Passeriformes

(Perching birds)

Class Aves

Order Passeriformes

Number of families Approximately 74

Number of genera, species Approximately 1,161 genera and 5,700 species

Evolution and systematics

With more than 5,700 species—approximately 59% of the total number of bird species—passerines make up the single largest order of birds in the world. Indeed, many researchers roughly divide all birds into two major categories: passerines, and everything else.

Other than the large size of the order, however, there is very little that can be generally said about passerines. Members of this species-rich order are usually small, morphologically uniform, terrestrial birds that eat mainly seeds, fruit, nectar, and/or insects. Australian lyrebirds (Menura) and ravens (Corvus corax; weight approximately 60 oz [1,700 g]) are the largest members of the order, and bushtits (Psaltriparus) and pygmy tits (Psaltria exilis) are the smallest.

Nearly all taxonomists agree that Passeriformes are monophyletic, meaning they share a common ancestor, but beyond that there is little agreement about the evolutionary history and genetic relationships of this order. Robert J. Raikow defines the group with five derived characters: a wing tendon architecture that is unique; except in one genus (Conopophaga), a distinctive palate called "aegithognathous"; unique, bundled sperm structure; and a highly specialized foot and leg that facilitate perching, with a large hallux (rear toe) that is specially arranged, deep plantar tendons, and simplified foot muscles. Researchers agree that these characters are unique to the order, but some also cite other, traditional morphological features as defining the group. These features include, among others, the arrangement of the toes (anisodactyl, or three toes forward, one toe pointing rearward), an incumbent (non-elevated), independently acting hallux, and distinctive syringeal architecture. Raikow, however, claims that all these features are more general within birds as a whole, and therefore not useful for establishing passerine monophyly.

DNA analysis may prove to be a critical tool for defining the phylogeny, or genealogical relationships, among birds, especially in the case of subdivision of the order. Except for the architecture of the syrinx and feet, passerines are remarkably similar in morphology. Differences in the syrinx have allowed for two generally recognized suborders, Tyranni (suboscines) and Passeri (oscines). However, beyond these large suborders, classification has been extremely problematic. Convergent and parallel evolution has produced structural features and behaviors that are remarkably similar in birds that are, in fact, not closely related. However, divergent features have evolved in some species that are closely related. As a consequence, many species and genera have been traditionally, but possibly incorrectly, grouped together in families on the basis of similar morphologic features. Charles Sibley, Jon Ahlquist, and Burt Monroe have proposed a reorganization of passerines, particularly oscines, using DNA hybridization techniques. However, though these techniques promise to provide additional insight into these relationships,

it may still take some time before passerine systematics are fully understood.

Fossil record

Although Passeriformes fossils are well represented in the Miocene, there is little in the way of a fossil record for the first passerine species. The oldest known fossils of passerine origin were two bones found in Upper and Uppermost Oligocene strata in France.

There are two competing hypotheses for the time and place of origin of the passerines. The paucity of fossil evidence for passerines prior to the Oligocene and the presence of numerous early fossils in the Northern Hemisphere are used to support the hypothesis that passerines arose in Laurasia sometime after the Cretaceous extinction. However, techniques using DNA molecular clock interpretations suggest that passerines may have had a southern, Gondwanan origin in the Early Cretaceous. According to some researchers, the primitive suboscines originated from early passerines in Gondwana when South America separated from Africa. This is a hypothesis that is strongly supported by the overwhelming number of passerines found in South America today, where there are more than 3,000 species.

Suborders Tyranni and Passeri

In spite of the many confusing relationships within the order, there is still a great deal of information that is known about the phylogeny of passerines. The two broadly defined suborders, oscine and suboscines, are rather easily separated, primarily on the basis of differences in the architecture of the syrinx, the special structure that birds use to produce sound.

In oscines, the so-called songbirds, there are more than three pairs of intrinsic syringeal muscles, while the more primitive suboscines have much less elaborate musculature. In spite of the complexity of the oscine syrinx, however, the musculature is very uniform throughout the suborder, which strongly suggests a monphyletic relationship among the species. On the other hand, the syringes (plural of syrinx) of suboscines are much more variable in design, and monophyly is suggested by a unique middle ear ossicle design that is highly uniform among suboscine species.

The complexity of the syrinx, as well as the fossil record, suggests that oscines are more evolved than primitive suboscines. In fact, oscines are considered to be among the most advanced of all bird species. As a result, they are traditionally placed at the very end of taxonomic lists of avian orders.

Three groups of birds, New Zealand wrens (Acanthisittidae), Australian lyrebirds (Menuridae), and scrub-birds (Atrichornithidae), are highly problematic when it comes to classification. Prior to 1975, these were considered to be suboscine, however, some later researchers placed them in the oscine suborder. Given the primitive nature of these birds, however, this has not been entirely satisfactory, with some researchers suggesting that they should be placed in separate suborders.

Tyranni (suboscines)

old world suboscines The most primitive suboscines (excluding the controversial New Zealand wrens) belong to three families found in the Old World: broadbills (Eurylaimidae), pittas (Pittidae), and asities (Philepittidae). Broadbills are brightly colored, arboreal, insectivors, and frugivorous birds that occur in Africa and Asia. Pittas are brightly colored, chubby, ground-dwelling carnivores found in Asia, Maylaysia, and parts of Africa and Australia. Asities resemble pittas in size, shape, and coloration, and feed on nectar and insects.

new world suboscines New World suboscines are often subdivided into two superfamilies, the Furnarioidea (ovenbirds, antbirds, tapaculos, and woodcreepers) and the Tyrannoidea (flycatchers, sharpbills, plantcutters, cotingas, and manakins). This subdivision as a formal classification is controversial, though it is not in dispute that these two groups, informally at least, represent two major radiations of South American passerines.

Tyrant flycatchers, the largest family in the suborder with more than 300 species, have a number of different body shapes owing to the diversity of their feeding strategies. Cotingas are medium-sized frugivores with broad bills. Manakins, also broad-billed frugivores, are small, with stubby tails and wings.

Passeri (oscines)

Passeri, or songbirds, make up about four-fifths of the passerine order with anywhere from 4,100 to 4,500 species. Although extensive adaptive radiation of oscines has produced a wide variety of ecotypes, the morphological features that are used for classification in this order are very uniform, making it difficult to assign them to families and genera with certainty. Many researchers have adopted Sibley's and his colleagues' classification of oscines, though more work will undoubtedly refine the systematics even further in the future.

Sibley and Ahlquist, using DNA hybridization, have subdivided Passeri into two broad groupings, the parvorders Corvida and Passerida, each further subdivided into three superfamilies. The parvorder Corvida consists of crows and allies, further subdivided into in the superfamilies Menuroidea, Meliphagoidea, and Corvoidea. The sister group Passerida consists of Muscicapoidea (thrushes and allies), Sylvioidea (sylvoid oscines and allies), and Passeroidea (oscine weavers and allies).

Physical characteristics

In spite of the very large size of the order Passeriformes, the exceptionally large distribution, and the diversity of life histories, there are some physical characteristics that most or all of the species share. Passerines are generally small in size (exceptions being the corvids and lyrebirds), with large wings relative to their total body mass, and all possess unique sperm. Two of the most notable physical features of the group, and the reasons they are commonly called songbirds or perching birds, are a distinctive syrinx and highly specialized feet and legs.

The syrinx is found at the junction between the trachea and the two primary bronchii and is responsible for the vast range of vocalizations in birds. When air passes across two thin, clear membranes—the internal tympaniform membranes, located on either side of the junction—the membranes vibrate and produce sound. Some birds are restricted to very simple sounds like grunts or hisses because they lack muscles to control the action of the syrinx. In birds that produce more complex sounds, such as the melodic sounds we call songs, there are special muscles to control the action of the syrinx. In passerines, especially oscines, these are highly developed and include up to six pairs of intrinsic syringeal muscles as well as two extrinsic muscles.

Although the anisodactyl foot is the most common design among birds and is not unique to passerines, the design is most commonly associated with the so-called perching birds. Anisodactyl feet evolved in arboreal species for the purpose of gripping tree branches, but modern passerines use them to

exploit all kinds of environments in addition to trees, such as grasses, telephone and fence wires, feeders, or anything that offers a place to perch. Structure of the anisodactyl foot is non-webbed and consists of toes two to four pointing forward, or anterior, and the large toe, the hallux, pointing rearward, or posterior. This arrangement differs from some other non-passerine perching birds such as woodpeckers, cuckoos, trogons, and owls that have zygodactyl feet (two toes forward and two toes rearward).

The hallux of the passerine foot is incumbent, or non-elevated. (The elevated hallux is commonly found in ground-dwelling birds rather than tree dwellers, and is usually reduced in size.) When the bird sits, deep tendons in the leg and foot flex and the large, opposable (independently moving) hallux of passerines enables the foot to automatically grasp the perch, effectively fastening the foot to the perch. Birds are thus able to sleep while perched. When the tendons are relaxed, for instance when a bird rises up from the sitting position to fly, the hallux releases and the grip is opened.

Although the specialized foot is uniform among Passeriformes species, the rich diversity of bills of passerines truly demonstrates how extraordinarily successful these birds have been at exploiting virtually any available ecological niche on land. For birds, the size and shape of the bill are functional morphologies that reflect the diet of individual species. Bill morphology is tremendously variable within Passeriformes. Their widely diverse diet has produced a variety of different

bill types that ranges from tiny, needle-like bills of insecteating warblers and vireos, to the generally massive, vise-like bills of finches, designed to crack the hard shells of seeds.

Isolated islands provide a wonderful breeding ground for speciation, or variability that arises from a single ancestor species. Another example of the rapid speciation that occurs under these conditions is found in the case of the Hawaiian honeycreepers, family Drepanididae. In the case of the honeycreepers, the many small mountains and valleys of the Hawaiian Islands have created small pocket environments that have allowed the finches to evolve from a single, primitive ancestral finch into several divergent species, a process called allopatric speciation. These birds also provide us with an excellent example of convergent evolution as some species of these finches evolved bills that mimic bills of the true honeycreepers of Central and South America.

Distribution

Passerines have a phenomenally widespread distribution and can be found on all continents except Antarctica. The historical distribution of passerines is somewhat unclear, though most researchers believe the order originated in the Southern Hemisphere, possibly in the Cretaceous. Fossil evidence for the first, primitive suboscines exists only from the early Tertiary. Sometime during the Middle Miocene, an explosive adaptive radiation occurred in which passerines quickly established their modern distribution patterns.

Old World suboscine birds (Pittidae, Eurylaimidae, and Philepittidae) occur in tropical Africa and Asia, including the Philippines and Sumatra. New World suboscines in the sub-order Tyranni are found in Central, South, and North America, Africa, Asia, Australia, New Zealand, Madagascar. Oscines are found throughout the world.

Habitat

Given the large numbers and diversity of Passeriformes, it is not at all surprising that they have managed to exploit a variety of habitats and ecological niches, far more than any other order of birds. They are found in grasslands, woodlands, scrublands, forests, deserts, mountains, and urban environments, and in arid to wet, temperate to tropical climates. In short, almost anywhere there is habitat without a permanent snow cover, one or more established passerine species can be found.

It is difficult to describe a typical habitat for passerines. Old World warblers, which consist of more than 350 species in the family Muscicapidae, can be found in virtually all terrestrial habitats. In general, however, passerines are arboreal birds that can be found in any woodland and forest setting. Also, there are numerous species that are found in what could be called atypical habitat, though they are certainly common enough within the order. These include species like the savannah sparrow (Passerculus sandwichensis), a bird of the grasslands, or the rock wren (Salpinctes obsoletus), a musical songbird that prefers to make a nest in the crevices provided by a rocky landscape.

Behavior

If a general behavior exists that can be associated with Passeriformes, it would probably be their complex, even melodic vocalizations. The physical differences in suboscine and oscine syringes have been discussed above, and primarily center on the architecture of the musculature. However, the differences between the two suborders extend beyond the physical characteristics of the syrinx. Oscines, in general, have more complex vocalizations than suboscines, and tend to learn their song repertoires through mimicry. There are three ways in which avian song can be acquired: through learning, inheritance, and invention. All birds have an innate ability to vocalize, although non-passerines, except for parrots and their relatives (Psittaciformes) and hummingbirds (Apodiformes), do not possess the ability to learn song. But even within passerines, learning of song repertoires tends to be more of an oscine specialty.

Passerines also make great mimics: 15–20% of the order practice some form of vocal copying. Many songbirds will listen to the songs of competing males within their own species and then incorporate parts of those repertoires into their own. Several species are famous for their accomplished mimicry, including northern mockingbirds, bowerbirds, European starlings, Australian lyrebirds, and scrub-birds. These birds are also capable of copying the sounds of insects, frogs, and mechanical sounds.

Feeding ecology and diet

Passerines, being generally small to medium-sized, have a high basal metabolic rate. Consequently, passerines need to feed often, and on a high-energy diet in order to maintain their energy reserves. Their diet, as a whole, is as diverse as the order.

There is a wide variety of feeding strategies among passerines, and these can range from the gleaning of insects from bark by creepers, to the hawking of insects by flycatchers, and to the specialized seed eating by the finches. Many species are highly opportunistic, like the truly omnivorous Corvidae, that have been known to feed on anything from carrion to potato chips.

Most species eat their food as they find it; some, however, will store their food for later consumption. Shrikes have a particularly unusual strategy for storing food. They impale prey, which are usually insects, but also small birds or lizards, on a thorn or barbed wire. This unusual practice has earned them the rather gruesome nickname of "butcher bird."

Dippers, so named for their habit of bobbing up and down while perched on a rock, are truly odd passerines in both their feeding ecology and habitat. Though they are undisputedly oscines, dippers qualify as water birds rather than land birds because they forage on aquatic invertebrates. With their stubby wings, thick down, strong legs and toes, and specialized eyes that can see both above and below the water, dippers are uniquely designed to walk or swim along the bottoms of fast-flowing streams and rivers.

Reproductive biology

All passerines are altricial, which means that they are born naked, blind, and completely helpless, making them totally dependent on the parents for food. Chicks grow very rapidly, however, and fledge between eight and 45 days.

Altricial eggs are small, and usually colored or otherwise marked. There are anywhere from one to 16 eggs in passerine clutches and incubation usually lasts around 14 days, but can last up to 28 days in some large species, and up to 50 days in lyrebirds. Some passerines are indeterminate layers, that is, they are capable of replacing eggs that are lost or destroyed.

Passerines as architects and builders

One of the great mysteries in ornithology has been the question of why there are so many passerines in the world. One interesting hypothesis looks to another example of rich passerine diversity, the nest, as a possible explanation. Some researchers believe that a remarkable ability to build elaborate nests out of a wide variety of materials and, in many cases, the skill to camouflage them coupled with the ability to utilize a diversity of nest sites, has provided passerines with a decided evolutionary advantage over non-passerines.

Passerines, more than any other group of birds, are no-table for the diversity and architectural complexity of their nests. Nicholas Collias has suggested that the incredibly rich diversity of modern passerine nests stems from only three nest types utilized by the earliest members of the order: hole nests, nests open above, and domed nests with constructed roofs. Modern passerine nests are all variations on these three nest types, but they range from relatively simple to highly elaborate. Although other bird species may also utilize these types of nest structures, species of Passeriformes have done so with unparalleled frequency. The domed nest, in particular, is found with much more frequency among passerine birds than among non-passerines.

There is such an incredible diversity of nest structures among the Passeriformes that it is impossible to discuss any of one type as being passerine in nature. A few, non-open nests, however, are worth noting simply for their ingenious architecture. Oscines, especially, are known for their remarkable nest structures. In particular, weavers (Ploceidae) are certainly among the champions of building nests. Most passerine nests are constructed from grass and twigs and have some sort of coherence because the nest material interlocks. But the weavers take this construction technique to a level that is unmatched by any other family of birds by literally weaving or stitching grass blades into a grass "fabric" that becomes the walls and floor of the nest.

Though there are more than 100 species of weavers, there are essentially only four nest shapes that are utilized: globular, kidney-shaped, retort-shaped with a funnel-shaped entrance, and retort-shaped with a much longer, hanging tunnel entrance. Construction of a weaver nest is a highly ritualized, six-stage event. It begins with knotting grass to form clumps on two separate, vertical stems or twigs, and then proceeds through constructing a ring between the two clumps, building up the roof and walls, adding a floor, and reinforcing the walls and floor. Finally, a platform is added.

Ovenbirds (Furnariidae) are also well known for their elaborate nests. With more than 200 species, there are numerous variations on the nest structure. Although they are all domed, nests range in design from excavated burrows in stream banks, to adobe-like ovens, to virtual avian mansions with many rooms. The most studied ovenbird, the rufous hornero (Furnarius rufus) of southern and central South America, builds the type of nest for which the family is named. A heavy, domed structure built of clay, the nest closely resembles the primitive clay ovens that are common throughout Latin America. The oven-like nest consists of an antechamber, or vestibule, that is separated by a wall from another room in which the eggs reside. The nest is around 9 in (23 cm) tall and a little bit wider at the base, with walls about 1 in (2.5 cm) thick. Horsehair, fibrous rootlets, and cow dung are common materials used as binders for the mud used to shape the walls. The nest is usually built on top of some other structure such as a fence post or roof, and away from the ground. In spite of being nearly indestructible when construction is complete, birds build new nests each year and abandon the old ones. However, Skutch reports that if a pair of birds particularly likes a site, it will build a second, or sometimes even a third, nest on top of the first.

Swallows and martins (Hirundinidae) also build nests of mud, often in association with humanmade structures. These nests are generally small, and may be cup-shaped or retort-shaped. Construction of the nests is sturdy enough that they may be used for many years.

Though the architectural diversity of the passerine nest certainly may have contributed to the enormous radiation of the order, nest site selection has played an equally important role. That many species are opportunistic in site selection probably has increased species survival. The wren family (Troglodytidae) illustrates both the diversity of nest types as well as the variety of sites. Cactus wrens (Campylorhynchus brunneicapillus) bury their football-shaped globular nests deep inside the thorns of cacti to discourage predators. Rock wrens (Salpinctes obsoletus) build their nest in holes in the ground, the crevices of rocky outcrops, or similar small shelters. Nests are usually cup-shaped structures, made of grasses, rootlets, or bark, and lined with finer materials like animal hair or spider webs. House wrens (Troglodytes aedon) also make small, cup-shaped nests, but evidence of their creativity in site selection appears in photographs showing a house wren nest tucked inside an unusual human-made item such as an old shoe or flowerpot. Nests are sometimes constructed for purposes other than brooding. Male wrens will occasionally build several decoy nests in their territory, believed to discourage predators searching for eggs.

Verdins (Auriparus flaviceps, family Remizidae) are scrappy little birds of the North American desert Southwest, also known to build several nests each year, some of which are used for hibernating during winter months. A separate nest is used for brooding.

Other structures built by birds are unrelated to either brooding or sleeping, and these might be the oddest of all. Bowerbirds (Ptilonorhynchidae) of Australia and New Guinea are, as a group, uniformly plain-looking birds. This has not, however, been an insurmountable problem for male bowerbirds that have turned to constructing elaborately decorated bowers, or secluded retreats, in order to attract and court females through visual stimulation. Gill reports that some researchers seem to have identified an apparent relationship between the absence of showy plumage and the ornate, somewhat fussy constructions fashioned by bower males. It seems that the plainer the plumage of the species, the more exquisitely bedecked the bower. Bowers come in two types: simple to complex mats of sticks built around a slender sapling, called maypole bowers, and bizarre tower structures that line the south side of a display court, called avenue bowers. The bowers, and the paths leading up to them, might be embellished with bright objects like fresh flowers (live orchids are popular), feathers, blue berries, yellow leaves or straw, or even, if the opportunity arises, shiny humanmade objects like coins or car keys, stolen from nearby camps. The importance of the decorations to some species cannot be underestimated. Some adornments are so highly prized that competing males often steal them from other bowerbirds in order to use them for their own structures.

Towers and mats are also often painted by the bowerbirds with shredded grass or charcoal dust and saliva or pulp from fruits. Bowerbirds are very particular about the arrangements of these decorations and will quickly tidy up anything that has been disturbed. Wilted flowers and leaves also are discarded and replaced on a daily basis.

Resources

Books

Brooke, M. "Order: Passeriformes." In The Cambridge Encyclopedia of Ornithology, edited by M. Brooke, and T. Birkhead. Cambridge: Cambridge University Press, 1991.

Catchpole, C. K., and P. J. B. Slater. Bird Song: Biological Themes and Variations. Cambridge, Cambridge University Press, 1995.

Ehrlich, P. R., D. S. Dobkin, and D. Wheye. The Birder's Handbook. Cambridge: Cambridge University Press, 1995.

Feduccia, A. The Origin and Evolution of Birds. 2nd ed. New Haven: Yale University Press, 1999.

Gill, F. B. Ornithology. 2nd ed. New York: W. H. Freeman and Company, 1995.

Short, L. L. The Lives of Birds. New York: Henry Holt and Company, 1993.

Sibley, C. G., and J. E. Ahlquist. Phylogeny and Classification of Birds. New Haven: Yale University Press, 1990.

Sibley, C. G., and B. L. Monroe Jr. Distribution and Taxonomy of Birds of the World. New Haven: Yale University Press, 1990.

Skutch, A. Antbirds and Ovenbirds. Austin: University of Texas Press, 1996.

Periodicals

Bledsoe, A. H. "Nuclear DNA Evolution and Phylogeny of the New World Nine-primaried Oscines." Auk 105 (1988): 559–571.

Collias, N. "On the Origin and Evolution of Nest Building by Passerine Birds." Condor 99 (1997): 253–270.

Conway, C. J., and T. E. Martin. "Evolution of Passerine Incubation Behavior: Influence of Food, Temperature, and Nest Predation." Evolution 54, no. 2 (2000): 670–685.

Cracraft, J. "Avian Evolution, Gondwana Biogeography and the Cretaceous-Tertiary Mass Extinction Event." Proc. Royal Society London, Series B 268 (2001): 459–469.

Olson, S. L., R. J. Raikow, and A. H. Bledsoe. "Why So Many Kinds of Passerine Birds?" BioScience 51, no. 4 (2001): 268–70.

Raikow, R. J., and A. H. Bledsoe. "Phylogeny and Evolution of the Passerine Birds." BioScience 50, no. 6 (2000): 487–499.

Sheldon, F. H., and D. Winkler. "Nest Architecture and Avian Systematics." Auk 116, no. 4 (1999): 875–877.

Susan L. Tomlinson, PhD