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Procellariiformes

 
Sci-Tech Dictionary: Procellariiformes
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(′prō·sə·lə′rī·ə′för′mēz)

(vertebrate zoology) An order of oceanic birds characterized by tubelike nostril openings, webbed feet, dense plumage, compound horny sheath of the bill, and, often, a peculiar musky odor.

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Animal Classification: Procellariiformes
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Family: Albatrosses
Family: Shearwaters, Petrels, and Fulmars
Family: Storm-Petrels
Family: Diving-Petrels

(Tubenosed seabirds)

Class: Aves

Order: Procellariiformes

Number of families: 4 families

Number of genera, species: 23 genera; 108 species

Introduction

Procellariiformes are exclusively marine birds. Also commonly known as petrels, tubinare, or tube-noses, this order is extremely diverse: from the massive, yet majestic, wandering albatross (Diomedea exulans) to the tiny, wave-dancing least storm-petrel (Halocyptena microsoma).

Traditionally there are four families within the order Procellariiformes: the Diomedeidae (albatrosses); the Procellariidae (giant petrels, fulmars, gadfly petrels, and shearwaters); the Hydrobatidae (storm-petrels); and the Pelecanoididae (diving-petrels). These four families include 23 genera and 108 species.

Evolution and systematics

The oldest Procellariiform fossil is from the early Paleocene, some 60 million years ago. However, a DNA-based study published in 1997 suggests that the order is even older and was distinct from penguins (order Sphenisciformes) and divers (order Gaviiformes) prior to the end of the Cretaceous. Thus, like many early avian groups, the Procellariiformes survived the mass extinction event at the end of Cretaceous about 65 million years ago. The fossil record of the Procellariiformes is generally poor, but a few sixteen million-year-old fossils show that even then albatrosses and shearwaters were very similar to modern-day species.

Procellariiformes are thought to have first evolved in the Southern Hemisphere and two-thirds of extant species are still found in this region. Surprisingly, most Procellariiform fossils have been found north of the equator. Many albatross fossils from the Pliocene (2 to 5 million years ago) have been recovered from Europe, North America, and Japan. This northern bias may simply reflect relative effort and the greater amount of landmass in the Northern Hemisphere. A few fossils from Australia, South Africa, and Argentina do confirm, however, the presence of albatrosses in the southern oceans over five million years ago.

DNA-DNA hybridization and DNA sequencing have confirmed the common ancestry of all Procellariiformes, but the taxonomy within the order is complex and subject to constant revision. John Warham, in his detailed book The Petrels, states that "the classification and systematics of Procellariiformes have long been the subject of controversy and a general agreement on species' limits in the near future seems unlikely." His prediction proved to be accurate. For example, in 1997 it was suggested that the number of albatross species should be revised from 14 to 24.

Physical characteristics

The unifying characteristic of Procellariiformes is their tubular nostrils. In the albatrosses (Diomedeidae) the tubular nostrils protrude from each side of the bill whereas in the three other Procellariiform families the nostrils are fused and sit prominently at the base of the upper bill. Unlike most other birds, petrels are thought to have a have a highly developed sense of smell, which they use to locate food and breeding sites. The tubular nostrils may enhance this sense or the tubes could simply act to keep the salty solution produced by the nasal glands away from the face and eyes.

Another unique feature of this order is the structure of the bill. Unlike any other birds, the bills of Procellariiformes are split into seven to nine distinct horny plates. The hooked bill of petrels is formed by a plate on the upper bill called the maxillary unguis. The hooked, stout, and very sharp unguis can firmly hold slippery food items such as fish and squid. In smaller Procellariiformes the cutting edges of the plates in the lower bill (tomia) are more comb-like and form filters for feeding on plankton and other small items of food.

Procellariiformes show the greatest range in body size of any avian order. The smallest species is the least storm-petrel (Halocyptena microsoma), which weighs less than 1 oz (20 g) and has a wingspan of 12.5 inches (32 cm). The largest species, the wandering albatross (Diomedea exulans), can weigh over 24 pounds (11 kg) and has a wingspan of up to 12 feet (3.6 m).

The plumages of Procellariiformes are generally quite plain and are composed of black, brown, gray, or white feathers. The legs and feet are usually black, but some are flesh-colored or mottled. In prions, diving-petrels, and little shearwaters (Puffinis assimilis) the feet and legs are blue. The bills of Procellariiformes are usually dark gray or black although some have yellow, orange, or pink coloration.

Also peculiar to Procellariiformes is stomach oil. This pale oil mainly contains wax esters and triglycerides and has a dietary origin. It is stored in the large, sac-like proventriculus that separates the esophagus and gizzard. Enzymes secreted within the proventriculus allow Procellariiformes to metabolize the wax esters. The oil is used by both chicks and adults as an energy-rich food source during the potentially long periods between meals. The oil has a strong smell and may give the Procellariiformes their characteristic musty odor. Giant petrels (Genus Macronectes) are particularly pungent, hence their nickname "stinkers."

The oil has a second function. If chicks or ground-nesting adults are threatened, the oil can be regurgitated from the proventriculus and sprayed over a considerable distance. When the oil cools it has a wax-like consistency and can damage the plumage of predatory birds such as skuas (Laridae; Stercorariinae).

Distribution

Procellariiformes have the widest distribution of any avian order. Antarctic petrels (Thalassoica antarctica) and snow petrels (Pagodroma nivea) breed so far south that birds have to fly over a hundred miles from their inland colony before they reach the coastline of the Antarctic continent. In the Northern Hemisphere, fulmars (Fulmaris glacialis) nest on the northeastern tip of Greenland, as far into the Arctic as any land reaches. Petrels occur in all oceans but are most numerous in the Southern Hemisphere and are least abundant in the tropics.

Habitat

Petrel colonies are mostly found on remote islands away from land-based predators. Those that nest on larger islands or mainland continents do so in areas with low numbers of predators, such as deserts or mountainsides.

The breeding sites of the larger petrels must be wind-swept. Albatrosses and other large petrels cannot take off or forage widely for food without the help of strong winds. The subantarctic islands so favored by Procellariiformes are in latitudes referred to by sailors as the 'Roaring Forties' and 'Furious Fifties' because of the powerful, westerly winds that blow throughout the year.

Outside the breeding season, Procellariiformes spend virtually all their time at sea. Their distribution is largely governed by the availability of food, which is in turn influenced by the distribution of currents, upwellings, and weather conditions. However, some Procellariiformes, such as short-tailed shearwaters (Puffinus tenuirostris) and Manx shearwaters (Puffinus puffinus), make predictable return migrations between the Northern and Southern Hemispheres. Although migrating at the same time and in the same direction, these two species do not breed in the same hemisphere. The Manx shearwater favors the northern summer whereas the short-tailed shearwater, like most petrels, breeds during the summer months of the Southern Hemisphere. Research published in 2000 has shown that wandering albatrosses (Diomedea exulans) also have predictable migrations. Adults that nest on the Crozet Islands near South Africa return to the same patch of ocean at the end of each breeding cycle. However, the favored area could be as far away as Australia and may be different for each adult albatross.

Behavior

Most petrels are gregarious. At sea they can occur in large multi-species flocks around natural food sources or fishing boats. Squabbles are common and the large, aggressive albatrosses and giant petrels usually displace other species.

Petrels are also gregarious during breeding and can form huge colonies. Surface-nesters usually build their nests just beyond the pecking distance of their nearest neighbor. Larger albatrosses and the northern giant petrel (Macronectes halli) nest on the ground but not in dense colonies. More commonly their nests are loosely scattered along hillsides, headlands, or mountain ridges. Smaller petrels nest in dense, single-species colonies but usually excavate burrows or squeeze behind rocks.

Many petrels have elaborate display rituals in order to choose a mate or maintain a pair bond. Diurnal species such as albatrosses perform terrestrial dances or synchronized "aerial-ballet" routines. The courtship display of other petrels can be equally impressive. The display of the black-winged petrel (Pterodroma nigripennis) consists of swooping aerial chases and loud high-pitched calls. Species that return to their breeding sites after dusk tend to have less elaborate displays but can still be extremely vocal.

Most Procellariiformes are silent at sea unless competing for food. On land, various piping calls, shrieks, croaks, and other calls are produced at the nest or burrow. Albatrosses produce a variety of calls that accompany their complex displays. Shearwaters are renowned for the eerie human-like cries they produce from within their burrows.

Feeding ecology and diet

Among seafarers, albatrosses were well known for their ability to effortlessly follow ships for thousands of miles. By gliding on long, narrow wings, albatrosses, fulmars, petrels, and shearwaters can use the ocean winds to cover vast distances in search of food. However, not all Procellariiformes fly so economically. The short, stubby wings and rounded, penguin-like body of diving-petrels is more adapted to a life under the water than above it.

Typically petrels search for their patchily distributed food either offshore or beyond the continental shelf. Their search can take them thousands of miles from their breeding colony. Studies using satellite-tracking devices have shown that some albatrosses breeding on the Crozet Islands forage up to 1,600 mi (2,600 km) away from their nest. In contrast, divingpetrels predominantly search for food in inshore waters close to their breeding sites.

Petrels usually find their food close to or on the surface of the ocean although shearwaters, diving-petrels, and even some albatrosses can dive more than 30 ft (10 m) below the surface. Squid is the principal food source for most large petrels, although they will opportunistically eat other seabirds and carrion. Carcasses of seals, whales, and cuttlefish will attract hungry albatrosses while other Procellariiformes such as gadfly petrels and storm-petrels will mop up any scraps. Only giant petrels regularly forage for food on land. Petrels also exploit the actions of whales, dolphins, sharks, and tuna.

These marine predators will push schools of fish close to the surface and within reach of the shallow-diving-petrels. Stormpetrels and prions eat zooplankton such as copepods, amphipods, and fish eggs, which they delicately pluck from the surface of the ocean.

Concentrations of sea life occur where upwellings bring nutrient-rich waters closer to the surface. But even in these regions the abundance of food is largely unpredictable and the physiology of Procellariiformes reflects the ephemeral nature of their food sources. At 100°F (38°C), the body temperature of petrels is lower than most birds (105°F; 41°C). Therefore, less energy is required to maintain body temperature and less heat is lost. When food is plentiful, layers of subdermal fat and stomach oil can store excess energy until it is needed. The digestive tract of Procellariiformes is unusual in that the esophagus passes unrestricted into the proventriculus, which fills a large proportion of the abdominal cavity. The size of the proventriculus allows very large meals to be consumed and stored.

Reproductive biology

Procellariiformes are long-lived, very slow breeders. None can breed in the first year, and the largest petrels wait over a decade before breeding for the first time. In each breeding attempt, all Procellariiformes lay a single white egg. The egg is large relative to body size and can be up to 28% of the mother's body weight. Incubation in petrels is prolonged (6 to 11 weeks): about twice as long as gull (Laridae) eggs of a similar size. A petrel chick takes between two and nine months to fledge, twice as long as gulls of the same body mass. The reasons behind such a slow growth rate are thought to be associated with breeding sites and the parents' ability to feed the young. Terrestrial predators are usually absent from the islands where petrels breed, which removes the pressure to fledge a chick quickly. Also, food is rarely abundant close to breeding sites, so a fast growing chick would be more likely to starve during the potentially long periods between meals.

All Procellariiformes form exclusive social pairings, but behavioral and DNA-based studies have shown that infidelity does occur and males are not always the genetic fathers of the chick they help to raise. Copulations occur at the nest and are often preceded by complex behaviors or mutual allopreening.

Both sexes build or excavate the nests, incubate the egg, and provision the chick. Initially, surface-nesting petrels protect the chick from potential predators. Later, both parents leave the chick while they forage for food. A healthy chick can defend itself by regurgitating the stomach oil stored in its proventriculus.

Petrels receive little or no post-fledging care. They spend their first 2–11 years at sea before returning to their natal site to breed. Rarely, a young bird will return to a different island or colony to make its first breeding attempt.

Conservation

There are 108 extant species of Procellariiformes. Of these, 23 are threatened with extinction. Only one species, the Guadalupe storm-petrel (Oceanodroma macrodactyla), has become extinct since 1600. The principal threats to petrels are mammalian predators introduced to breeding islands and interactions with fishing vessels.

Humans have accidentally or deliberately introduced cats, rodents, possums, pigs, mustelids, rabbits, goats, foxes, and other mammals to petrel breeding sites. They usually have a severe impact. On Marion Island in the Indian Ocean, the 2000 or so feral cats targeted diving-petrels and killed nearly half a million seabirds each year. Eradication schemes have now successfully removed mammalian predators from many petrel breeding sites. On Australia's subantarctic Macquarie Island, an intensive effort to remove cats saw immediate success when in 2000 gray petrels (Procellaria cinerea) bred successfully on the main island for the first time in 40 years.

Before being banned in 1991, drift-net fisheries were thought to be responsible for killing up to 500,000 seabirds each year. Currently, the greatest threat to foraging seabirds are long-line and trawl fishing boats that annually kill thousands of petrels and have been linked to the decline of many albatross populations. One study published in 1991 estimated that 44,000 albatrosses are killed by the Japanese longline fishery each year. Longline fishers are now expected to use bird-scaring lines and other bycatch mitigation measures in an attempt to reduce the death toll of seabirds.

Significance to humans

Not surprisingly, Procellariiformes have been of most significance to fishermen, whalers, and other seafarers. They are sometimes used to pinpoint fish shoals or a surfacing whale and are the subject of many superstitions. Some thought albatrosses were good omens and to kill one would bring ill fortune. At other times, to see an albatross or touch a stormpetrel was considered to be bad luck. Procellariiformes were also seen as the embodiment of the souls of cruel captains or drowned sailors that were destined to wander the seas for all time.

Petrels have long been used as a source of food for humans and have been found among archaeological remains around the world. Petrels have also sustained many a sailor shipwrecked in the southern oceans. In Alaska, Kodiak Islanders harpooned short-tailed albatrosses (Diomedea albatrus) from canoes, and royal albatross chicks (Diomedea epomophora) were highly prized by New Zealand tribes. Until the late 1980s, the inhabitants of Tristan Island in the Indian Ocean harvested the eggs of yellow-nosed mollymawks (Diomedea chlororhynchos) and sooty albatrosses (Phoebetria fusca). In many places, humans harvested shearwater chicks, also known as "muttonbirds." Tasmanian aborigines ate short-tailed shear-waters (Puffinus tenuirostris) at least 2000 years ago and a highly regulated harvest continues today. In New Zealand, there is a traditional harvest of sooty shearwater chicks (Puffinus griseus). Meticulous records track the number of Manx shearwaters (Puffinus puffinus) harvested from colonies on the Isle of Man in the United Kingdom. In the mid 1600s, the annual harvest was 10,000 chicks. However, like most petrel colonies, this population was vulnerable to introduced predators. By 1789, the colony disappeared after a shipwreck introduced rats to the island.

Many places where albatrosses and other petrels breed or forage now attract humans that simply wish to marvel at their size, elegance, and beauty.

Resources

Books:

del Hoyo, J., A. Elliot, and J. Sargatal, eds. "Ostrich to Ducks." Vol. 1 of Handbook of the Birds of the World. Barcelona: Lynx Edicions, 1992.

Marchant, S., and P.J. Higgins, eds. "Ratites to Ducks." Vol. 1 of Handbook of Australian, New Zealand and Antarctic Birds. Melbourne: Oxford University Press, 1990.

Tickell, W.L.N. Albatrosses. Sussex: Pica Press, 2000.

Robertson, G., and R. Gales, eds. Albatross Biology and Conservation. Chipping Norton: Surrey Beatty, 1998.

Warham, J. The Petrels. London: Academic Press, 1990.

Periodicals:

Brothers, N. "Albatross Mortality and Associated Bait Loss in the Japanese Longline Fishery in the Southern Ocean." Biological Conservation 55 (1991): 255-268.

Cooper, A., and D. Penny. "Mass Survival of Birds across the Cretaceous-Tertiary Boundary: Molecular Evidence." Science 275 (1997): 1109-1113.

Huyvaert, K. P., D.J. Anderson, T.C. Jones, W.R. Duan, and P.G. Parker. "Extra-pair Paternity in Waved Albatrosses." Molecular Ecology 9 (2000): 1415-1419.

Nunn, G.B. and S.E. Stanley. "Body Size Effects and Rates of Cytochrome b Evolution in Tube-nosed Seabirds." Molecular Biology and Evolution 15 (1998): 1360-1371.

Roby D.D., J.R.E. Taylor, and A.R. Place. "Significance of Stomach Oil for Reproduction in Seabirds: an Interspecies Cross-fostering experiment." The Auk 114 (1997): 725-736.

Weimerskirch, H., N. Brothers, and P. Jouventin. "Population Dynamics of Wandering Albatross Diomedea exulans and Amsterdam albatross D. amsterdamensis in the Indian Ocean and Their Relationships with Long-line Fisheries - Conservation Implications." Biological Conservation 79(1997): 257-270.

Weimerskirch, H. and R.P. Wilson. "Oceanic Respite for Wandering Albatrosses." Nature (2000): 955-956.

[Article by: Michael Colin Double, PhD]

Sci-Tech Encyclopedia: Procellariiformes
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A large order of strictly marine birds found far offshore except when breeding. The procellariforms, or tube-nosed swimmers, are most closely related to their descendant group, the penguins. The Procellariiformes comprise four families: Diomedeidae (albatrosses; 13 species); Procellariidae (shearwaters, petrels, and fulmars; 66 species); Hydrobatidae (storm petrels; 21 species); and Pelecanoididae (diving petrels; 4 species).

The tube-nosed swimmers are characterized by having their nostrils enclosed in a tube, which is paired in albatrosses; dense plumage; webbed feet; and long wings. They range in size from the sparrow-sized storm petrels to large albatrosses, which have the greatest wingspan of all living birds, up to 12 ft (3.7 m). The procellariiforms are excellent fliers, as evidenced by the migratory—actually nomadic wandering—flights of many thousands of miles. Procellariiforms swim well, but only the pelecanoidids dive under water, using their wings for propulsion. They are highly pelagic and feed on fish, squids, and crustaceans. Procellariiforms have a well-developed olfactory sense to locate food and apparently to locate their nesting burrows at night. The larger species mature slowly; some albatrosses begin breeding only after reaching 6 to 8 years of age. Tight pair bonds are formed during courtship, which can take elaborate forms, as is seen in albatrosses. See also Aves.

WordNet: Procellariiformes
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Note: click on a word meaning below to see its connections and related words.

The noun has one meaning:

Meaning #1: petrels; albatrosses; shearwaters; diving petrels
  Synonym: order Procellariiformes

Wikipedia: Procellariiformes
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Procellariiformes
Fossil range: Eocene–Present
Middle Eocene – Recent
Cape Petrel Daption capense
Scientific classification
Kingdom: Animalia
Phylum: Chordata
Class: Aves
Infraclass: Neognathae
Superorder: Neoaves
Order: Procellariiformes
Fürbringer, 1888[1]
Families

Procellariidae
Diomedeidae
Hydrobatidae
Pelecanoididae
Diversity
4 Families, 23 Genera, 108 Species

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

Procellariiformes 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. Procellariiformes are monogamous and form long-term pair bonds which are formed over several years and may last for the life of the pair. Only a single egg is laid per nesting attempt, and usually only 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 fledgling periods. Once a chick has fledged there is no further parental care.

Procellariiformes 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. They have also been the subject of numerous cultural depictions, particularly albatrosses. Procellariiformes are one 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.

Contents

Etymology

Procellariiformes comes from the Latin word procella which means a violent wind or a storm, and iformes which is added to symbolize order. Therefore a violent wind or a storm refers to the fact that members of this order like stormy and windy weather.[4]

Biology

Distribution and movements

The Procellariiformes 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 furthest north piece of land.[5] The most cosmopolitan family is the Procellariidae, although within that family there are some gaps in distribution. 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. The shearwaters have the most widespread distribution, although they are absent from the Pacific north of Japan as breeding birds.

The storm-petrels are almost as widespread as the procellariids, and fall into two distinct subfamilies; the Oceanitinae have a mostly southern hemisphere distribution and the Hydrobatinae 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.[6] Finally the diving-petrels are restricted to the southern hemisphere.

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 longest measured annual migration of any bird.[7] A number of other petrel species undertake trans-equatorial migrations, including the Wilson's Storm-petrel and the Providence Petrel, but no albatrosses cross do due to their reliance on wind assisted flight. There are other long-distant migrants within the order; Swinhoe's Storm-petrels breed in the western Pacific and migrates to the western Indian Ocean,[8] and Bonin Petrels nesting in Hawaii migrate to the coast of Japan during the non-breeding season.[9]

Morphology and flight

The Southern Royal Albatross is the largest of the Procellariiformes

Procellariiformes range in size from the very large Wandering Albatross, at 11 kg (24 lb) and a 3.6 m (12 ft) wingspan, to the tiny Least Storm-petrel, at 20 g (0.71 oz) and a 32 cm (13 in).[5] They have their nostrils enclosed in one or two tubes on their straight, deeply grooved bills with hooked tips. The beaks are made up from several plates. Wings are long and narrow; feet are webbed, and the hind toe is undeveloped or non-existent. Plumage is predominantly black, white and grey.

The order has a few unifying characteristics, starting with their tubular nasal passage which is used for olfaction.[10] This ability to smell helps to locate patchily distributed prey at sea and may also help locate their nests within nesting colonies.[11] The structure of the bill, which contains seven to nine distinct horny plates, is anothery unifying feature, although there are differences within the order. Petrels have a plate called Maxillary unguis that forms a hook on their upper bill. The smaller members of the order have a comb-like lower bill, made by the tomia plate, for plankton feeding. Finally, they have a stomach oil stored in their provemtriculus that can be used as a food source during their long flights and also as a defense mechanism.[5]

Procellariiformes have a need to lower their salt content due to their drinking of ocean water. All birds have an enlarged nasal gland at the base of the bill, above they eyes. This gland is inactive in species that don't require it; however the Procellariiformes do require its use. Scientists are uncertain as to its exact processes, but do know in general terms that it removes salt that forms a 5% saline solution that drips out of their nose or is forcibly ejected in some petrels.[12]

Most albatrosses and procellariids use two techniques 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.[13]

Most 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 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 as well as for defence.

Breeding behaviour

Breeding colonies

Christmas Shearwaters are one of the surface nesting tropical Procellariiformes.

All Procellariiformes 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.[14] For almost all species the need to breed is the only reason that Procellariiformes 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.[5] Within the colonies pairs defend usually small territories (the giant petrels and some albatrosses can have very large territories) which is either the small area around the nest or a burrow. Competition between pairs can be intense, as can 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.[15] 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. Colonies are often composed of several different species of both petrels and other seabirds.

Procellariiformes 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. In the ringing studies birds ringed as chicks are recapatured close to their original nests, a tendency which can be extreme at times; in Laysan Albatross the average distance between hatching site and the site where a bird established its own territory was 22 m (72 ft),[16] and a study of Cory's Shearwaters nesting near Corsica found that of nine out of 61 male chicks that returned to breed at their natal colony actually bred in the burrow they were raised in.[17] Mitochondrial DNA provides evidence of restricted gene flow between different colonies, strongly suggesting philopatry.[18]

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 which returned to the same site for 25 years. The average number of birds returning to the same nesting sites is high in all species studied, with figures of around 91% for Bulwer's Petrels,[19] and 85% of males and 76% of females for Cory's Shearwaters (after a successful breeding attempt).[20]

Pair bonds and life history

Wandering Albatrosses performing their mating dances on the Kerguelen Islands.

Procellariiformes are monogamous breeders and form long term pair-bonds. These pair bonds take several years to develop in some species, particularly with the albatrosses. Having formed they will last for many breeding seasons, in some cases for the life of the pair. Petrel courtship can be an elaborate affair. It reaches its extreme with the albatrosses, where pairs of albatrosses spend many years perfecting and elaborate mating dances.[21] 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).[22] Each particular pair will develop their own individual version of the dance. The breeding behaviour of other Procellariiformes are less elaborate, although similar bonding behaviours are involved, particularly for the surface nesting procellariids. These can involve synchronised flights, mutual preening and calling. Calls are important for helping birds locate potential mates and distinguish between species and may also serve a function in helping individuals assess the quality of potential mates.[23] After pair formation has occurred calls also serve to help them reunite, the ability of individuals to recognise their own mate has also been demonstrated in several species.

Procellariiformes are k-selected. Breeding is delayed for several years after fledging, sometimes for as long as eight or ten years in the case of larger species. Once they begin breeding they make only a single breeding attempt per nesting season, even if the egg is lost early on in the season they will seldom relay. Large amounts of effort are placed into laying a single (proportionally) large egg and raising a single chick. Procellariiformes are long-lived, the longest living albatross known survived for 51 years but was probably older,[24] even the tiny storm-petrels are known to have survived for 30 years.[25]

Nesting and chick rearing

A semi-precocial Wedge-tailed Shearwater chick with guarding parent.

The majority of Procellariiformes nest once a year and do so seasonally.[26] 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 consecutive years. Most temperate and polar species nest over the spring-summer, although some albatrosses and procellariids nest over the winter. In the tropics some species breed throughout the year, but most nest in discreet periods. Procellariiformes return to the nesting colonies several months before laying, and attend their nesting sites regularly before copulation. Prior to laying females embark on a pre-laying exodus to build up reserves of energy to lay the comparably large egg.

When the female returns and lays the male takes the first incubation stint and the female returns to sea. Incubation is shared between both sexes. The duration of individual stints varies from just a few days to several weeks, during which the incubating bird can lose a considerable amount of weight.[27] 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 be as long as 70 to 80 days, which is the longest incubation period of any bird.[28]

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, for surface nesting species, which have to deal with a greater range of weather and also have to content with predators like skuas and frigatebirds, and consequently have longer guard phases, as long as two weeks in procellariids and three weeks in albatrosses.[29]

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.

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.[30] This can be a real advantage for species that range over huge distances to provide food for hungry chicks.[31] The oil is also used in defence. All Procellariiformes create stomach oil except the diving-petrels.[30]

The chick fledges between two and nine months 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 not a lot of predators at the nesting colonies, therefore there is no pressure to fledge quickly. Second, the time between feedings is long due to the distance and a chick the had a higher growth rate would stand a better chance of starving to death.[5] The durations between feedings vary between species and during the stages of development. Small feeds are frequent during the guard phase, but afterwards become less frequent.

Relationship with humans

Role in culture

The most important family in terms of cultural importance is the albatrosses, which have been described by one author as "the most legendary of birds".[32] Albatrosses have featured in poetry in the form of Samuel Taylor Coleridge's famous poem The Rime of the Ancient Mariner, which in turn gave rise to the usage of albatross as metaphor for a burden.[33] 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.[34] However, there also has been the belief that albatrosses were good omens and to kill one would bring bad luck.[5]

In Russian, many petrel species from the Hydrobatidae and Pelecanoididae 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".[35] 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.[36]

Exploitation

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,[37] although it is likely that they were exploited prior to this. Since then many other marine cultures, both subsistence and industrial, have exploited Procellariiformes, in some cases almost to extinction. Some cultures continue to harvest shearwaters (a practice known as muttonbirding); for example the Maori of New Zealand,who 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 have been harvesting the eggs of the Yellow-nosed Mollymawks, Diomedea chlororhynchos, and Sooty Albatrosses, Phoebetria fusca.[5] 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.[38]

Threats and conservation

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".[15] 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 the Wilson's Storm Petrel (an estimated 20 million individuals) and the Short-tailed Shearwater (an estimated 30 million individuals); while the total population of some other species barely reaches more than two hundred individuals. There are less than 200 Magenta Petrels breeding on the Chatham Islands, only 400 Zino's Petrels and only 80 Amsterdam Albatrosses. Only one species is thought to have become extinct since 1600, the Guadalupe Storm-petrel of Mexico, although a number of species had died out before this. Numerous species are very poorly known, the Fiji Petrel has only been seen a handful of times since its discovery and the breeding colonies of the New Zealand Storm-petrel, Hornby's Storm-petrel and Heinroth's Shearwater have never been located. So little is known about the New Zealand Storm-petrel that is was thought extinct for 150 years until its rediscovery in 2003, although this record is dwarfed by that of the Bermuda Petrel which was considered extinct for 330 years.

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.[39][40] However bad this number is, before 1991 and the ban on drift-net fisheries, it was estimated that 500,000 seabirds a year died as a result.[5] This has led to spectacular declines in some species, as Procellariiformes are slow breeders and cannot replace their numbers fast enough.

Exotic species introduced to the remote breeding colonies is also a threat to all types of Procellariiformes. These principally take the form of predators; most albatross and petrel species are clumsy on land and are unable to defend themselves from mammals such as rats, feral cats and pigs. This phenomenon, known as ecological naivete, has resulted in numerous declines in many species and has been strongly implicated in the extinction of the Guadalupe Storm-petrel.[41] Introduced herbivores can also cause problems if they unbalance the ecology of the island; introduced rabbits destroyed the forest understory on Cabbage Tree Island off New South Wales; this both 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 birdlime tree (Pisonia umbellifera), a native plant. 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.[42]

This albatross bolus was 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 and death.

In the past exploitation was a threat (see above), although this is less of a threat now. Other threats the ingestion of plastic flotsam. Once swallowed, this 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.[43] This can also be picked up by foraging adults and fed to chicks, stunting their development and reducing the chances of successfully fledging.[44] Procellariids are also vulnerable to general marine pollution, as well as oil spills. Some species, such as the Barau's Petrel and the Newell's Shearwater, which nest high up on large developed islands are victims of light pollution. Chicks that are fledging are attracted to streetlights and are unable to reach the sea. An estimated 20–40% of fledging Barau's Petrels are attracted to the streetlights on Réunion.[45]

Taxonomy and systematics

At one point (until the beginning of the 20th century), the family Hydrobatidae was named Procellariidae, and the family now called Procellariidae was rendered "Puffinidae." The order itself was called Tubinares. A major early work on this group is F. DuCane Godman's Monograph of the Petrels, five fascicles, 1907—1910., with portraits of figures by John Gerrard Keulemans.

In the Sibley-Ahlquist taxonomy, the tubenoses are included in a greatly enlarged order "Ciconiiformes". This taxonomic treatment is almost certainly erroneous, but the assumption of a close evolutionary relationship with other "higher waterbirds" – such as loons (Gaviiformes) and penguins (Sphenisciformes) – appears to be correct[citation needed].

There are a total of around 125 living species of Procellariiformes worldwide,[3] and the order is typically divided into four extant and one prehistorically extinct families:

The Hydrobatidae's two subfamilies, Oceanitinae and Hydrobatinae, are probably better treated as distinct families.[46]

Primodroma, a fossil procellariiform from the Early Eocene London Clay of England, may belong to the Hydrobatidae (perhaps specifically to the Oceanitinae) or maybe the Diomedeoididae.

A few rather fragmentary Late Cretaceous and Paleogene fossils have been occasionally allied with or even placed in the Procellariiformes. Marinavis, Neogaeornis, Novacaesareala, Torotix and Tytthostonyx seem to be "higher waterbirds" but cannot be reliably assigned to any of the modern lineages; rather, most of them appear to be still very close to the last common ancestor of Procellariiformes, cormorants, loons, pelicans, penguins, and perhaps also grebes, flamingos, storks, tropicbirds and waders. If they can be assigned to a modern order (which is highly doubtful), with the possible exception of Marinavis they would probably not be considered Procellariiformes. Eopuffinus and Manu on the other hand are more likely members of the Procellariiformes; the former might be an ancestral petrel, the latter an ancient albatross. As regards Lonchodytes (or rather its type species L. estesi), it is the best candidate for the most ancient procellariiform known to date; it pre-dates the evolutionary radiation that brought about the modern families and hence would occupy a basal position in the order. Parascaniornis on the other hand was formerly assigned to the Procellariiformes by some, but it is actually a hesperornithiform synonymous with Baptornis.

Evolution

Fossil records indicate that Procellariiformes have been around at least 60 million years, but a DNA-based study from 1997 states that they have been around into the Cretaceous Period and survived the Cretaceous–Tertiary extinction event. This Order was distinct from Sphenisciformes, Penguins, and Gaviiformes, Divers, before the extinction event. Fossil records are rare but 16 million year old fossils show that Albatrosses and Shearwaters haven't changed much since then. It is believed that they evolved first in the Southern Hemisphere, even though the majority of the fossils have been found in the Northern Hemisphere. This is likely due to the fact that there is more land to find fossils in the north. DNA evidence has confirmed common ancestry for all Procellariiformes, however, the taxonomy within the order is complex and fluctuating.[5] The fossil record of the diving-petrels goes back to the Miocene, with a species from that family being described in 2007.[47] 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.[48]

References

  1. ^ * Brands, Sheila (Aug 14 2008). "Systema Naturae 2000 / Classification - Parker (1982)". Project: The Taxonomicon. http://sn2000.taxonomy.nl/Parker/1982/Classification/51469.htm. Retrieved 12 Feb 2009. 
  2. ^ Warham, J. (1996). The Behaviour, Population, Biology and Physiology of the Petrels. London: Academic Press, ISBN 0-12-735415-8
  3. ^ a b Brooke, M. (2004). Albatrosses And Petrels Across The World Oxford University Press, Oxford, UK ISBN 0-19-850125-0
  4. ^ * Gotch, A. F. (1995) [1979]. "Albatrosses, Fulmars, Shearwaters, and Petrels". Latin Names Explained. A Guide to the Scientific Classifications of Reptiles, Birds & Mammals. New York, NY: Facts on File. p. 190. ISBN 0 8160 3377 3. 
  5. ^ a b c d e f g h i * Double, D. C. (2003). "Procellariiformes". in Hutchins, Michael. Grzimek's Animal Life Encyclopedia. 8 Birds I Tinamous and Ratites to Hoatzins (2 ed.). Farmington Hills, MI: Gale Group. pp. 107–110. ISBN 0 7876 5784 0. 
  6. ^ Olson, S.L., Hearty, P.J. (2003) "Probable extirpation of a breeding colony of Short-tailed Albatross (Phoebastria albatrus) on Bermuda by Pleistocene sea-level rise." Proceedings of the National Academy of Science 100: (22) 12825–12829.
  7. ^ Shaffer S.A., Tremblay Y., Weimerskirch H., Scott D., Thompson D.R., Sagar P.M., Moller H., Taylor G.A., Foley D.G., Block B.A., Costa D.P. (2006) "Migratory shearwaters integrate oceanic resources across the Pacific Ocean in an endless summer." Proc Natl Acad Sci. 103(34): 12799–12802
  8. ^ Van Den Berg AB, Smeenk C, Bosman CAW, Haase BJM, Van Der Niet AM, Cadée GC (1990) "Barau’s petrel Pterodroma baraui, Jouanin’s petrel Bulweria fallax and other seabirds in the northern Indian Ocean in June–July 1984 and 1985." Ardea 79:1–14
  9. ^ Seto, N. W. H., and D. O’Daniel. (1999). Bonin Petrel (Pterodroma hypoleuca). In The Birds of North America, No. 385 (A. Poole and F. Gill, eds.). The Birds of North America, Inc., Philadelphia, PA.
  10. ^ Lequette, B., Verheyden, C., Jowentin, P. (1989) "Olfaction in Subantarctic seabirds: Its phylogenetic and ecological significance" The Condor 91: 732-135. [1]
  11. ^ Bonadonna, Francesco, Cunningham, Gregory B., Jouventin, Pierre, Hesters, Florence, Nevitt, Gabrielle A. (2003) Evidence for nest-odour recognition in two species of diving petrel. J. Exp. Biol. 206:3719-3722 abstract
  12. ^ Ehrlich, Paul R.; Dobkin, David, S.; Wheye, Darryl (1988). The Birders Handbook (First ed.). New York, NY: Simon & Schuster. pp. 29–31. ISBN 0 671 65989 8. 
  13. ^ Pennycuick, C. J. (1982). "The flight of petrels and albatrosses (Procellariiformes), observed in South Georgia and its vicinity". Philosophical Transactions of the Royal Society of London B 300: 75–106.
  14. ^ West, J. & Nilsson, R. (1994) "Habitat use and burrow densities of burrow-nesting seabirds on South East Island, Chatham Islands, New Zealand" Notornis (Supplement) 41 27-37 [2]
  15. ^ a b Medeiros R., Hothersall B. and Campos A. (2003) "The use of artificial breeding chambers as a conservation measure for cavity-nesting procellariiform seabirds: a case study of the Madeiran storm petrel (Oceanodroma castro)" Biological Conservation 116(1): 73-80 http://dx.doi.org/10.1016/S0006-3207(03)00178-2
  16. ^ Fisher, H.I., (1976) "Some dynamics of a breeding colony of Laysan Albatrosses. Wilson Bulletin 88: 121–142.
  17. ^ Rabouam, C., Thibault, J.-C., Bretagnolle, V., (1998) "Natal Philopatry and Close Inbreeding in Cory's Shearwater (Calonectris diomedea)" Auk 115(2): 483–486 [3]
  18. ^ Ovenden, J.R., Wust-Saucy, A., Bywater, R., Brothers, N., White, R.W.G. (1991) " Genetic evidence for philopatry in a colonially nesting seabird. the Fairy Prion (Pachyptila turtur)" Auk 108: 688–694. [4]
  19. ^ Mouguin, J-L., (1996) "Faithfulness to mate and nest site of Bulwer's Petrel, Bulweria bulweria at Selvagem Grande" Marine Ornithology 24: 15–18. [5]
  20. ^ Thibault, J-C., (1994) "Nest-site tenacity and mate fidelity in relation to breeding success in Cory's Shearwater Calonectris diomedea" Bird Study 41(1): 25–28.
  21. ^ Jouventin, P., Monicault, G. de & Blosseville, J.M. (1981) "La danse de l'albatros, Phoebetria fusca". Behaviour 78: 43–80.
  22. ^ Pickering, S.P.C., & Berrow, S.D., (2001) "Courtship behaviour of the Wandering Albatross Diomedea exulans at Bird Island, South Georgia" Marine Ornithology 29: 29–37 [6]
  23. ^ Genevois, F; Bretagnolle, V (1994) "Male Blue Petrels reveal their body mass when calling" Ethology Ecology & Evolution 6(3): 377–383.
  24. ^ Robertson, C.J.R. (1993). "Survival and longevity of the Northern Royal Albatross Diomedea epomophora sanfordi at Taiaroa Head" 1937–93. Emu 93: 269–276.
  25. ^ Klimkiewicz, M. K. 2007. Longevity Records of North American Birds. Version 2007.1. Patuxent Wildlife Research Center. Bird Banding Laboratory. Laurel MD.
  26. ^ Brooke, M. (2004) p.46
  27. ^ Warham, J. (1990) The Petrels - Their Ecology and Breeding Systems London: Academic Press. ISBN 978-0127354200
  28. ^ Brooke, M. (2004) p.67
  29. ^ Brooke, M. (2004) p.75
  30. ^ a b Warham, J. (1976) "The Incidence, Function and ecological significance of petrel stomach oils." Proceedings of the New Zealand Ecological Society 24 84-93 [7]
  31. ^ Roby, Daniel D, Taylor, Jan R E, Place, Allen R (1997) "Significance of stomach oil for reproduction in seabirds: An interspecies cross-fostering experiment." The Auk 114 (4) 725-736. [8]
  32. ^ Carboneras, C. (1992) "Family Diomedeidae (Albatross)" in Handbook of Birds of the World Vol 1. Barcelona:Lynx Edicions, ISBN 84-87334-10-5
  33. ^ Lasky E (1992). "A Modern Day Albatross: The Valdez and Some of Life's Other Spills." The English Journal, 81 (3): 44–46. doi:10.2307/820195
  34. ^ Carboneras, C. (1992) "Family Hydrobatidae (Storm-petrels)" P.p 258-265 in Handbook of Birds of the World Vol 1. Barcelona:Lynx Edicions, ISBN 84-87334-10-5
  35. ^ "A Legend Exhumed", review of "STORMY PETREL: THE LIFE AND WORK OF MAXIM GORKY" by Dan Levin. 329 pages. Appleton-Century. Review published in the Time Magazine, Friday, Jun. 25, 1965
  36. ^ "The Song of the Stormy Petrel", Translation by Sally Ryan
  37. ^ Simeone, A. & Navarro, X. (2002) "Human exploitation of seabirds in coastal southern Chile during the mid-Holocene" Rev. chil. hist. nat 75(2): 423–431 [9]
  38. ^ Higham, J (1998). "Tourists and albatrosses: the dynamics of tourism at the Northern Royal Albatross Colony, Taiaroa Head, New Zealand". Tourism Management 19 (6): 521–531. doi:10.1016/S0261-5177(98)00054-5. 
  39. ^ BirdLife International/RSPB (2005) Save the Albatross: The Problem Retrieved March 17, 2006
  40. ^ Brothers NP. 1991. "Albatross mortality and associated bait loss in the Japanese longline fishery in the southern ocean." Biological Conservation 55: 255–268.
  41. ^ A contemporary account of the decline of the Guadalupe Storm-petrel can be found here - Thayer, J. & Bangs, O (1908) "The Present State of the Ornis of Guadaloupe Island" Condor 10(3): 101-106 [10]
  42. ^ Carlile, N., Proiddel, D., Zino, F., Natividad, C. & Wingate, D.B. (2003) "A review of four successful recovery programmes for threatened sub-tropical petrels" Marine Ornithology 31: 185–192
  43. ^ Pierce, K., Harris, R., Larned, L., Pokras, M., (2004) "Obstruction and starvation associated with plastic ingestion in a Northern Gannet Morus bassanus and a Greater Shearwater Puffinus gravis" Marine Ornithology 32: 187–189 [11]
  44. ^ Auman, H.J., Ludwig, J.P., Giesy, J.P., Colborn, T., (1997) "Plastic ingestion by Laysan Albatross chicks on Sand Island, Midway Atoll, in 1994 and 1995." in Albatross Biology and Conservation, (ed by G. Robinson and R. Gales). Surrey Beatty & Sons: Chipping Norton. Pp. 239-44 [12]
  45. ^ Le Correa, M., Ollivier, A., Ribesc S., Jouventin, P., (2002) "Light-induced mortality of petrels: a 4-year study from Réunion Island (Indian Ocean)" Biological Conservation 105: 93–102
  46. ^ Nunn, G & Stanley, S. (1998): Body Size Effects and Rates of Cytochrome b Evolution in Tube-Nosed Seabirds. Molecular Biology and Evolution 15(10): 1360-1371 PDF fulltext Corrigendum
  47. ^ Worthy, Trevor; Tennyson, Alan J. D.; Jones, C.; McNamara, James A.; Douglas, Barry J. (2007). "Miocene waterfowl and other birds from central Otago, New Zealand". Journal of Systematic Palaeontology 5 (1): 1–39. doi:10.1017/S1477201906001957. ISSN 1477-2019. 
  48. ^ Mayr, Gerald (2009). "Notes on the osteology and phylogenetic affinities of the Oligocene Diomedeoididae (Aves, Procellariiformes)". Fossil Record 12 (2): 133–140. doi:10.1002/mmng.200900003. 

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