Procellariidae

The family Procellariidae are a group of seabirds which contains four natural groups, the fulmars, the gadfly petrels, the prions and the shearwaters.

This family is part of the bird order Procellariiformes, which also includes the albatrosses, the storm-petrels, and the diving petrels. Although the four groups in the family are uncontroversial, there is widespread disagreement over the number of species and genera.

The procellariids are the most numerous family of tubenoses, and the most diverse, characterised by united nostrils with medium septum, and a long outer functional primary. They range in size from the giant petrels which are almost as large as the albatrosses to the prions which are as small as the diving petrels. They feed on fish, squid and crustacea, with many also taking offal. All species are accomplished long distance foragers and many species undertake long trans-equatorial migrations. They are colonial breeders, exhibiting long term mate fidelity and site philopatry. All species lay a single egg. Incubation times and the chick rearing period are exceptionally long for all procellariids.

Many procellariids are exceptionally common with breeding populations over several million pairs, others number less than 200 birds. Humans have traditionally exploited several species of fulmar and shearwater (known as muttonbirds) for food, fuel and bait, a practice that continues in a controlled fashion today. Several species are threatened by introduced species attacking adults and chicks in breeding colonies, and by long-line fisheries.

Taxonomy and evolution

The procellariid family is usually broken up into four fairly distinct groups; the fulmarine petrels, the gadfly petrels, the prions, and the shearwaters. The fulmarine petrels include the largest procellariids, the giant petrels, as well as the two fulmar species, the Snow Petrel, Antarctic Petrel and Cape Petrel. The fulmarine petrels are a diverse group with differing habits and appearances, but are linked morphologically by their skull features, particularly the long prominent nasal tubes. The are mostly seabirds of the polar and sub-polar environment, and found in the southern hemisphere, with the exception of the Northern Fulmar which is found in the North Atlantic and Pacific, and which regularly disperses into more temperate waters (as does the Cape Petrel).

The gadfly petrels, so named due to their helter-skelter flight, are a group of tropical and temperate procellariids. They comprise the 37 species in the genus Pterodroma and have traditionally included the two species in the genus Bulweria. The individual species vary from small to medium sizes, and uniformly black on their upperparts and white or pale grey below. Some experts assert that not all the Pterodroma petrels are closely related and often split the genus, though not enough work has been done on the family to be certain.

The prions comprise 5 species of true prion in the genus Pachyptila and the closely related Blue Petrel. The prions are often known as whalebirds, and have large bills filled lamellae that are used to filter plankton. They are small procellariids with grey patterned plumage.

The shearwaters are a widespread group, breeding in most of the world's tropical and temperate seas (though absent as a breeding bird from most of the North Pacific), and migrating over and even larger area of the world's seas and oceans. The shearwaters are, to a lesser or greater degree, adapted for diving after prey instead of simply foraging on the ocean's surface; one species has been recorded diving as deep as 70 metres. The shearwaters are the large genus Puffinus, as well as the five large Procellaria species and the three Calonectris species.

According to the famous study by Sibley and Ahlquist into avian DNA hybridization, the split of the Procellariiformes into the four families occurred around 30 million years ago, though the order has an older history, with a fossil attributed to the order, a seabird known as Tytthostonyx, being found in late Cretaceous rocks (70 mya). The molecular evidence suggests that the storm-petrels were the first to diverge from the ancestral stock, and the albatrosses next, with the procellarids and diving petrels splitting most recently.

The more traditional taxonomy of the family is being increasingly questioned by newer research, for example a recent splits the shearwater genus Puffinus into two separate clades or subgroups, Puffinus and Neonectris. This split into two clades is thought to have occured soon after Puffinus split from the other procellariids, with the genus orginating in the north Atlantic Ocean and the Neonectris clade evolving in the southern hemisphere.Austin, J., (1996) "Molecular Phylogenetics of Puffinus Shearwaters: Preliminary Evidence from Mitochondrial Cytochrome b Gene Sequences" Molecular Phylogenetics and Evolution 6 (1): 77–88 The two genera, Pseudobulweria and Lugensa have been split from the gadfly petrel genus Pterodroma, with Pseudobulweria being phylogenetically closer to the Puffinus shearwaters than the Pterodroma gadfly-petrels, Bretangnole, V., Attié, C., Pasquet, E., (1998) "Cytochrome-B evidence for validity and phylogenetic relationships of Pseudobulweria and Bulweria (Procellariidae)" Auk 115(1):188-195 ^* and Lugensa (the Kerguelen Petrel) possibly being closely related to the prions.Penhallurick, J. and Wink, M. (2004). "Analysis of the taxonomy and nomenclature of the Procellariformes based on complete nucleotide sequences of the mitochondrial cytochrome b gene." Emu 104: 125-147. The genus Pterodroma itself which is now split into four sub genera. Imber, M.J., (1985) "Origins, phylogeny and taxonomy of the gadfly petrels Pterodroma spp." Ibis 127: 197-229 The two petrels in the genus Bulweria are no longer considered close to the gadfly petrels either. Many of the confusion species are amongst the least known of all seabirds, some of which like the Fiji Petrel have not been seen more than 10 times since their discovery by science, and others which have never had their breeding ground found (like the Heinroth's Shearwater).

Morphology and flight

The procellariids are small to medium sized seabirds. The largest, the giant petrels, are almost as large as albatrosses; the smallest, such as the prions and some of the shearwaters, are slightly bigger than the diving petrels. There are no obvious differences between the sexes, although females tend towards being slighter. Like all Procellariiformes the procellariids have a characteristic tubular nasal passage which is used for olfactionLequette, B., Verheyden, C., Jowentin, P. (1989) "Olfaction in Subantarctic seabirds: Its phylogenetic and ecological significance" The Condor 91: 732-135. ^*. This ability to smell helps to locate patchy areas of prey at sea, and may also help locate nesting colonies. The plumage of the procellariids is usually dull, with greys, blues, blacks and browns being the usual colours, although some species have striking patterns (like the Cape Petrel).

All of the procellariids fly well, though there is some variation in technique dependent on foraging methods. Compared to an average bird all procellariids have a high aspect ratio (meaning their wings are long and narrow), and a heavy wing loading. This means that they must maintain a high speed in order to remain in the air. Most procellariids use two techniques to do this, dynamic soaring and slope soaring. Dynamic soaring enables them to minimise the effort needed by gliding across wave fronts gaining energy from the vertical wind gradient. Slope soaring is more straightforward: the procellariid turns to the wind, gaining height, from where it can then glide back down to the sea. Most procellariids can aid their flight by means of flap-glides, where bursts of flapping and followed by a period of gliding; the amount of flapping dependent on the strength of the wind and the choppiness of the water.Warham, J. (1996). The Behaviour, Population, Biology and Physiology of the Petrels. London:Academic Press, ISBN 0-12-735-4158 Shearwaters and other larger petrels, which have heavier wing loadings, must make more use of flapping to remain airborne than gadfly petrels with lighter wing loadings. Because of the high speeds required to sustain flight procellariids need to either run or face into a strong wind in order to take off.

Like the albatrosses, the giant petrels have a shoulder-lock, a sheet of tendon that locks the wing when fully extended, allowing the wing to be kept up and out without any muscle expenditure.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. Gadfly petrels often feed on the wing, snapping prey up without landing on the water. The flight of the smaller prions is reminiscent of that of the storm-petrels, being highly erratic and involving weaving and even looping the loop. The wings of all species are long and stiff, in some species of shearwater the wings are also used to power the birds underwater while diving for prey. These heavier wing loadings than the other surface-feeding procellariids shearwaters which allows them to achieve considerable depths (below 70 m in the case of the Short-tailed Shearwater). Weimerskirch, H., Cherel, Y., (1998) Feeding ecology of short-tailed shearwaters: breeding in Tasmania and foraging in the Antarctic? Marine Ecology Progress Series 167: 261-274

Procellariids have weak legs for the most part and many species move around on land by resting on the breast and pushing themselves forward, often with the help of their wings. The exception to this are the two species of giant petrel, which like the albatrosses, have strong legs used to feed on land (see below). The feet of shearwaters are set far back on the body for use in swiming and are of little use when on the ground.

Distribution and range at sea

The procellariids have a cosmopolitan distribution in the world's oceans and are present in all the oceans and most of the seas. They are absent from the Bay of Bengal and the Hudson Bay, but are present year round or seasonally in the rest. The seas north of New Zealand are the centre of procellariid biodiversity, with the most species. Schreiber, Elizabeth A. & Burger, Joanne.(2001.) Biology of Marine Birds, Boca Raton:CRC Press, ISBN 0-8493-9882-7 Among the four groups, the fulmarine petrels have a mostly polar distribution, with most species living around Antarctica and one, the Northern Fulmar ranging in the Northern Atlantic and Pacific Oceans. The prions are restricted to the Southern Ocean, and the gadfly petrels are found mostly in the tropics with some temparate species. The shearwaters are the most widespread group and breed in most temparate and tropical seas, although by a biogeographical quirk are absent as breeders from the North Pacific.

Many procellariids undertake long annual migrations in the non-breeding season. Southern species od shearwater such as the Sooty Shearwater and Short-tailed Shearwater breeding on islands off Australia, New Zealand and Chile undertake transequatorial migrations of millions of birds up to the waters off Alaska and back again each year during the austral winter. Manx Shearwaters from the North Atlantic also undertake transequatorial from Western Europe and North America to the waters off Brazil in the South Atlantic. The mechanisms of navigation are poorly understood, but displacement expermiments where individuals wwre removed from colonies and flown to far-flung release sites have shown that they are able to home in on their colonies with remarkable precision. A Manx Shearwater released in Boston was able to return to its colony in Skomer, Wales within 13 days, a distance of 3,200 miles (5,150 km). Matthews, G.V.T., (1953) "Navigation in the Manx Shearwater" 30 Journal of Experimental Biology(3): 370-396 ^*

Diet

The diet of the procellariids is the most diverse of all the Procellariiformes, as are the methods employed to obtain it. With the exception the giant petrels all procellariids are exclusively marine, and the diet of all species is dominated by either fish, squid, crustaceans and carrion, or some combination thereof.

The majority of species are surface feeders, obtaining food that has been pushed to the surface by other predators, currents or death. Among the surface feeders some, principally the gadfly petrels, can obtain food by dipping from flight, while most of the rest feed while sitting on the water. These surface feeders are dependent on their prey being close to the surface, and for this reason procellariids are often found in conjunction with other predators or oceanic convergences. Studies have shown strong associations between many different kinds of seabirds, including Wedge-tailed Shearwaters, and dolphins and tuna which push shoaling fish up towards the surface. Au, D.W.K. & Pitman, R.L. (1986) Seabird interactions with Dolphins and Tuna in the Eastern Tropical Pacific. Condor, 88: 304-317. ^* The fulmarine petrels are generalists which for the most part take many species of fish and crustacea. The giant petrels, uniquely for Procellariiformes, will feed on land, eating the carrion of seals and other seabirds. They will also attack the chicks of other seabirds. The diet of the giant petrels varies according to sex, with the females taking more krill and the males more carrion.

Three of the six prion species have bills filled with lamellae which act as filters to sift zooplankton from the water.Cherel, Y., Bocher, P., De Broyer, C., Hobson, K.A., (2002) "Food and feeding ecology of the sympatric thin-billed Pachyptila belcheri and Antarctic P. desolata prions at Iles Kerguelen, Southern Indian Ocean" Marine Ecology Progress Series 228: 263–281 ^* Water is forced through the lamellae and small prey items are collected. This technique is often used in conjenction with a method known as hydroplaning where the bird dips its bill beneath the surface and propels itself forward.

Breeding

Procellariid colonies

The procellariids are colonial, nesting for the most part on islands. These colonies vary in size from over a million birds to just a few pairs, and can be densely concentrated or widely spaced. At one extreme the Greater Shearwater nests in concentrations of 1 pair per m² in three colonies of more than 1 million pairs, Brooke, M. (2004). Albatrosses And Petrels Across The World Oxford University Press, Oxford, UK ISBN 0-19-850125-0 whereas the giant petrels nest in clumped but widely spaced territories that barely qualify as colonial. Colonies are usually located near the coast, but some species nest far inland and even at high altitudes.

Most seabirds are colonial, and the reasons for colonial behaviour are assumed to be similar, if incompletely understood by scientists. Procellariids for the most part have weak legs and are unable to easily take off, making them highly vulnerable to mammalian predators. Most procellariid colonies are located on islands that have historically been free of mammals; and for this reason some species cannot help but be colonial as they are limited to a few locations to breed. Even species that breed on continental Antarctica, like the Antarctic Petrel, are forced by habitat preference (snow-free north facing rock) to breed in just a few locations.

Most procellariids nest on open ground, with a smaller number nesting under the cover of vegetation. All the fulmarine petrels bar the Snow Petrel nest in the open, the Snow Petrel instead nesting inside natural crevices. Of the rest of the procellariids the majority nest in burrows or crevices, with a few tropical species nesting in the open. There are several reasons for these differences. The fulmarine petrels are probably precluded from burrowing by their large size (the crevice nesting Snow Petrel is the smallest fulmarine petrel) and the high lattitudes they breed in where frozen ground is difficult to burrow into. The smaller size of the other species, and their lack of agility on land, means that even on islands free from mammal predators they are still vulnerable to skuas,Reinhard, K., Hahn, S., Peter, H.-U., Wemhoff, H., (2000)."A review of the diets of Southern Hemisphere skuas." Marine Ornithology 28: 7–19. gulls and other avian predators, something the aggressive oil-spitting fulmars are not. The chicks of all species are vulnerable to predation, but the chicks of fulmarine pertels can defend themselves in a similar fashion to their parents. There are also a thermodynamic advantages to burrow nesting, as the temperature is more stable in the higher lattitudes than it would be on the surface, and there is no wind-chill to contend with. The absence of skuas, gulls and other predatory birds on tropical islands is why some shearwaters and two species of gadfly petrel are able to nest in the open, there are advantages in this as it reduces competition with burrow nesters from other species and allows them to nest on coralline islets without soil for burrowing. Procellariids that burrow in order to avoid predation almost always attend their colonies nocturnally in order to reduce predation as well,Keitt, B.S., Tershy, B.R. & Croll, D.A (2004). "Nocturnal behavior reduces predation pressure on Black-vented Shearwaters Puffinus opisthomelas" Marine Ornithology 32 (3): 173-178.^* those species of shearwater that attend their burrows at night are the larger species that are able to defend themselves. Of the ground nesting species the majority attend their colonies during the day, the exception being the Herald Petrel which is thought to be vulnerable to the diurnal White-bellied Sea Eagle.

Procellariids display high levels of philopatry, exhibiting both natal philopatry and site fidelity. Natal philopatry, the tendency of a particular bird to breed close to where it hatched, is strong amongst all the Procellariiformes. The evidence for natal philopatry comes from several sources, not the least of which is the existence of several procellariid species that are endemic to a single island.Brooke, M. (2004). Albatrosses And Petrels Across The World Oxford University Press, Oxford, UK ISBN 0-19-850125-0 The study of mitochondrial DNA also provides evidence of restricted gene flow between different colonies, and has been used to show philopatry in Fairy Prions.Ovenden, J.R., Wust-Saucy, A., Bywater, R., Brothers, N., White, R.W.G. (1991) " Genetic evidence for philopatry in an colonially nesting seabird. the Fairy Prion (Pachyptila turtur)" Auk 108: 688-694. Bird ringing also provides compelling evidence of philopatry, 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.Rabouam, C., Thibault, J.-C., Bretagnole, V., (1998) "Natal Philopatry and Close Inbreeding in Cory's Shearwater (Calonectris diomedea)" Auk 115(2): 483-486 [http://elibrary.unm.edu/sora/Auk/v115n02/p0483-p0486.pdf This tendency towards philopatry is stronger in some species than others, and several species readily prospect potential new colony sites and colonise them. It is hypothesised that there is a cost to dispersing to a new site, the chance of not finding a mate of the same species, that selects against it for rarer species, whereas there is probably an advantage to dispersal for species which have colony sites that change dramatically during periods of glacial advance or retreat. There are also differences in the tendency to disperse based on sex, with females being more likely to breed away from the natal site.

Mate and site fidelity

Procellariids, as well as having strong natal philopatry, exhibit strong site fidelity, returning to the same nesting site, burrrow or territory in sequential years. The figure varies for different species but is still high for most species, an estimated 91% for Bulwer's Petrels.Mouguin, J-L., (1996) "Faithfulness to mate and nest site of Bulwer's Petrel, Bulweria bulweria at Selvagem Grande" Marine Ornithology 24: 15–18. The strength of this fidelity can also vary with sex; almost 85% of male Cory's Shearwaters return to the same burrow to breed the year after a successful breeding attempt, the figure for females is around 76%. 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. This tendency towards using the same site from year to year is matched by strong mate fidelity, with birds breeding with the same partner for many years; in fact it has been suggested that the two are linked, Bried, J.L., Pontier, D., Jouventin, P., (2003) "Mate fidelity in monogamous birds: a re-examination of the Procellariiformes" Animal Behaviour 65: 235–246 [http://www.cefe.cnrs.fr/ecomp/PDF%20papers/2003MateFidelProcAnBeh.pdf site fidelity being a means by which partnered birds could meet at the beginning of the breeding season. One pair of Northern Fulmars bred as a pair in the same site for 25 years. Carboneras, C. (1992) "Family Procellariidae (Petrels and Shearwaters)" in Handbook of Birds of the World Vol 1. Barcelona:Lynx Edicions, ISBN 84-87334-10-5 Like the albatrosses the procellariids take seveal years to reach sexual maturity, though to the greater variety of sizes and lifestyles the age of first breeding streches from just three years in the smaller species to 12 years for the larger ones.

The procellariids lack the elaborate breeding dances of the albatrosses, in no small part due to the tendency of most of them to attend colonies at night and breed in burrows, where visual displays are useless. The fulmarine petrels, which nest on the surface and attend their colonies diurnally, do use a repetoire of stereotyped behaviours such as cackling, preening, head waving nibbling and preening, but most for species courtship interactions are limited to some billing in the burrow and the vocalisations made by all species. The calls serve a number of functions, they are used territorially to protect burrows or territories and to call for mates. Each call type is unique to a particular species and indeed it is possible for procellariids to identify the sex of the bird calling as well. It may also be possible to assess the quality of potential mates; a study of Blue Petrels found a link between the rhythm and duration of calls and the body mass of the bird. Genevois, F; Bretagnolle, V (1994) "Male Blue Petrels reveal their body mass when calling" Ethology Ecology & Evolution 6(3): 377-383.^* The ability of an individual to recognise its mate has also been demonstrated in several species.

Breeding season

Like most seabirds, the majority of procellariids breed once a year. There are exceptions; many individuals of the larger species, like the White-headed Petrel, will skip a breeding season after successfully fledging a chick, and some of the smaller species (like Christmas Shearwaters) breed on a nine month schedule. Of those that breed annually, there is considerable variation as to the timing, some species breed in a fixed season whilst others breed all year round. Climate and the availability of food resources are important influences on the timing of procellariid breeding, species that breed at higher latitudes always breed in the summer as conditions are too harsh in the winter. At lower latitudes many, but not all, species breed continuously. Some species breed in the seasons to avoid competition with other species for burrows, to avoid predation or to take advantage of seasonally abundant food. Others, like the tropical Wedge-tailed Shearwater, breed seasonally for reasons unknown. Among the species that exhibit seasonal breeding there can be high levels of synchronization, both of time of arrival at the colony and of lay date.

Procellariids begin to attend their nesting colony around one month prior to laying. Males will arrive first and attend the colony more frequently than females, partly in order to protect a site or burrow from potential competitors. Prior to laying there is a period where both the male and female are away from the colony known as the pre-laying exodus, where both the female and male build up reserves in order to lay and undertake the first incubation stint repectively. This pre-laying exodus can vary in length from 9 days (like the Cape Petrel) Weidinger, K (1996) " Patterns of colony attendance in the Cape Petrel Daption capense at Nelson Island, South Shetland Islands, Antarctica" Ibis.138(2): 243-249. to around 50 days in Atlantic Petrels. Cuthbert, R., (2004) "Breeding biology of the Atlantic Petrel, Pterodroma incerta, and a population estimate of this and other burrowing petrels on Gough Island, South Atlantic Ocean" Emu 104(3): 221 - 228 All procellariids lay one egg, in common with the rest of the Procellariiformes. The egg is large, compared to that of other birds, between weighing 6-24% of the female's weight. Immediately after laying the male takes over incubation duties while the female goes back to sea to feed. Incubation duties are shared by both sexes in shifts that vary in length between species, individuals and even the stage of incubation. The longest recorded shift was 29 days by a Murphy's Petrel from Henderson Island, the typical length of a gadfly petrel stint is between 13-19 days. Fulmarine petrels, shearwaters and prions tend to have shorter stints, averaging between 3 to 13 days. Incubation takes a long time, between 40 days for the smaller species (like prions) to around 55 days for the larger species. The incubation period is longer if eggs are abandoned temporarily; procellariid eggs are resistant to chilling and can still hatch after being left unattended for a few days. After hatching the chick is brooded by a parent until it is large enough to thermoregulate efficiently, and in some cases defend itself from predation. This guard stage lasts a short while for burrow nesting species (2-3 days) but longer for surface nesting fulmars (around 16-20 days) and giant petrels (20-30 days). After the guard stage both parents feed the chick. In many species the parent's foraging stratergy alternates between short trips lasting between 1-3 days and longer trips of 5 days.Weimerskirch, H., Chastel, O., Ackermann, L., Chaurand, T., Cuenot-Chaillet, F., Hindermeyer, X. & Judas, J., (1994) "Alternate long and short foraging trips in pelagic seabird parents" Animal Behaviour 47: 472-476 The shorter trips, which are taken over the continental shelf, benefit the chick with faster growth but longer trips to more productive pelagic feeding grounds are needed for the parents to maintain their own body condition. Chick development is quite slow for birds, with fledging taking place at around 2 months after hatching for the smaller species and 4 months for the largest species. The chicks of some species are abandoned by the parents, other species continue to bring food to the nesting site after the chick has left. All procellariids chicks fledge by themselves, and there is no further parental care after fledging.

Procellariids and humans

Exploitation of procellariids

Procellariids have been a seasonally abundant source of food for people wherever people have been able to reach their colonies. Early records of human exploitation of shearwaters (along with albatrosses and cormorants) come from the remains of hunter-gatherer middens in southern Chile, where Sooty Shearwaters were taken 5000 BP.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 ^* More recently procellariids have been hunted for food by Europeans, particularly the Northern Fulmar in Europe and by the sailors around the world. The hunting pressure on the Bermuda Petrel, or Cahow, was so intense that the species nearly went extinct and did go missing for 300 years. The name of one species, the Providence Petrel, is derived from its (seemingly) miraculous arrival on Norfolk Island where it provided a windfall for starving European settlers;Anderson, A. (1996) "Origins of Procellariidae Hunting in the Southwest Pacific" International Journal of Osteoarcheology 6: 403-410 within ten years the Providence Petrel was extinct on Norfolk. Several species of procellariid have gone extinct in the Pacific since the arrival of man, and their remains have been found in middens dated to that time. More sustainable shearwtaer harvesting industries developed in Tasmania and New Zealand, where the pratice of harvesting what are known as muttonbirds continues today.

Species

''see List of Procellariidae

References

Procellariidae | Seabirds

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