any of the group of seabirds that includes the albatrosses (albatross) (family Diomedeidae); shearwaters (shearwater), fulmars (fulmar), prions (prion), and large petrels (petrel) (Procellariidae); storm petrels (storm petrel) (Hydrobatidae); and diving petrels (diving petrel) (Pelecanoididae). There are approximately 117 living species of diverse sizes and ranges. All Procellariiformes are recognizable by their conspicuous tubular nostrils, which project upon the culmen (upper bill). This feature gives the order its alternative name, Tubinares, meaning “tube-nosed.” The feet of the birds (bird) are webbed, and the hind toe is either vestigial or missing. All species have a characteristic powerful musky odour, which is caused by the excretion of stomach oil. The oil can be used as a defensive discharge through the mouth when the bird becomes alarmed.

General features

Importance to humans
      The tube-nosed seabirds have been of considerable local economic importance as a source of protein food, feathers (feather), and oil wherever humans have colonized or have been able to raid the coastal and oceanic islands where they breed. This situation has resulted in the partial or complete extermination locally of certain species. Humans, moreover, have been responsible for the introduction of various predators, including rats, pigs, and cats. In regions where bird populations have survived, people have continued to harvest the eggs, the plump young birds (at fledging time), or both. Many thousands of slender-billed, or short-tailed, shearwaters (shearwater) (Puffinus tenuirostris) are taken on the Bass Strait islands off Tasmania and sold fresh, salted, or deep-frozen as “muttonbirds (muttonbird).” In all likelihood, the name muttonbird was derived from the use of the flesh as a supplement for mutton by the early settlers of New South Wales. The numbers of muttonbirds now harvested are regulated so as to preserve a substantial breeding stock.

      In New Zealand the Maori people have harvested young titi (shearwaters of several species) from time immemorial, a right assured them in perpetuity by treaty with Queen Victoria. On the other side of the world, hundreds of Manx shearwaters (Puffinus puffinus) were formerly collected for food and as lobster bait on the Welsh islands of Skomer and Skokholm, which are now nature preserves estimated to contain about 200,000 Manx shearwaters and 2,000 storm petrels (Hydrobates pelagicus). On the Tristan da Cunha Islands in the South Atlantic, resident islanders harvest the eggs and squab (young) of a large mixed seabird population, which includes more than 6,000,000 greater shearwaters (Puffinus gravis).

      The harvesting of northern fulmar petrels (Fulmarus glacialis) is an ancient practice among peoples inhabiting the cool northern coasts where the birds choose to breed. In Iceland about 50,000 fulmars (fulmar) were taken annually between 1897 and 1925; however, the occurrence in 1939 of psittacosis (a virulent avian disease) among processors of the birds resulted in prohibition of the use of fulmars for food.

      During the early 17th-century colonization of Bermuda, millions of cahows, or Bermuda petrels (petrel) (Pterodroma cahow), were eaten almost to extinction by the colonists. For nearly 300 years the species was believed extinct, but in 1951 a few pairs were discovered nesting on an offshore islet, where a remnant now survives under strict protection. The related black-capped petrel, or diablotin (P. hasitata), of the West Indies was also thought extinct (because of predation by humans, rats, and mongooses) until in 1961 a substantial population, estimated to number at least 4,000 birds, was found breeding in the inaccessible forested cliffs of Hispaniola.

      In the 18th and 19th centuries, huge numbers of albatrosses (albatross) were taken for food (largely by whalers) and for the millinery trade. With the disappearance of sailing vessels, changes in fashions, and the establishment of many nesting grounds as sanctuaries, such predation has virtually disappeared, but albatrosses have not entirely escaped stress at the hands of man.

      On Sand Island in the Midway Atoll, Laysan albatrosses (Diomedea immutabilis) increased from a few pairs in 1900 to about 60,000 pairs in the early 1960s, the increase resulting from shelter provided by introduced vegetation. The use of the island by aircraft after 1935, air raids by the Japanese during World War II, and the loss of 30,000 birds humanely killed by the U.S. Navy (in a control program designed to reduce collisions between birds and aircraft) did not deter the albatrosses from this favoured nesting area. The control program was abandoned after the discovery that leveling certain sand dunes effected a 70 percent reduction in collisions by removing the updrafts near aircraft runways.

      At present, the food supply of many of the world's albatrosses is threatened by fishing fleets that overharvest critical squid populations. Albatrosses also suffer high mortality as the bycatch of unregulated longline fishing.

      The majority of procellariiforms breed in the Southern Hemisphere, but several species migrate thousands of miles north across the Equator to winter in the northern summer seas, where they molt, feed, and rest in preparation for the return home in the southern spring. Similarly, species that breed in the Northern Hemisphere also live in perpetual summer by migrating far south to winter in the southern summer. A number are less migratory and do not cross the Equator. Several species are almost sedentary, chiefly smaller petrels breeding in tropical and subtropical latitudes, and the subantarctic prions (prion) (Pachyptila) and diving petrels (diving petrel). All latitudes of the unfrozen oceans are thus occupied, but there are fewer living in the calm equatorial region, where there is little wind to lift their long wings (wing) and where the pelagic (open-ocean) crustacean food on which so many seabirds basically depend is scarce. The zone of upwelling water in the windy latitudes of the Antarctic convergence, between 40° and 60° south latitude, is richest in the shrimplike krill (Euphausia species), attracting surface-feeding tubinares and the diving penguins (penguin), prions, and diving petrels. Some feed along the edge of the ice off the Antarctic continent, and four tubinares (the Antarctic fulmar [Fulmarus glacialoides], the giant petrel [Macronectes giganteus], the snowy petrel [Pagodroma nivea], and the tiny but very numerous Wilson's petrel [Oceanites oceanicus]) actually breed on its shores. The nesting burrows of Wilson's petrel may be blocked by snow for days during the protracted breeding season. The only tubinare nesting near the ice limits in the high Arctic is the fulmar, which reaches Franz Josef Land, Greenland, and the Arctic Circle north of the Aleutian Islands.

      Of the albatrosses (family Diomedeidae), only the two Midway species and the short-tailed albatross (Diomedea albatrus) nest well north of the equatorial doldrums. The latter was brought close to extinction by plume hunters and by a volcanic eruption at its nesting island of Torishima. There were enough immature birds at sea at the time to allow a partial recovery; the rebounding population stands at over 1,800 individuals at present. About 10 albatross species range the Southern Hemisphere, gliding on the eternal winds of the “Roaring Forties” (the region between 40° and 50° latitude) and moving north with the food-rich cold currents along the west coasts of South America, South Africa, Australia, and New Zealand. One species, the waved albatross (D. irrorata), is unique in that it breeds only in the Galapagos Islands at the Equator, where probably not more than 3,000 pairs nest on Hood Island.

      The family Procellariidae includes the larger petrels, such as the northern and southern fulmars (F. glacialis and F. glacialoides), the gadfly petrels (Pterodroma), several genera of shearwaters, and the prions or whalebirds. Several of the shearwaters and larger petrels breed in burrows far inland on mountain crags in the Andes, West Indies, Madeira, and New Zealand. The largest members of this family are the giant, or stinker, petrels (Macronectes)—albatross-like scavengers and circumpolar wanderers with a heavy beak and a wingspan of 2.4 metres (8 feet). Smallest are the prions, four species of small, stocky, little-studied birds, 22 to 30 cm (9 to 12 inches) long, with broad bills and a restricted cold-water range; they breed on subantarctic islands, keeping much to the water, as do the diving petrels.

      The storm petrel family, Hydrobatidae, ranges in both hemispheres but is strongest numerically in the Pacific, where Halocyptena microsoma, the least petrel of Baja California, rivals the European storm petrel as the smallest procellariiform. The word petrel (“little Peter”) derives from a habit of the storm petrels (storm petrel) of walking on the waves.

      The diving petrels form a family (Pelecanoididae) and genus (Pelecanoides) with four species. They are small, rather sedentary, coast-dwelling birds confined to cool southern islands, including Tristan da Cunha, the Falklands, New Zealand, and southeastern Australia. Diving petrels are specialized birds with short black-and-white bodies; they closely resemble externally and in habits the small auks (auk) (family Alcidae, order Charadriiformes (charadriiform)) of the Northern Hemisphere.

Natural history

 All tube-nosed birds (bird) have a protracted life cycle conditioned by their evolution and oceanic environment. Because they spend most of their lives at sea, they are clumsy on land, laboriously using their wings (wing) as props to assist locomotion; their legs are too far to the rear to effect a well-balanced bipedal progress. The smaller species nest in burrows and rock crevices and are nocturnal, being helpless and unable to maneuver quickly on land when attacked by predators. As a rule, the incubating bird is tame and does not associate the approach of man with danger but often allows him to stroke and fondle it. Albatrosses (albatross) are especially docile—hence the name mollymawk (mallemuck), from the Dutch mollemok (“stupid gull”).

 The long-winged tubinares require a smooth runway for takeoff on a calm day; over rough ground they will utilize the bill to hook along, and either climb a rock or tree to gain a launching height or flop over the edge of the nearest cliff. On the wing, they are perfect aviators, riding out the severest storms of their normally windy oceanic feeding grounds with ease and grace. The great albatrosses can overtake and circle a fast ship at sea, with long glides rarely interrupted by wingbeats. The ability of albatrosses to move upwind without flapping depends on the fact that wind velocity is appreciably lower near the waves than a few metres in the air. The flight pattern is a series of broad ellipses that build sustaining momentum in the upper layers of air, followed by movement upwind in the lower layers of air with less wind. It then glides downwind again to gather fresh momentum. The same flight pattern may be used, of course, to travel crosswind or downwind. The normal air speed of the royal and wandering albatrosses (Diomedea epomophora and D. exulans), whose wingspans reach about 3.4 metres (11 feet), is 80 to 110 km (50 to 70 miles) per hour. Although the flight appears effortless, some energy is expended in the muscular action that keeps the long, narrow wings fully extended.

      The medium-sized shearwaters (shearwater) and petrels (petrel) have a flight pattern similar to that of albatrosses, but their shorter wings are flapped regularly between the briefer gliding periods. The little storm petrels (storm petrel) have an altogether more erratic darting, fluttering, and sometimes hovering flight, their feet hanging down to walk on the water surface.

Feeding habits
      Shearwaters, storm petrels, and diving petrels (diving petrel) feed by taking small fish and crustaceans close to the surface; they make short dives as necessary. Many of the larger procellariids consume substantial amounts of squid. Albatrosses, giant petrels, and fulmars (fulmar) dive little; they are surface feeders, often settling on the water. At night they devour squid that rise to the surface; during the day they take schooling fish; garbage from ships; wounded, exhausted, or dead birds; and carrion, including the flesh of dead whales and other cetaceans. The giant petrel is probably the only tubinare agile enough on land to kill other birds; at its nesting grounds it will attack young penguins (penguin) inadequately guarded by their parents.

Reproduction and growth
      As a general rule, the mature adults return to the established breeding site many weeks before the single white egg is laid. There is often severe competition for nesting territories in large crowded colonies on small islands. Returning each year to the same nest site, the male and female remain faithful to it and thus to each other for life. It is believed that some albatross pairs also remain together at sea in the nonbreeding season. In contrast, many of the burrowing shearwaters and petrels, meeting on land only at night, may never see their mates clearly when ashore (recognition being by voice, touch, and possibly smell) and probably do not deliberately consort in pairs at sea.

      At each fresh encounter ashore between breeding birds, there is an elaborate greeting ceremony; the birds clash and fence with the bills, cackling and screaming. These antics occur in both the nocturnal procellariids and the diurnal albatrosses, and in the latter there is also a bowing and dancing display. Such behaviour provides time for mate recognition and relieves and displaces any natural aggression or fear.

      The nest type varies somewhat among species. Albatrosses scrape a shallow depression or build a mound of soil and vegetation; the fulmars and other diurnal petrels nest on ledges or on level ground; most shearwaters, diving petrels, and some storm petrels dig burrows in soft soil; other storm petrels utilize natural crevices.

      Once the nest site has been adopted, one member of the pair usually remains on guard against usurpation by other birds that are still in search of a suitable nest site. The male may remain on guard for several days and nights, while the female feeds at sea in order to meet the nutritional requirements of the developing egg. In some species the female may depart on a recuperative feeding cruise within a few hours after laying if her mate is there to take over incubation. Mated birds do not feed each other; instead they incubate for periods of several days each, the bird at home fasting and losing weight while the bird at sea is feasting and fattening.

      The egg is incubated for a long period, about 80 days in the wandering albatross, 52 days in the Manx shearwater, 40 days in the smallest petrels (the last about equal to the incubation period of the ostrich). For the first week or so after hatching, the helpless downy chick requires the warmth of the parental body for survival. During this period it is brooded and fed tenderly on an oily broth of semidigested marine organisms pumped from the adult esophagus, which is muscularly constricted to control the flow to the infant's needs. Instinctively, the chick seeks the open, warm, fishy-smelling mouth of the parent, thrusting and groping blindly with its tiny bill crosswise in the open maw of the adult.

      The down grows rapidly; a second down sprouts (to which the first remains attached), and the baby is soon homeothermic—that is, able to keep itself warm while its parents forage far at sea and return with increasingly large crop loads of food. Some of the fishing trips of the parents are real voyages, involving absences of several days; the Manx shearwater may travel nearly 1,000 km (more than 600 miles) from Wales to the Bay of Biscay and back to load up with its favourite food, sardines. Albatrosses may leave their well-developed nestling for a week or two. If both parents happen to return at the same time, the nestling may ingest food equal to its own weight in one meal. It becomes very fat in the later stages of the long fledgling period, which is not less than two months in the small petrels and reaches nine months in the largest albatrosses.

      Before it leaves the nest, the chick is deserted by the parents, who retire to molt at sea. This begins a starvation period, which may last a week in the smallest petrels, 12 days in the medium-sized shearwaters, and considerably longer in the largest species, before the fledgling goes to sea. When deserted, it is well-feathered and fatter and heavier than the adult; it needs a period of thinning and exercise before it is capable of flight. After days of fasting and wing flapping, it may become airborne one windy night, especially if hatched in a burrow on a gale-swept mountain height from which it can flap and glide to the sea. Calm weather is its enemy; many island-born young tumble down to the sea, too heavy to take off again in still air. They are expert swimmers, however, and can dive deeply to avoid attacks by aerial predators.

      Rapidly paddling away from the dangers of land and soon gaining flight, the young procellariiform sets off along the traditional migration route, alone and unguided by the long-departed adults. Driven by an innate impulse to keep flying, it reaches winter quarters that it has never seen before, often at a surprising speed. One Manx shearwater, banded in Wales as a fledgling, travelled 9,900 km (about 6,200 miles) to southern Brazil in 16.5 days. Allowing half of each day for resting and feeding, this is equivalent to an average surface speed of 50 km (30 miles) per hour over the period, a remarkable achievement for a bird just out of the nest.

      The young albatross remains longest in the nest—so long in the case of the royal and wandering albatrosses that the nestling is overtaken by the Antarctic winter. It endures blizzards and savage winds that force it to grip the nesting mound tightly with its claws, yet it is warm enough under its oily plumage to survive fasting for many wintry days until a parent appears with food. Because of the protracted nesting period, these great albatrosses cannot rear more than one young every other year. To compensate for the slow rate of reproduction, albatrosses are long-lived; life expectancy, once breeding age is reached, appears to be several decades. Marking of Laysan albatrosses has shown that they do not breed successfully until seven years old. In order to maintain their numbers, the wandering and royal albatrosses, breeding for the first time even later, must have the highest average longevity among birds. The Manx and other medium-sized shearwaters lay the first egg when five years old, and the least petrel does so in the third or fourth summer.

      There is always a large proportion of each tubinare population that is nonbreeding. During its first year at sea, the young bird may not even approach the land. While the mature birds have completed their migration and settled to breed at home, the yearlings may lag far behind on the route, spending the summer at sea. In the next few years, adolescents arrive at the breeding islands and shores too late to make more than a preliminary landing and exploration of the ground for a future partnership. At midsummer in the nesting colonies, there is a considerable arrival of immature birds familiarizing themselves with prospective breeding territories. Where a colony is already overcrowded, it is always the young eligible but inexperienced birds that leave to form new peripheral colonies in the region of their birthplace.

Form and function

General features
 The general body plan of procellariiform birds (bird) varies from family to family. In general, they are long-winged, short-necked birds with short to moderate tails and legs. Webbing is present between the front toes, and the hind toe (hallux) is small or lacking. In contrast to their strong-flying relatives, the diving petrels (diving petrel) have short wings (wing). At the other extreme, the aspect ratio (the ratio of wingspan to the chord, or width) of the wing may exceed 14:1 in some albatrosses (albatross). This long narrow wing with a high-lift airfoil is an extreme adaptation for fixed-wing gliding.

      The bill (beak) varies from rather short and broad in diving petrels to medium in length (somewhat more than half the total length of the head) in some albatrosses. It is sheathed in horny plates and has a distinct hooked nail at the tip. In albatrosses the two nasal tubes lie separated on the right and left upper lateral surfaces of the bill. In all other procellariiforms the nostrils are fused into a single tube lying on the dorsal midline of the bill. In this single-tube arrangement, a dividing wall or septum, which may end short of the end of the tube, results in a single opening.

      Procellariiforms are totally lacking in bright plumage colours, being entirely black, white, or shades of brown or gray. Strikingly contrasting patterns of light and dark are often found, however, and the bills or feet of a few species are yellow or pink. A number of shearwaters (shearwater) and procellariid petrels (petrel) and a few albatrosses are polymorphic (polymorphism); that is, they occur in light and dark phases (plumage types). Some species also have intermediate forms. The polymorphism may be restricted to certain parts of the plumage, such as the underparts of the body or the upper surface of the wings.

Stomach oil
      Most tubinares, when handled or threatened, eject the oily contents of the stomach with some force. In some species, notably the cliff-nesting fulmars, this habit, a fear reaction that also serves to lighten the bird for flight, has been exploited as a defensive weapon. Facing an intruder, the disturbed bird ejects a spurt of foul-smelling fluid a metre or so in his direction, often with apparently planned accuracy. The habit is instinctive; a baby fulmar, on hatching, has been observed to squirt yellow oil before it is fully out of the shell. Later the downy chick squirts oil at any visitor, even its parents. Mated fulmars may exchange little squirts of oil during the excitement of bill-fencing ceremonies.

      Analysis of this unique oil shows that it is a waxy secretion of the proventriculus (the first chamber of the stomach), rich in vitamins A and D. In most birds the walls of the proventriculus produce an acid fluid that rapidly breaks down raw food entering from the esophagus. In the tubinares, which feed their young a soup of predigested marine organisms, the proventriculus is much enlarged and internally folded, increasing the surface when dilated and enabling a larger number of glands to function. The latter are groups, or follicles, of oil-producing cells. The colour of the oil varies according to the type of food; it is often reddish from the presence of astacin, a pigment found in crustaceans.

      The discharge of stomach oil is partly excretion of surplus fat, which might upset the bird's metabolism if retained in quantity. Ejected through the mouth and nose, it also disposes of excess vitamins and salt in the diet of marine food and seawater. Similar in character to the secretions of the oil glands of other birds, the crop oil may also assist in waterproofing the feathers (feather) as the tubinare preens its plumage with its oil-stained bill.

Evolution and paleontology
      The oldest tubinare fossil is a giant albatross (Gigantornis) from the Eocene Epoch (about 50 million years ago) of Nigeria. It may have had a wingspan of 6 metres (20 feet) and was contemporary with the now extinct giant penguins (penguin) (order Sphenisciformes). It is generally agreed that the two orders had a common ancestor from which they may have evolved. The penguins occupied the ecological niche of diving and feeding under the surface and became flightless; the tube-nosed seabirds specialized in flight and surface feeding. Support for a common origin comes from the facts that the oldest fossil penguin had a bill with distinct tube-nosed apertures; the young of the blue penguin Eudyptula, considered to be the most primitive of penguins living today, exhibits tubelike openings to its nostrils. Mutual displays of bill fencing and wing movements in courtship, as well as the method of regurgitating digested food, are almost identical in tubinare and penguin. The short-winged diving petrels (petrel), which “fly” much underwater but little in air, seem to parallel an early stage in the evolution of penguins, especially during a few weeks of the annual molt when they lose their quills and must live in the water.


Distinguishing taxonomic features
      The families of the Procellariiformes are separated mainly by the general body plan, the condition of the nostrils, and, in the case of the Procellariidae and Hydrobatidae (long considered one family), the osteology of the skull and sternum. At the genus level, characters used include the shape of the beak, wings, and tail; the degree of flattening of the tarsus (lower leg); size of the hallux; and the relative lengths of the leg bones.

Annotated classification
Order Procellariiformes (tubinares)
 Oceanic birds with tubular nostrils; bill covered with horny plates and hooked at the tip. Anterior toes webbed; hallux short or lacking. Wing with 11 primary feathers (the outer minute); secondaries short; diastataxic (that is, with the 5th secondary absent). 2 coats of nestling down. Oil gland feathered. Strong musky smell. Single white egg; long incubation and nestling periods. 4 families, about 25 genera, some 117 living species; all marine; worldwide.
      Family Diomedeidae (albatrosses (albatross))
 Middle Eocene to present. Extremely long, narrow wings; short tail. Bill longer than remainder of head; nostrils semitubular, small, situated near the base of long groove. Length 50–125 cm (20–50 inches); wingspan to 3.4 metres (11 feet). 4 genera and about 14 species; North Pacific and all southern oceans.

      Family Procellariidae (large petrels (petrel), fulmars (fulmar), prions (prion), shearwaters (shearwater))
 Middle Oligocene to present. Long-winged, short-tailed. Nostrils united on top of bill. Length 22–75 cm (9–30 inches). 14 genera, 78 species; all oceans, but greatest diversity in Southern Hemisphere.

      Family Hydrobatidae (storm petrels (storm petrel))
 Late Miocene to present. Small black and brown birds, usually with conspicuous white rump; wings rounded; tail square or forked. Length 15–20 cm (6–8 inches). Often walk on water. 7 genera, 21 species; all oceans, but more species breeding in Southern Hemisphere.

      Family Pelecanoididae (diving petrels (diving petrel))
 Late Pleistocene to present. Small stocky birds with short wings and tails. Black above, white below. Length 16–20 cm (6.5–8 inches). 1 genus, 4 species; cool subantarctic seas.

Critical appraisal
      In a system positing evolutionary relationships on the basis of structural affinities, the tube-nosed seabirds seem to fit conveniently between the penguins (penguin) and the pelecaniform birds. Nonetheless, some authorities classify procellariiforms as a subset of order Ciconiiformes (ciconiiform) (the storks and similar birds). In addition, the species taxonomy of tube-nosed seabirds has an extremely unsettled history largely because of the lack of morphological characters to distinguish or relate isolated populations. At present, long-standing debates are being resolved with the help of DNA analyses and critical comparisons of remote and poorly known species.

R.M. Lockley

Additional Reading
R.M. Lockley, The Island (1969, reissued 1980), includes life histories of Manx shearwaters and storm petrels and the results of homing experiments, and Man Against Nature (1970), describes New Zealand tubinares and muttonbirding. Other notable works include W.B. Alexander et al., “The Families and Genera of the Petrels and Their Names,” Ibis, 107:401–405 (1965), a taxonomic reorganization of the order Procellariiformes; P.E. Davis, “The Breeding of the Storm Petrel,” British Birds, 50:85–101, 371–384 (1957), a follow-up of an earlier study by Lockley; James Fisher, The Fulmar (1952, reissued 1984), a classic monograph; William Jameson, The Wandering Albatross (1958), a readable account of the biology of the largest albatross; R.M. Lockley, Shearwaters (1942, reissued 1961), another classic monograph; M.K. Rowan, “The Greater Shearwater Puffinus gravis at Its Breeding Grounds,” Ibis, 94:97–121 (1952); J. Warham, “The Biology of the Giant Petrel Macronectes giganteus,Auk, 79:139–160 (1962); and D.B. Wingate, “Discovery of Breeding Black-Capped Petrels on Hispaniola,” Auk, 81:147–159 (1964).R.M. Lockley Ed.

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Universalium. 2010.

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