNA data ally it with other bulbuls. Similarly, Nicator has also been allied with the shrikes, but feather protein and DNA evidence suggest the birds are bulbuls. Because the three Nicator species and Neolestes lack a thin sheet of nostril-covering bone that is present in the rest of the bulbuls, they are sometimes placed elsewhere.

Whatever their relationships, it is clear that birds considered bulbuls evolved in the last 10 million years and much of the family may have radiated more recently, probably during the Plio-Pleistocene, about 2.8 million years ago. During the Tertiary, northern Africa experienced general drying, and the eastern lowland forests became isolated as mountains swelled and rifted in the region. Andropadus probably colonized these "new" mountain habitats, which became centers of speciation for the group.

Physical characteristics

Most of the bulbuls are dressed in somber browns, olive tones, or grays, and are often heard before they are seen. However, several species have distinctive face markings with a bright splash of red, yellow, orange, or white plumage. The plumage of Pycnonotus tends to be more variable than other genera, and these birds usually have are a red, yellow, orange, or white "vent" which contrasts with the rest of their underparts. Many species, especially among the Pycnonotus, Criniger, and some Hypsipetes, have long crown feathers that form a prominent head crest; the crest is absent in Andropadus. Almost all have at least a few bristles on the nape of their short necks and a small area without feathers, such that a bulbul with its neck stretched out shows a small bare patch between the nape and upper back. The tail can be fairly long, usually with a round tip, although it is slightly forked in some species.

Small to medium-sized birds, bulbuls range in size from 3.6 to 11.5 in (9.3–29 cm); and between 0.5 and 2 oz (15–59g). Except for the finchbills (Spizixos spp.), the pycnonotids have medium-sized, slender, notched bills. Among the Criniger, the bill is usually strongly hooked at the tip. Bulbuls tend to have short, weak legs and short, rounded wings. Males and females usually look alike, though the female is often slightly smaller; this size difference is greatest in Phyllastrephus. Likewise, the juveniles look like the adults, but their plumage is duller and often more brown.

Distribution

Bulbuls occur mainly in forest and wooded areas across Africa and Madagascar, north to the Middle East and Japan, and east to the Philippines and Indonesia. Except for recently introduced species, there are no bulbuls in the New World. Of the roughly 120 species, there are 27 species in China. About 52 species (in 11 genera) are African, and bulbuls are widely distributed across that continent, being absent only from desert regions. Nine genera are found exclusively in Africa, and two of the larger genera (Pycnonotus and Criniger) are found in both Africa and Asia. The most ubiquitous of the Pycnonotus species is the common bulbul (P. barbatus). This bold and noisy bird is well adapted to man-made habitats and is one of the most widespread and abundant birds in Africa.

Many bulbuls are endemics and have quite restricted distributions, especially those on oceanic islands. The yellow-eared bulbul (Pycnonotus pencillatus) is found exclusively in the montane areas of Sri Lanka; the Nicobar bulbul (Hypsipetes nicobariensis) occurs only on the southern Nicobar Islands south of Burma. Others are widespread and common, the yellow-vented bulbul (Pycnonotus goaivier), occurring from southern Vietnam to the Malay Peninsula and the Philippines, is probably the most commonly seen bulbul of the region. An opportunistic bird, it is often seen around gardens, feeding on food scraps and using potted plants to nest in.

In 1960 a population of red-whiskered bulbuls (Pycnonotus jocosus) became established in Florida when a few birds escaped while being transported from one aviary to another. This population had increased to 500 birds by 1973, at which time it was still expanding in a southerly direction. Redwhiskered bulbuls also became established in Los Angeles County, California, in 1968. Both the red-whiskered and red-vented bulbuls (P. cafer), were introduced to the Hawaiian island of O'ahu in the late 1960s. Populations of both birds have dramatically increased. Red-vented bulbuls are now found across the island, while the red-whiskered bulbul is found throughout southeastern areas. These birds are considered serious pests and threats to native bird populations.

Habitat

Forest, open woodland, gardens, and cultivated areas all constitute bulbul habitat. Essentially arboreal birds, the majority of pycnonotids live in or next to forested areas, but many are well adapted to human-made habitats. Many bulbuls show a preference for a particular level of the forest canopy. So as long as there is enough fruit and insects, a relatively small area of forest may support a large number of birds.

The majority of Andropadus species keep to the forest interior, as do many others, such as Finsch's bulbul (Criniger finschii) of Indonesia, and the African gray-headed greenbul (Phyllastrephus poliocephalus). Other species prefer more open areas and are found frequently in edge habitat. The gray-headed bristlebill (Bleda canicapilla) and the white-throated greenbul (Phyllastrephus albigularis), both found exclusively in western north-central Africa, are typically found at forest clearings and edges where there is tangled vegetation in which they can forage for insects. Pycnonotus species are well adapted to drier habitats, and are frequently found in areas that have been cultivated by humans. A few are confined to the forest, but they generally inhabit open country with scattered trees and shrubs. The yellow-throated leaf-love (Chlorocichla flavicollis) actually avoids large forest blocks, occurring mainly in brushy, more open areas. This bird also adapts extremely well to man-made habitats; and can be found in plantations, abandoned cultivated sites, orchards, parks, and gardens.

Several bulbuls show a preference for water and are found alongside rivers and forest streams. The gray-olive bulbul (Phyllastrephus cerviniventris) is one such bird. Infrequently entering the forest, this smallish bulbul frequently inhabits streamside thickets. Primarily an insect eater in Zambia, it is especially fond of feeding on logs that have fallen across streams or ravines. The swamp greenbul (Thescelocichla leucopleura) and the leaf-love (Pyrrhurus scandens) are also partial to water, both prefer swampy areas with luxuriant vegetation and palm trees, especially Raphia and the oil palm Elaeis.

Although most bulbuls prefer areas with lots of green vegetation, a small number are found in drier scrub habitats, especially Pycnonotus. The African red-eyed bulbul (Pycnonotus nigricans) occupies drier areas, including savanna, semiarid scrub, and bushy hillsides. The northern brownbul (Phyllastrephus strepitans) also prefers scrub, and is often the only bulbul present in the driest parts of its range.

Behavior

Many bulbuls are quite social; some readily join mixed-species groups, others flock with members of their own species. Perhaps the most gregarious bulbul is the spotted greenbul (Ixonotus guttatus). A distinctively colored bird, gray-olive with white spots on its wings and rump, the spotted greenbul is very social, traveling in monospecific groups of five to 50 birds. The groups work their way quickly through trees, never staying long, even if there is plenty of fruit. While briefly at rest they sit very close together on a branch, preening and flicking the wings and tail. The striated bulbul (Pycnonotus striatus), so named because of the yellow-streaking on its underparts and white-streaked upper body, lives in active noisy flocks of six to 15 birds, as does the yellow-browed bulbul (Hypsipetes indicus). The yellow-streaked greenbul (Phyllastrephus flavostriatus), Cabanis's greenbul (P. cabanisi), and Sjöstedt's honeyguide green-bul (Baeopogon clamans) often join mixed-species flocks, traveling right behind or mixed in with other bird species.

Bulbuls can be quite aggressive towards members of their own species, and other species as well. Some, such as the puff-throated bulbul (Criniger pallidus) and the mountain bulbul (Hypsipetes mcclellandii) will aggressively mob birds of prey. If the face-off is against a bulbul of the same species, the threat display may be different than against other birds. Among Pycnonotus, there are roughly three to seven threat displays. These include tail-flicking, tail-spreading, crest-raising, undertail-covert spreading, wing-flicking-and-spreading, and crouch display (the latter may also be an appeasement display). The red-vented bulbul has been observed attacking birds by poking with its bill. The red-tailed greenbul (Criniger calurus) and other Criniger bulbuls will puff out their fluffy beard-like throat feathers, both as a preening gesture and as an aggressive display.

Most bulbuls have distinctive voices, and often the best way of distinguishing similar species is by their song. All over the map, their calls may be jolly phrases of three to six notes (Pycnonotus flavescens), cacophonous explosions of loud discordant babbles (Pycnonotus luteolus), or mewing cat-like calls (Hypsipetes mcclellandii and H. leucocaphalus). Typically, their voices have a gravelly quality, many are chattery and noisy, some with whistles. Very few are actually musical. Most sing in the morning or evening, and many of the more social species will chatter as they forage. The somber greenbul (Pycnonotus importunus) constantly advertises its presence with its distinctive song, a series of clear strong notes "ti-ti-wer cheeocheeo cheeo-wer chi-wee chi-wer chi-wee." A most persistent vocalist, this bird sings all day, even at midday, and all year. The name importunus is from "importunate," named because it sings persistently to the point of annoyance.

Sadly, the species with the most celebrated song, the straw-headed bulbul (Pycnonotus zeylanicus) is now threatened as a result of being highly prized and traded for its voice. Described as "a prolonged series of magnificently warbled notes, richer and more powerful by far than the songs of such celebrated performers as the Nightingale and the blackbird," the song of the straw-headed bulbul is by no means typical of the Pycnonotidae.

The majority of the Pycnonotidae are nonmigratory, either sedentary or only locally nomadic. Banding and recapture records from Asia indicate that some bulbuls remain in the same few hundred yard area for several years. A handful of the cooler-climate, temperate-zone species, such as the black bulbul (Hypsipetes madagascariensis), are partly migratory. Flocks of several hundred of these birds move to southern China in winter.

Feeding ecology and diet

The bulbul diet spans the range of fruits and berries to insects and other arthropods, as well as small vertebrates such as frogs, snakes, and lizards. A few eat nectar and pollen. The jaw apparatus of Pycnonotids is rather generalized compared to other Passeriform birds, and while some Pycnonotids eat mainly fruit or insects, most can and do have a mixed diet. This flexibility may be critical during the dry season: since most bulbuls are non-migratory, they must take advantage of the food sources available within in their range, which can mean shifting to feeding on more plant matter when insects are not as abundant.

Among Phyllastrephus and Criniger, diets tend more toward insects such as caterpillars, dragonflies, wood lice, and ants. The diets of Chlorocichla and Hypsipetes include more fruit, and many of these bulbuls are important for dispersing the seeds of forest plants and as pollinators. Fruit-eating species typically forage in trees, shrubs, and bushes, gathering fruits and berries while perched on twigs and stems. They will often consume smaller fruits whole, and will repeatedly peck fruits with hard, thick walls until they have torn a hole in the outer coat to get at the pulp. Figs (Ficus spp.), are present in the diet of most fruit-eating bulbuls, as well as Schefflera, Musanga, and Lantana berries. These birds can do serious damage to orchards and other cultivated fruit crops. Indiscriminate in their preference for native or exotic berries, fruit-eating bulbuls often disperse noxious, weedy plant seeds.

Most insect-eating bulbuls forage on and among vegetation, but will also sally for insects in the air and hunt along the ground on fallen logs and branches. Many favor caterpillars and dragonflies, and several species have been found attending swarms of army ants. The yellow-bellied greenbul (Chlorocichla flaviventris) frequently forages on antelopes, landing on the animal and grooming its head, ears, and even eyes, presumably searching for small insects in the antelope's coat.

Although most bulbuls are omnivorous, a few specialize in certain foods. Sjöstedt's honeyguide greenbul is closely associated with the small, black wasps Polybioides melaina that build large paper nests in riverbank trees. The bird will tear apart the nests, despite the vicious retaliation of the wasps, and the young birds are fed exclusively on the wax, larvae, and pupae of the insect.

Reproductive biology

Most bulbuls are found in pairs, or in small groups that tend to be family parties and often include juveniles. Mostly monogamous and territorial, except for the yellow-whiskered greenbul (Pycnonotus latirostris), a lekking species, some bulbuls will form groups that defend a large home range together. Both the leaf-love and the swamp greenbul will gather and chorus to defend communal territory. In the case of the swamp greenbul, the loud vocalizations are accompanied by displays of spread wings and tail.

The timing of bulbul reproduction varies greatly, depending on the climate and region. In some areas breeding appears to be tied to rainfall, and many species have two broods per year, usually before and after the monsoon season. Breeding is common year-round in other species, and some African species may breed throughout the rainy season, or after the rains. Most bulbuls are monogamous and territorial, often the pair-bond is maintained year after year. One species, the yellow-whiskered greenbul, has a quite flexible social system, and in high density areas uses leks, but is monogamous and territorial in lower-density areas. There is evidence of cooperative breeding in a handful of species including, the spotted greenbul, the yellow-throated leaf-love, and Ixonotus. Groups of four to six birds will feed the young, usually both in the nest and after leaving it.

Pre-copulatory displays have been observed in some bulbuls, in which the birds chase each other while softly calling. Little is known about the selection of the nest. It is usually built by both parents, although in some cases just the female. Nests tend to be an untidy cup nestled in the fork of a tree. The construction materials vary, but usually include a variety of twigs, rootlets, plant stems, grasses, cobwebs, and hairs. Some species "decorate" the outside of the nest with fern fronds or bark strips. There are usually two eggs per clutch, although there may be as many as five, and there is great variation in the egg color and markings, even within a single species. Some eggs are elongated ovals, others truncated ovate, they may be glossy white, pinkish, lilac, gray, brown, and mauve with scratchy markings, blotches, or spots, sometimes concentrated at one end so the egg appears to be "capped." In some species both parents incubate the eggs, in others the female only, usually for 10–14 days. Young are born naked and are usually cared for by both parents. They are often just given insects at first, even among the species that primarily eat fruit. They generally fledge at 14 days, but as early as seven days in some species.

Conservation status

The primary threat to the Endangered (two species) and Vulnerable (five species) bulbuls is habitat loss, though hybridization and trapping for the caged bird trade are also problematic. The effect of destruction of habitat is especially pronounced because so many of these birds have quite restricted ranges. The Endangered streak-breasted bulbul (Hypsipetes siquijorensis) is endemic to four islands of the Philippines, and while it lives in open areas, forest in some condition appears to be essential to its survival. Forest destruction has severely affected population numbers, and although on the island of Siquijor the remaining four forest patches are now reserves, suitable protection of the rest of its habitat may be critical to its survival. Habitat loss is also a problem for the Nicobar bulbul (Hypsipetes nicobarensis), found exclusively on the Nicobar islands of India. This bird also suffers from competition with the recently introduced Andaman red-whiskered bulbul (Pycnonotus jocosus), which has flourished throughout the islands. Expansion of the Great Nicobar Biosphere Reserve would provide adequate protection for this bird, and controlling the populations of introduced species might also help. The Vulnerable Styan's bulbul (Pycnonotus taivanus), endemic to the lowlands of Taiwan, is also threatened by habitat loss. Also problematic is hybridization with the Chinese bulbul (Pycnonotus sinensis), whose range has expanded to overlap with Pycnonotus taivanus. The only genetically distinct Taiwan bulbuls left live in the coastal mountains. A protected species since 1995, captive-breeding programs and protected areas from which Chinese bulbuls are excluded have been proposed. Habitat loss is also a concern for the hook-billed bulbul (Setornis criniger), confined to the islands of Borneo, Sumatra, and Bangka in the greater Sundas, and the yellow-throated bulbul (Pycnonotus xantholaemus), found exclusively on the southern peninsula of India. Although both birds have some generic protection, preservation of suitable habitat is recommended for both.

The straw-headed bulbul (Pycnonotus zeylanicus) is now threatened as a result of being highly prized for its voice and hence traded as a caged bird. Listed on Appendix II of CITES, some measures have been taken to protect this bird, but it is still widely traded, and captive-breeding programs are subject to theft. Habitat protection might also help as long as areas are guarded.

In addition to habitat protection, the ecology and behavior of these birds must be studied further to better understand survival rates and ecological needs. Efforts to protect these birds by local governments and international groups will do little without the involvement of local people.

Significance to humans

It is not surprising that these vocal birds, many well adapted to human-made habitats, often figure in the folk-tales and songs of the regions in which they live. In each region where bulbuls are common, local lore is often associated with the more conspicuous birds. In Ghana, the noisy swamp greenbul is known as the "talky-talky bird," and children purportedly refuse to eat the flesh of these birds, for fear if they do they will never stop talking. The redwhiskered bulbul is mentioned in many local songs of the Lanna people in Thailand, and is considered a symbol of the old Lanna kingdom. Sadly, like the highly prized straw-headed bulbul, the red-whiskered bulbul is seen less and less in Thailand, as more and more are captured for the southern Thailand bird market. Known as "Nok Krong Hua Juk" (the caged bird with a crest), the red-whiskered bulbul was frequently entered in fighting contests in the early 1960s. Owners would put two of these fiercely territorial birds in a cage until one almost killed the other. In the early 1970s these contests were replaced with the less bloody singing contests, in which two caged birds are placed next to each other and both sing effusively, as though defending their territory. Although the Thai government began requiring permits for owning these birds in 1992, they are still widely traded. As recently as June 2001, 500 captured bulbuls were discovered in transport to the south of Thailand. Seen as a symbol of wealth and prestige, owning these birds has been described as a way of broadcasting the owner's status to the neighborhood, and unless attitudes surrounding their ownership change, they will continue to be captured for the caged bird trade.

Species accounts

Resources

BirdLife International. Threatened Birds of Asia: BirdLife International Red Data Book. Cambridge: BirdLife International, 2001.

Grimmett, Richard, et al. Birds of the Indian Subcontinent. London: Christopher Helm Ltd., 1998.

Hagemeijer, Ward J.M., and Michael J. Blair, eds. The EBCC Atlas of European Breeding Birds. London: T.& A.D. Poyser, 1997.

Islam, K., and R.N. Williams. "Red-Vented Bulbul (Pycnonotus cafer), Red-Whiskered Bulbul (Pycnonotus jocosus)." In The Birds of North America. 520 (2000).

Jeyarajasingam, A., and A. Pearson. A Field Guide to the Birds of West Malaysia and Singapore. New York: Oxford University Press, 1999.

Keith, S., E. Urban, and C.H. Fry, eds. The Birds of Africa. Vol. IV. San Diego: Academic Press, 2000.

MacKinnon, J., and K. Phillips. A Field Guide to the Birds of China. New York: Oxford University Press, 2000.

Brosset, A. "The Social Life of the African Forest Yellow-Whiskered Greenbull Andropadus latirostris." Z. Tierpsychol. 60 (1981): 239–255.

Cibois, A., B. Slikas, T.S. Schulenberg, and E. Pasquet. "An Endemic Radiation of Malagasy Songbirds is Revealed by Mitochondrial Sequence Data." Evolution 55, no. 6 (2001).

Dowsett, R.J., S.L. Olson, M.S. Roy, and F. Dowsett-Lemaire. "Systematic Status of the Black-Collared Bulbul Neolestes torquatus." Ibis 141 (1999): 22–28.

Narang, M.L., R.S. Rana, and P. Mukesh. "Avian Species Involved in Pollination and Seed Dispersal of Some Forestry Species in Himachal Pradesh." Journal of the Bombay Natural History Society 97, no. 2 (2000): 215–222.

Pasquet, E., L. Han, O. Khobkhet, and A. Cibois. "Towards a Molecular Systematics of the Genus Criniger, and a Preliminary Phylogeny of the Bulbuls (Aves, Passeriformes, Pycnonotidae)." Zoosystema 23, no. 4 (2001): 857–863.

Roy, M.S. "Recent Diversification in African Greenbuls (Pycnonotidae: Andropadus) Supports a Montane Speciation Model." Proceedings of the Royal Society of London B, 264 (1997): 1337–1344.

The Bird Conservation Society of Thailand. 69/12 Rarm Intra 24, Jarakhebua Lat Phrao, Bangkok 10230 Thailand. Phone: 943-5965 or 519-3385. E-mail: bcst@box1.a-net.net.th Web site:

"Zoonomen Nomenclatural Data." January 19, 2002. 18 March 18, 2002.

[Article by: Rachel Ehrenberg, MS]

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