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Procellariiformes

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Procellariiformes
Temporal range: Eocene–Present Possible Late Cretaceous record
Buller's albatross (Thalassarche bulleri)
Scientific classification Edit this classification
Kingdom: Animalia
Phylum: Chordata
Class: Aves
Clade: Austrodyptornithes
Order: Procellariiformes
Fürbringer, 1888
Families

Diomedeoididae
Procellariidae
Diomedeidae
Hydrobatidae
Oceanitidae

Diversity
4 extant families, 26 genera, 147 species

Procellariiformes /prɒsɛˈlɛəri.ɪfɔːrmz/ is an order of seabirds that comprises four families: the albatrosses, the petrels and shearwaters, and two families of storm petrels. Formerly called Tubinares and still called tubenoses in English, procellariiforms are often referred to collectively as the petrels, a term that has been applied to all members of the order,[1] or more commonly all the families except the albatrosses.[2] They are almost exclusively pelagic (feeding in the open ocean), and have a cosmopolitan distribution across the world's oceans, with the highest diversity being around New Zealand.[3]

Procellariiforms are colonial, mostly nesting on remote, predator-free islands. The larger species nest on the surface, while most smaller species nest in natural cavities and burrows. They exhibit strong philopatry, returning to their natal colony to breed and returning to the same nesting site over many years. Procellariiforms are monogamous and form long-term pair bonds that are formed over several years and may last for the life of the pair. A single egg is laid per nesting attempt, and usually a single nesting attempt is made per year, although the larger albatrosses may only nest once every two years. Both parents participate in incubation and chick rearing. Incubation times are long compared to other birds, as are fledging periods. Once a chick has fledged there is no further parental care.

Procellariiforms have had a long relationship with humans. They have been important food sources for many people, and continue to be hunted as such in some parts of the world. The albatrosses in particular have been the subject of numerous cultural depictions. Procellariiforms include some of the most endangered bird taxa, with many species threatened with extinction due to introduced predators in their breeding colonies, marine pollution and the danger of fisheries by-catch. Scientists, conservationists, fishermen, and governments around the world are working to reduce the threats posed to them, and these efforts have led to the signing of the Agreement on the Conservation of Albatrosses and Petrels, a legally binding international treaty signed in 2001.

Taxonomy

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Pterodroma macroptera from Godman's Monograph of the Petrels, 1907–1910
Procellariiformes

Diomedeidae – albatrosses (21 species)

Oceanitidae – austral storm petrels (10 species)

Hydrobatidae – northern storm petrels (18 species)

Procellariidae – petrels and shearwaters (100 species)

Phylogeny of the extant procellariforms based on a study by Richard Prum and colleagues published in 2015.[4] The number of species is taken from the list maintained by Frank Gill, Pamela C. Rasmussen and David Donsker on behalf of the International Ornithological Committee (IOC).[5]

The order was named Procellariiformes by German anatomist Max Fürbringer in 1888.[6] The word comes from the Latin word procella, which means a violent wind or a storm, and -iformes for order.[7] Until the beginning of the 20th century, the family Hydrobatidae was named Procellariidae, and the family now called Procellariidae was rendered "Puffinidae."[8] The order itself was called Tubinares.[9][8] A major early work on this group is Frederick DuCane Godman's Monograph of the Petrels, five fascicles, 1907–1910, with figures by John Gerrard Keulemans.[9]

In the Sibley-Ahlquist taxonomy, the tubenoses were included in a greatly enlarged order "Ciconiiformes". This taxonomic treatment was almost certainly erroneous, but its assumption of a close evolutionary relationship with other "higher waterbirds" – such as loons (Gaviiformes) and penguins (Sphenisciformes) – appears to be correct.[10] The procellariiforms are most closely related to penguins,[11] having diverged from them about 60 million years ago.[12]

The diving petrels in the genus Pelecanoides were formerly placed in their own family Pelecanoididae.[13] When genetic studies found that they were embedded within the family Procellariidae, the two families were merged.[4][5]

All the storm petrels were once placed in the family Hydrobatidae but genetic data indicated that Hydrobatidae consisted of two deeply divergent clades that were not sister taxa.[14][15][4][16] In 2018 the austral storm petrels were moved to the new family Oceanitidae.[5][17] The northern storm petrels in the family Hydrobatidae are more closely related to the family Procellariidae than they are to the austral storm petrels in the family Oceanitidae.[4]

Earlier molecular phylogenetic studies found the family Oceantidae containing the austral storm petrels as the most basal with differing branching topologies for other three families.[14][18][15] More recent large-scale studies have found a consistent pattern with the albatross family Diomedeidae as the most basal and Hydrobatidae sister to Procellariidae.[4][16][19]

There are 147 living species of procellariiform worldwide,[5] and the order is divided into four extant families, with a fifth prehistorically extinct:

  • Family Diomedeidae (albatrosses) are very large seabirds with a large strong hooked bill. They have strong legs, enabling them to walk well on land.[20]
  • Family Oceanitidae (Austral storm petrels) are among the smallest seabirds, with fluttering flight and long but weak legs. Most have dark upperparts and a white underside.[21]
  • Family Hydrobatidae (northern storm petrels) are similar to the austral storm petrels but have longer more pointed wings and most species have forked tails.[21]
  • Family Procellariidae (shearwaters, fulmarine petrels, gadfly petrels, and prions) are a varied group of small or medium-sized seabirds, the largest being the giant petrels. They are heavy for their size, with a high wing loading, so they need to fly fast. Most, except the giant petrels, have weak legs and are nearly helpless on land.[22]
  • Family †Diomedeoididae (Early Oligocene – Early Miocene) is an extinct group that had narrow beaks and feet with wide, flat phalanges, especially on the fourth toe.[23]

Fossils of a bird similar to a petrel from the Eocene have been found in the London Clay and in Louisiana.[24][25] Diving petrels occurred in the Miocene, with a species from that family (Pelecanoides miokuaka) being described in 2007.[26] The most numerous fossils from the Paleogene are those from the extinct family Diomedeoididae, fossils of which have been found in Central Europe and Iran.[23]

Biology

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Distribution and movements

[edit]

The procellariiforms have a cosmopolitan distribution across the world's oceans and seas, although at the levels of family and genus there are some clear patterns. Antarctic petrels, Thalassoica antarctica, have to fly over 100 mi (160 km) to get to the ocean from their breeding colonies in Antarctica, and northern fulmars breed on the northeastern tip of Greenland, the northernmost piece of land.[27] The most cosmopolitan family is the Procellariidae, which are found in tropical, temperate and polar zones of both the Northern and the Southern Hemispheres, though the majority do not breed in the tropics, and half the species are restricted to southern temperate and polar regions.[28] The gadfly petrels, Pterodroma, have a generally tropical and temperate distribution, whereas the fulmarine petrels are mostly polar with some temperate species. The majority of the fulmarine petrels, along with the prions, are confined to the Southern Hemisphere.[29]

The storm petrels are almost as widespread as the procellariids, and fall into two distinct families; the Oceanitidae have a mostly Southern Hemisphere distribution and the Hydrobatidae are found mostly in the Northern Hemisphere. Amongst the albatrosses the majority of the family is restricted to the Southern Hemisphere, feeding and nesting in cool temperate areas, although one genus, Phoebastria, ranges across the north Pacific. The family is absent from the north Atlantic, although fossil records indicate they bred there once.[30] Finally the diving petrels are restricted to the Southern Hemisphere.[31]

Migration

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The various species within the order have a variety of migration strategies. Some species undertake regular trans-equatorial migrations, such as the sooty shearwater which annually migrates from its breeding grounds in New Zealand and Chile to the North Pacific off Japan, Alaska and California, an annual round trip of 64,000 km (40,000 mi), the second longest measured annual migration of any bird.[32] A number of other petrel species undertake trans-equatorial migrations, including the Wilson's storm petrel and the Providence petrel, but no albatrosses cross the equator, as they rely on wind assisted flight. There are other long-distance migrants within the order; Swinhoe's storm petrels breed in the western Pacific and migrate to the western Indian Ocean,[33] and Bonin petrels nesting in Hawaii migrate to the coast of Japan during the non-breeding season.[34]

[edit]

Many species in the order travel long distances over open water but return to the same nest site each year, raising the question of how they navigate so accurately.[35] The Welsh naturalist Ronald Lockley carried out early research into animal navigation with the Manx shearwaters that nested on the island of Skokholm. In release experiments, a Manx shearwater flew from Boston to Skokholm, a distance of 3,000 miles (4,800 kilometres) in 1212 days.[35][36] Lockley showed that when released "under a clear sky" with sun or stars visible, the shearwaters oriented themselves and then "flew off in a direct line for Skokholm", making the journey so rapidly that they must have flown almost in a straight line. But if the sky was overcast at the time of release, the shearwaters flew around in circles "as if lost" and returned slowly or not at all, implying that they navigated using astronomical cues.[35]

Researchers have also begun investigating olfaction's role in procellariiform navigation. In a study where Cory's shearwaters were rendered anosmic with zinc sulphate, a compound which kills the surface layer of the olfactory epithelium, and released hundreds of kilometers away from their home colony at night, control birds found their way to their home nests before night was over, whereas anosmic birds did not home until the next day.[37] A similar study that released Cory's shearwaters 800 km from their home nests, testing both magnetic and olfactory disturbances' effects on navigation, found that anosmic birds took longer to home than magnetically disturbed or control birds.[38]

Morphology and flight

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massive white bird with black wings and pink bill sits on the surface of the water
The southern royal albatross is one of the largest of the Procellariiformes.

Procellariiforms range in size from the very large wandering albatross, at 11 kg (24 lb) and a 3.6-metre (12-foot) wingspan, to tiny birds like the least storm petrel, at 20 g (0.71 oz) with a 32-centimetre (13-inch) wingspan,[27] and the smallest of the prions, the fairy prion, with a wingspan of 23 to 28 cm (9.1 to 11.0 in).[22] Their nostrils are enclosed in one or two tubes on their straight deeply-grooved bills with hooked tips. The beaks are made up of several plates. Their wings are long and narrow; the feet are webbed, and the hind toe is undeveloped or non-existent; their adult plumage is predominantly black, white, and grey.[39]

The order has a few unifying characteristics, starting with their tubular nasal passage which is used for olfaction.[40] Procellariiformes that nest in burrows have a strong sense of smell, being able to detect dimethyl sulfide released from plankton in the ocean.[41] This ability to smell helps to locate patchily distributed prey at sea and may also help locate their nests within nesting colonies.[42] In contrast, surface nesting Procellariiformes have increased vision, having six times better spatial resolution than those that nest in burrows.[43] The structure of the bill, which contains seven to nine distinct horny plates, is another unifying feature, although there are differences within the order. Petrels have a plate called the maxillary unguis that forms a hook on the maxilla. The smaller members of the order have a comb-like mandible, made by the tomial plate, for plankton feeding. Most members of the order are unable to walk well on land, and many species visit their remote breeding islands only at night. The exceptions are the huge albatrosses, several of the gadfly petrels and shearwaters and the fulmar-petrels. The latter can disable even large predatory birds with their obnoxious stomach oil, which they can project some distance. This stomach oil, stored in the proventriculus, is a digestive residue created in the foregut of all tubenoses except the diving petrels, and is used mainly for storage of energy-rich food during their long flights.[44] The oil is also fed to their young, as well as being used for defense.[27][45]

White bird with grey upperparts and black face mask jumps off water surface with elongated legs.
The white-faced storm petrel moves across the water's surface in a series of bounding leaps.

Procellariiforms drink seawater, so they have to excrete excess salt. All birds have an enlarged nasal gland at the base of the bill, above the eyes, and in the Procellariiformes the gland is active. In general terms, the salt gland removes salt from the system and forms a 5 percent saline solution that drips out of the nostrils, or is forcibly ejected in some petrels.[46] The processes behind this involve high levels of sodium ion reabsorption into the blood plasma within the kidneys, and secretion of sodium chloride via the salt glands using less water than was absorbed, which essentially generates salt-free water for other physiological uses. This high efficiency of sodium ion absorption is attributed to mammalian-type nephrons.[47]

Most albatrosses and procellariids use two techniques to minimise exertion while flying, namely, dynamic soaring and slope soaring. The albatrosses and giant petrels share a morphological adaptation to aid in flight, a sheet of tendon which locks the wing when fully extended, allowing the wing to be kept up and out without any muscle effort.[48] Amongst the Oceanitinae storm-petrels there are two unique flight patterns, one being surface pattering. In this they move across the water surface holding and moving their feet on the water's surface while holding steady above the water, and remaining stationary by hovering with rapid fluttering or by using the wind to anchor themselves in place.[49] A similar flight method is thought to have been used by the extinct petrel family Diomedeoididae.[23] The white-faced storm petrel possesses a unique variation on pattering: holding its wings motionless and at an angle into the wind, it pushes itself off the water's surface in a succession of bounding jumps.[50]

Diet and feeding

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The procellariiforms are for the most part exclusively marine foragers; the only exception to this rule are the two species of giant petrel, which regularly feed on carrion or other seabirds while on land. While some other species of fulmarine and Procellaria petrels also take carrion, the diet of most species of albatrosses and petrels is dominated by fish, squid, krill and other marine zooplankton. The importance of these food sources varies from species to species and family to family. For example, of the two albatross species found in Hawaii, the black-footed albatross takes mostly fish, while the Laysan feeds mainly on squid.[51] The albatrosses in general feed on fish, squid and krill. Among the procellariids, the prions concentrate on small crustacea, the fulmarine petrels take fish and krill but little squid, while the Procellaria petrels consume mainly squid. The storm petrels take small droplets of oil from the surface of the water,[52] as well as small crustaceans and fish.[53]

Petrels obtain food by snatching prey while swimming on the surface, snatching prey from the wing or diving down under the water to pursue prey. Dipping down from flight is most commonly used by the gadfly petrels and the storm petrels. There have been records of wedge-tailed shearwaters snatching flying fish from the air, but as a rule this technique is rare. Some diving birds may aid diving by beginning with a plunge from the air, but for the most part petrels are active divers and use their wings to move around under the water. The depths achieved by various species were determined in the 1990s and came as a surprise to scientists; short-tailed shearwaters have been recorded diving to 70 m (230 ft) and the Light-mantled sooty albatross to 12 m (39 ft).[54]

Breeding behaviour

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Breeding colonies

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Christmas shearwaters are one of the surface-nesting tropical procellariiforms.

All procellariiforms are colonial, predominantly breeding on offshore or oceanic islands. The few species that nest on continents do so in inhospitable environments such as dry deserts or on Antarctica. These colonies can vary from the widely spaced colonies of the giant petrels to the dense 3.6 million-strong colonies of Leach's storm petrels.[55] For almost all species the need to breed is the only reason that procellariiforms return to land at all. Some of the larger petrels have to nest on windswept locations as they require wind to take off and forage for food.[27] Within the colonies, pairs defend usually small territories (the giant petrels and some albatrosses can have very large territories) which is the small area around either the nest or a burrow. Competition between pairs can be intense, as is competition between species, particularly for burrows. Larger species of petrels will even kill the chicks and even adults of smaller species in disputes over burrows.[56] Burrows and natural crevices are most commonly used by the smaller species; all the storm petrels and diving petrels are cavity nesters, as are many of the procellariids. The fulmarine petrels and some tropical gadfly petrels and shearwaters are surface nesters, as are all the albatrosses.[57]

Procellariiforms show high levels of philopatry, both site fidelity and natal philopatry. Natal philopatry is the tendency of an individual bird to return to its natal colony to breed, often many years after leaving the colony as a chick. This tendency has been shown through ringing studies and mitochondrial DNA studies. Birds ringed as chicks have been recaptured close to their original nests, sometimes extremely close; in the Laysan albatross the average distance between hatching site and the site where a bird established its own territory was 22 m (72 ft),[58] and a study of Cory's shearwaters nesting near Corsica found that nine out of 61 male chicks that returned to breed at their natal colony actually bred in the burrow they were raised in.[59] Mitochondrial DNA provides evidence of restricted gene flow between different colonies, strongly suggesting philopatry.[60]

The other type of philopatry exhibited is site fidelity, where pairs of birds return to the same nesting site for a number of years. Among the most extreme examples known of this tendency was the fidelity of a ringed northern fulmar that returned to the same nest site for 25 years. The average number of birds returning to the same nest sites is high in all species studied, with around 91 percent for Bulwer's petrels,[61] and 85 percent of males and 76 percent of females for Cory's shearwaters (after a successful breeding attempt).[62]

Pair bonds and life history

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Three massive birds stand on low grasslands, the closest bird has its long wings outstretched and its head pointing upward
Wandering albatrosses performing their mating dances on the Kerguelen Islands

Procellariiforms are monogamous breeders and form long-term pair bonds. These pair bonds take several years to develop in some species, particularly with the albatrosses. Once formed, they last for many breeding seasons, in some cases for the life of the pair. Petrel courtship can be elaborate. It reaches its extreme with the albatrosses, where pairs spend many years perfecting and elaborating mating dances.[63] These dances are composed of synchronised performances of various actions such as preening, pointing, calling, bill clacking, staring, and combinations of such behaviours (like the sky-call).[64] Each particular pair will develop their own individual version of the dance. The breeding behaviour of other procellariiforms is less elaborate, although similar bonding behaviours are involved, particularly for surface-nesting species. These can involve synchronised flights, mutual preening and calling. Calls are important for helping birds locate potential mates and distinguishing between species, and may also help individuals assess the quality of potential mates.[65] After pairs have been formed, calls serve to help them reunite; the ability of individuals to recognise their own mate has been demonstrated in several species.[66]

Procellariiforms are K-selected, being long-lived and caring extensively for their few offspring. Breeding is delayed for several years after fledging, sometimes for as long as ten years in the largest species. Once they begin breeding, they make only a single breeding attempt per nesting season; even if the egg is lost early in the season, they seldom re-lay. Much effort is placed into laying a single (proportionally) large egg and raising a single chick. Procellariiforms are long-lived: the longest living albatross known survived for 51 years, but was probably older,[67] and even the tiny storm-petrels are known to have survived for 30 years.[68] Additionally, the oldest living bird is Wisdom, a female Laysan albatross.

Nesting and chick rearing

[edit]
A semi-precocial wedge-tailed shearwater chick with guarding parent

The majority of procellariiforms nest once a year and do so seasonally.[69] Some tropical shearwaters, like the Christmas shearwater, are able to nest on cycles slightly shorter than a year, and the large great albatrosses (genus Diomedea) nest in alternate years (if successful). Most temperate and polar species nest over the spring-summer, although some albatrosses and procellariids nest over the winter. In the tropics, some species can be found breeding throughout the year, but most nest in discreet periods. Procellariiforms return to nesting colonies as much as several months before laying, and attend their nest sites regularly before copulation. Prior to laying, females embark on a lengthy pre-laying exodus to build up energy reserves in order to lay the exceptionally large egg. In the stormy petrel[clarification needed], a very small procellariiform, the egg can be 29 percent of the body weight of the female, while in the grey-faced petrel, the female may spend as much as 80 days feeding out at sea after courtship before laying the egg.[70]

When the female returns and lays, incubation is shared between the sexes, with the male taking the first incubation stint and the female returning to sea. The duration of individual stints varies from just a few days to as much as several weeks, during which the incubating bird can lose a considerable amount of weight.[71] The incubation period varies from species to species, around 40 days for the smallest storm-petrels but longer for the largest species; for albatrosses it can span 70 to 80 days, which is the longest incubation period of any bird.[72]

A Laysan albatross feeds its chick. The parent pumps food from a modified foregut, the proventriculus, and the chick catches the meal in its lower mandible.

Upon hatching, the chicks are semi-precocial, having open eyes, a dense covering of white or grey down feathers, and the ability to move around the nesting site. After hatching, the incubating adult remains with the chick for a number of days, a period known as the guard phase. In the case of most burrow-nesting species, this is only until the chick is able to thermoregulate, usually two or three days. Diving-petrel chicks take longer to thermoregulate and have a longer guard phase than other burrow nesters. However, surface-nesting species, which have to deal with a greater range of weather and to contend with predators like skuas and frigatebirds, consequently have a longer guard phase (as long as two weeks in procellariids and three weeks in albatrosses).[73]

The chick is fed by both parents. Chicks are fed on fish, squid, krill, and stomach oil. Stomach oil is oil composed of neutral dietary lipids that are the residue created by digestion of the prey items. As an energy source for chicks it has several advantages over undigested prey, its calorific value is around 9.6 kcal per gram, which is only slightly lower than the value for diesel oil.[74] This can be a real advantage for species that range over huge distances to provide food for hungry chicks.[75] The oil is also used in defence. All procellariiforms create stomach oil except the diving-petrels.[74]

The chick fledges between two and nine months after hatching, almost twice as long as a gull of the same body mass. The reasons behind the length of time are associated with the distance from the breeding site to food. First, there are few predators at the nesting colonies, therefore there is no pressure to fledge quickly. Second, the time between feedings is long due to the distance from the nest site that adults forage, thus a chick that had a higher growth rate would stand a better chance of starving to death.[27] The duration between feedings vary among species and during the stages of development. Small feeds are frequent during the guard phase, but afterward become less frequent. However, each feed can deliver a large amount of energy; both sooty shearwater and mottled petrel chicks have been recorded to double their weight in a single night, probably when fed by both parents.[70]

Relationship with humans

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Role in culture

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The Albatross about my Neck was Hung: 1896 etching by William Strang illustrating Coleridge's 1798 poem The Rime of the Ancient Mariner

The most important family culturally is the albatrosses, which have been described by one author as "the most legendary of birds".[76] Albatrosses have featured in poetry in the form of Samuel Taylor Coleridge's famous 1798 poem The Rime of the Ancient Mariner, which in turn gave rise to the usage of albatross as metaphor for a burden.[77] More generally, albatrosses were believed to be good omens, and to kill one would bring bad luck.[27] There are few instances of petrels in culture, although there are sailors' legends regarding the storm petrels, which are considered to warn of oncoming storms. In general, petrels were considered to be "soul birds", representing the souls of drowned sailors, and it was considered unlucky to touch them.[78]

In the Russian language, many petrel species from the Hydrobatidae and Procellariidae families of the order Procellariiformes are known as burevestnik, which literally means 'the announcer of the storm'. When in 1901, the Russian writer Maxim Gorky turned to the imagery of subantarctic avifauna to describe Russian society's attitudes to the coming revolution, he used a storm-announcing petrel as the lead character of a poem that soon became popular in the revolutionary circles as "the battle anthem of the revolution".[79] Although the species called "stormy petrel" in English is not one of those to which the burevestnik name is applied in Russian (it, in fact, is known in Russian as an entirely un-romantic kachurka), the English translators uniformly used the "stormy petrel" image in their translations of the poem, usually known in English as The Song of the Stormy Petrel.[80]

Various tubenose birds are relevant to the mythologies and oral traditions of Polynesia. The Māori used the wing bones of the albatross to carve flutes.[81] In Hawaiian mythology, Laysan albatrosses are considered aumakua, being a sacred manifestation of the ancestors, and quite possibly also the sacred bird of Kāne.[82] The storm petrel features prominently in the "Origin of Birds" myth.[83]

Exploitation

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A tail-piece engraving in Bewick's A History of British Birds, showing men exploiting birds nesting on sea cliffs, 1804

Albatrosses and petrels have been important food sources for humans for as long as people have been able to reach their remote breeding colonies. Amongst the earliest-known examples of this is the remains of shearwaters and albatrosses along with those of other seabirds in 5,000-year-old middens in Chile,[84] although it is likely that they were exploited prior to this. Since then, many other marine cultures, both subsistence and industrial, have exploited procellariiforms, in some cases almost to extinction. Some cultures continue to harvest shearwaters (a practice known as muttonbirding); for example, the Māori of New Zealand use a sustainable traditional method known as kaitiakitanga. In Alaska, residents of Kodiak Island harpoon short-tailed albatrosses, Diomedea albatrus, and until the late 1980s residents of Tristan Island in the Indian Ocean harvested the eggs of the Yellow-nosed Mollymawks, Diomedea chlororhynchos, and sooty albatrosses, Phoebetria fusca.[27] Albatrosses and petrels are also now tourist draws in some locations, such as Taiaroa Head. While such exploitation is non-consumptive, it can have deleterious effects that need careful management to protect both the birds and the tourism.[85]

The English naturalist William Yarrell wrote in 1843 that "ten or twelve years ago, Mr. Gould exhibited twenty-four [storm petrels], in a large dish, at one of the evening meetings of the Zoological Society".[86]

The engraver Thomas Bewick wrote in 1804 that "Pennant, speaking of those [birds] which breed on, or inhabit, the Isle of St Kilda, says—'No bird is of so much use to the islanders as this: the Fulmar supplies them with oil for their lamps, down for their beds, a delicacy for their tables, a balm for their wounds, and a medicine for their distempers.'"[87] A photograph by George Washington Wilson taken about 1886 shows a "view of the men and women of St Kilda on the beach dividing up the catch of Fulmar".[88] James Fisher, author of The Fulmar (1952)[89] calculated that every person on St Kilda consumed over 100 fulmars each year; the meat was their staple food, and they caught around 12,000 birds annually. However, when the human population left St Kilda in 1930, the population did not suddenly grow.[90]

Threats and conservation

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The poorly known New Zealand storm petrel was considered extinct for 150 years before being rediscovered in 2003.

The albatrosses and petrels are "amongst the most severely threatened taxa worldwide".[56] They face a variety of threats, the severity of which varies greatly from species to species. Several species are among the most common of seabirds, including Wilson's storm petrel (an estimated 12 to 30 million individuals)[91] and the short-tailed shearwater (23 million individuals);[92] while the total population of some other species is a few hundred. There are less than 200 Magenta petrels breeding on the Chatham Islands,[93] only 130 to 160 Zino's petrels[94] and only 170 Amsterdam albatrosses.[95] Only one species is thought to have become extinct since 1600, the Guadalupe storm petrel of Mexico,[96] although a number of species had died out before this. Numerous species are very poorly known; for example, the Fiji petrel has rarely been seen since its discovery.[97] The breeding colony of the New Zealand storm petrel was not located until February 2013;[98] it had been thought extinct for 150 years until its rediscovery in 2003,[99] while the Bermuda petrel had been considered extinct for nearly 300 years.[100]

Black-browed albatross hooked on a long-line

The principal threat to the albatrosses and larger species of procellariids is long-line fishing. Bait set on hooks is attractive to foraging birds and many are hooked by the lines as they are set. As many as 100,000 albatrosses are hooked and drown each year on tuna lines set out by long-line fisheries.[101][102] Before 1991 and the ban on drift-net fisheries, it was estimated that 500,000 seabirds a year died as a result.[27] This has caused steep declines in some species, as procellariiforms are extremely slow breeders[103] and cannot replace their numbers fast enough. Losses of albatrosses and petrels in the Southern Ocean were estimated at between 1 percent and 16 percent per year, which these species cannot sustain for long.[104]

Exotic species introduced to the remote breeding colonies threaten all types of procellariiform. These principally take the form of predators; most albatross and petrel species are clumsy on land and unable to defend themselves from mammals such as rats, feral cats and pigs. This phenomenon, ecological naivete, has resulted in declines in many species and was implicated in the extinction of the Guadalupe storm petrel.[105] Already in 1910 Godman wrote:

Owing to the introduction of the mongoose and other small carnivorous mammals into their breeding haunts, some species, such as Oestrelata jamaicensis and newelli, have already been completely exterminated, and others appear to be in danger of extinction.

— Frederick Du Cane Godman, 1910, vol 1, p. 14.[9]

This albatross bolus found in the Hawaiian Islands includes flotsam that was ingested but successfully ejected along with other indigestible matter. If such flotsam cannot be ejected it may cause sickness or death.

Introduced herbivores may unbalance the ecology of islands; introduced rabbits destroyed the forest understory on Cabbage Tree Island off New South Wales, which increased the vulnerability of the Gould's petrels nesting on the island to natural predators, and left them vulnerable to the sticky fruits of the native birdlime tree (Pisonia umbellifera). In the natural state these fruits lodge in the understory of the forest, but with the understory removed the fruits fall to the ground where the petrels move about, sticking to their feathers and making flight impossible.[106]

Exploitation has decreased in importance as a threat. Other threats include the ingestion of plastic flotsam. Once swallowed, plastic can cause a general decline in the fitness of the bird, or in some cases lodge in the gut and cause a blockage, leading to death by starvation.[107] It can also be picked up by foraging adults and fed to chicks, stunting their development and reducing the chances of successfully fledging.[108] Procellariids are also vulnerable to marine pollution, as well as oil spills. Some species, such as Barau's petrel, Newell's shearwater and Cory's shearwater, which nest high up on large developed islands, are victims of light pollution.[109] Fledging chicks are attracted to streetlights and may then be unable to reach the sea. An estimated 20 to 40 percent of fledging Barau's petrels and 45 to 60 percent of fledging Cory's shearwater are attracted to the streetlights on Réunion and Tenerife, respectively.[110][111]

References

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Bibliography

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from Grokipedia
Procellariiformes is an order of seabirds distinguished by tubular nostrils that enhance their sense of smell for detecting prey such as krill and squid over vast ocean expanses.[1][2] The order encompasses four families—Diomedeidae (albatrosses), Procellariidae (petrels and shearwaters), Hydrobatidae (northern storm-petrels), and Oceanitidae (southern storm-petrels)—comprising approximately 127 species adapted for pelagic existence with long, narrow wings suited to dynamic soaring, hooked bills, and webbed feet.[3] These birds exhibit a cosmopolitan distribution, with greatest diversity in Southern Hemisphere oceans, spending most of their lives at sea and returning to remote, predator-free islands to breed in dense colonies, often exhibiting delayed maturity and exceptional longevity exceeding 50 years in larger species.[4][5] While renowned for efficient flight mechanics that minimize energy expenditure during long migrations, many species face severe threats from incidental capture in longline fisheries and plastic ingestion, contributing to high rates of endangerment.[3][6]

Taxonomy and Phylogeny

Families and Genera

The order Procellariiformes comprises five families, as recognized in recent phylogenetic classifications that incorporate molecular data to distinguish morphological similarities from evolutionary relationships. These families are Diomedeidae (albatrosses), Procellariidae (petrels and shearwaters), Pelecanoididae (diving petrels), Hydrobatidae (northern storm-petrels), and Oceanitidae (southern storm-petrels), encompassing approximately 143 species across 26 genera.[7][8] Diomedeidae contains 21 species in four genera: Diomedea (great albatrosses, four species including the wandering albatross D. exulans), Phoebastria (North Pacific albatrosses, four species such as Laysan albatross P. immutabilis), Thalassarche (mollymawks, eight species like the black-browed albatross T. melanophris), and Phoebetria (sooty albatrosses, two species). These large, long-winged seabirds are adapted for dynamic soaring over oceans, with species distributed primarily in the Southern Hemisphere except for Phoebastria.[9] Procellariidae, the largest family with about 100 species, includes 16 genera divided into subgroups such as fulmarine petrels (Macronectes with two giant petrel species, Fulmarus with two fulmar species, Thalassoica, Daption, and Pagodroma), prions (Pachyptila, seven species), gadfly petrels (Pterodroma with 35 species, Pseudobulweria, Lugensa, Aphrodroma), and shearwaters (Procellaria with four species, Ardenna with nine large shearwaters, Calonectris with three, and remaining Puffinus species). This family dominates in diversity, with species ranging from burrow-nesting petrels to surface-foraging shearwaters, many exhibiting long migrations.[10][11] Pelecanoididae consists of a single genus, Pelecanoides, with four small species (South Georgian, Peruvian, common, and Magellanic diving-petrels) specialized for wing-propelled underwater diving in cold southern waters, resembling auks in foraging but differing in tube-nosed nostrils.[12] Hydrobatidae (northern storm-petrels) includes 18 species primarily in two genera: Hydrobates (about 13 species, such as European storm-petrel H. pelagicus) and Oceanodroma (five species like Leach's storm-petrel O. leucorhoa), characterized by erratic fluttering flight over tropical and temperate waters. Oceanitidae (southern storm-petrels) has 10 species in four genera: Oceanites (three species including Wilson's storm-petrel O. oceanicus), Fregetta (five species), Garrodia (one), and Nesofregetta (one), often pattering on water surfaces to feed. The split between Hydrobatidae and Oceanitidae reflects genetic divergence, with Oceanitidae showing basal placement in Procellariiformes phylogenies.[8]
FamilyNumber of GeneraNumber of SpeciesKey Genera Examples
Diomedeidae421Diomedea, Phoebastria, Thalassarche, Phoebetria
Procellariidae16~100Pterodroma, Ardenna, Pachyptila, Macronectes
Pelecanoididae14Pelecanoides
Hydrobatidae218Hydrobates, Oceanodroma
Oceanitidae410Oceanites, Fregetta

Recent Phylogenetic Insights

Molecular phylogenetic analyses employing ultraconserved elements (UCEs) have yielded a well-supported phylogeny for Procellariiformes, encompassing representatives from all four families and addressing prior ambiguities in branching order. Estandía et al. (2021) generated a dataset from 2,307 UCE loci across 94 taxa, producing a time-calibrated tree that positions Oceanitidae as the basal family, followed by Hydrobatidae, with Diomedeidae sister to Procellariidae. This framework reveals higher substitution rates in terminal branches of smaller-bodied species, uncorrelated primarily with body mass, population size, or life-history traits, thus refining divergence estimates to approximately 50-60 million years ago for major clades. Within Oceanitidae, recent genetic and morphological studies have affirmed the family's monophyly and resolved intra-generic relationships previously muddled by convergent evolution in plumage and morphology. Poulsen et al. (2023) integrated mitochondrial and nuclear markers from Weddell Sea specimens, corroborating Oceanitidae's distinct status from Hydrobatidae via coalescent-based analyses and low inter-family gene flow. Complementing this, Norambuena et al. (2024) analyzed cytochrome b sequences from 120 Oceanites individuals alongside morphometrics, delineating four reciprocally monophyletic clades and elevating three subspecies to full species, including the newly described Oceanites barrosi from southern oceanic waters; genetic divergences exceeded 3% between clades, supporting seven species total.[13] These insights underscore the utility of multi-locus approaches in overcoming rate heterogeneity and morphological convergence, with implications for revising taxonomy in vagile seabirds; for instance, the resolved Oceanites phylogeny highlights cryptic diversity in Antarctic and sub-Antarctic realms, potentially warranting targeted conservation.[13] Ongoing genomic efforts, including whole-genome comparisons, continue to refine genus-level relationships within Procellariidae, such as shearwater radiations, though deeper sampling is needed for fossil-calibrated timelines.

Evolutionary History

Fossil Record

The fossil record of Procellariiformes is sparse compared to other avian orders, with most early discoveries from the Northern Hemisphere and limited Southern Hemisphere material until the Neogene. The earliest putative procellariiform is Tytthostonyx glauconiticus, represented by a partial humerus from the late Maastrichtian or early Danian (approximately 66–65 million years ago) of New Jersey, United States, though its referral to the order remains tentative due to fragmentary preservation and potential stem-group affinities.[14] The oldest undisputed record is a petrel-like bird from the late Eocene (about 37–34 million years ago) of Louisiana, United States, based on a well-preserved tarsometatarsus exhibiting diagnostic tube-nosed features such as a narrow trochlea for the second toe.[15] Paleogene fossils are predominantly from Europe and North America, including the extinct family Diomedeoididae, known from isolated bones in central Europe and Iran dating to the Eocene–Oligocene, which display primitive albatross-like morphology but lack modern dynamic soaring adaptations.[16] Oligocene records include fulmarine petrels like Frigidafons brodkorbi from France and Germany, marking early diversification within the Procellariidae.[17] By the Miocene, fossils indicate wider dispersal, with Plotornis archaeonautes, a stem albatross from the earliest Miocene (about 23–21 million years ago) of New Zealand, representing the order's oldest Southern Hemisphere occurrence and suggesting trans-equatorial migration capabilities in early lineages.[18] Neogene deposits, particularly in New Zealand's Pliocene (5.3–2.6 million years ago) Taranaki region, yield diverse assemblages including shearwaters (Puffinus spp.), a deep-billed petrel, and Procellaria species, with at least four taxa identified from marine sediments, indicating established breeding populations predating Pleistocene glaciation.[19][20] Holocene subfossils from oceanic islands reveal extensive extinctions, such as at least 16 Pterodroma petrel species in Macaronesia (e.g., Azores, Madeira, Canary Islands), lost since human arrival around 2,000–500 years ago, likely due to predation and habitat alteration rather than climatic shifts.[21] Overall, the record underscores a Northern Hemisphere origin followed by adaptive radiation into southern oceans, with many insular endemics unpreserved due to poor fossilization in seabird habitats.

Origins and Adaptive Radiation

The order Procellariiformes likely originated in the aftermath of the Cretaceous-Paleogene extinction event, with the earliest putative fossil evidence consisting of a humerus attributed to Tytthostonyx glauconiticus from the Hornerstown Formation of New Jersey, dated to approximately 66 million years ago at the Cretaceous-Paleogene boundary.[22] This specimen exhibits morphological affinities to both Pelecaniformes and Procellariiformes, suggesting it represents a stem-group tubenose, though its precise phylogenetic placement remains debated due to the fragmentary nature of early seabird fossils and limited diagnostic traits.[23] Undisputed records of procellariiforms appear in the Eocene, including a large marine bird from the Tavda Formation in western Siberia around 50 million years ago and other tubenose-like remains from North American and African deposits, indicating rapid post-extinction colonization of pelagic niches by early members of the clade.[24] Molecular clock estimates, calibrated with fossil constraints, place the divergence of Procellariiformes from closely related waterbird lineages (such as Sphenisciformes) in the late Paleocene to early Eocene, roughly 60-50 million years ago, aligning with the expansion of open ocean habitats following global cooling and the establishment of modern ocean currents.[25] Genome-wide analyses further support a deep Cenozoic history, with intra-order splits—such as between storm-petrel families—occurring around 35-40 million years ago, reflecting vicariance driven by tectonic shifts like the separation of southern continents and the uplift of ocean barriers.[26] This origin facilitated an extensive adaptive radiation, one of the most successful among vertebrate clades, resulting in over 100 extant species across four families (Diomedeidae, Procellariidae, Hydrobatidae, and Oceanitidae) that exploit diverse ecological roles in marine ecosystems worldwide.[3] Key drivers included innovations in flight efficiency, such as elongated wings for dynamic soaring in albatrosses and shearwaters, and sensory adaptations like tubular nostrils for olfaction-guided foraging, enabling partitioning of resources from surface skimming to shallow dives across latitudinal gradients.[27] The radiation accelerated during the Oligocene-Miocene (ca. 34-5 million years ago), coinciding with cooling climates, Antarctic divergence, and nutrient upwelling zones that supported prey booms, leading to size disparities from minute storm-petrels (under 50 g) to giant albatrosses (over 10 kg) and genus-level bursts in southern oceans.[28] Fossil evidence of stem albatrosses like Plotornis from the early Miocene underscores this diversification into polar and temperate realms previously unoccupied by competitors.[29]

Physical Characteristics and Adaptations

Morphology and Anatomy

Procellariiformes exhibit a diverse range of body sizes, from small storm-petrels under 30 cm in length to large albatrosses exceeding 120 cm, with streamlined bodies optimized for aerial efficiency and marine foraging. The bill is robust, featuring a hooked tip and rhamphotheca divided into multiple horny plates, adaptations that facilitate grasping slippery prey such as squid and fish. In Antarctic fulmarine petrels, the skull is dorsoventrally flattened, enhancing the elongated bill's functionality for surface-seizing behaviors.[30] A defining feature is the pair of tubular nostrils fused into a single dorsal tube on the upper mandible, unique to the order and associated with both olfactory sensitivity and salt management. These tubes connect to highly developed supraorbital nasal glands that excrete hypertonic NaCl solutions via ducts emptying into the nostrils, allowing birds to process seawater and maintain osmotic balance; the secretion drips from the bill tip without contaminating the eyes or feathers.[31] Procellariiformes also possess enlarged olfactory bulbs, with the bulb-to-hemisphere diameter ratio reaching 0.29–0.30 in species like the snow petrel, supporting chemosensory detection of prey patches over vast ocean distances.[32] Wing morphology emphasizes high aspect ratios and narrow, elongated primaries suited to dynamic soaring, with wing loading increasing predictably with body mass across 48 studied species (log10 wing area scales allometrically with log10 body weight). Larger taxa, such as albatrosses, incorporate tendinous locks to maintain extended wing positions effortlessly during gliding. The coracoid bone varies phylogenetically, featuring distinct procoracoid processes and articular facets that underpin shoulder girdle diversity for sustained flight. [33] Feet are webbed for aquatic propulsion, with front toes connected by extensive interdigital membranes and a reduced or vestigial hallux; phalanges are often flattened, and in some lineages, the proximal phalanx of the fourth toe is widened, aiding in water takeoff and minimal terrestrial locomotion.[33] Plumage is dense and oiled for waterproofing, while internal skeletal elements include pneumatic lightening in long bones to minimize mass without compromising strength.[3]

Flight and Sensory Adaptations

Procellariiformes display specialized flight morphologies enabling efficient long-distance travel over oceans, with wing structures featuring high aspect ratios and narrow, elongated primaries that minimize drag during gliding. Larger taxa, including albatrosses (family Diomedeidae), utilize dynamic soaring, a technique verified through observations and modeling where birds exploit vertical wind shear near wave crests to cycle between low-speed ascents and high-speed descents, achieving ground speeds up to 28 m/s with negligible flapping.[34][35] This method, predominant among Procellariiformes, allows energy-efficient coverage of thousands of kilometers by converting wind energy into mechanical power via repeated transfers between kinetic and potential states.[36] Smaller species, such as petrels and shearwaters, favor flap-gliding, alternating powered flaps with passive glides to maintain speed against headwinds, adapting to patchier resources in pelagic environments.[37][38] Morphological aids include a tendinous sheet in albatrosses and giant petrels that locks extended wings, reducing muscular effort during sustained soaring.[37] Flight performance correlates with body size and wing loading, with larger birds achieving higher speeds via slope-soaring along wave faces, while all species increase velocity into headwinds to optimize lift.[34] These adaptations underpin their exploitation of remote marine habitats, where wind consistency supports minimal-energy locomotion over extended periods. Sensory adaptations in Procellariiformes emphasize olfaction, facilitated by tubular nostrils (hence "tube-noses") that channel scents and enlarged olfactory bulbs comprising up to 1/8 of brain volume in some species, far exceeding most birds.[39] This enables detection of prey-associated volatiles like krill odors or dimethyl sulfide from distances exceeding 10 km, as demonstrated in field experiments where birds approached odor plumes over visual blanks.[40][41] Olfactory receptors show adaptive evolution, with expanded gene repertoires supporting foraging, homing, and nest recognition in chicks.[42] While vision aids surface prey spotting, olfaction dominates in locating dispersed patches, with species-specific sensitivities—e.g., procellariids strongly attracted to krill scents—enhancing survival in low-visibility oceanic conditions.[39][40]

Ecology

Global Distribution and Habitat Preferences

Procellariiformes exhibit a cosmopolitan distribution across all major ocean basins, ranging from high Arctic and Antarctic latitudes to equatorial waters, though species diversity and abundance peak in the Southern Hemisphere's temperate and subantarctic regions.[43] [3] The order comprises over 90 species, with families like Diomedeidae (albatrosses) largely confined to southern oceans and Procellariidae (petrels and shearwaters) showing broader representation in both hemispheres.[44] Northern Hemisphere species, such as certain storm-petrels and fulmars, occur in the North Atlantic and Pacific, but overall biomass is dominated by southern populations.[3] These seabirds are obligate pelagics, spending 80-90% of their annual cycle over open ocean far from land, associating with dynamic marine features including oceanic fronts, mesoscale eddies, upwelling zones, and convergence areas that enhance prey availability.[45] They favor habitats with consistent winds exceeding 10-15 m/s to facilitate dynamic soaring, a key energy-efficient flight mechanism, and avoid calm equatorial doldrums where possible.[46] Foraging depths vary by family, with surface-seizing species like storm-petrels targeting neuston layers and pursuit divers like albatrosses accessing deeper scatters via kleptoparasitism or scavenging.[3] Breeding occurs exclusively on terrestrial sites, predominantly remote oceanic and subantarctic islands free from mammalian predators, such as those in the Southern Ocean (e.g., South Georgia, Crozet Islands) or isolated northern archipelagos.[47] Nesting preferences include burrow systems in soft soil or tussock grass for petrels, cliff ledges for albatrosses, and surface scrapes for smaller species, often in colonies numbering thousands to millions of pairs to leverage olfactory and acoustic defenses. These sites are selected for accessibility to surrounding productive seas and minimal disturbance, with many populations showing strong philopatry to natal colonies.[48]

Migration Patterns and Navigation

Procellariiformes exhibit diverse migration patterns characterized by extensive pelagic journeys, often spanning thousands of kilometers across ocean basins. Many species undertake trans-equatorial or circumpolar migrations, leveraging prevailing wind systems to minimize energy expenditure during dynamic soaring flight. For instance, sooty shearwaters (Ardenna grisea) perform figure-eight circuits around the Pacific Ocean, with individual circumnavigations averaging 40,000 km, though shorter migrations range from 12,000 to over 30,000 km.[49] Wind patterns significantly influence these routes, prompting detours or alignments that optimize foraging opportunities while avoiding adverse conditions, as observed in procellariiform species crossing hemispheres.[50] Smaller petrels and storm-petrels, such as Leach's storm-petrel (Hydrobates leucorhous), follow coastal or offshore paths with defined stopover areas during non-breeding periods, molting primary feathers en route to sustain flight efficiency.[51] Navigation in Procellariiformes relies heavily on olfactory cues rather than magnetic fields or celestial landmarks alone. Cory's shearwaters (Calonectris diomedea) and other procellariiforms construct cognitive olfactory maps from wind-borne odors, enabling precise homing over oceanic expanses; displacement experiments demonstrate that birds with occluded olfactory senses fail to orient correctly initially, though they may compensate via topographic cues over time.[52] Sensitivity to volatile compounds like dimethyl sulfide, emitted from phytoplankton blooms, facilitates both navigation and prey localization, underscoring olfaction's dual role in migration and foraging.[53] Magnetic perturbations do not substantially disrupt orientation in species like wandering albatrosses (Diomedea exulans), indicating limited dependence on magnetoreception for open-ocean travel.[54] Albatrosses may additionally employ infrasound detection for long-range orientation, as movement data reveal alignments with distant acoustic sources during foraging, potentially aiding in detecting productive upwelling zones or avoiding storms.[55] This multisensory integration, combining olfaction with possible acoustic and visual inputs, supports efficient traversal of featureless seas, where birds maintain speeds up to 28 m/s in favorable winds.[46] Age-related differences emerge, with juveniles often detouring more due to inexperience with wind exploitation, gradually refining paths to match adults' streamlined trajectories.[50]

Foraging Ecology and Diet

Procellariiformes forage extensively in open ocean habitats, employing strategies suited to locating patchily distributed epipelagic and mesopelagic prey over scales from tens to thousands of square kilometers.[56] During the breeding season, central-place constraints lead many species to adopt bimodal foraging patterns, interspersing short trips (1-9 days) proximate to colonies for efficient chick provisioning with extended offshore journeys (5-29 days) that prioritize adult energy restoration.[48] This dual approach predominates in albatrosses (Diomedeidae) and gadfly petrels and shearwaters (Procellariidae), yielding meal delivery rates of about 9.8% chick body mass per day on short trips versus 2.6% on long ones, with long-trip destinations often correlating to elevated ocean productivity as indicated by chlorophyll a concentrations around 0.30 mg m⁻³.[48] Sensory adaptations underpin these behaviors, particularly the exceptional olfactory capabilities that allow detection of prey-associated volatile compounds such as dimethyl sulfide (DMS) at thresholds of 10⁻¹² to 5×10⁻⁹ mol l⁻¹, signaling productive patches from krill swarms or decaying organic matter.[56] Species vary in reliance: burrow-nesting procellariids like blue petrels (Halobaena caerulea) exhibit strong olfactory responses even as chicks, while surface-nesters such as albatrosses integrate olfaction with visual scouting and social information from mixed-species flocks.[56][57] Social foraging amplifies success, as visual foragers cue off olfactory specialists, mitigating risks from cryptic or low-density prey like Antarctic krill (Euphausia superba).[57] Direct capture techniques include surface-seizing, pursuit-plunging, and shallow dives, supplemented in larger albatrosses by kleptoparasitism—harassing other seabirds or pinnipeds to steal food—and scavenging of carrion.[56] Diets are opportunistic and marine-centric, dominated by cephalopods (e.g., squid, frequently as carrion), mesopelagic fishes such as myctophids, and crustaceans including euphausiid krill and hyperiid amphipods.[56] Compositional shifts occur seasonally and by taxon; for example, black-browed albatrosses (Thalassarche melanophris) partition intake roughly equally among squid, krill, and fish during breeding, while wedge-tailed shearwaters (Ardenna pacifica) emphasize fish (e.g., Mullidae) alongside cephalopods and minor crustacean elements.[56][58] Smaller storm-petrels (Hydrobatidae) favor planktonic crustaceans via surface pattering, underscoring trophic flexibility tied to body size and habitat access.[48]

Behavior and Reproduction

Social Structure and Vocalizations

Procellariiformes exhibit a social structure marked by solitary foraging across expansive marine habitats juxtaposed with dense colonial breeding aggregations on remote islands or coastal cliffs. This coloniality, prevalent across families like Procellariidae and Diomedeidae, facilitates benefits such as enhanced predator vigilance and information transfer on foraging grounds, with some petrel colonies exceeding 2 million breeding pairs. [59] [60] Pair bonds are typically socially monogamous and enduring, often lasting multiple years or the birds' lifetimes, which supports the intensive biparental investment required for rearing a single large chick over extended periods. [61] [10] Within colonies, non-breeding immatures prospect sites and engage in social attraction behaviors, reinforcing colony persistence through philopatry and conspecific cues. [62] Vocalizations serve as primary acoustic signals in these often nocturnal species, enabling communication in low-visibility burrow-nesting environments where visual cues are limited. Calls function in mate attraction, pair synchronization, territorial advertisement, alarm signaling, and parent-chick recognition, with repertoires including groans, rattles, purrs, barks, and whines tailored to specific contexts. [63] [64] In shearwaters and petrels, adults vocalize prominently upon arriving at or departing colonies, often at night, while non-paired individuals contribute to choruses during prospecting flights. [65] [66] This vocal activity, though effective for social cohesion, elevates predation vulnerability from nocturnal predators like skuas, underscoring a trade-off in colonial signaling strategies. [67] Species-specific call variations also aid in taxonomic discrimination and individual recognition amid dense aggregations. [68]

Mating Systems and Pair Bonds

Procellariiformes are characterized by social monogamy, with individuals forming long-term pair bonds that persist across multiple breeding seasons or even lifetimes, facilitated by their extended lifespans and high reproductive costs.[61] These bonds enhance breeding success through synchronized parental care for a single chick per season.[69] Mate fidelity remains strong, as re-pairing incurs risks such as delayed breeding and reduced offspring viability.[70] Courtship rituals are elaborate and species-specific, serving to assess mate quality and reinforce bonds. In albatrosses (Diomedeidae), diurnal pairs perform synchronized terrestrial displays including mutual preening, bowing, bill-touching (billing), head-swinging, and loud vocalizations like sky-pointing calls, often lasting several years before full pair formation.[71] Nocturnal procellariids such as petrels and shearwaters engage in aerial chases, synchronized noisy flights, and ground-based duets with throat-puffing and wailing calls to establish or maintain pairs.[3] These displays emphasize visual, auditory, and olfactory cues, with olfactory recognition aiding individual pair identification.[56] Divorce, or pair dissolution, is infrequent but linked to prior reproductive failure, where unsuccessful pairs are up to three times more likely to separate than successful ones.[72] In wandering albatrosses, lifetime divorce rates average 3-5%, though recent studies report increases to 8% correlated with elevated sea surface temperatures, suggesting environmental stress disrupts bonds.[73] Personality traits influence stability, with bolder males exhibiting lower divorce rates.[74] Sex ratio imbalances, such as female scarcity, also elevate divorce in species like wandering albatrosses, reaching 13% in skewed populations.[75] Extra-pair copulations occur but yield low extra-pair paternity rates, preserving genetic monogamy in most cases; for instance, shy albatrosses show minimal genetic infidelity despite long-term bonds.[76] In petrels like Antarctic petrels, molecular analyses confirm rare extrapair events amid abundant mating opportunities.[77] Shearwaters and prions similarly maintain high social and genetic fidelity, with extrapair paternity below 5% in studied populations.[78] This system aligns with ecological constraints, including burrow competition and biparental investment, minimizing benefits of infidelity.[79]

Breeding Cycles and Chick Rearing

Procellariiformes exhibit extended breeding cycles adapted to their pelagic lifestyles, with most species returning to remote island colonies annually for reproduction, though larger albatrosses often breed biennially due to the high energetic costs of chick rearing. Breeding seasonality varies by latitude and species; southern hemisphere populations, such as wandering albatrosses (Diomedea exulans), typically initiate courtship in austral summer (November–December), with egg-laying following in December–January.[80] Northern hemisphere shearwaters, like the sooty shearwater (Ardenna griseus), arrive at colonies in September–October for egg-laying in November. Colonies are densely packed, with nesting habits differing by size: albatrosses nest on open ground or slopes, while petrels and smaller procellariids excavate burrows to evade predators.[3] Pairs engage in mutual preening and vocal displays to reaffirm bonds before the female lays a single large egg, reflecting a strategy of high parental investment in few offspring.[81] Incubation is biparental, with both sexes sharing duties in shifts lasting from days to weeks, depending on species and environmental conditions; periods range from approximately 40 days in storm-petrels to 50–53 days in shearwaters and 78–80 days in albatrosses.[82] [80] The egg's large yolk supports extended development, and parents endure fasting spells ashore, losing significant body mass. Hatching success varies but can reach 80% in monitored populations, with chicks emerging semi-precocial, covered in down, and brooded continuously for the first few weeks by alternating parents to maintain thermoregulation.[83] Chick rearing involves protracted nestling periods, enabling slow growth rates suited to infrequent, nutrient-dense meals delivered via regurgitation of lipid-rich stomach oil and prey items, allowing chicks to fast for days or weeks between feeds as parents forage vast oceanic distances. Nestling durations span 70–80 days in smaller shearwaters like Audubon's (Puffinus lherminieri), 86–106 days in sooty shearwaters, and up to 240–300 days in royal and wandering albatrosses, during which chicks undergo rapid mass gain followed by pre-fledging starvation to reduce weight for flight.[84] [85] Fledging success often exceeds 90% in predator-free sites, with no post-fledging parental care; chicks depart independently to sea, relying on accumulated fat reserves.[83] This K-selected strategy prioritizes offspring quality over quantity, correlating with adult longevity exceeding decades.[81]

Human Interactions

Cultural and Historical Significance

Procellariiform seabirds, especially albatrosses, have long held symbolic importance in maritime folklore as embodiments of the sea's mysteries and harbingers of fate. Sailors historically viewed albatrosses as benevolent spirits or souls of deceased mariners, whose presence signaled calm winds and good luck, while their killing was thought to summon storms and calamity.[86] Storm-petrels, by contrast, earned nicknames like "Mother Carey's chickens" for their pattering flight over waves, interpreted as omens of impending gales, leading to superstitions that harming them invited divine wrath from "Mother Carey," a folk personification of the ocean's perils.[87][88] This albatross lore profoundly influenced Western literature, most notably in Samuel Taylor Coleridge's 1798 poem The Rime of the Ancient Mariner, where a mariner's shooting of an albatross curses his ship with supernatural retribution, coining the enduring idiom "an albatross around one's neck" for a self-inflicted, inescapable burden.[89] The poem drew from real 18th-century seafaring accounts, amplifying the bird's role as a moral emblem of harmony with nature disrupted by hubris.[86] In indigenous Pacific cultures, shearwaters and other procellariiforms carried navigational and spiritual weight; Hawaiian traditions integrated species like the Newell's shearwater ('a'o) into the Kumulipo creation chant, viewing their nocturnal returns to islands as guides for voyagers sighting land after long oceanic passages.[90][91] These birds thus symbolized resilience and cosmic order, aiding empirical wayfinding across vast distances without modern instruments.[91]

Exploitation for Resources

Procellariiform seabirds, including albatrosses, petrels, and shearwaters, have been historically harvested for feathers, which were prized in the millinery trade for hat decorations and other uses. In the late 19th and early 20th centuries, feather poaching targeted breeding colonies, with an estimated 3.5 million seabird feathers collected across Pacific islands between 1897 and 1914.[92] The short-tailed albatross (Phoebastria albatrus) suffered severe declines from systematic harvesting of adults and chicks for feathers, meat, and bones (used as fertilizer) at its Japanese breeding sites, reducing its population to near extinction by the 1940s, with only about 20-30 individuals remaining.[93] Egg collection represented another major resource extraction, with historical records indicating up to 7 million seabird eggs harvested annually in some regions for food.[92] On Laysan Island in the Northwestern Hawaiian Islands, commercial egg harvesting began in the late 19th century, peaking with operations that removed thousands of eggs from procellariiform species like Laysan albatrosses (Phoebastria immutabilis) and shearwaters, contributing to nest site trampling and early population stresses before guano mining intensified impacts.[94] Guano, the accumulated excrement from dense procellariiform colonies on remote islands, was mined extensively as a nitrogen-rich fertilizer starting in the mid-19th century under the U.S. Guano Islands Act of 1856.[95] Petrel and shearwater rookeries provided substantial deposits, but extraction involved destructive scraping of soil and vegetation, leading to habitat loss and incidental bird mortality; on Laysan, guano operations from 1891 onward employed up to 150 Chinese laborers who cleared burrows and nests, exacerbating declines in species like black-footed albatrosses.[94][95] Birds were also rendered for oil, used in lighting and lubrication, and consumed as food, with deliberate capture at sea or on land documented for albatrosses and large petrels through shooting or netting.[96] Storm-petrels were harvested for oil and bait in European and Atlantic contexts, while meat from shearwaters and petrels supplemented diets in island communities.[97] These practices have largely ceased due to legal protections and population crashes, though limited subsistence hunting persists in some remote areas.[96]

Conservation Status

Identified Threats and Causal Factors

Procellariiformes face multiple anthropogenic threats, with bycatch in fisheries, invasive predators, plastic ingestion, and climate change identified as primary drivers of population declines based on global assessments of seabird vulnerabilities.[98] These factors interact causally: fisheries deplete prey while directly killing birds, invasives exploit island naivety evolved without mammalian predators, plastics mimic olfactory and visual cues of natural forage, and climatic shifts disrupt phenological synchrony between breeding and prey availability.[99] Bycatch in pelagic longline fisheries constitutes a direct mortality source, attracting surface-foraging species to baited hooks trailed behind vessels. Globally, longline operations kill an estimated 160,000 seabirds annually, disproportionately affecting albatrosses and large petrels whose life histories—delayed maturity and low fecundity—amplify per-individual impacts.[100] In the Hawaii-based fleet alone, 268 albatrosses were bycaught yearly on average from 2010 to 2016, with higher risks in areas of unregulated or illegal fishing.[101] Causal mechanisms include bait loss rates exceeding 20% in some operations, drawing birds into hook sets, though mitigation like bird-scaring lines reduces incidents by up to 90% where implemented.[102] Invasive alien predators, introduced via human transport to breeding islands, prey opportunistically on unguarded eggs and chicks, exploiting the burrow-nesting habits of many petrels and shearwaters. Rats, cats, and mice cause near-total reproductive failure in affected colonies, with historical introductions linked to extinctions of at least 10 Procellariiform taxa.[44] For instance, in Hawaii, multiple predators depress survival of Newell's shearwaters and Hawaiian petrels, with burrow raids reducing fledging by orders of magnitude compared to predator-free sites.[103] Eradication restores breeding success, as evidenced by post-removal increases exceeding 300% in some Procellariiform populations, underscoring human-mediated introductions as the root cause.[104] Ingestion of marine plastics occurs when debris, conditioned by bacterial films mimicking prey odors like dimethyl sulfide from krill, is mistaken for food during surface sieving. Procellariiformes exhibit the highest ingestion frequencies among seabirds, with 59% of species affected and 29% of individuals containing plastics averaging 5.5 pieces per bird in global reviews up to 2012.[105] This leads to gut blockages, reduced nutrient absorption, and bioaccumulated toxins, with sublethal effects compounding fishery and predation pressures; southern hemisphere studies report plastics in 62% of petrels versus 12% of albatrosses.[106][107] Climate change induces trophic mismatches, with ocean warming shifting prey like myctophid fish poleward and altering krill phenology, forcing extended foraging trips that lower chick provisioning rates.[108] Extreme events, such as 2019-2020 heatwaves, correlate with breeding success dropping to 0-6% in burrow-nesters due to adult overheating and dehydration during incubation.[109] These pressures, ranked third globally after invasives and bycatch, stem from greenhouse gas emissions altering sea surface temperatures by 0.5-1°C per decade in key foraging grounds.[99] Population dynamics in Procellariiformes vary by taxon and region, with long-lived species exhibiting slow intrinsic growth rates that amplify vulnerability to extrinsic mortality factors such as fisheries bycatch and predation. Empirical assessments indicate that approximately 66% of albatross and large petrel species (key subgroups within the order) are classified as threatened with extinction, while 38% show documented population declines, primarily driven by incidental capture in longline fisheries.[110] Smaller petrels and shearwaters often maintain larger, more stable populations, though subsets face localized declines from habitat alteration and invasive species.[99] Long-term monitoring reveals heterogeneous trends: for instance, the Tristan albatross (Diomedea dabbenena) population has decreased by over 2,000 individuals since 2004, despite stable breeding pair counts, due to elevated chick mortality from invasive house mouse predation offsetting adult survival.[111] In contrast, the short-tailed albatross (Phoebastria albatrus) has recovered from fewer than 30 breeding pairs in the mid-20th century to over 650 pairs by 2009, attributed to cessation of feather harvesting and protection from shooting, yielding an annual population increase exceeding 7%.[112] Regional studies, such as in the Indian Ocean, document a 73% rise in breeding populations of large procellariiforms from 1980 to 2005 (annual rate λ = 1.016), yet highlight precipitous declines in subtropical sooty albatrosses (Phoebetria fusca and P. palpebrata), underscoring taxon-specific sensitivities.[113] Empirical data from breeding colony censuses underscore the order's demographic constraints: generation times often exceed 15–20 years, with low fecundity (typically one egg per clutch) resulting in doubling times of 8–40 years under optimal conditions, which delays detection of declines until populations fall below critical thresholds.[114] In the California Current system, 31 populations of 14 Procellariiformes species increased significantly from historical baselines, while 11 populations of seven species declined, reflecting localized responses to varying oceanographic productivity and threat mitigation efficacy.[115] Grey petrels (Procellaria cinerea) exemplify ongoing declines, with suspected moderate rates linked to bycatch at Kerguelen Islands colonies.[116] These trends emphasize the need for sustained, data-driven monitoring to distinguish natural variability from anthropogenic impacts.

Management Strategies and Effectiveness

Management strategies for Procellariiformes focus on mitigating bycatch in commercial fisheries and eradicating invasive predators from breeding islands, with additional efforts in habitat protection and pollution reduction. Bycatch mitigation techniques include bird-scaring lines (tori lines), which deploy streamers from vessels to deter seabirds from baited hooks; night setting to reduce bird activity during line deployment; and weighted branch lines to sink hooks faster beyond seabird reach.[117] These measures have demonstrated substantial effectiveness in reducing incidental capture rates for albatrosses and petrels. For instance, fleet-wide implementation in certain longline fisheries resulted in significant decreases in overall seabird bycatch, with albatross captures nearly eliminated and petrel bycatch greatly reduced in areas like the Kerguelen Islands.[118] Night setting alone achieved bycatch rates as low as 0.046 birds per 1000 hooks in albacore tuna fisheries, compared to over 1 bird per 1000 hooks without it.[119] Branch line weighting has experimentally confirmed reductions in seabird bycatch in high-risk zones.[120] Eradication of invasive mammals such as rats, cats, and mice from islands has proven one of the most successful interventions for Procellariiformes, enabling recovery of breeding populations by eliminating nest predation. Over 1,000 islands worldwide have undergone such eradications targeting 25 invasive predator species, with Procellariiformes showing improved breeding success and colonization post-removal.[104] Seabird assemblages on cleared islands become more diverse over time compared to those never invaded, with species like petrels exhibiting population growth rates indicative of positive demographic responses.[121] [114] For example, following predator removal, monitored Procellariiform populations have displayed increased chick survival and adult return rates, though full recovery can span decades depending on site-specific factors like island size and remaining threats.[122] Despite these advances, effectiveness varies by implementation scale and compliance; while localized successes have stabilized or increased populations for some species, many Procellariiformes remain vulnerable due to incomplete global adoption of mitigation in fisheries and persistent plastic pollution impacts. Demographic modeling of bycatch-vulnerable species like the white-chinned petrel shows that consistent mitigation can shift populations from decline to stability.[123] Conservation translocations and monitoring complement these strategies, aiding restoration on restored islands.[124] Overall, targeted actions under frameworks like the Agreement on the Conservation of Albatrosses and Petrels have averted extinctions but require broader enforcement to reverse broader declines.[117]

References

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