Procellariiformes

(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.

Michael Colin Double, PhD