84 PROCEEDINGS OF THE NEW ZEALAND ECOLOGICAL SOCIETY, VOL. 24, 1977

THE INCIDENCE, FUNCTIONS AND ECOLOGICAL SIGNIFICANCE OF STOMACH OILS

JOHN WARHAM

Department of Zoology, University of Canterbury, Chrb;tchurch

SUMMARY: Recent research into the origins and compositions of the stomach oils unique to sea~ of the Procellariifonnes is reviewed. The sources of these oils, most of which contain mainly wax esters and/or trigIycerides, is discussed in relation to the presence of such compounds in the marine environment. A number of functions are proposed as the ecological roles of the oils, including their use as slowIy~mobilisable energy and water reserves for adults and chicks and as defensive weaponry for surface-nesting . Suggestions are made for further research, particularly into physiological and nutritional aspects.

INTRODUCTION their table, a balm for their wounds, and a medicine Birds of the Order Procellariiforrnes (, for their distempers." In New Zealand, Travers and fuJmars, shearwaters and other ) are peculiar Travers (1873) described how the Chatham Island in being able to store oil in their large, glandular and Morioris held young petrels over their mouths and very distensible fore-guts or proventriculi.. All petrel allowed the oil to drain directly into them. In some spedes so far examined, with the significant excep- years the St Kildans exported part of thei.r oil har~ tion of the diving petrels, Fam. Pelecanoididae, have vest, as the Australian mutton-birders stilI do with been found to contain oil at various times. The oi.1 oil from the chicks of P. tenuirostris. This has been occurs in both adults and chicks, in breeders and used as a basis for sun~tan lotions, but most nowa- non~breeders, and in birds taken at sea and on land. days ;.<;used as a food stock supplement: a small The oil is a light (specific gravity 0.88), low viscosity quantity is said to impart a shiny coat to horses. Some fluid, often solidifying to a wax in cool conditions, 2796 gallons (12711 n were sold after the] 976 season with a sweet, slightly fishy smell. It may be colour- as a by product of the! harvesting of 549352 squabs less or straw-coloured, but it is often darker - from (B. S. Simmonds, pers. comm.). It is also possible amber to a deep reddish-brown. The colour is that has been used medicinally in neither constant nor species-specific. For example, the east for thousands of years. that from the (Daption capense) is bright A surgeon, John Scouler (1826), was among the orange before egg laying but becomes duller during first in modern times to discuss stomach oil from the birds 4 to 6 day incubation stints and at the end personal experience. He wrote of Daption capen.se, of these is normally dull green (Pinder, 1966). This caught off Patagonia, which "never failed to vomit a green tinge is common also in oil samples collected considerable quantity of yellowish oily fluid on his from fasting adult petrels and may be due to the enemy, and on dissection the source of this supply is presence of bile pigments. easi,ly detected. The first stomach is large and mem- Many surface-nesting petrels spit oil in defense or branous and thickly set with numerous glandular offense, but copious amounts are often found in the follicles, which appear to be the organs which secrete chicks of burrowing species and these seldom spit this oily fluid, the only defensive weapon this oil. Northern (Fulmarus f?/aciaUs) chicks at St possesses." Kilda yielded about 280 ml of oil each; sooty shear- A number of papers describing aspects of the bio~ water (PufJinus f?dseus) chicks may contain 120 ml, chemistry of petrel oi,ls appeared in the 1920's and while Murphy (1936) reports 200 mI of oil being 1930's, but the analyses were incomplete by modern taken from a short~tailed shearwater (PufJinus tenui- standards. The investigators seem to have known rostris) chick: this would amount to about 30% of little of the birds in life and so made erroneous the adult's body mass. deductions such as that of Otago chemists Carter Petrel oil has been used medicinally, as a lubricant and Malcolm (1927) who concluded that mutton- and as an iItuminant. The was a oil was ingested preen gland secretion. Tn some mainstay of the St Kildans' economy, supplying "oil accounts the species from which the oil was drawn for their lamps, down for their beds, a delicacy for were misidentified e.g~ oil from the Australian and W AlHHM' fNrmf:Nrf: FUNCfIONS AND EcOLOGICAL SIGNIFICANCEOF PETREL STOMACH OILS 85

New Zealand mutton-birds (P. tenuirostris and P. COMPOSITIONS griseus) was attributed to a quite different petrel The main components of the oil samples so far Pterodroma lessoni (Serventy, Serventy and Warham, analysed (by thin-layer and gas-liquid chroma- 1971). tography and infra-red spectroscopy) are summarised In the early 1960's this writer circulated a review in Table 1. of current knowledge about petrel stomach oils In 24 of the species-samples either triglycerides or among procellariiformists asking for samples of oil wax esters predominated. Many samples contained so that analyses using modern techniques could be both. In a few oils there were no wax esters, in others run to establish, a. whether the oils were of similar no triglycerides. Oil from one species. Oceanodroma composition and therefore probably of a secretory leucorhoa, had neither: instead, large quantities of nature, or b. of varied composit~on and therefore glycerylether diesters were found. These were also more likely to be food-derived. These analyses have present in oils from Pterodroma mallis, Puffinus recently been published (Warham, Watts and Dainty, carneipes and aequinoctialis but in 1976; Watts and Warham, 1976) and with compar- smaller proportions and only in association with wax able analyses by other workers they provide inform- ester or triglyceride. ation on oils from 25 petrels, There are about 100 In addition to the components shown in the table, species in the order. most oils contained small quanties of di-and mono~

TABLE 1. The main constituents of petrel stomach oi/s. (X = principal constituent, X = less abundant constituent, WE = wax ester, TG = triglyceride, Ch = cholesterol, DAG = diacylglycerol, S = squalene.)

Species WE TG Ch DAG S Authority

Dioffiedeidae Diomedea epomophora X X X Warham et al., 1976 D. exulans X x x Lewis, 1969a D. melanophris x X Warham et al., 1976; Clarke & Prince, 1976 D, chrysostoma x X Clarke & Prince, 1976 D. bulleri X Warham et al., 1976 Phoebe tria palpebrata X Warham et al., 1976 Macronectes giganteus X X Clarke & Prince, 1976 M.halli X X Warham et aI., 1976; Clarke & Prince, 1976 Fulmarus glacialis X x Cheah & Hansen, 1970a; Warham et al., 1976 Dap/ion capense X x Warham et al., 1976 Pagodroma nivea X Warham et aI., 1976 Pterodroma macroptera X Cheah & Hansen, 1970b Pt. lessoni X Warham e/ al., 1976 Pt. inexpectata X X Warham et al., 1976 Pt. mol/is X x x X Warham e/ al., 1976 Halobaena caerulea X x Clarke & Prince, 1976 desolata X x Clarke & Prince, 1976 Proal/aria aequinoctialis x x x x Warham et al., 1976 Pro westlandica x X x Lewis, 1969a Puffinus griseus X x Warham et al., 1976 P. tenuirostris X x Cheah & Hansen, 1970a ; Warham et al., 1976 P. carneipes X X x Lewis, 1969a P. pacijicus X X Cheah & Hansen, 1970b Hydrobatidae Hydrobates pelagicus X Warham et al., 1976 Oceanodroma leucorhoa x X Lewis, 1966 86 PROCEEDINGS OF THE NEW ZEALAND ECOLOGICAL SOCIETY, VOL. 24, 1977 glycerides and cholesterol, some free fatty acid and ated and there were smaller amounts of alcohols. However, one of two samples of oil from triglyceride and squalene. Puffin us pacificus contained substantial proportions 3. The constJ.tuents of the petrel oils show strong of cholesterol (43 % by weight), one from Pterodroma similarities to those of oils from crustacea, macl'optera 30% of cholesterol ester, whUe oils from and either eaten by petrels or related Daption capense and Procellaria aequinoctialis con- to known foods of petrels. This also includes tained 23-43 % of long chain alcohols. the hydrocarbons pristane and squalene: the latter could originate from shark's flesh or liver ORIGINS eaten by scavenging albatrosses, pristane from Tne origin of these oils has been the subject of copepods and planktonic herbivores lower some dISCUSSIonsmce Scouler and later anatomists down in the food chain. drew altention to the copious glands in the petrel An example of the correspondence in proventncuJUs. One school believed that the constitutions is given by the fatty acid and were fooo residues, even excretory products, of birds alcohol components of the wax esters and the with an excess of fat in their diet; another that the fatty acids of the triglycerides from marine oils were internal secretions of the proventricular and petrel stomach oils. Both show a glands. Harrison Matthews (1949) examined stained preponderance of 16:0, 16: 1,18: 1,20: 1,20:5 sections of proventri.cular epithelia and concluded and 22: 6 carbon chain compounds. Oil from that the glands were probably secreting lipid into the Daption capense, however. was unique in lack- lumen of the stomach. ing 14: 0 or 16: 0 a1cohols in its wax esters. However, the intra~cellular fat that Matthews This suggests that there is something special observed stained wi.th Sudan Black but not with about this petrel's foods, at least around the Sudan III or IV. and as Sudan stains pick out all Snares Islands where the birds were sampled. neutral lipids whereas only Sudan Black stains Imber (1976), who also believes in the phospholipids, it seems likely that the lipid Matthews dietary origin of stomach oils, emphasises that detected was dietary phospholipid being taken up many petrels feeding at night take vertically with the aid of an acid phospholipase (Watts, pers. migrating mesopelagic crustacea, fish and squid cornm.). There is very little phospholipid in the whose lipids contain much wax ester. He also stomach oils so far examined. though a good deal in draws attention to the similarity between the potential prey organisms. cephalopod diet of the albatrosses Diomedea All the analyses indicate that the oUs are derived exu/ans and D. epomophora and that of the from the petrels' diets, for the following reasons:- sperm whale Physeter catodon. The whale's 1. The intra-specific variations in the compositions tissues are rich in wax esters as are their of the oils are far greater than would be cephalopod prey. So too are the birds' stomach expected of a secretion, such as that of the oils (Table I). proventriculus. For example, Clarke and Prince 4. The pigments of the oils are the same as natural (1976) analysed the individual oils from 35 lipid-soluble pigments in marine invertebrates. adult Halobaena cael'u/ea and found a wide Thus carotenoid astaxanthins in oil from alba~ range in the proportions of the main constit~ trosses. giant petrels and prions resemble those uents. The wax esters had a mean value with from decapods and euphausids (Lewis, 1969a; one standard deviation of 68.9 + 21.7% of Clarke and Prince, 1976). One exception con- total lipid, while the triglycerides at 12.1 :t cerns the pigments of P. tenuirostris oil which 10.8 % were even more variable. Similarly were different fwm those of the euphausid Lewis (1966) found that the glycerylether Nyctophanes australis which forms this bird's contents of oils from four adult O. leucorhoa main pTey (Cheah and Hansen, 1970a). varied between 20% and 84% of the total lipid. 5. In the only analysis of organochlorine com- 2. The inter-specific variations in the compositions pounds in stomach oils so far published, Bogan is even greater (Table 1) and there seems to be and Bourne (1972) found that F. glacialis oil no correlation between composition and tax~ contained only 1.3 p.p.m. of polychlorinated onomic status. For example, two of the oils of biphenyls in contrast to 42 p.p.m. in the bird's the six albatrosses contained mostly triglyceride, body fat. The adults evidently did not pass on two others mainly triglyceride with lesser the high levels of PCB's to their young when amounts of wax ester, one contained about they fed them oil and Dr Bourne (pers. comm.) equal proportions of tri-glyceride, wax ester and points out that the oil's low PCB values provide squalene while in the sixth wax ester predomin- further evidence of its non~secretory origin: WARHAM: INCIDENCE, FUNCTIONS AND ECOLOGICAL SIGNIFICANCE OF PETREL STOMACH OILS 87

had the oil been synthesised in the bird a con- The quantities of lipid and the proportions of wax centration of organochlorines would have been ester to triglyceride may not only vary with age and expected to occur, as in the fat. breeding status, but also with the animal's stage of 6. Watts and Warham (1976) found that the intact starvation and with environmental factors. Polar and lipids of the oils consist of randomly associated deep sea copepods tend to be rich in wax ester fatty alcohols and/ or acids. These authors point whereas those of sub-tropical seas are high in out that this is what would be expected in oils triglyceride (Lee et ai., 1971). The of dietary origin, whereas with lipids synthe- t.uphausia superba lacks waxes but contains substan- sised by glands, e.g. mammalian mammary tial quantities of triglycerides, whereas E. crystallor- glands or liver, there are specific associations ophias, which lives in colder water near or under the between particular fatty alcohols and/or fatty pack ice, lacks triglycerides but contains significant acids. levels of wax esters (Bottino, 1975). 7. Variations in the compositions of oils from An important function of both wax esters and different members of the same petrel species triglycerides in marine organisms is in energy meta- are readily explained by mixed diets. Further- bolism (Nevenzel, 1970; Ackman et aI., 1970; Benson more, even if the birds fed on the same prey, el ai., 1972). Also marine species, like arid zone land differences in the resulting stomach oils would animals, tend to use lipid metabolism for the produc- be expected because the lipids of particular tion of water. Copepods have been dubbed "camels prey species are not of constant composition of the sea" for this reason and polar species of cope~ but may change during the annual cycle or pods store great amounrs of wax during the short with alterations of water temperature, so that summer and draw on this reserve to fuel moulting, their wax ester/triglyceride ratios vary in time mating and egg production during the dark part of and space. the yea,r (Benson et a/" 1972; Sargent, 1976.) These animals can use up their stores at controlled rates due WAX EsTERS, TRIGLYCERIDES, GLYCERYL ETHERS, to the actions of wax ester and triglyceride lipases. PRISTANE AND SQUALENE IN THE MARINE Trigly!cerides form the usual energy reserves in ENVIRONMENT diatoms, dinoflagellates, teleosts and many pelagic Both wax esters and triglycerides are found in crustacea (Benson et aI., 1972). small to large amounts in many organisms whi.ch are Starvation experiments have shown how these eaten or likely to be eaten directly or indirectly, by reserves may help marine animals to withstand bad petrels. For example, wax ester in the copepod feeding conditions. Lee (1974) starved four species Calanus helgolandicus composed 30-40% of total of copepod for a month with little mortality occurr- lipid; in mullet eggs 70%, and in Latimeria muscle ing. The triglycerides were first utilised and only 93 % (N evenzel, 1970). Whale blubber contains when these were nearly or completely exhausted were 50~80% wax ester, the remainder of the lipid being the wax esters slowly consumed. The ability to wi.th- triglyceride. Some copepods contain up to 40% dry stand long periods of starvation is also pronounced weight of triglyceride and others up to 50% dry in deep sea copepods and has been interpreted in the weight of wax ester (Lee et al., 1971). Spermaceti is light of their uncertain food supply (Benson et al., mainly wax ester and this, and the mutton-bird oils 1972). referred to earlier, appear to he the only wax esters Large amouts of wax esters also occur in deep of animal origin sold commercially. One squid had living fish (Nevenzel, 1970; Lee et aI., 1971), evidently 27 % of its lipid as wax ester, 6 % as triglyceride derived from deep water copepods. These latter (Benson et aI., 1972). Triglyceride was the principal authors pointed out that for carnivorous species lipid in zooplanktonic ostracods, pteropods, occupying regions where the standing stock of food euphausids, amphipods and decapods collected in the is low, it would be advantageous to have an efficient Strait of Georgia, British Columbia (Lee. 1974). digestive system, a low average metabolic rate and Most marine animals so far analysed contain both large energy reserves. Wax esters would supply the wax ester and triglyceride, but with much inter- latter. Benson et. aI., (1972) suggested that at least half specific variation in their proportions. These of the earth's photosynthesis production is stored. for proportions may also be dramatically different in the a time, as wax. same species at different times. Thus the eggs and Petrels readily feed on fat and oil released onto early nauplii. of Calanus helgolandicus have 60 % the sea during whaling, sealing and fishing operations. triglyceride in their lipid reserve but no wax ester, Indeed fat has long been used as a lure for petrels. whereas the eggs are laid by adults containing largely In the open , oil slicks also occur naturally, wax ester (Benson et al., 1972). like those containing wax ester and triglyceride 88 PROCEEDINGS OF THE NEW ZEALAND EcOLOGICAL SOCIETY, VOL. 24, 1977 described by Lee and Williams (1974) which probably that the stomach oil contains from 5 to 35 resulted from a massive mortality of Calanus species. times the energy content of the prey at the time Such slicks may provide yet another source of petrol of capture. stomach oil. In this role the oH would supplement the According to Nevenzel (1970), the wax esters in more conventional energy reserves of sub- most marine species result from biosynthesis in the dermal and visceral fat that are laid down by animal itself. He referred to experimental work with petrels and other sea-birds and which are also elasmobranchs and lantern and suggested a drawn on during fasts. route for the synthesis and breakdown of wax esters The oil is certainly fed to the chicks and as from and to fatty acids and alcohols. This scheme these may have to go for days without meals, also allows for the transformation of wax ester to despite exposure to inclement weather, the and from triglyceride via fatty acid intermediates. ability to draw on a high energy resource would Benson et al.. (1972) thought that the unsaturated have obvious value. The protein needed for wax esters of Calanus helgolandicus were probably growth would be gained from the tissues of formed directly from triglyceride esters of their algal squid, fish and other prey that are normally foods. Sargent et at.. (1974) also demonstrated the fed with the oil. However, not only the chicks synthesis of wax esters by the copepod Euchaeta must fast; so too must many adults like breed- norveglca. ing Puffinwi tenuirostris during their 12-day The other major components found in stomach stints on their egg. Many pelagic petrels also oils are less widespread in the marine environment. appear to fast at sea where their foods are Glyceryl ether diesters, found in four species of patchily distributed. Thus both when at sea and petrels (Table 1) occur also in squid, anchovies, ashore the availability of a rich energy store chimaeras, elasmobranchs, penaid and would have great survival value. pteropods (Lewis, 1966; Lee, 1974). Pristane is a Ashmole and Ashmole (1967), who also post- prominent hydrocarbon in copepods which are near ulated that the oil was an energy source, pointed the base of food webs and it occurs particularJy in out that the excretion of water from the P.rey marine herbivores (Ackman et aI., 1970). This sub~ and the concentration of the lipids as stomach stance probably originates from phytol in chloro- oil would reduce energy expenditure by the plasts of phytoplankton and is also found in the liver parent birds during long flights back to the oils of sharks and whales (Blumer et at.. 1963). nesting grounds from the feeding places. Squalene is an intermediate in the biosynthesis of There is little direct evidence that the oils are cholesterol. It occurs in shark liver oils (Lewis, 1969b) assimilable in the birds, but there is some and is used by some deep sea elasmobranchs as a indirect evidence. For example, in highly buoyancy agent (Comer et al.. 1969.) migratory species like P. tenuirostris, the oil content falls as the chicks approach fledging FUNCTIONS OF PETREL STOMACH OILS time (Serventy et aI., 1971). This is certainly These oils probably serve a variety of functions, not due to excretion of the oil, as the ejection but few of the following possibilities have been con- of large amounts in burrows or elsewhere firmed by field or laboratory experiment, so that could not be overlooked. The oil evidently can these ideas must be regarded as tentative. be metabolised in man and in rats and has 1. It seems likely that the primary function of the been broken down experimentally with marn~ oil is to act as an energy reserve. This was the malian lipases (Carter and Malcolm, 1927; initial hypothesis when the present investigation Gunstone and Sealey, 1964). Reptiles too can was started: it appeared improbable that birds probably digest the oil: Fleming (1939) des- capabJe of laying, at most, one egg annually, cribed how skinks (Lygosoma dendyi) drank had access to so much food that they could be from pools of oil ejected by Diomedea cauta wasting what was clearly a hi.gh-energy resource chicks. -the material burnt. Lipid releases more heat 2. As a water source, particularly for land-based per unit mass than either protein or carbohy- chicks which can normally only get water from drate and bomb caJodmetry has confirmed the their food. Combustion of the oil to carbon high energy contents. Thirty~one samples from dioxide and water could provide heat and 11 species had a mean calorific value with one water for growth and maintenance during their standard deviation of 9646 + 266 ca1s1g long fasts between meats. This function was (Warham et at., 1976). This is slightly below first proposed by KritzIer (1948) in the course the value for commercial diesel oil. I calculated of his work on oaptive F. glacialis. WARHAM: INCIDENCE, FUNCnONS AND ECOLOGICAL SIGNIFICANCE OF PETREL STOMACH OILS 89

Petrel chicks must need more water than other Young petrels may discharge oil many days after chicks of comparable size as their growth fates their last meal. Murphy (1936) gave several instances. are low, nestling periods ranging from 47 days Warham (1956) recorded a nestling Ptel'odroma in small species to 278 days in giant albatrosses; macroptera that had not been fed for 6 days spitting the chicks' uncontrolled water losses will be oil, while a chick of Macronectes giganteus spat 14 correspondingly high. days after its last meal (Warham, 1962). 3. As a device to help retard digestion. In labor~ In young Fulmams gladalis, the oil~spitting ability atory experiments it was found that the oils is well developed by the time the chick ~s large had a significant preservative power for enough to be left nattended in the nest, freeing both crustacea. Thus it seems possible that in the parents to forage for food. In this species spitting presence of stomach oil the digestion of food is has been stated to occur even from a chick not com- slowed down. Such a facility would be beneficial pletely free from the egg (Lees, 1950). The suggestion for pelagic species dependent on patchy food by Clarke and Prince (1976) that this chick was sources and allow the birds to metabolise both actuaUy spitting bile, seems Ji.kely, as more recent food and oil slowly so that energy and nutrients data suggests that several days elapse after hatching were made available over an extended period before oil spitting behaviour appears. Williamson instead of being rapidly consumed. Slow (1965) never saw vomiting by the very many young assimilation of lipids would also help to explain and hatching F. gladalis he handled, nor did the writer the ability of chicks to discharge oil many days when weighing many hatching and new~born after they have been fed. Macronectes gigantew,' and M. halli chicks, which are Clearly these ,rhree roles could be complementary notorious spitters. Conroy (1972) found that the and they suggest interesting parallels with the ecolog- young M. giganteus first spat oil at 6 days old. ical roles of lipid stores in the planktonic crustacea The adult F. gladalis is one of the most proficient already mentioned. Significantly, Pelecanoides at repelling aggressors or potential competitors by urinatrix. the common , which is a spitting oil. I have seeD this bird displace a kittiwake coastal bird and feeds its chicks daily, is the only (Rissa tridactyla) from a nesting ledge and Fisher petrel not known to contain oil either as chick or as (1952) Tefers to a young herring (Lams argentat- adult. us) being drenched with oil by a sitting fulmar. Murdo The defensive/offensive role for stomach oil seems A. Macdonald (pers. comm.) saw northern fulmars to be a secondary development from the widespread spitting at jackdaws (Corvus monedula), one of which habit among frightened of ejecting their became drenched, its feathers matted and their stomach contents to lighten their bodies for escape insulation evidently destroyed. He has also noted that (Matthews, 1964). Qil ejection is used almost exclus- these petrels may spit at alien conspecmcs, but such ively by surface~nesting species, notably by fulmars reports are few. Brown (1966) described fighting of the genera Fulmarus. Daption, Thalassoica, between male Pagodroma nivea in which stomach oil Pagodroma and Macronectes. and also by chicks of was forcefully ejected during disputes over partners Diomedea and Phoebetria albatrosses. Fulmars can or nest-sites. The combatants' white plumage was squirt oil with some accuracy for one or two metres. stained orange and to clean the feathers the birds They can make several discharges before the supply resorted to "bathing" jn dry snow or pushed their is exhausted, the first consisting of the lighter oil bills into the snow and vigorously rotated their heads and subsequent ones containing an increasing propor~ from side to side. Pinder (1966) noted that breeding tion of food material, evidently representing the Daption capense occasionally ejected oil at intruders evacuation of the lower part of the proventriculus. which landed at or approached their nests, but that Most chicks have less control and tend to this appeared to be a last line of defence. splatter the oil in the general direction of the stimulus, Until recently it had been thought that the effects A few burrowing gadfly petrels like Pterodroma of contamination by stomach oil were minor and macroptera, Pt. lessoni and Pt. inexpectata and at temporary, though probably effective in deterring least one shearwater (Procellaria aequinoctialis) may many natural predators. Recent evidence from free- also discharge small quantities of oil, but usually living and captive birds shows that oil-spitting caD quite ineffectively (Warham. 1956; 1967 and be a formidable weapon. Substantial contamination unpublished). The defensive discharge of oil is made may lead to death due to matting of the victim's through the mouth, not through the nostrils, as stated feathers leading to Joss of flying ability and of water by some early authors. However. live storm petrels repellancy. often allow oil to dribble from their nostrils when The deadly effect of oil contamination was held in the hand. dramatically illustrated by the fate of a fledgling 90 PROCEEDINGS OF THE NEW ZEALAND EcOLOGICAL SOCIETY, VOL. 24, 1977

white-tailed sea eagle (Hallaetlls a,bicilia) re-.intro~ ism must be operating with petrels-perhaps a ouceo to raJr ISlaoo, Scotlano (Dennis, 1~::f/0).Tnese difference in feather structure. Further study is eagles IOcluoe nonnern !UJmars 10 tneH prey but one clearly needed. or IDe eagle hcaghngs, altnougn well teo, was lOuna The readiness of F. glacialis to eject oil suggests Wltn ils plUmage mattegulls, not confer total immunity. Despite their dangerous eveD a few passerines) are believed or known to have armoury, surface-nesting petrels and their chicks been killed as a result of stomach Oil contamination are eaten by a variety of natural enemies. For (Dennis, 1970; Broad, 1974; Booth, 1976). At ralf example, chicks of Daption capense and of Isle, c1I1ts are the main resting places for migrant Macronectes gigantew.' are killed and eaten by birds, but these are also heavily populated by fulmars southern (Catharacta ) (Pinder, 1966). Even and it seems that many of the victims blundered into northern fulmars are eaten by bald, white-tailed and the petrels' indiviaual distances and hence were golden eagles (lfaliaetus leucocephalus. If. albiciila repelled by oil: the passerines may perhaps have and Aquila chrysaetos), by the falcons Falco pere~ been caught in cross-fire! grinus and F. ru.~.ticolusand by the fox Vulpes fulva Confirmation of the potential danger of o~l (Fisher, 1952; Hawker, 1975). Large gulls also get contamination was given by Swennen (1974) who some fulmar chicks. The falcons, striking on the kept a single F. glaciaiis (fed on thawed deep~frozen wing, would be expected to take fulmars with fish) in captivity with gulls and auks. The fulmar impunity, but even peregrines seem to fall victim killed 5 of its cage mates merely by spitting oil at times (Clarke, 1977). during aggressive attacks. Deaths resulted from chilling and/or drowning. Vigorous bathing by the "MUMIYO" soiled birds failed to restore feather structure whereas Snow petrels use oil~spitting to good effect in the fulmar appeared to be able to remove any self. deterring predatory skuas and during intra-specific contamination by bathing and preening. conflicts over nest sites. In the cold climate the spilled Mammals are also attacked. The oils seem in no oil, usually mixed with the excreta of the chicks, way harmful to man, have no burning action on the sets as hard as stone and accumulates around the skin, but rabbits soaked with oil have been found nesting places as these are used year after year. Up dead where nesting northern fulmars were taking to 9 kg of this frozen oil has been recovered in a over rabbit-burrowed ground at the top of a cliff single lump. (Fisher, 1952). Shetland crofters are currently Geologists examining this material determined its experiencing financial losses due to their sheep being biological nature and thought that it was formed soiled with fulmar oil. The sheep remain healthy but from the petrel's excreta (Ardus, 1964; Jones and their fleeces are unsaleable owing to matting by the Walker, 1964), but Winsnes (1969) realised that it oil to which heather, grass and other debris adhere was mainly stomach oiL Meanwhile Russian scientists (Robertson, 1975). had noted the Antarctic material's similarity to I have only one report of an encounter between a "mumiyo", a deposit of biological origin found in cat and an oil-spitting petrel. Knowles Kerry (pers. rocks in Iran, India and China. The infra-red and comm.) saw a nestling Phaebetria palpebrata discharge uLtraviolet spectra of "mumiyo" and the Antarotic oil at a feral cat at Macquarie Island. As the oil deposits were similar (Korotkevich et ai., 1967). Some struck, the cat leapt out of the way and rolled over samples of "mumiyo" are also known to contain frantically on the grass as if trying to remove the waxes (poroshin et. at. 1964). contamination. If this reaction is typical, it is unfort- "Mumiyo" has been known from antiquity, was unate that the chicks of burrowing species are unable described by Avicenna and others, and is still believed to spit oil, for it is these that suffer the greatest to be a valuable aid in mending broken bones in losses from by introduced cats. some circles of oriental medicine. One obvious problem that arises from the discovery There seems no doubt as to the origin of Antarctic of the deadly results of oil contamination is how "mumiyo", but that of the Asian substance is so far the petrels themseJves achieve immunity. They appear undetermined. It seems rather unlikely that it will to eliminate soiling by bathing in water or snow but prove to be fossilised stomach oil but if so would as this fails with other seabirds, some special mechan- reflect nesting sites along the shores of some former WARHAM: INCIDENCE, FUNCTIONS AND ECOLOGICAL SIGNIFICANCE OF PETREL STOMACH OILS 91

coastline, perhaps that of the Tethys Sea. However, that phospholipids are absorbed here (particularly even if Asian "mumiyo" proves to have a single the 20: 5 and 22: 6 polyunsaturated fatty acid com- origin and from animal ratner than plant material, ponents) with the help of an acid phospholipase, has there are possible sources: of fossH oils and waxes already been mentioned. Clarke and Prince (1976) other .than petrels. For example, at Bute Inlet, British noted that while oil from an adult D. melanophris Columbia, copious submarine deposits of wax have was rich in wax esters, that from four chicks con- been found. Analyses suggest that these may be a sisted mainly of triglyceride with some free fatty consequence of massive kills of Co/anus sp. through acid. They suggested that this might indicate some unknown causes (Benson et 01., 1972). Conceivably digestion in the proventriculus. However, the con- such deposits could be preserved under appropriate tents of the proventriculus seem to be highly acid, conditions to form "mumiyo". and this in an unlikely environment for normal lipase activity which needs alkaline or neutral con- FURTHER WORK ditions. Nor is there any special route for pancreatic Although the origins of the oils seem clearly or bile secretions to reach the proventriculus, established, many unresolved problems remain con- although the last discharges of oil tend to be green in cerning functions and particularly concerning the colour suggesting that bile can be regurgitated. An metabolic pathways involved in the birds' processing ability to transform wax esters into triglycerides in of the oils. Do the chicks manufacture it? How much the proventriculus, with or without absorption there, of the energy actually available is used? How is the would provide yet another source of variability in combustion of the stomach oils and the depot fats the ratios of these compounds jn oils from different controlled? Is there any re-incorporation into protein conspecifics. which Lee (1974) suggested as a role for the wax Imber (1976) also speculates as to whether petrel esters from the copepods eaten by the ctenophore stomachs can preferentially utilise triglycerides duri,ng Pleurobrachia and by arrow worms of the fasting periods as in the crustacea experiments of Sagitta? Lee et al., (1971), so that the wax ester moities The course of digestion in petrels seems unknown. increase propOrrtionately in the course of digestion. Presumably the fragile oil-sacs of small crustacea On the other hand, if food and lipids are all mainly would be ruptured in the proventriculus as happens absorbed in the intestine, then the functions of the with calanoids which, when netted, release quantities copious proventricular glands remain in question. of oil into the water. Cheah and Hansen (l970a) Even if absorption of phospholipids from food occurs considered that the oil accumulated in the petrel there, phosphoHpid is not a significant constituent because protein was digested more rapidly than lipid, of the oils, and the glands, which in some species but if so, how is the protein moiety able to pass into are known to have different forms when the lumen the gizzard and intestine leaving the low viscosity is full than when it is empty, seem too numerous and oil behind? This may be aided by the operation of specialised merely to be producing gastrin and the pyloric valve and by the unusual arrangement in absorbing phospholipid. which the duodenum ascends from the gizzard The ability of proventricular epithelium to break before looping around the pancreas: this will help down or absorb stomach oi.Js could be tested in to stop the oil draining down to the intestine. Also, vitro. This was attempted by Cheah and Hansen being heavier, the food tends to lie at the bottom of (I970b) who found some evidence of lipase activity the proventriculus and hence will be the first to pass in P. pacificus but only between pH 6.5 and 9.0. into the gizzard. They concluded that under the acid conditions Or is protein absorbed in the proventriculus obtaining in the proventriculus there could have itself? However, it is customary to consider that been little effective lipolysis. Additional in vitro work chemical digestion in birds occurs in the small seems to be required together with some in vivo intestine. In some species the proventriculus has been experiments using radioctively-Iabelled oil, and, in shown to be the site of acid gastrin production. This view of the absence of oi.l in Pelecanoides, a compar- begins the breakdown of proteins which is completed ative examination of the morphology and metabolic further along the intestinal tract. In the small intesti.ne activity of the proventricular epithelia of that petrel bile and bile salts emulsify fats while pancreatic and and others could prove rewarding. mucosal secretions help neutralise the acid chyme and One possible approach for following the progress allow lipases, carbohydrases and proteinases to work. of digestion in the proventriculus would he to analyse Another possibility is that protein and carbohy- samples of oil extracted at regular intervals from a drate are absorbed intestinally while lipids are taken fasting adult or chick, perhaps using the pipette up by the proventricu1ar epithelium. Watts' sugestion technique of Grubb (1971), and look for changes in 92 PROCEEDINGS OF THE NEW ZEALAND EcOLOGICAL SOCIETY, VOL. 24, 1977 the proportions of wax esters to triglycerictes with BLUMER, M.; MULLIN, M.; THOMAS,D. W. 1963. Pristane time. in zooplankton. Science 140: 974. Yet another problem concerns the mechanisms for BOGAN,J. A.; BOURNE,W. R. P. 1972. Organochlorine breaking down waxes. These are usually regarded as levels in Atlantic seabirds. Nature 240: 3.58. highly indigestible and in only one other bird group, BOOTH,C. 1. 1976. Peregrine and Raven possibly con- taminated by Fulmar oiL British Birds 69: 61. the passerine honey-guides Fam. Indicatoridae, is BOTTINO,N. R. 1975. Lipid composition of two species ceratophagy normal. Wax digestion in these birds is of Antarctic : Euphausia superba and E. believed to be achieved through the lipolytic activity crystallorophias. Comparative Biochemistry and of an intestinal microflora (Friedmann and Kern, Phy!,iology SOB: 479-484. 1956). B;{OAD,R. A. 1974. Contamination of birds with fulmar CONCLUSION oiL British Birds 67: 297-301. The appearance of stomach oil in petrels may BROWN, D. A. 1966. Breeding biology of the Snow result from the slow digestion of an unusual food Pelrel Pagodroma nivea (Forster). Australian which the birds have learned to use with difficulty National Antarctic Research Expeditions Scientific Reports Series B( 1) Zoulogy, No. 89: 63 p. but which confers significant advantages in providing CARTER, C. L.; MALCOLM,J. 1927. Observation on the an energy and water reserve, food and water for biochemistry of "Mutton Bird Oil". Biochemical chicks and an offensive/defensive weapon. Journal 21: 484-493. Storage and use of stomach oil appears to be CHEAH, C. c.; HANSEN, I. A. 1970a. Wax esters in the another adaptation that helps proceUaciiform birds stomach oils of petrels. International Journal of to exploit pelagic foods which are patchily distributed Biochemistry 1: 198-202. and which involve parents in long journeys to find CHEAH, C. C.; HANSEN, I. A. 1970b. Stomach oil and food and both parents and chicks in substantial tissue lipids of the petrels PufJinus pacificus and fasts. Utilisation of stomach oil as energy and Pterodroma macroptera. International Journal of water sources complement other energy~saving Biochemistry 1: 203~208. adaptations that fit petrels for this Hfestyle, such as CLARKE, A. 1977. Contamination of peregrine falcons their low body temperatures (which presuppose low (Falco peregrinus) with fulmar stomach oiL Journal of Zoology. London. 181: 1I~20. basic metabolic rates), and the ability of many species CLARKE,A.; PRINCE, P. A. 1976. The origin of stomach to travel by dynamic soaring. oil in marine birds: analysis of the stomach oil from ACKNOWLEDGEMENTS six species of procellariiform birds. Journal of Experimental Marine Biology and J am grateful to Dr Knowles Kerry and Mr Murdo Ecology 23: 15~30. Macdonald for field observations, to Mr B. S. Simmonds CONROY,J. W. H. 1972. Ecological aspects of the biology for mutton-bird harvesting figures and to Mr A. K. of the Macronectes giganteus (Gmefin), Lojkine for translating Russian literature. Des W. R. P. in the maritime Antarctic. 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