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

THE INCIDENCE, FUNCTIONS AND ECOLOGICAL

SIGNIFICANCE OF PETREL 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 tosea~birds of the order Procellariifonnes is reviewed. The sources of these oils, most of whichcontain mainly wax esters and/or trigIycerides, is discussed in relation to the presence of suchcompounds in the marine environment. A number of functions are proposed as the ecologicalroles of the oils, including their use as slowIy~mobilisable energy and water reserves for adultsand chicks and as defensive weaponry for surface-nesting species. Suggestions are made forfurther research, particularly into physiological and nutritional aspects.

INTRODUCTION

Birds of the Order Procellariiforrnes (albatrosses,fuJmars, shearwaters and other petrels) are peculiarin being able to store oil in their large, glandular and

very distensible fore-guts or proventriculi.. All petrelspedes so far examined, with the significant excep-tion of the diving petrels, Fam. Pelecanoididae, havebeen found to contain oil at various times. The oi.1occurs in both adults and chicks, in breeders andnon~breeders, and in birds taken at sea and on land.The oil is a light (specific gravity 0.88), low viscosityfluid, often solidifying to a wax in cool conditions,with a sweet, slightly fishy smell. It may be colour-less or straw-coloured, but it is often darker - fromamber to a deep reddish-brown. The colour isneither constant nor species-specific. For example,that from the cape petrel (Daption capense) is brightorange before egg laying but becomes duller duringthe birds 4 to 6 day incubation stints and at the endof these is normally dull green (Pinder, 1966). Thisgreen tinge is common also in oil samples collectedfrom fasting adult petrels and may be due to thepresence of bile pigments.Many surface-nesting petrels spit oil in defense or

offense, but copious amounts are often found in thechicks of burrowing species and these seldom spitoil. Northern fulmar (Fulmarus f?/aciaUs) chicks at StKilda yielded about 280 ml of oil each; sooty shear-water (PufJinus f?dseus) chicks may contain 120 ml,while Murphy (1936) reports 200 mI of oil beingtaken from a short~tailed shearwater (PufJinus tenui-rostris) chick: this would amount to about 30% ofthe adult's body mass.Petrel oil has been used medicinally, as a lubricant

and as an iItuminant. The northern fulmar was amainstay of the St Kildans' economy, supplying "oilfor their lamps, down for their beds, a delicacy for

their table, a balm for their wounds, and a medicinefor their distempers." In New Zealand, Travers andTravers (1873) described how the Chatham IslandMorioris held young petrels over their mouths andallowed the oil to drain directly into them. In someyears the St Kildans exported part of thei.r oil har~vest, as the Australian mutton-birders stilI do withoil from the chicks of P. tenuirostris. This has beenused as a basis for sun~tan lotions, but most nowa-days ;.<;used as a food stock supplement: a small

quantity is said to impart a shiny coat to horses. Some2796 gallons (12711 n were sold after the] 976 seasonas a by product of the! harvesting of 549352 squabs(B. S. Simmonds, pers. comm.). It is also possiblethat fossil stomach oil has been used medicinally inthe east for thousands of years.A surgeon, John Scouler (1826), was among the

first in modern times to discuss stomach oil frompersonal experience. He wrote of Daption capen.se,caught off Patagonia, which "never failed to vomit aconsiderable quantity of yellowish oily fluid on hisenemy, and on dissection the source of this supply iseasi,ly detected. The first stomach is large and mem-branous and thickly set with numerous glandularfollicles, which appear to be the organs which secretethis oily fluid, the only defensive weapon this animalpossesses."A number of papers describing aspects of the bio~

chemistry of petrel oi,ls appeared in the 1920's and1930's, but the analyses were incomplete by modernstandards. The investigators seem to have knownlittle of the birds in life and so made erroneousdeductions such as that of Otago chemists Carterand Malcolm (1927) who concluded that mutton-bird oil was ingested preen gland secretion. Tn someaccounts the species from which the oil was drawnwere misidentified e.g~ oil from the Australian and

Species WE TG Ch DAG S Authority

DioffiedeidaeDiomedea epomophora X X X Warham et al., 1976D. exulans X x x Lewis, 1969aD. melanophris x X Warham et al., 1976;

Clarke & Prince, 1976D, chrysostoma x X Clarke & Prince, 1976D. bulleri X Warham et al., 1976Phoebe tria palpebrata X Warham et al., 1976

ProcellariidaeMacronectes giganteus X X Clarke & Prince, 1976M.halli X X Warham et aI., 1976;

Clarke & Prince, 1976Fulmarus glacialis X x Cheah &Hansen, 1970a;

Warham et al., 1976Dap/ion capense X x Warham et al., 1976Pagodroma nivea X Warham et aI., 1976Pterodroma macroptera X Cheah & Hansen, 1970bPt. lessoni X Warham e/ al., 1976

Pt. inexpectata X X Warham et al., 1976Pt. mol/is X x x X Warham e/ al., 1976Halobaena caerulea X x Clarke & Prince, 1976Pachyptila desolata X x Clarke & Prince, 1976Proal/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, 1969aP. pacijicus X X Cheah & Hansen, 1970b

HydrobatidaeHydrobates pelagicus X Warham et al., 1976

Oceanodroma leucorhoa x X Lewis, 1966

W AlHHM' fNrmf:Nrf: FUNCfIONS AND EcOLOGICAL SIGNIFICANCEOF PETREL STOMACH OILS 85

New Zealand mutton-birds (P. tenuirostris and P.griseus) was attributed to a quite different petrelPterodroma lessoni (Serventy, Serventy and Warham,1971).

In the early 1960's this writer circulated a reviewof current knowledge about petrel stomach oilsamong procellariiformists asking for samples of oilso that analyses using modern techniques could berun to establish, a. whether the oils were of similarcomposition and therefore probably of a secretorynature, or b. of varied composit~on and thereforemore likely to be food-derived. These analyses haverecently been published (Warham, Watts and Dainty,1976; Watts and Warham, 1976) and with compar-able analyses by other workers they provide inform-ation on oils from 25 petrels, There are about 100species in the order.

COMPOSITIONS

The main components of the oil samples so faranalysed (by thin-layer and gas-liquid chroma-tography and infra-red spectroscopy) are summarisedin Table 1.In 24 of the species-samples either triglycerides or

wax esters predominated. Many samples containedboth. In a few oils there were no wax esters, in othersno triglycerides. Oil from one species. Oceanodromaleucorhoa, had neither: instead, large quantities ofglycerylether diesters were found. These were alsopresent in oils from Pterodroma mallis, Puffinuscarneipes and Procellaria aequinoctialis but insmaller proportions and only in association with waxester or triglyceride.In addition to the components shown in the table,

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.)

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

glycerides and cholesterol, some free fatty acid andalcohols. However, one of two samples of oil fromPuffin us pacificus contained substantial proportionsof cholesterol (43 % by weight), one from Pterodroma

macl'optera 30% of cholesterol ester, whUe oils fromDaption capense and Procellaria aequinoctialis con-tained 23-43% of long chain alcohols.

ORIGINS

Tne origin of these oils has been the subject ofsome dISCUSSIonsmce Scouler and later anatomistsdrew altention to the copious glands in the petrelproventncuJUs. One school believed that the lipidswere fooo residues, even excretory products, of birdswith an excess of fat in their diet; another that theoils were internal secretions of the proventricularglands. Harrison Matthews (1949) examined stainedsections of proventri.cular epithelia and concludedthat the glands were probably secreting lipid into thelumen of the stomach.However, the intra~cellular fat that Matthews

observed stained wi.th Sudan Black but not withSudan III or IV. and as Sudan stains pick out allneutral lipids whereas only Sudan Black stainsphospholipids, it seems likely that the lipid Matthewsdetected was dietary phospholipid being taken upwith the aid of an acid phospholipase (Watts, pers.cornm.). There is very little phospholipid in thestomach oils so far examined. though a good deal inpotential prey organisms.All the analyses indicate that the oUs are derived

from the petrels' diets, for the following reasons:-

1. The intra-specific variations in the compositionsof the oils are far greater than would beexpected of a secretion, such as that of theproventriculus. For example, Clarke and Prince(1976) analysed the individual oils from 35adult Halobaena cael'u/ea and found a widerange in the proportions of the main constit~uents. The wax esters had a mean value withone standard deviation of 68.9 + 21.7% oftotal lipid, while the triglycerides at 12.1 :t10.8 % were even more variable. SimilarlyLewis (1966) found that the glycerylethercontents of oils from four adult O. leucorhoavaried between 20% and 84% of the total lipid.

2. The inter-specific variations in the compositionsis even greater (Table 1) and there seems to beno correlation between composition and tax~onomic status. For example, two of the oils ofthe six albatrosses contained mostly triglyceride,two others mainly triglyceride with lesseramounts of wax ester, one contained aboutequal proportions of tri-glyceride, wax ester andsqualene while in the sixth wax ester predomin-

ated and there were smaller amounts oftriglyceride and squalene.

3. The constJ.tuents of the petrel oils show strongsimilarities to those of oils from crustacea,squid and fish either eaten by petrels or relatedto known foods of petrels. This also includesthe hydrocarbons pristane and squalene: thelatter could originate from shark's flesh or livereaten by scavenging albatrosses, pristane fromcopepods and planktonic herbivores lowerdown in the food chain.An example of the correspondence in lipid

constitutions is given by the fatty acid andalcohol components of the wax esters and thefatty acids of the triglycerides from marineanimals and petrel stomach oils. Both show apreponderance of 16:0, 16: 1,18: 1,20: 1,20:5and 22: 6 carbon chain compounds. Oil fromDaption capense, however. was unique in lack-ing 14: 0 or 16: 0 a1cohols in its wax esters.This suggests that there is something specialabout this petrel's foods, at least around theSnares Islands where the birds were sampled.Imber (1976), who also believes in the

dietary origin of stomach oils, emphasises thatmany petrels feeding at night take verticallymigrating mesopelagic crustacea, fish and squidwhose lipids contain much wax ester. He alsodraws attention to the similarity between thecephalopod diet of the albatrosses Diomedeaexu/ans and D. epomophora and that of thesperm whale Physeter catodon. The whale'stissues are rich in wax esters as are theircephalopod prey. So too are the birds' stomachoils (Table I).

4. The pigments of the oils are the same as naturallipid-soluble pigments in marine invertebrates.Thus carotenoid astaxanthins in oil from alba~trosses. giant petrels and prions resemble thosefrom decapods and euphausids (Lewis, 1969a;Clarke and Prince, 1976). One exception con-cerns the pigments of P. tenuirostris oil whichwere different fwm those of the euphausidNyctophanes australis which forms this bird'smain pTey (Cheah and Hansen, 1970a).

5. In the only analysis of organochlorine com-pounds in stomach oils so far published, Boganand Bourne (1972) found that F. glacialis oilcontained only 1.3 p.p.m. of polychlorinatedbiphenyls in contrast to 42 p.p.m. in the bird'sbody fat. The adults evidently did not pass onthe high levels of PCB's to their young whenthey fed them oil and Dr Bourne (pers. comm.)points out that the oil's low PCB values providefurther 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-centration of organochlorines would have beenexpected to occur, as in the fat.

6. Watts and Warham (1976) found that the intactlipids of the oils consist of randomly associatedfatty alcohols and/ or acids. These authors pointout that this is what would be expected in oilsof dietary origin, whereas with lipids synthe-sised by glands, e.g. mammalian mammaryglands or liver, there are specific associationsbetween particular fatty alcohols and/or fattyacids.

7. Variations in the compositions of oils fromdifferent members of the same petrel speciesare readily explained by mixed diets. Further-more, even if the birds fed on the same prey,differences in the resulting stomach oils wouldbe expected because the lipids of particularprey species are not of constant compositionbut may change during the annual cycle orwith alterations of water temperature, so thattheir wax ester/triglyceride ratios vary in timeand space.

WAX EsTERS, TRIGLYCERIDES, GLYCERYL ETHERS,

PRISTANE AND SQUALENE IN THE MARINE

ENVIRONMENT

Both wax esters and triglycerides are found insmall to large amounts in many organisms whi.ch areeaten or likely to be eaten directly or indirectly, bypetrels. For example, wax ester in the copepodCalanus helgolandicus composed 30-40% of totallipid; in mullet eggs 70%, and in Latimeria muscle93 % (Nevenzel, 1970). Whale blubber contains50~80% wax ester, the remainder of the lipid beingtriglyceride. Some copepods contain up to 40% dryweight of triglyceride and others up to 50% dryweight of wax ester (Lee et al., 1971). Spermaceti ismainly wax ester and this, and the mutton-bird oilsreferred to earlier, appear to he the only wax estersof animal origin sold commercially. One squid had27 % of its lipid as wax ester, 6 % as triglyceride(Benson et aI., 1972). Triglyceride was the principallipid in zooplanktonic ostracods, pteropods,euphausids, amphipods and decapods collected in theStrait of Georgia, British Columbia (Lee. 1974).Most marine animals so far analysed contain both

wax ester and triglyceride, but with much inter-specific variation in their proportions. Theseproportions may also be dramatically different in thesame species at different times. Thus the eggs andearly nauplii. of Calanus helgolandicus have 60 %triglyceride in their lipid reserve but no wax ester,whereas the eggs are laid by adults containing largelywax ester (Benson et al., 1972).

The quantities of lipid and the proportions of waxester to triglyceride may not only vary with age andbreeding status, but also with the animal's stage ofstarvation and with environmental factors. Polar anddeep sea copepods tend to be rich in wax esterwhereas those of sub-tropical seas are high intriglyceride (Lee et ai., 1971). The crustaceant.uphausia superba lacks waxes but contains substan-

tial quantities of triglycerides, whereas E. crystallor-ophias, which lives in colder water near or under thepack ice, lacks triglycerides but contains significantlevels of wax esters (Bottino, 1975).An important function of both wax esters and

triglycerides in marine organisms is in energy meta-bolism (Nevenzel, 1970; Ackman et aI., 1970; Bensonel ai., 1972). Also marine species, like arid zone landanimals, tend to use lipid metabolism for the produc-tion of water. Copepods have been dubbed "camelsof the sea" for this reason and polar species of cope~pods store great amounrs of wax during the shortsummer and draw on this reserve to fuel moulting,mating and egg production during the dark part ofthe yea,r (Benson et a/" 1972; Sargent, 1976.) Theseanimals can use up their stores at controlled rates dueto the actions of wax ester and triglyceride lipases.Trigly!cerides form the usual energy reserves indiatoms, dinoflagellates, teleosts and many pelagiccrustacea (Benson et aI., 1972).Starvation experiments have shown how these

reserves may help marine animals to withstand badfeeding conditions. Lee (1974) starved four speciesof copepod for a month with little mortality occurr-ing. The triglycerides were first utilised and onlywhen these were nearly or completely exhausted werethe wax esters slowly consumed. The ability to wi.th-stand long periods of starvation is also pronouncedin deep sea copepods and has been interpreted in thelight of their uncertain food supply (Benson et al.,1972).Large amouts of wax esters also occur in deep

living fish (Nevenzel, 1970; Lee et aI., 1971), evidentlyderived from deep water copepods. These latterauthors pointed out that for carnivorous speciesoccupying regions where the standing stock of foodis low, it would be advantageous to have an efficientdigestive system, a low average metabolic rate andlarge energy reserves. Wax esters would supply thelatter. Benson et. aI., (1972) suggested that at least halfof the earth's photosynthesis production is stored. fora time, as wax.Petrels readily feed on fat and oil released onto

the sea during whaling, sealing and fishing operations.Indeed fat has long been used as a lure for petrels.In the open oceans, oil slicks also occur naturally,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 probablyresulted from a massive mortality of Calanus species.Such slicks may provide yet another source of petrolstomach oil.According to Nevenzel (1970), the wax esters in

most marine species result from biosynthesis in theanimal itself. He referred to experimental work withelasmobranchs and lantern fishes and suggested aroute for the synthesis and breakdown of wax estersfrom and to fatty acids and alcohols. This schemealso allows for the transformation of wax ester toand from triglyceride via fatty acid intermediates.Benson et al.. (1972) thought that the unsaturated

wax esters of Calanus helgolandicus were probablyformed directly from triglyceride esters of their algalfoods. Sargent et at.. (1974) also demonstrated thesynthesis of wax esters by the copepod Euchaetanorveglca.The other major components found in stomach

oils are less widespread in the marine environment.Glyceryl ether diesters, found in four species ofpetrels (Table 1) occur also in squid, anchovies,chimaeras, elasmobranchs, penaid shrimps andpteropods (Lewis, 1966; Lee, 1974). Pristane is aprominent hydrocarbon in copepods which are nearthe base of food webs and it occurs particularJy inmarine herbivores (Ackman et aI., 1970). This sub~stance probably originates from phytol in chloro-plasts of phytoplankton and is also found in the liveroils of sharks and whales (Blumer et at.. 1963).

Squalene is an intermediate in the biosynthesis ofcholesterol. It occurs in shark liver oils (Lewis, 1969b)and is used by some deep sea elasmobranchs as abuoyancy agent (Comer et al.. 1969.)

that the stomach oil contains from 5 to 35times the energy content of the prey at the timeof capture.In this role the oH would supplement the

more conventional energy reserves of sub-dermal and visceral fat that are laid down bypetrels and other sea-birds and which are alsodrawn on during fasts.The oil is certainly fed to the chicks and as

these may have to go for days without meals,despite exposure to inclement weather, theability to draw on a high energy resource wouldhave obvious value. The protein needed forgrowth would be gained from the tissues ofsquid, fish and other prey that are normallyfed with the oil. However, not only the chicksmust fast; so too must many adults like breed-ing Puffinwi tenuirostris during their 12-daystints on their egg. Many pelagic petrels alsoappear to fast at sea where their foods arepatchily distributed. Thus both when at sea andashore the availability of a rich energy storewould have great survival value.Ashmole and Ashmole (1967), who also post-

ulated that the oil was an energy source, pointedout that the excretion of water from the P.reyand the concentration of the lipids as stomachoil would reduce energy expenditure by theparent birds during long flights back to thenesting grounds from the feeding places.There is little direct evidence that the oils are

assimilable in the birds, but there is someindirect evidence. For example, in highlymigratory species like P. tenuirostris, the oilcontent falls as the chicks approach fledgingtime (Serventy et aI., 1971). This is certainlynot due to excretion of the oil, as the ejectionof large amounts in burrows or elsewherecould not be overlooked. The oil evidently canbe metabolised in man and in rats and hasbeen broken down experimentally with marn~malian lipases (Carter and Malcolm, 1927;Gunstone and Sealey, 1964). Reptiles too canprobably digest the oil: Fleming (1939) des-cribed how skinks (Lygosoma dendyi) drankfrom pools of oil ejected by Diomedea cautachicks.

2. As a water source, particularly for land-basedchicks which can normally only get water fromtheir food. Combustion of the oil to carbondioxide and water could provide heat andwater for growth and maintenance during theirlong fasts between meats. This function wasfirst proposed by KritzIer (1948) in the courseof his work on oaptive fulmars F. glacialis.

FUNCTIONS OF PETREL STOMACH OILS

These oils probably serve a variety of functions,but few of the following possibilities have been con-firmed by field or laboratory experiment, so thatthese ideas must be regarded as tentative.

1. It seems likely that the primary function of theoil is to act as an energy reserve. This was theinitial hypothesis when the present investigationwas started: it appeared improbable that birdscapabJe of laying, at most, one egg annually,had access to so much food that they could bewasting what was clearly a hi.gh-energy resource-the material burnt. Lipid releases more heatper unit mass than either protein or carbohy-drate and bomb caJodmetry has confirmed thehigh energy contents. Thirty~one samples from11 species had a mean calorific value with onestandard deviation of 9646 + 266 ca1s1g(Warham et at., 1976). This is slightly belowthe value for commercial diesel oil. I calculated

WARHAM: INCIDENCE, FUNCnONS AND ECOLOGICAL SIGNIFICANCE OF PETREL STOMACH OILS 89

Petrel chicks must need more water than otherchicks of comparable size as their growth fatesare low, nestling periods ranging from 47 daysin small species to 278 days in giant albatrosses;the chicks' uncontrolled water losses will becorrespondingly high.

3. As a device to help retard digestion. In labor~atory experiments it was found that the oilshad a significant preservative power forcrustacea. Thus it seems possible that in thepresence of stomach oil the digestion of food isslowed down. Such a facility would be beneficialfor pelagic species dependent on patchy foodsources and allow the birds to metabolise bothfood and oil slowly so that energy and nutrientswere made available over an extended periodinstead of being rapidly consumed. Slowassimilation of lipids would also help to explainthe ability of chicks to discharge oil many daysafter they have been fed.

Clearly these ,rhree roles could be complementaryand they suggest interesting parallels with the ecolog-ical roles of lipid stores in the planktonic crustaceaalready mentioned. Significantly, Pelecanoidesurinatrix. the common diving petrel, which is acoastal bird and feeds its chicks daily, is the onlypetrel not known to contain oil either as chick or asadult.The defensive/offensive role for stomach oil seems

to be a secondary development from the widespreadhabit among frightened seabirds of ejecting theirstomach contents to lighten their bodies for escape(Matthews, 1964). Qil ejection is used almost exclus-ively by surface~nesting species, notably by fulmarsof the genera Fulmarus. Daption, Thalassoica,Pagodroma and Macronectes. and also by chicks ofDiomedea and Phoebetria albatrosses. Fulmars cansquirt oil with some accuracy for one or two metres.They can make several discharges before the supplyis exhausted, the first consisting of the lighter oiland subsequent ones containing an increasing propor~tion of food material, evidently representing theevacuation of the lower part of the proventriculus.Most albatross chicks have less control and tend tosplatter the oil in the general direction of the stimulus,A few burrowing gadfly petrels like Pterodromamacroptera, Pt. lessoni and Pt. inexpectata and atleast one shearwater (Procellaria aequinoctialis) mayalso discharge small quantities of oil, but usuallyquite ineffectively (Warham. 1956; 1967 andunpublished). The defensive discharge of oil is madethrough the mouth, not through the nostrils, as statedby some early authors. However. live storm petrelsoften allow oil to dribble from their nostrils whenheld in the hand.

Young petrels may discharge oil many days aftertheir last meal. Murphy (1936) gave several instances.Warham (1956) recorded a nestling Ptel'odromamacroptera that had not been fed for 6 days spittingoil, while a chick of Macronectes giganteus spat 14days after its last meal (Warham, 1962).In young Fulmams gladalis, the oil~spitting ability

is well developed by the time the chick ~s largeenough to be left nattended in the nest, freeing bothparents to forage for food. In this species spittinghas been stated to occur even from a chick not com-pletely free from the egg (Lees, 1950). The suggestionby Clarke and Prince (1976) that this chick wasactuaUy spitting bile, seems Ji.kely, as more recentdata suggests that several days elapse after hatchingbefore oil spitting behaviour appears. Williamson(1965) never saw vomiting by the very many youngand hatching F. gladalis he handled, nor did the writerwhen weighing many hatching and new~bornMacronectes gigantew,' and M. halli chicks, which arenotorious spitters. Conroy (1972) found that theyoung M. giganteus first spat oil at 6 days old.The adult F. gladalis is one of the most proficient

at repelling aggressors or potential competitors byspitting oil. I have seeD this bird displace a kittiwake(Rissa tridactyla) from a nesting ledge and Fisher(1952) Tefers to a young herring gull (Lams argentat-us) being drenched with oil by a sitting fulmar. MurdoA. Macdonald (pers. comm.) saw northern fulmarsspitting at jackdaws (Corvus monedula), one of whichbecame drenched, its feathers matted and theirinsulation evidently destroyed. He has also noted thatthese petrels may spit at alien conspecmcs, but suchreports are few. Brown (1966) described fightingbetween male Pagodroma nivea in which stomach oilwas forcefully ejected during disputes over partnersor nest-sites. The combatants' white plumage wasstained orange and to clean the feathers the birdsresorted to "bathing" jn dry snow or pushed theirbills into the snow and vigorously rotated their headsfrom side to side. Pinder (1966) noted that breedingDaption capense occasionally ejected oil at intruderswhich landed at or approached their nests, but thatthis appeared to be a last line of defence.Until recently it had been thought that the effects

of contamination by stomach oil were minor andtemporary, though probably effective in deterringmany natural predators. Recent evidence from free-living and captive birds shows that oil-spitting caDbe a formidable weapon. Substantial contaminationmay lead to death due to matting of the victim'sfeathers leading to Joss of flying ability and of waterrepellancy.The deadly effect of oil contamination was

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~

ouceo to raJr ISlaoo, Scotlano (Dennis, 1~::f/0).Tneseeagles IOcluoe nonnern !UJmars 10 tneH prey but oneor IDe eagle hcaghngs, altnougn well teo, was lOunaWltn ils plUmage matte<! ano Its feathers soaked wltn

fUlmar oil. It COULd.no longer by and was presumed.to have been snatching !Ulmar chicks from theirnestmg leoges, but had. been unable to avoid. the 011

salvoes. ThJ.S eagle is thought to have died. and some20 other specIes (raptors, crows, owls, herons, gulls,eveD a few passerines) are believed or known to havebeen killed as a result of stomach Oil contamination(Dennis, 1970; Broad, 1974; Booth, 1976). At ralfIsle, c1I1ts are the main resting places for migrantbirds, but these are also heavily populated by fulmarsand it seems that many of the victims blundered intothe petrels' indiviaual distances and hence wererepelled by oil: the passerines may perhaps havebeen caught in cross-fire!Confirmation of the potential danger of o~l

contamination was given by Swennen (1974) whokept a single F. glaciaiis (fed on thawed deep~frozenfish) in captivity with gulls and auks. The fulmarkilled 5 of its cage mates merely by spitting oilduring aggressive attacks. Deaths resulted fromchilling and/or drowning. Vigorous bathing by thesoiled birds failed to restore feather structure whereasthe fulmar appeared to be able to remove any self.contamination by bathing and preening.Mammals are also attacked. The oils seem in no

way harmful to man, have no burning action on theskin, but rabbits soaked with oil have been founddead where nesting northern fulmars were takingover rabbit-burrowed ground at the top of a cliff(Fisher, 1952). Shetland crofters are currentlyexperiencing financial losses due to their sheep beingsoiled with fulmar oil. The sheep remain healthy buttheir fleeces are unsaleable owing to matting by theoil to which heather, grass and other debris adhere(Robertson, 1975).I have only one report of an encounter between a

cat and an oil-spitting petrel. Knowles Kerry (pers.comm.) saw a nestling Phaebetria palpebrata dischargeoil at a feral cat at Macquarie Island. As the oilstruck, the cat leapt out of the way and rolled overfrantically on the grass as if trying to remove thecontamination. If this reaction is typical, it is unfort-unate that the chicks of burrowing species are unableto spit oil, for it is these that suffer the greatestlosses from predation by introduced cats.One obvious problem that arises from the discovery

of the deadly results of oil contamination is howthe petrels themseJves achieve immunity. They appearto eliminate soiling by bathing in water or snow butas this fails with other seabirds, some special mechan-

ism must be operating with petrels-perhaps adifference in feather structure. Further study isclearly needed.The readiness of F. glacialis to eject oil suggests

not only that this species has adequate food resourcesbut also that the offensive role of oil may be animportant element in the bi.rds' successful and con-tinuing expansion of breeding range.Like other anti~predator devices, oil spitting does

not confer total immunity. Despite their dangerousarmoury, surface-nesting petrels and their chicksare eaten by a variety of natural enemies. Forexample, chicks of Daption capense and ofMacronectes gigantew.' are killed and eaten bysouthern skuas (Catharacta skua) (Pinder, 1966). Evennorthern fulmars are eaten by bald, white-tailed andgolden eagles (lfaliaetus leucocephalus. If. albiciilaand Aquila chrysaetos), by the falcons Falco pere~grinus and F. ru.~.ticolusand by the fox Vulpes fulva(Fisher, 1952; Hawker, 1975). Large gulls also getsome fulmar chicks. The falcons, striking on thewing, would be expected to take fulmars withimpunity, but even peregrines seem to fall victimat times (Clarke, 1977).

"MUMIYO"

Snow petrels use oil~spitting to good effect indeterring predatory skuas and during intra-specificconflicts over nest sites. In the cold climate the spilledoil, usually mixed with the excreta of the chicks,sets as hard as stone and accumulates around thenesting places as these are used year after year. Upto 9 kg of this frozen oil has been recovered in asingle lump.Geologists examining this material determined its

biological nature and thought that it was formedfrom the petrel's excreta (Ardus, 1964; Jones andWalker, 1964), but Winsnes (1969) realised that itwas mainly stomach oiL Meanwhile Russian scientistshad noted the Antarctic material's similarity to"mumiyo", a deposit of biological origin found in

rocks in Iran, India and China. The infra-red anduLtraviolet spectra of "mumiyo" and the Antaroticdeposits were similar (Korotkevich et ai., 1967). Somesamples of "mumiyo" are also known to containwaxes (poroshin et. at. 1964)."Mumiyo" has been known from antiquity, was

described by Avicenna and others, and is still believedto be a valuable aid in mending broken bones insome circles of oriental medicine.There seems no doubt as to the origin of Antarctic

"mumiyo", but that of the Asian substance is so farundetermined. It seems rather unlikely that it willprove to be fossilised stomach oil but if so wouldreflect nesting sites along the shores of some former

WARHAM: INCIDENCE, FUNCTIONS AND ECOLOGICAL SIGNIFICANCE OF PETREL STOMACH OILS91

coastline, perhaps that of the Tethys Sea. However,even if Asian "mumiyo" proves to have a singleorigin and from animal ratner than plant material,there are possible sources: of fossH oils and waxesother .than petrels. For example, at Bute Inlet, BritishColumbia, copious submarine deposits of wax havebeen found. Analyses suggest that these may be aconsequence of massive kills of Co/anus sp. throughunknown causes (Benson et 01., 1972). Conceivablysuch deposits could be preserved under appropriateconditions to form "mumiyo".

FURTHER WORK

Although the origins of the oils seem clearlyestablished, many unresolved problems remain con-cerning functions and particularly concerning themetabolic pathways involved in the birds' processingof the oils. Do the chicks manufacture it? How muchof the energy actually available is used? How is thecombustion of the stomach oils and the depot fatscontrolled? Is there any re-incorporation into proteinwhich Lee (1974) suggested as a role for the waxesters from the copepods eaten by the ctenophorePleurobrachia and by arrow worms of the genusSagitta?The course of digestion in petrels seems unknown.

Presumably the fragile oil-sacs of small crustaceawould be ruptured in the proventriculus as happenswith calanoids which, when netted, release quantitiesof oil into the water. Cheah and Hansen (l970a)considered that the oil accumulated in the petrelbecause protein was digested more rapidly than lipid,but if so, how is the protein moiety able to pass intothe gizzard and intestine leaving the low viscosityoil behind? This may be aided by the operation ofthe pyloric valve and by the unusual arrangement inwhich the duodenum ascends from the gizzardbefore looping around the pancreas: this will helpto stop the oil draining down to the intestine. Also,being heavier, the food tends to lie at the bottom ofthe proventriculus and hence will be the first to passinto the gizzard.Or is protein absorbed in the proventriculus

itself? However, it is customary to consider thatchemical digestion in birds occurs in the smallintestine. In some species the proventriculus has beenshown to be the site of acid gastrin production. Thisbegins the breakdown of proteins which is completedfurther along the intestinal tract. In the small intesti.nebile and bile salts emulsify fats while pancreatic andmucosal secretions help neutralise the acid chyme andallow lipases, carbohydrases and proteinases to work.Another possibility is that protein and carbohy-

drate are absorbed intestinally while lipids are takenup by the proventricu1ar epithelium. Watts' sugestion

that phospholipids are absorbed here (particularlythe 20: 5 and 22: 6 polyunsaturated fatty acid com-ponents) with the help of an acid phospholipase, hasalready been mentioned. Clarke and Prince (1976)noted that while oil from an adult D. melanophriswas rich in wax esters, that from four chicks con-sisted mainly of triglyceride with some free fattyacid. They suggested that this might indicate somedigestion in the proventriculus. However, the con-tents of the proventriculus seem to be highly acid,and this in an unlikely environment for normallipase activity which needs alkaline or neutral con-ditions. Nor is there any special route for pancreaticor bile secretions to reach the proventriculus,although the last discharges of oil tend to be green incolour suggesting that bile can be regurgitated. Anability to transform wax esters into triglycerides inthe proventriculus, with or without absorption there,would provide yet another source of variability inthe ratios of these compounds jn oils from differentconspecifics.Imber (1976) also speculates as to whether petrel

stomachs can preferentially utilise triglycerides duri,ngfasting periods as in the crustacea experiments ofLee et al., (1971), so that the wax ester moitiesincrease propOrrtionately in the course of digestion.On the other hand, if food and lipids are all mainly

absorbed in the intestine, then the functions of thecopious proventricular glands remain in question.Even if absorption of phospholipids from food occursthere, phosphoHpid is not a significant constituentof the oils, and the glands, which in some speciesare known to have different forms when the lumenis full than when it is empty, seem too numerous andspecialised merely to be producing gastrin andabsorbing phospholipid.The ability of proventricular epithelium to break

down or absorb stomach oi.Js could be tested invitro. This was attempted by Cheah and Hansen(I970b) who found some evidence of lipase activityin P. pacificus but only between pH 6.5 and 9.0.They concluded that under the acid conditionsobtaining in the proventriculus there could havebeen little effective lipolysis. Additional in vitro workseems to be required together with some in vivoexperiments using radioctively-Iabelled oil, and, inview of the absence of oi.l in Pelecanoides, a compar-ative examination of the morphology and metabolicactivity of the proventricular epithelia of that petreland others could prove rewarding.One possible approach for following the progress

of digestion in the proventriculus would he to analysesamples of oil extracted at regular intervals from afasting adult or chick, perhaps using the pipettetechnique 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 withtime.Yet another problem concerns the mechanisms for

breaking down waxes. These are usually regarded ashighly indigestible and in only one other bird group,the passerine honey-guides Fam. Indicatoridae, isceratophagy normal. Wax digestion in these birds isbelieved to be achieved through the lipolytic activityof an intestinal microflora (Friedmann and Kern,1956).

CONCLUSION

The appearance of stomach oil in petrels mayresult from the slow digestion of an unusual foodwhich the birds have learned to use with difficultybut which confers significant advantages in providingan energy and water reserve, food and water forchicks and an offensive/defensive weapon.Storage and use of stomach oil appears to be

another adaptation that helps proceUaciiform birdsto exploit pelagic foods which are patchily distributedand which involve parents in long journeys to findfood and both parents and chicks in substantialfasts. Utilisation of stomach oil as energy andwater sources complement other energy~savingadaptations that fit petrels for this Hfestyle, such astheir low body temperatures (which presuppose lowbasic metabolic rates), and the ability of many speciesto travel by dynamic soaring.

ACKNOWLEDGEMENTS

J am grateful to Dr Knowles Kerry and Mr MurdoMacdonald for field observations, to Mr B. S. Simmondsfor mutton-bird harvesting figures and to Mr A. K.Lojkine for translating Russian literature. Des W. R. P.Bourne, M. B. Jones and R. Watts read the manuscriptand made valuable suggestions for improvements.

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