Unusual seabird breeding behavior
Encyclopedia
The term seabird
is used for many families of birds in several orders that spend the majority of their lives at sea. Seabirds make up some, if not all, of the families in the following orders: Procellariiformes
, Sphenisciformes, Pelecaniformes
, and Charadriiformes
. Many seabirds remain at sea for several consecutive years at a time, without ever seeing land. Breeding is the central purpose for seabirds to visit land. The breeding period (courtship, copulation, and chick-rearing) is usually extremely protracted in many seabirds and may last over a year in some of the larger albatrosses ; this is in stark contrast with passerine birds. Seabirds nest in single or mixed-species colonies
of varying densities, mainly on offshore islands devoid of terrestrial predators . However, seabirds exhibit many unusual breeding behaviors during all stages of the reproductive cycle that are not extensively reported outside of the primary scientific literature.
stage of breeding is when pair bonds are formed and occurs before copulation and occasionally continues through the copulatory and chick-rearing stages of the breeding phenology
. The sequence and variety of courting behaviors vary widely among species, but they typically begin with territorial defense, followed by mate-attraction displays, and selection of a nest site . Seabirds are long-lived, socially monogamous
, birds that usually mate for life. This makes selecting a mate extremely important with lifelong implications for the reproductive success of both individuals in the pair.
Seabirds are one of the only avian families that include ritualized dances in their courtship. These dances are complex and can include displays and vocalizations that vary greatly between families and orders. Albatrosses are well known for their intricate mating dances. All species of albatross have some form of ritualized dance, with many species displaying very similar forms . Albatrosses’ complex visual and vocal dances are considered some of the most developed mating displays in any long-lived animal . Both members of the pair use these dances as a proxy for mate quality and it is believed to be a very important aspect of mate choice in this family . For Black-footed
(Phoebastria nigripes) and Laysan Albatross
es (P. immutabilis) there are ten described parts to their mating dance which can be given in various sequences . Several parts include “billing” where one individual gently touches the others bill and “sky pointing” where the bird rises on the tips of its toes, stretches its neck and points its bill upward. In the Wandering Albatross
(Diomedea exulans), sky pointing is accompanied with “sky calling” where the displaying individual spreads its wings, revealing his massive 12 foot wingspan while pointing and vocalizing skyward . The mating dance may last for several minutes. It has been noted that many albatross species dance upon reuniting with their partner every year; however, for Waved Albatross
(P. irrorata), the dance is longer and more involved in new pairs, or in pairs that failed to breed the previous season .
Boobies are another group of seabirds known for their mating displays. Brown (Sula leucogaster), Red-footed (S. sula) and Blue-footed Boobies (S. nebouxii) have at least nine described parts to their mating display . Sky pointing in boobies is similar to albatrosses; in the Brown Booby
, sky pointing is described as a display where the male throws his head backwards, stretches his neck out, and usually gives a whistling vocalization . Parading is a well-known display in boobies as well; in this display, one individual in the pair - usually the male - walks upright, with his tail erect, swaying in an exaggerated manner from side to side while taking small steps . In Blue-footed and Red-footed Boobies, parading also includes lifting their brightly colored feet to flaunt to their partner.
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Frigatebirds are known for their unusual displays and breeding system. Unlike other seabirds, frigatebirds have a lek-breeding system where displaying males aggregate in groups of up to 30 individuals with prospecting females flying overhead . However, unlike classic leks, the pair then builds a nest on the male’s display site. The male then participates fully in nest defense, incubation, and chick-rearing . The main display that male frigatebirds use to attract females is a “gular presentation” where the male inflates his bright red throat pouch, points his head upwards and opens his wings . Interestingly, it has been shown experimentally that there is no correlation between energy expended by males during courtship display and mate selection by females .
Courtship feeding is seen in many gull and tern species. In Common Tern
s (Sterna hirundo), courtship feeding begins right at the start of pair formation with male terns carrying a fish around the breeding colony, displaying it to prospective mates. The direct benefits hypothesis (where the female obtains some immediate benefit for copulating with the male, food in this case) may explain why courtship feeding has evolved; however, this theory has recently been disputed with the suggestion that the rate of courtship feeding is a way for females to determine the quality of their mate through the handicap principle
.
There are many examples of homosexual behavior in wild gulls. In Herring Gull (Larus argentatus) populations nesting on the Great Lakes, Fitch (1980) reported a low, yet consistent prevalence of female-female pairs. It appears that female-female Herring Gull pairs are more common in colonies with a female-biased operational sex ratio
(OSR) and occasionally these homosexual pairs will remain stable for several breeding seasons . In Western Gull
s (Larus occidentalis), female-female pairs are often associated with supernormal clutches (clutches of 4-6 eggs; a normal clutch for Larus gull species is 2-3 eggs) and these clutches are usually infertile . Female-female pairs have also been widely reported in wild populations of Ring-billed Gull
s (Larus delawarensis). Studies of Ring-billed Gulls has shown that same sex pairs are rare (<1% of pairs in a colony) but consistent interannually and that they also lay supernormal clutches at a significantly higher rate than do heterosexual pairs. It has also been shown that these clutches of female-female pairs have significantly lower hatching and fledging success than heterosexual pairs . There is even one example of an unusual mixed female-female pair of two gull species, the Caspian
(Larus cachinnans) and Yellow-legged Gull
(Larus michahellis) .
Female-female pairing has also been documented and studied in several tern
species including Whiskered
(Chlidonias hybyida), Roseate
(Sterna dougalii) and Caspian Tern
s (Hydroprogne caspia) with similar attributes (supernormal clutches and reduced hatching/fledging success as compared to heterosexual pairs) to same-sex gull pairs . Also in the order Charadriiformes
(family Chionididae), there has been one reported occurrence of a female-female pair in the Black-faced Sheathbill
(Chionis minor), but eggs in the clutch proved to be inviable .
Same-sex pairing has also been shown in several families of true seabirds
including the petrels and shearwaters. Antarctic Petrel
s (Thalassoica antarctica) have been shown to form female-female pairs in colonies where there is a surplus of females; it is hypothesized that “pairing” with another female may be a favorable strategy for some females because it allows them to become established in the colony. The experience with a site gained through forming a female-female pair may greatly improve the chances of future successful breeding for the non-genetic parent, which explains why it might be worth the short-term cost of raising another bird’s offspring . In another member of this family, the Cory’s Shearwater (Calonectris diomedea), same-sex pairing was recently discovered for the first time in a burrow-nesting seabird . This study proposed that similar factors cause female-female pairs to form in burrow-nesting seabirds as in surface-nesting seabirds (a female-biased OSR), and that female-female pairing in burrow-nesting seabirds might have remained undetected for so long due to the secretive nature of these animals.
In albatrosses, female-female pairing has recently received major press coverage. Last year, when a Southern Royal Albatross
(D. epomophora) couple hatched a chick in New Zealand, it represented the first record of a successful same-sex pair in this species . In a landmark study by Young et al. (2008), she reported over 30% of Laysan Albatrosses in a colony in Oahu, Hawaii were same sex pairs. Even though these female-female pairs had less reproductive success than heterosexual pairs, it was better than not breeding at all. Young et al. (2008) also cited a female-biased OSR as the primary reason for such a high proportion of same-sex pairs. Additionally, an unsuccessful female-female pair of highly endangered of Short-tailed Albatross
es (P. albatrus) was recently documented on Kure Atoll
, Hawaii
.
Penguins represent the only known examples of male-male pairings in seabirds. On the Otago Peninsula
of New Zealand
, two-male Yellow-eyed Penguin
s (Megadyptes antipodes) were recently reported incubating an egg. In captivity, Chinstrap
(Pygoscelis antarcticus), Humboldt
(Spheniscus humboldti), Magellanic
(S. magellanicus), and African Black-footed Penguins (S. demersus) have all been documented to form male-male pairs.
usually occurs after, and occasionally concurrently, with the formation of the pair bond
. Copulation occurs mainly on land at the breeding colony. Usually the pair copulates several times, even in orders that lay only one egg per-clutch. These additional copulations are thought of as a mechanism to strengthen the pair bond . This is important for strongly monogamous, long-lived organisms and is especially important in seabirds that spend most of the non-breeding season apart on the open ocean.
is the dominant mating system . Prior to the advent of genetic techniques, it was assumed that the majority of monogamous birds remained faithful to their partners . However, it is now known that extra-pair copulations (EPCs), extra-pair fertilizations (EPFs), and extra-pair paternity (the raising of another’s offspring, EPP) are actually quite common in a variety of avian orders and families . Roughly 70% of birds that used to be considered genetically monogamous actually engage in EPCs and raise extra-pair young (reviewed by:). Furthermore, it has been proposed that birds that nest in high densities, as seabirds do in breeding colonies, have higher rates of EPCs and EPFs than birds that do not nest colonially. Despite this, Westneat and Sherman (1997) found no significant correlation between nesting density and EPFs in a meta-analysis. Many seabird species raise only one chick per breeding season, which would make the prevalence of EPFs and EPP in seabirds surprising due to the fact that the male’s entire breeding success for a year is dependent on the lone egg/chick he is raising to be his genetic offspring. Moreover, all seabirds have obligate biparental care, so it would be evolutionarily costly for the male to spend months of effort raising a chick that is not his genetic offspring.
In line with this prediction, many studies of seabirds have revealed no EPCs or EPFs. Several genetic studies of Storm-Petrel
s, show no evidence of EPCs or EPFs, which is not surprising considering these are burrow-nesting seabirds that lay only one egg per year. Dovekie (Alle alle), a surface nesting alcid that raises one chick per year, has shown no EPFs or EPP . Nazca Boobies
(Sula granti) have been well studied at breeding colonies in the Galapagos for decades and also show no evidence of EPCs or EPFs; also not a surprising result since they only have one surviving offspring per year . Chinstrap Penguins, which raise two chicks annually, have also shown no EPCs or EPFs.
Contrary to these empirical results, there has been a multitude of studies where EPCs or EPFs have been found in seabirds. Perhaps the most surprising EPFs have been found in the Procellariid family because all members of this family only lay one egg per year and some do not even breed every year . Waved Albatross show high rates (up to 25% of offspring are extra-pair young) of both EPCs and EPFs and behavioral observations have shown that many of the EPCs are forced by the extra-pair male. Studies of Wandering Albatross have shown over 10% of chicks are extra-pair young; an extremely surprising result since adult Wandering Albatrosses only breed once every other year at most. Similar results were seen in Black-browed
(Thalassarche melanophris) and Grey-headed Albatross
es (T. chrysostoma) nesting on South Georgia Island. EPFs have also been shown in Antarctic Petrels. Perhaps the most unexpected result was when EPCs and EPFs were documented in a burrow-nesting Procellariid, the Short-tailed Shearwater
(Puffinus tenuirostris), because the female would have to leave her burrow to solicit an EPC .
EPCs and EPFs have also been demonstrated to occur in other families of seabirds. In contrast to the results found in genetic studies of Dovekie, EPP has been shown in several species of alcid including Common Murre (Uria aalge) and Razorbill
(Alca torda), both of which raise only one chick per year. Interestingly, it has been shown that female Razorbills can determine whether or not an EPC leads to an EPF and only accept extra-pair sperm
when it gives them a fitness
advantage over their current mate . A low-rate of EPP has also been shown in the sexually dimorphic
Great Frigatebird
(Fregata minor).
with related individuals is rare in naturally occurring populations of birds due to the production of lower quality offspring suffering from the genetic effects of inbreeding depression
. Seabirds have an inherently high risk of inbreeding
because most are natally philopatric
, and many are highly endangered with some species’ entire populations breeding on one small island . Despite this, inbreeding was observed no more than expected by random chance in the Wandering Albatross and the critically endangered Amsterdam Albatross
(D. amsterdamensis). In contrast, some studies of seabirds have shown evidence of inbreeding. Huyvaert and Parker (2010) detected low frequencies of inbreeding in Waved Albatrosses and genetic similarity was negatively related to EPFs, which is an unusual result that does not support the inbreeding avoidance hypothesis. Close inbreeding was observed at low frequencies in the Cory’s Shearwater where two mother-son pairs were reported.
during a breeding season. Chick-rearing includes brooding, feeding, defending, and in some cases, teaching the chick skills it will need to know to survive independently. Chick-rearing can be totally absent in some birds (the Brush-Turkeys of southeast Asia), to a couple weeks long in many passerines, to several months long in larger birds . Seabirds have the longest chick-rearing stage of any bird on earth . It is not unusual for many seabirds to spend 3–4 months raising their chicks until they are able to fledge and forage independently. In the great albatrosses, chick-rearing can take over 9 months . It is because of this extremely protracted chick-rearing stage that many of the larger procellariiform seabirds can breed only once every other year.
Siblicide
, the death of an individual due to the actions of members of its own clutch, is seen in several avian orders including egret
s and kingfisher
s, some raptors
, and grackle
s. In most of these examples, siblicide is facultative
(i.e. not obligate
) and only occurs when there is a shortage of food. However in some seabirds, siblicide proves to be obligate
and occurs no matter how productive the breeding season is. The Nazca Booby is one species that practices obligate siblicide . The parents lay two eggs, several days apart. The second egg laid is seen as fertility insurance if the first egg is inviable. If both eggs hatch, the elder chick will push its sibling out of the nest area, leaving it to die of thirst or cold. The parent booby will not intervene and the younger chick will inevitably die. Research has shown that high hormone levels in Nazca Booby chicks are responsible for inciting their murderous behavior. Facultative siblicide is seen in the closely related Blue-footed Booby. Unlike the Nazca Booby, Blue-footed Boobies chicks only perform siblicide when food is scarce. Furthermore, the parents actually try to suppress the siblicidal behavior, rather than ignoring or encouraging it.
. Reasons for divorce in seabirds are wide ranging and include asynchronous arrival of mates to the breeding colony, declining reproductive success of the pair, and competition for mates. Coercive divorce is seen in the Nazca Booby and Common Murre where one member of the pair actively desserts the other or where an intruder enters and forcibly splits the breeding pair to form a new pair.
Divorce is relatively common in gulls and their relatives (reviewed by:); in one study, Black-legged Kittiwake
s (Rissa tridactyla) proved to be more faithful to their nesting site than their partner. Divorce rates are surprisingly high (>80% of pairs annually) in King
(Aptenodytes patagonicus) and Emperor Penguin
s (A. forsteri). Asynchronous arrival of mates at the breeding colony is cited as the main reason for this because these penguins have extreme time constraints on their breeding. In Great Skua
s (Stercorarius skua) divorce occurs annually, but at low frequencies (6-7% of pairs annually) and death is responsible for approximately three times more pair interruptions than divorce. Divorce is uncommon in procellariiforms and usually only occurs after several years of breeding failure. However, one study of Short-tailed Shearwaters observed the divorce rate in a colony to be as high as 16% annually.
Seabird
Seabirds are birds that have adapted to life within the marine environment. While seabirds vary greatly in lifestyle, behaviour and physiology, they often exhibit striking convergent evolution, as the same environmental problems and feeding niches have resulted in similar adaptations...
is used for many families of birds in several orders that spend the majority of their lives at sea. Seabirds make up some, if not all, of the families in the following orders: Procellariiformes
Procellariiformes
Procellariiformes is an order of seabirds that comprises four families: the albatrosses, petrels and shearwaters, storm petrels, and diving petrels...
, Sphenisciformes, Pelecaniformes
Pelecaniformes
The Pelecaniformes is a order of medium-sized and large waterbirds found worldwide. As traditionally—but erroneously—defined, they encompass all birds that have feet with all four toes webbed. Hence, they were formerly also known by such names as totipalmates or steganopodes...
, and Charadriiformes
Charadriiformes
Charadriiformes is a diverse order of small to medium-large birds. It includes about 350 species and has members in all parts of the world. Most Charadriiformes live near water and eat invertebrates or other small animals; however, some are pelagic , some occupy deserts and a few are found in thick...
. Many seabirds remain at sea for several consecutive years at a time, without ever seeing land. Breeding is the central purpose for seabirds to visit land. The breeding period (courtship, copulation, and chick-rearing) is usually extremely protracted in many seabirds and may last over a year in some of the larger albatrosses ; this is in stark contrast with passerine birds. Seabirds nest in single or mixed-species colonies
Bird colony
A bird colony is a large congregation of individuals of one or more species of bird that nest or roost in close proximity at a particular location. Many kinds of birds are known to congregate in groups of varying size; a congregation of nesting birds is called a breeding colony...
of varying densities, mainly on offshore islands devoid of terrestrial predators . However, seabirds exhibit many unusual breeding behaviors during all stages of the reproductive cycle that are not extensively reported outside of the primary scientific literature.
Courtship Stage
The courtshipCourtship
Courtship is the period in a couple's relationship which precedes their engagement and marriage, or establishment of an agreed relationship of a more enduring kind. In courtship, a couple get to know each other and decide if there will be an engagement or other such agreement...
stage of breeding is when pair bonds are formed and occurs before copulation and occasionally continues through the copulatory and chick-rearing stages of the breeding phenology
Phenology
Phenology is the study of periodic plant and animal life cycle events and how these are influenced by seasonal and interannual variations in climate...
. The sequence and variety of courting behaviors vary widely among species, but they typically begin with territorial defense, followed by mate-attraction displays, and selection of a nest site . Seabirds are long-lived, socially monogamous
Monogamy
Monogamy /Gr. μονός+γάμος - one+marriage/ a form of marriage in which an individual has only one spouse at any one time. In current usage monogamy often refers to having one sexual partner irrespective of marriage or reproduction...
, birds that usually mate for life. This makes selecting a mate extremely important with lifelong implications for the reproductive success of both individuals in the pair.
Mating Dances
Black-footed Albatross
The Black-footed Albatross, Phoebastria nigripes, is a large seabird from the North Pacific of the albatross family Diomedeidae. It is one of three species of albatross that range in the northern hemisphere, nesting on isolated tropical islands...
(Phoebastria nigripes) and Laysan Albatross
Laysan Albatross
The Laysan Albatross, Phoebastria immutabilis, is a large seabird that ranges across the North Pacific. This small two-tone gull-like albatross is the second most common seabird in the Hawaiian Islands, with an estimated population of 2.5 million birds, and is currently expanding its range to new...
es (P. immutabilis) there are ten described parts to their mating dance which can be given in various sequences . Several parts include “billing” where one individual gently touches the others bill and “sky pointing” where the bird rises on the tips of its toes, stretches its neck and points its bill upward. In the Wandering Albatross
Wandering Albatross
The Wandering Albatross, Snowy Albatross or White-winged Albatross, Diomedea exulans, is a large seabird from the family Diomedeidae, which has a circumpolar range in the Southern Ocean. It was the first species of albatross to be described, and was long considered the same species as the Tristan...
(Diomedea exulans), sky pointing is accompanied with “sky calling” where the displaying individual spreads its wings, revealing his massive 12 foot wingspan while pointing and vocalizing skyward . The mating dance may last for several minutes. It has been noted that many albatross species dance upon reuniting with their partner every year; however, for Waved Albatross
Waved Albatross
The Waved Albatross, Phoebastria irrorata - also known as Galapagos Albatross - is the only member of the Diomedeidae family located in the tropics. When they forage, the Waved Albatross follow straight paths to a single site off the coast of Peru, about distant to the east...
(P. irrorata), the dance is longer and more involved in new pairs, or in pairs that failed to breed the previous season .
Boobies are another group of seabirds known for their mating displays. Brown (Sula leucogaster), Red-footed (S. sula) and Blue-footed Boobies (S. nebouxii) have at least nine described parts to their mating display . Sky pointing in boobies is similar to albatrosses; in the Brown Booby
Brown Booby
The Brown Booby is a large seabird of the booby family, Sulidae. The adult brown booby reaches about in length. Its head and upper body are covered in dark brown, with the remainder being a contrasting white. The juvenile form is gray-brown with darkening on the head, wings and tail...
, sky pointing is described as a display where the male throws his head backwards, stretches his neck out, and usually gives a whistling vocalization . Parading is a well-known display in boobies as well; in this display, one individual in the pair - usually the male - walks upright, with his tail erect, swaying in an exaggerated manner from side to side while taking small steps . In Blue-footed and Red-footed Boobies, parading also includes lifting their brightly colored feet to flaunt to their partner.
Courtship Feeding
Once the pair bond is formed, courtship feeding occurs in some species. Courtship feeding is when one member of the pair presents the other with food in a ritualized way. Often the male feeds the female, but in certain species where the sex roles are reversed, the female may feed the male. Several reasons proposed as to why courtship feeding occurs is: 1) to help strengthen the pair bond 2) to reduce aggression between males and females and 3) to provide additional nutrition to the females during the egg-laying stage.Courtship feeding is seen in many gull and tern species. In Common Tern
Common Tern
The Common Tern is a seabird of the tern family Sternidae. This bird has a circumpolar distribution, breeding in temperate and sub-Arctic regions of Europe, Asia and east and central North America. It is strongly migratory, wintering in coastal tropical and subtropical regions. It is sometimes...
s (Sterna hirundo), courtship feeding begins right at the start of pair formation with male terns carrying a fish around the breeding colony, displaying it to prospective mates. The direct benefits hypothesis (where the female obtains some immediate benefit for copulating with the male, food in this case) may explain why courtship feeding has evolved; however, this theory has recently been disputed with the suggestion that the rate of courtship feeding is a way for females to determine the quality of their mate through the handicap principle
Handicap principle
The handicap principle is a hypothesis originally proposed in 1975 by biologist Amotz Zahavi to explain how evolution may lead to "honest" or reliable signaling between animals who have an obvious motivation to bluff or deceive each other...
.
Same-sex Pairing
Homosexual behavior has been well documented in over 500 species of non-human animals ranging from insects to lizards to mammals (reviewed in:). In birds, same-sex pairing has been shown in many families of non-passerines including vultures, ducks, and pigeons . There is also a remarkably high incidence of homosexual behavior in seabirds. Here, homosexual behavior refers to same-sex pair-formation and chick-rearing, not to same-sex copulation, for which there are very few documented examples. Almost all the examples of same-sex pairing in seabirds are of female-female pairs. Furthermore, this phenomenon doesn’t seem to be phylogenetically constrained to any specific order or family of seabirds.There are many examples of homosexual behavior in wild gulls. In Herring Gull (Larus argentatus) populations nesting on the Great Lakes, Fitch (1980) reported a low, yet consistent prevalence of female-female pairs. It appears that female-female Herring Gull pairs are more common in colonies with a female-biased operational sex ratio
Operational sex ratio
In the evolutionary biology of sexual reproduction, the operational sex ratio is the ratio of sexually competing males that are ready to mate to sexually competing females that are ready to mate...
(OSR) and occasionally these homosexual pairs will remain stable for several breeding seasons . In Western Gull
Western Gull
The Western Gull, Larus occidentalis, is a large white-headed gull that lives on the western coast of North America. It was previously considered conspecific, the same species, with the Yellow-footed Gull of the Gulf of California...
s (Larus occidentalis), female-female pairs are often associated with supernormal clutches (clutches of 4-6 eggs; a normal clutch for Larus gull species is 2-3 eggs) and these clutches are usually infertile . Female-female pairs have also been widely reported in wild populations of Ring-billed Gull
Ring-billed Gull
The Ring-billed Gull is a medium-sized gull.Adults are length and with a wingspan. The head, neck and underparts are white; the relatively short bill is yellow with a dark ring; the back and wings are silver gray; and the legs are yellow. The eyes are yellow with red rims...
s (Larus delawarensis). Studies of Ring-billed Gulls has shown that same sex pairs are rare (<1% of pairs in a colony) but consistent interannually and that they also lay supernormal clutches at a significantly higher rate than do heterosexual pairs. It has also been shown that these clutches of female-female pairs have significantly lower hatching and fledging success than heterosexual pairs . There is even one example of an unusual mixed female-female pair of two gull species, the Caspian
Caspian Gull
Caspian Gull is a name applied to the gull taxon Larus cachinnans, a member of the Herring Gull/Lesser Black-backed Gull complex.- Description :...
(Larus cachinnans) and Yellow-legged Gull
Yellow-legged Gull
The Yellow-legged Gull , sometimes referred to as Western Yellow-legged Gull , is a large gull of Europe, the Middle East and North Africa, which has only recently achieved wide recognition as a distinct species...
(Larus michahellis) .
Female-female pairing has also been documented and studied in several tern
Tern
Terns are seabirds in the family Sternidae, previously considered a subfamily of the gull family Laridae . They form a lineage with the gulls and skimmers which in turn is related to skuas and auks...
species including Whiskered
Whiskered Tern
The Whiskered Tern is a seabird of the tern family Sternidae. This bird has a number of geographical races, differing mainly in size and minor plumage details....
(Chlidonias hybyida), Roseate
Roseate Tern
The Roseate Tern is a seabird of the tern family Sternidae. This bird has a number of geographical races, differing mainly in bill colour and minor plumage details....
(Sterna dougalii) and Caspian Tern
Caspian Tern
The Caspian Tern is a species of tern, with a subcosmopolitan but scattered distribution. Despite its extensive range, it is monotypic of its genus, and has no subspecies accepted either...
s (Hydroprogne caspia) with similar attributes (supernormal clutches and reduced hatching/fledging success as compared to heterosexual pairs) to same-sex gull pairs . Also in the order Charadriiformes
Charadriiformes
Charadriiformes is a diverse order of small to medium-large birds. It includes about 350 species and has members in all parts of the world. Most Charadriiformes live near water and eat invertebrates or other small animals; however, some are pelagic , some occupy deserts and a few are found in thick...
(family Chionididae), there has been one reported occurrence of a female-female pair in the Black-faced Sheathbill
Black-faced Sheathbill
The Black-faced Sheathbill , also known as the Lesser Sheathbill or Paddy bird, is one of only two species of sheathbills, aberrant shorebirds which are terrestrial scavengers of subantarctic islands.-Description:...
(Chionis minor), but eggs in the clutch proved to be inviable .
Procellariiformes
Procellariiformes is an order of seabirds that comprises four families: the albatrosses, petrels and shearwaters, storm petrels, and diving petrels...
including the petrels and shearwaters. Antarctic Petrel
Antarctic Petrel
The Antarctic Petrel is a boldly marked dark brown and white petrel, found in Antarctica, most commonly in the Ross and Weddell seas. They eat Antarctic krill, fish, and small squid...
s (Thalassoica antarctica) have been shown to form female-female pairs in colonies where there is a surplus of females; it is hypothesized that “pairing” with another female may be a favorable strategy for some females because it allows them to become established in the colony. The experience with a site gained through forming a female-female pair may greatly improve the chances of future successful breeding for the non-genetic parent, which explains why it might be worth the short-term cost of raising another bird’s offspring . In another member of this family, the Cory’s Shearwater (Calonectris diomedea), same-sex pairing was recently discovered for the first time in a burrow-nesting seabird . This study proposed that similar factors cause female-female pairs to form in burrow-nesting seabirds as in surface-nesting seabirds (a female-biased OSR), and that female-female pairing in burrow-nesting seabirds might have remained undetected for so long due to the secretive nature of these animals.
In albatrosses, female-female pairing has recently received major press coverage. Last year, when a Southern Royal Albatross
Southern Royal Albatross
The Southern Royal Albatross, Diomedea epomophora, is a large seabird from the albatross family. At an average wingspan of around , it is the second largest albatross, behind the Wandering Albatross.-Taxonomy:...
(D. epomophora) couple hatched a chick in New Zealand, it represented the first record of a successful same-sex pair in this species . In a landmark study by Young et al. (2008), she reported over 30% of Laysan Albatrosses in a colony in Oahu, Hawaii were same sex pairs. Even though these female-female pairs had less reproductive success than heterosexual pairs, it was better than not breeding at all. Young et al. (2008) also cited a female-biased OSR as the primary reason for such a high proportion of same-sex pairs. Additionally, an unsuccessful female-female pair of highly endangered of Short-tailed Albatross
Short-tailed Albatross
The Short-tailed Albatross or Steller's Albatross, Phoebastria albatrus, is a large rare seabird from the North Pacific. Although related to the other North Pacific albatrosses, it also exhibits behavioural and morphological links to the albatrosses of the Southern Ocean...
es (P. albatrus) was recently documented on Kure Atoll
Kure Atoll
Kure Atoll or Ocean Island is an atoll in the Pacific Ocean beyond Midway Atoll in the Northwestern Hawaiian Islands at . The only land of significant size is called Green Island and is habitat for hundreds of thousands of seabirds...
, Hawaii
Hawaii
Hawaii is the newest of the 50 U.S. states , and is the only U.S. state made up entirely of islands. It is the northernmost island group in Polynesia, occupying most of an archipelago in the central Pacific Ocean, southwest of the continental United States, southeast of Japan, and northeast of...
.
Penguins represent the only known examples of male-male pairings in seabirds. On the Otago Peninsula
Otago Peninsula
The Otago Peninsula is a long, hilly indented finger of land that forms the easternmost part of Dunedin, New Zealand. Volcanic in origin, it forms one wall of the eroded valley that now forms Otago Harbour. The peninsula lies south-east of Otago Harbour and runs parallel to the mainland for...
of New Zealand
New Zealand
New Zealand is an island country in the south-western Pacific Ocean comprising two main landmasses and numerous smaller islands. The country is situated some east of Australia across the Tasman Sea, and roughly south of the Pacific island nations of New Caledonia, Fiji, and Tonga...
, two-male Yellow-eyed Penguin
Yellow-eyed Penguin
The Yellow-eyed Penguin or Hoiho is a penguin native to New Zealand. Previously thought closely related to the Little Penguin , molecular research has shown it more closely related to penguins of the genus Eudyptes...
s (Megadyptes antipodes) were recently reported incubating an egg. In captivity, Chinstrap
Chinstrap Penguin
The Chinstrap Penguin is a species of penguin which is found in the South Sandwich Islands, Antarctica, the South Orkneys, South Shetland, South Georgia, Bouvet Island and Balleny...
(Pygoscelis antarcticus), Humboldt
Humboldt Penguin
The Humboldt Penguin is a South American penguin, that breeds in coastal Peru and Chile. Its nearest relatives are the African Penguin, the Magellanic Penguin and the Galápagos Penguin...
(Spheniscus humboldti), Magellanic
Magellanic Penguin
The Magellanic Penguin, Spheniscus magellanicus, is a South American penguin, breeding in coastal Argentina, Chile and the Falkland Islands, with some migrating to Brazil where they are occasionally seen as far north as Rio de Janeiro. It is the most numerous of the Spheniscus penguins. Its nearest...
(S. magellanicus), and African Black-footed Penguins (S. demersus) have all been documented to form male-male pairs.
Copulatory Stage
In seabirds, the copulatory stageMating
In biology, mating is the pairing of opposite-sex or hermaphroditic organisms for copulation. In social animals, it also includes the raising of their offspring. Copulation is the union of the sex organs of two sexually reproducing animals for insemination and subsequent internal fertilization...
usually occurs after, and occasionally concurrently, with the formation of the pair bond
Pair bond
In biology, a pair bond is the strong affinity that develops in some species between the males and females in a pair, potentially leading to breeding. Pair-bonding is a term coined in the 1940s that is frequently used in sociobiology and evolutionary psychology circles...
. Copulation occurs mainly on land at the breeding colony. Usually the pair copulates several times, even in orders that lay only one egg per-clutch. These additional copulations are thought of as a mechanism to strengthen the pair bond . This is important for strongly monogamous, long-lived organisms and is especially important in seabirds that spend most of the non-breeding season apart on the open ocean.
Extra-pair Copulation/Fertilization/Paternity
Birds are one of the only major taxa where monogamyMonogamy
Monogamy /Gr. μονός+γάμος - one+marriage/ a form of marriage in which an individual has only one spouse at any one time. In current usage monogamy often refers to having one sexual partner irrespective of marriage or reproduction...
is the dominant mating system . Prior to the advent of genetic techniques, it was assumed that the majority of monogamous birds remained faithful to their partners . However, it is now known that extra-pair copulations (EPCs), extra-pair fertilizations (EPFs), and extra-pair paternity (the raising of another’s offspring, EPP) are actually quite common in a variety of avian orders and families . Roughly 70% of birds that used to be considered genetically monogamous actually engage in EPCs and raise extra-pair young (reviewed by:). Furthermore, it has been proposed that birds that nest in high densities, as seabirds do in breeding colonies, have higher rates of EPCs and EPFs than birds that do not nest colonially. Despite this, Westneat and Sherman (1997) found no significant correlation between nesting density and EPFs in a meta-analysis. Many seabird species raise only one chick per breeding season, which would make the prevalence of EPFs and EPP in seabirds surprising due to the fact that the male’s entire breeding success for a year is dependent on the lone egg/chick he is raising to be his genetic offspring. Moreover, all seabirds have obligate biparental care, so it would be evolutionarily costly for the male to spend months of effort raising a chick that is not his genetic offspring.
In line with this prediction, many studies of seabirds have revealed no EPCs or EPFs. Several genetic studies of Storm-Petrel
Storm-petrel
Storm petrels are seabirds in the family Hydrobatidae, part of the order Procellariiformes. These smallest of seabirds feed on planktonic crustaceans and small fish picked from the surface, typically while hovering. The flight is fluttering and sometimes bat-like.Storm petrels have a cosmopolitan...
s, show no evidence of EPCs or EPFs, which is not surprising considering these are burrow-nesting seabirds that lay only one egg per year. Dovekie (Alle alle), a surface nesting alcid that raises one chick per year, has shown no EPFs or EPP . Nazca Boobies
Nazca Booby
The Nazca Booby, Sula granti, is a booby which is found in the eastern Pacific Ocean, namely on the Galápagos Islands where it can be seen by eco-tourists, and on Clipperton Island...
(Sula granti) have been well studied at breeding colonies in the Galapagos for decades and also show no evidence of EPCs or EPFs; also not a surprising result since they only have one surviving offspring per year . Chinstrap Penguins, which raise two chicks annually, have also shown no EPCs or EPFs.
Contrary to these empirical results, there has been a multitude of studies where EPCs or EPFs have been found in seabirds. Perhaps the most surprising EPFs have been found in the Procellariid family because all members of this family only lay one egg per year and some do not even breed every year . Waved Albatross show high rates (up to 25% of offspring are extra-pair young) of both EPCs and EPFs and behavioral observations have shown that many of the EPCs are forced by the extra-pair male. Studies of Wandering Albatross have shown over 10% of chicks are extra-pair young; an extremely surprising result since adult Wandering Albatrosses only breed once every other year at most. Similar results were seen in Black-browed
Black-browed Albatross
The Black-browed Albatross or Black-browed Mollymawk, Thalassarche melanophrys, is a large seabird of the albatross family Diomedeidae, and it is the most widespread and common albatross.-Taxonomy:...
(Thalassarche melanophris) and Grey-headed Albatross
Grey-headed Albatross
The Grey-headed Albatross, Thalassarche chrysostoma, also known as the Grey-headed Mollymawk, is a large seabird from the albatross family. It has a circumpolar distribution, nesting on isolated islands in the Southern Ocean and feeding at high latitudes, further south than any of the other...
es (T. chrysostoma) nesting on South Georgia Island. EPFs have also been shown in Antarctic Petrels. Perhaps the most unexpected result was when EPCs and EPFs were documented in a burrow-nesting Procellariid, the Short-tailed Shearwater
Short-tailed Shearwater
The Short-tailed Shearwater or Slender-billed Shearwater , also called Yolla or Moonbird, and commonly known as the muttonbird in Australia, is the most abundant seabird species in Australian waters, and is one of the few Australian native birds in which the chicks are commercially harvested...
(Puffinus tenuirostris), because the female would have to leave her burrow to solicit an EPC .
EPCs and EPFs have also been demonstrated to occur in other families of seabirds. In contrast to the results found in genetic studies of Dovekie, EPP has been shown in several species of alcid including Common Murre (Uria aalge) and Razorbill
Razorbill
The Razorbill is colonial seabird that will only come to land in order to breed. It is the largest living member of the Auk family. This agile bird will choose only one partner for life and females will lay one egg per year. Razorbills will nest along coastal cliffs in enclosed or slightly exposed...
(Alca torda), both of which raise only one chick per year. Interestingly, it has been shown that female Razorbills can determine whether or not an EPC leads to an EPF and only accept extra-pair sperm
Female sperm storage
Female sperm storage is a biological process in which sperm cells transferred to a female during mating are temporarily retained within a specific part of the reproductive tract before the oocyte, or egg, is fertilized...
when it gives them a fitness
Fitness (biology)
Fitness is a central idea in evolutionary theory. It can be defined either with respect to a genotype or to a phenotype in a given environment...
advantage over their current mate . A low-rate of EPP has also been shown in the sexually dimorphic
Sexual dimorphism
Sexual dimorphism is a phenotypic difference between males and females of the same species. Examples of such differences include differences in morphology, ornamentation, and behavior.-Examples:-Ornamentation / coloration:...
Great Frigatebird
Great Frigatebird
The Great Frigatebird is a large dispersive seabird in the frigatebird family. Major nesting populations are found in the Pacific and Indian Oceans, as well as a population in the South Atlantic....
(Fregata minor).
Inbreeding
MatingMating
In biology, mating is the pairing of opposite-sex or hermaphroditic organisms for copulation. In social animals, it also includes the raising of their offspring. Copulation is the union of the sex organs of two sexually reproducing animals for insemination and subsequent internal fertilization...
with related individuals is rare in naturally occurring populations of birds due to the production of lower quality offspring suffering from the genetic effects of inbreeding depression
Inbreeding depression
Inbreeding depression is the reduced fitness in a given population as a result of breeding of related individuals. It is often the result of a population bottleneck...
. Seabirds have an inherently high risk of inbreeding
Inbreeding
Inbreeding is the reproduction from the mating of two genetically related parents. Inbreeding results in increased homozygosity, which can increase the chances of offspring being affected by recessive or deleterious traits. This generally leads to a decreased fitness of a population, which is...
because most are natally philopatric
Philopatry
Broadly, philopatry is the behaviour of remaining in, or returning to, an individual's birthplace. More specifically, in ecology philopatry is the behaviour of elder offspring sharing the parental burden in the upbringing of their siblings, a classic example of kin selection...
, and many are highly endangered with some species’ entire populations breeding on one small island . Despite this, inbreeding was observed no more than expected by random chance in the Wandering Albatross and the critically endangered Amsterdam Albatross
Amsterdam Albatross
The Amsterdam Albatross or Amsterdam Island Albatross, Diomedea amsterdamensis, is a huge albatross which breeds only on Amsterdam Island in the southern Indian Ocean. It was only described in 1983, and was thought by some researchers to be a sub-species of the Wandering Albatross, exulans...
(D. amsterdamensis). In contrast, some studies of seabirds have shown evidence of inbreeding. Huyvaert and Parker (2010) detected low frequencies of inbreeding in Waved Albatrosses and genetic similarity was negatively related to EPFs, which is an unusual result that does not support the inbreeding avoidance hypothesis. Close inbreeding was observed at low frequencies in the Cory’s Shearwater where two mother-son pairs were reported.
Chick-rearing Stage
Chick-rearing is the most crucial stage of the reproductive cycle in determining final reproductive successReproductive success
Reproductive success is defined as the passing of genes onto the next generation in a way that they too can pass those genes on. In practice, this is often a tally of the number of offspring produced by an individual. A more correct definition, which incorporates inclusive fitness, is the...
during a breeding season. Chick-rearing includes brooding, feeding, defending, and in some cases, teaching the chick skills it will need to know to survive independently. Chick-rearing can be totally absent in some birds (the Brush-Turkeys of southeast Asia), to a couple weeks long in many passerines, to several months long in larger birds . Seabirds have the longest chick-rearing stage of any bird on earth . It is not unusual for many seabirds to spend 3–4 months raising their chicks until they are able to fledge and forage independently. In the great albatrosses, chick-rearing can take over 9 months . It is because of this extremely protracted chick-rearing stage that many of the larger procellariiform seabirds can breed only once every other year.
Siblicide
Siblicide
Siblicide is the killing of an infant individual by its close relatives . It may occur directly between siblings or be mediated by the parents. The evolutionary drivers may be either indirect benefits for the genetic viability of a population or direct benefits for the perpetrators...
, the death of an individual due to the actions of members of its own clutch, is seen in several avian orders including egret
Egret
An egret is any of several herons, most of which are white or buff, and several of which develop fine plumes during the breeding season. Many egrets are members of the genera Egretta or Ardea which contain other species named as herons rather than egrets...
s and kingfisher
Kingfisher
Kingfishers are a group of small to medium sized brightly coloured birds in the order Coraciiformes. They have a cosmopolitan distribution, with most species being found in the Old World and Australia...
s, some raptors
Bird of prey
Birds of prey are birds that hunt for food primarily on the wing, using their keen senses, especially vision. They are defined as birds that primarily hunt vertebrates, including other birds. Their talons and beaks tend to be relatively large, powerful and adapted for tearing and/or piercing flesh....
, and grackle
Grackle
Grackle can refer to any of eleven black passerine birds native to North and South America. All are members of the Icterid family but belong to multiple genera.* Genus Quiscalus** Boat-tailed Grackle, Quiscalus major...
s. In most of these examples, siblicide is facultative
Facultative
Facultative means "optional" or "discretionary" , used mainly in biology in phrases such as:* Facultative anaerobe, an organism that can use oxygen but also has anaerobic methods of energy production...
(i.e. not obligate
Obligate
Obligate means "by necessity" and is used mainly in biology in phrases such as:* Obligate aerobe, an organism that cannot survive without oxygen* Obligate anaerobe, an organism that cannot survive in the presence of oxygen...
) and only occurs when there is a shortage of food. However in some seabirds, siblicide proves to be obligate
Obligate
Obligate means "by necessity" and is used mainly in biology in phrases such as:* Obligate aerobe, an organism that cannot survive without oxygen* Obligate anaerobe, an organism that cannot survive in the presence of oxygen...
and occurs no matter how productive the breeding season is. The Nazca Booby is one species that practices obligate siblicide . The parents lay two eggs, several days apart. The second egg laid is seen as fertility insurance if the first egg is inviable. If both eggs hatch, the elder chick will push its sibling out of the nest area, leaving it to die of thirst or cold. The parent booby will not intervene and the younger chick will inevitably die. Research has shown that high hormone levels in Nazca Booby chicks are responsible for inciting their murderous behavior. Facultative siblicide is seen in the closely related Blue-footed Booby. Unlike the Nazca Booby, Blue-footed Boobies chicks only perform siblicide when food is scarce. Furthermore, the parents actually try to suppress the siblicidal behavior, rather than ignoring or encouraging it.
Divorce
For most seabirds if breeding is successful they will continue breeding with the same partner year after year until one member of the pair dies or doesn’t return to the breeding colony. However, these pair bonds occasionally dissolve or are forced apart while both members of the pair are still alive, a process known as divorceDivorce
Divorce is the final termination of a marital union, canceling the legal duties and responsibilities of marriage and dissolving the bonds of matrimony between the parties...
. Reasons for divorce in seabirds are wide ranging and include asynchronous arrival of mates to the breeding colony, declining reproductive success of the pair, and competition for mates. Coercive divorce is seen in the Nazca Booby and Common Murre where one member of the pair actively desserts the other or where an intruder enters and forcibly splits the breeding pair to form a new pair.
Divorce is relatively common in gulls and their relatives (reviewed by:); in one study, Black-legged Kittiwake
Black-legged Kittiwake
The Black-legged Kittiwake is a seabird species in the gull family Laridae.This species was first described by Linnaeus in his Systema naturae in 1758 as Larus tridactylus....
s (Rissa tridactyla) proved to be more faithful to their nesting site than their partner. Divorce rates are surprisingly high (>80% of pairs annually) in King
King Penguin
The King Penguin is the second largest species of penguin at about , second only to the Emperor Penguin. There are two subspecies—A. p. patagonicus and A. p...
(Aptenodytes patagonicus) and Emperor Penguin
Emperor Penguin
The Emperor Penguin is the tallest and heaviest of all living penguin species and is endemic to Antarctica. The male and female are similar in plumage and size, reaching in height and weighing anywhere from . The dorsal side and head are black and sharply delineated from the white belly,...
s (A. forsteri). Asynchronous arrival of mates at the breeding colony is cited as the main reason for this because these penguins have extreme time constraints on their breeding. In Great Skua
Great Skua
The Great Skua, Stercorarius skua, is a large seabird in the skua family Stercorariidae. In Britain, it is sometimes known by the name Bonxie, a Shetland name of unknown origin.-Description:...
s (Stercorarius skua) divorce occurs annually, but at low frequencies (6-7% of pairs annually) and death is responsible for approximately three times more pair interruptions than divorce. Divorce is uncommon in procellariiforms and usually only occurs after several years of breeding failure. However, one study of Short-tailed Shearwaters observed the divorce rate in a colony to be as high as 16% annually.
See also
- SeabirdSeabirdSeabirds are birds that have adapted to life within the marine environment. While seabirds vary greatly in lifestyle, behaviour and physiology, they often exhibit striking convergent evolution, as the same environmental problems and feeding niches have resulted in similar adaptations...
- MatingMatingIn biology, mating is the pairing of opposite-sex or hermaphroditic organisms for copulation. In social animals, it also includes the raising of their offspring. Copulation is the union of the sex organs of two sexually reproducing animals for insemination and subsequent internal fertilization...
- Animal sexual behavior
- Homosexual behavior in animals
- MonogamyMonogamyMonogamy /Gr. μονός+γάμος - one+marriage/ a form of marriage in which an individual has only one spouse at any one time. In current usage monogamy often refers to having one sexual partner irrespective of marriage or reproduction...
- Bird colonyBird colonyA bird colony is a large congregation of individuals of one or more species of bird that nest or roost in close proximity at a particular location. Many kinds of birds are known to congregate in groups of varying size; a congregation of nesting birds is called a breeding colony...
- AlbatrossAlbatrossAlbatrosses, of the biological family Diomedeidae, are large seabirds allied to the procellariids, storm-petrels and diving-petrels in the order Procellariiformes . They range widely in the Southern Ocean and the North Pacific...
- ProcellariiformesProcellariiformesProcellariiformes is an order of seabirds that comprises four families: the albatrosses, petrels and shearwaters, storm petrels, and diving petrels...
- PenguinPenguinPenguins are a group of aquatic, flightless birds living almost exclusively in the southern hemisphere, especially in Antarctica. Highly adapted for life in the water, penguins have countershaded dark and white plumage, and their wings have become flippers...
- PelecaniformesPelecaniformesThe Pelecaniformes is a order of medium-sized and large waterbirds found worldwide. As traditionally—but erroneously—defined, they encompass all birds that have feet with all four toes webbed. Hence, they were formerly also known by such names as totipalmates or steganopodes...
- CharadriiformesCharadriiformesCharadriiformes is a diverse order of small to medium-large birds. It includes about 350 species and has members in all parts of the world. Most Charadriiformes live near water and eat invertebrates or other small animals; however, some are pelagic , some occupy deserts and a few are found in thick...