Abstract

A variety of terrestrial vertebrates have evolved mechanisms of chemical defense. For example, neotropical poison dart frogs synthesize and store neurotoxic alkaloids in their skin. One of the compounds produced by the poison dart frog has recently been discovered in birds of the genus Pitohui, leading to increased interest in the possibility that other birds may be chemically defended. Although it has been reported that no other examples of chemical defense are known among birds, this paper reports a case which may have been previously overlooked.

A group of seabirds called the fulmars have an unusual method of defense. When an intruder approaches the nest, a fulmar ejects yellowish stomach oil from its mouth. The oil has an unpleasant smell that may serve as an aposematic repellent. Stomach oil may also be used to drive off intra- and inter-specific competitors for nesting sites. In this paper, the behavior of fulmars with respect to nest defense is summarized. The composition and synthetic origin of stomach oil are also reviewed.

Cage experiments have shown that fulmar stomach oil clings to feathers or hair, causes them to become matted, and destroys their insulating properties. Seabirds drown when feathers become waterlogged. A fulmar may itself become contaminated but can remove the oil by bathing and preening. Because other birds are unable to eliminate the oil by these same methods, some mechanism must be at work which gives fulmars 'immunity' to the effects of stomach oil.

The fulmars belong to the order Procellariiformes, which includes albatrosses and petrels. Except for diving petrels, all procellariiform seabirds produce stomach oil and feed it to their young. To explore the evolutionary origins of their use in defense, I also describe the production, composition, and function of stomach oils in sea birds which are closely related to the fulmars.
 

Introduction

A variety of terrestrial vertebrates have evolved mechanisms of chemical defense. These mechanisms range from the relatively benign odors used by skunks, porcupines, and peccaries to warn off predators to the offensively used venoms of snakes and other herpetofauna. Neotropical poison-dart frogs of the genus Phyllobates, for example, synthesize and store neurotoxic alkaloids in their skin (Anonymous 1997, Dumbacher et al 1992).

Birds, however, are generally not considered to be chemically defended, although a few species such as Eurasian quail and the ruffed rouse are known to be poisonous and have caused human deaths (Dumbacher and Pruett-Jones 1996). In addition, homobatrachotoxin, one of the compounds produced by the poison dart frog, was recently discovered in three bird species in the genus Pitohui. The highest concentrations of the toxin are found in the feathers and skin and lower concentrations are present in muscle and internal organs (Dumbacher et al 1992), indicating that the compound may serve to deter would-be predators.

The discovery of an alkaloid toxin in the Pitohui species has led to increased interest in the possibility that other birds may use chemical means of defense. For example, a recent survey by Weldon and Rappole (1997) tallied 80 genera of birds which are malodorous and 30 which are unpalatable. These bird species use odor as an aposematic cue of their unpalatability and/or the presence of chemicals used in their defense.

This paper examines the oil-spitting behavior of fulmars as a possible case of avian chemical defense which may have been previously overlooked. I review the defensive behavior of fulmars as chicks and adults, the synthesis and composition of the oil, and taxonomic relationships which may give clues to the evolution of oil-spitting as a defensive tactic.
 

Chemical defense in birds

Chemical defense, as defined by Dumbacher and Pruett-Jones (1996, p. 139), "occurs when an individual contains or uses behaviorally one or more chemical substances that deter predators and/or parasites." Most definitions of chemical defense identify predators or pathogens as the targets of the defense, although testing this notion may prove to be difficult. For example, the Pitohui toxin has been shown to cause convulsions and death when injected into mice (Dumbacher et al 1992) but has not been tested against any of the Pitohui species' actual predators or parasites (Glendinning 1993).

Although it has been reported that there are no known examples of chemical defense among birds outside of the genus Pitohui (Dumbacher et al 1992), Dumbacher and Pruett-Jones (1996) list ten species which are either toxic or use chemicals maleficently. One of those species is the Northern Fulmar Fulmarus glacialis. While this and related species of fulmars use stomach oil to befoul invaders, as described below, whether the behavior actually deters predators, and thus whether fulmars can truly be considered to be chemically defended, remains largely undetermined.

Methods of chemical defense in birds. In birds, the definition of a chemical defense used is especially important because the manner in which the bird is defended is often behavioral in nature. Preening, for example, may be done primarily to distribute waxes which have anti-pathogen activity (Pugh 1972). Birds have also been observed applying ants, millipedes, lime, and plant materials to their bodies in a behavior known as "anting" (Ehrlich et al 1986), and this activity may repel arthropod parasites. The use of fresh plant material in nests may be a chemical defense against pathogenic bacteria, fungi, lice and mites (Dumbacher and Pruett-Jones 1996). When birds make use of compounds which deter, damage, injure or harm predators, the chemical may be used offensively, as in Eurasian Hoopoes, which squirt secretions from their anal glands (Dumbacher and Pruett-Jones 1996), or in the fulmars described here.
 

Chemical defense in fulmars

The fulmars (Procellariiformes: Procellariidae) are pelagic sea birds which have specialized aerial locomotion that allows them to exploit food resources at or near the surface of the open sea (Warham 1990). Their habitat encompasses the circumpolar regions of both the northern and southern hemispheres (Warham 1990). While the Northern Fulmar Fulmarus glacialis (Figure 1) is the only fulmar in the northern hemisphere, its distribution extends as far south as Japan and southern England (Fisher 1952). There are seven species of fulmars in five genera. They are closely related to the albatrosses and are members of the order of marine birds which are collectively known as "the petrels" (Procellariiformes, Table 1).

Fulmars exhibit an unusual behavior which may be viewed, using the above definition, as a chemical method of defense. When an intruder approaches its nest, a fulmar makes coughing noises, lunges at the interloper (Figure 2a), and ejects volleys of yellowish stomach oil from its mouth (Warham 1990, Figure 2b). The oil has an unpleasant sweet, fishy smell that may enhance the repellent effect (Weldon and Rappole 1997). In addition to foul smelling stomach oil, all species of fulmars have a characteristic musky odor which permeates even the eggs. In the giant petrel, the egg shells smell strongly even after 100 years in museum collections (Warham 1990, Sick 1993) and the odor may itself serve to deter egg predators. The name "fulmar" is from the Norse ful + mar, meaning "foul gull" and probably refers to the oil spitting behavior (Warham 1990) but may also allude to their odor.

Oil-spitting by fulmar chicks. Fulmar chicks have long been renowned for their readiness to "spit" stomach oil at anything approaching them. As early as 1697, a visitor to the island of St. Kilda in the Hebrides recorded this behavior: "When the young Fulmar is ... approached, [it] ejects a quantity of pure oil out at his bill, and will be certain to hit any that attack him, in the face, though seven paces distant; this he uses by way of defence..." (M. Martin, as quoted in Fisher 1952). Very young chicks show the spitting reflex and can reportedly eject small amounts of oil even before hatching is completed (Lees 1950). Chicks are more coordinated than adults in directing their discharge (Armstrong 1951), and at four days old can send the ejected oil a distance of 0.3 m (1 ft, Pinder 1966). This range increases with age up to a maximum of about 1.5 m (5 ft, Fisher 1952). The birds may eject oil three or more times in succession (Fisher 1952).

Fulmar chicks are left alone in the nest for relatively long periods while their parents forage at sea, leaving the young vulnerable to predation by cats, otters, skuas, crows, gulls, and raptors. The chick will discharge oil at the parents, when they return from foraging, as readily as if a predator were approaching, until the chick begins to distinguish its parents from other intruders at around three weeks of age (Duffey 1951).

Nest defense by adults. In addition to its use in defense against predators, stomach oil is used by adult fulmars to drive off intra- and inter-specific competitors for nesting sites. This behavior intensifies during the breeding season: The cape petrel Daption capense uses stomach oil only as a last defense during its pre-egg-laying period, first using hissing and lunges, but displays both defensive and oil-spitting behavior after the single egg has been laid (Pinder 1966). The warning dance and vocalizations may do more than conserve stomach oil: conspicuous displays are associated with unpalatability and the presence of chemical defenses in other birds (Dumbacher and Pruett-Jones 1996).

Effects of stomach oil on other animals. Cage experiments have shown that fulmar stomach oil clings to feathers or hair, causes them to become matted, and destroys their insulating properties (Warham 1976). Seabirds drown when feathers become waterlogged (Swennen 1974) and oxidation of the oil by air results in resination and permanent feather damage (Jacob 1982).

A fulmar may itself become contaminated but can remove the oil by bathing and preening. Because other birds are unable to eliminate the oil by these same methods, some mechanism must be at work which gives fulmars 'immunity' to the effects of stomach oil. Fisher (1952) even reports that fulmars apply small amounts of stomach oil to their plumage when preening. Warham (1977) suggests that fulmars may have a special feather structure.

Effectiveness of oil-spitting as a defense. The oil-spitting behavior of fulmars has been seen to repel skuas and feral cats (Warham 1977) and may be effective against raptors and other seabirds, as evidenced by the dramatic effects of oiling their plumage (Swennen 1974). However, little is known about the ability of this defense to repel fulmar predators in the wild.

The combination of musty odor, putative unpalatability, and oil-spitting would seem to be effective defenses against human predators (Weldon and Rappole 1997). On the contrary, the Northern Fulmar Fulmarus glacialis was a mainstay for some North Atlantic island communities. On St. Kilda, residents harvested nearly 10,000 young birds a year from 1829 to 1911, snaring an average of 115 birds per capita (Fisher 1952).

Although the strong smell of fulmar permeated their homes (and persisted for at least 20 years after the buildings were abandoned), the birds provided many products to humans. Fulmar eggs and meat were eaten, stomach oil was gathered and burned in lamps, feathers were used in bedding and to pay rent, bones were made into hooks, and carcasses were used as bait (Fisher 1952, Warham 1990).

Synthetic origin and composition of stomach oil. In all of the procellariiform birds except the diving petrels (Table 1), large quantities of stomach oil are stored in the large, distensible fore-gut, or proventriculus (Warham et al 1976, Warham 1977). The oil of Fulmarus glacialis is composed mainly of triglyceride and free fatty acids and has a low viscosity with a specific gravity of 0.88 (Warham 1977). The oil will solidify to a wax at cool temperatures and has a sweet and somewhat fishy smell. The color varies from colorless to deep reddish-brown but is often reported as yellowish.

Warham (1977, see also Warham et al 1976) has used thin-layer and gas-liquid chromatography to analyze the composition of oil samples from 25 species of petrels. The main components were triglyceride and wax esters, but alcohols and hydrocarbons were also present in substantial amounts in some species. The oil may also contain vitamins A and D (Fisher 1952). The composition of petrel stomach oils is more fully reviewed by Jacob (1982).

There has been considerable debate over whether stomach oils are secreted by the numerous glandular cells of the proventriculus or are derived from the birds' diets. Reports that "unborn" chicks can expel oil (Lees 1950) and that chicks can spit oil even after long periods without food (Warham 1977) seem to support a secretory origin for the oil. However, there is wide variety in the color of the oil even within individuals of a single species (Pinder 1966) and a reddish color has long been attributed to dietary sources, including zooplankton and squid (Fisher 1952).

Warham and colleagues (1976, Warham 1977) also found wide variety in the lipid composition of petrel oils, with no pattern between lipids present and bird genus. Because a glandular secretion would be expected to remain fairly constant in composition, both within individuals of a species and between closely related species (Jacob 1982), petrel stomach oil is now considered to be dietary in origin (Roby et al 1997). This conclusion is confirmed by the fact that the wax esters and pigments in petrel oils can also be found in Crustacea, squid and fish (Warham et al 1976, Warham 1977).
 

Evolutionary relationships

The fulmars belong to the order Procellariiformes, which includes albatrosses and petrels (Table 1). The Procellariiformes have are known collectively as "the petrels" and have evolved from a single ancestor (Warham 1990). Petrels are identified by the horny tubes which sheath their nostrils and may form a hump at the dorsal base of the bill. These are especially large in the fulmars (Figure 3).

Oil-spitting as an exaptation. Except for diving petrels, all procellariiform seabirds produce stomach oil and feed it to their young. Stomach oil is, in fact, necessary for proper nutrition and provisioning of young petrels (Roby et al 1997) and provides a good source of energy which may be slowly "mobilized" and may also retard digestion and serve as a food preservative (Warham et al 1976, Warham 1977). The fatty alcohols in the oil act as lipase inhibitors and regulate lipid digestion; the low pH of the fore-gut also allows protease action but inhibits lipolysis, allowing the bird to retain fats from its diet (Jacob 1982). Stomach oil is also exchanged between adults during courtship feeding (Jacob 1982).

The non-defensive functions of stomach oils indicate that production of stomach oil is an exaptation, a trait which evolved primarily for nutritive purposes and was secondarily adapted for defensive purposes (Warham 1977). The fact that other petrels, including albatross chicks, spit small quantities of stomach oil when disturbed but do so with poor coordination or aim (Warham 1977, 1990) may provide evidence for this evolution.

The defensive use of stomach oil may have evolved first in young petrels, which are far more adept at aiming their volleys of oil. In albatrosses, the chicks spit but adults do not, confirmation that the better coordinated defensive behavior in chicks is due to its earlier development (Fisher 1952).

While spitting calorie-rich oil may seem like a waste of resources, Armstrong (1951) suggests three ways in which the evolution of oil-spitting behavior benefitted the fulmars. First, having a well-defended chick allowed fulmars to nest in more open sites, where chicks are more exposed to predation, thus increasing their distribution. Second, the parents are able to leave the chick alone and forage simultaneously, decreasing the chance that the chick will starve. Third, the parents can forage during daylight hours, allowing them to make more trips to feed the chick, again decreasing the chance of starvation. These advantages must have outweighed the energetic losses of ejecting the stomach oil rather than metabolizing it.

Why do fulmar chicks spit at their parents? Chicks which move even a few feet from the nest are abandoned by their parents and become 'starvelings' (Pinder 1966). Therefore, the chick cannot flee the nest in response to a predator; its defense must be one which can be employed in situ. The defense must also be very rapidly initiated, owing to the speed of attack by avian predators, since any delay in the spitting action would not allow the chick to escape. Thus, chicks must spit oil at any bird or other animal approaching the nest for the defense to be effective and there is no opportunity for the evolution of appeasement behavior in the parents (Armstrong 1951).

The importance of nest location. Adult petrels have low mobility on land due to their special adaptations for flight (Sick 1993), and the incubation and chick rearing times are prolonged, making petrels vulnerable to predation during the breeding season. Presumably, it is for this reason that nesting sites are located on mid-ocean islands, promontories, mountains, or inland Antarctica, areas which are protected from mammalian (but not avian) predators (Warham 1990). All petrels are social breeders (Warham 1990) and thus susceptible to predators (which can locate colonies by the strong, characteristic smell). In addition, the Snow and Antarctic Petrels are parasitized by McCormick's Skua Stercorarius maccormicki (Warham 1990)

There is a relationship between the use of stomach oil for defense and type of nesting site chosen by a petrel species. Nests of the smaller petrels are located in rock crevices, ledges or underground burrows, while the larger giant petrels and albatrosses are surface nesters (Warham 1990). Burrowing species do not spit; ledge and surface nesters, including albatross chicks, do spatter oil at intruders (Warham et al 1976 ). It can be inferred that the relative exposure of the nestling has been important in the evolution of oil-spitting behavior, with higher levels of predation risk providing selection pressure for the ability of a chick to defend itself.

Why are diving petrels the exception? The diving petrels are inshore pursuit feeders when nesting and do not need to leave their chicks for long periods to find patchy food resources (Warham 1990). Therefore, the chicks of diving petrels have far less need for either a slowly metabolizable energy source or a chemical defense. In contrast, the fulmars are pelagic surface feeders and must fly far from the nest to forage, leaving their chicks alone and undefended but for their stomach oil-spitting behavior.
 

Summary and conclusions

While birds have often been overlooked as chemically defended creatures, many employ various methods of chemical defense against predators, parasites, and competitors. One of the more unusual methods is used by fulmars, namely the ejection of stomach oil at approaching enemies. This defensive behavior may have evolved from the need to provision chicks by parents which must range far from the nest for food. Whether this behavior is effective at reducing predation rates is yet unproven, and further study is needed before fulmars can be conclusively described as chemically defended birds.
 

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