The Auk 111(2):285-291, 1994

OLFACTORY BEHAVIOR OF FORAGING PROCELLARIIFORMS

CHRISTOPHEVERHEYDEN AND PIERREJOUVENTIN Centred'Etudes Biologiques de Chiz•,Centre National de la RechercheScientifique, 79360 Beauvoir-sur-Niort, France

ABSTRACT.--OIfactoryforaging, although very rare among , is frequently found in membersof the ;this finding is basedon a small number of field studies using a standardized method (i.e. raft tests). Reactions of seven speciespreviously tested under artificial conditionswere testedagain under natural feeding conditions(-oil slicks) to check validity. Concurrently, we comparedthe flight behavior of two groups of (with and without olfactory capacities) when approaching an odor source. A large-scale experiment was then conductedin pelagic waters to test the reaction of a community of procellariiforms (15 species)to a food-related odor diffusing within a principal feeding area. We observed the same reactions (attraction or indifference) to oil slicks as to test rafts in all speciesevaluated. Results obtained with the standardized method thus hold under natural conditions.Species guided by oilaction approachedthe odor sourceby flying against the wind very dose to (< 1 m) the surface, whereas other speciesapproached from a direction independentof wind direction and from a greater height (>6 m). Thus, specificsearching behavioris associatedwith olfactoryforaging and we found it to be closelyrelated to direction, height, and speed of odor diffusion by wind. Reactionto the odor test varied accordingto families or subfamilies,some taxa showing consistentresponses (attraction or indifference) to several experimentsand some taxa showing conflicting reactions.We obtained some ev- idence that olfactory behavior may differ before and after locating odor sources,as well as vary according to oceanic zones (coastalvs. pelagic). We discussthe hypothesisthat certain speciesrely mainly on visual cues,recognizing and following speciesthat are tracking food- related odors. Finally, we proposesome new ideasabout the evolution of oilaction in birds. Received3 August 1992, accepted25 November1992.

ALTHOUGHOLFACTORY sensitivity in birds is from a small number of field studies in the North now documented in a growing number of spe- Atlantic (Grubb 1972), the North Pacific (Hutch- cies (seea review in Waldvogel 1989), olfactory ison and Wenzel 1980, Hutchison et al. 1984), foraging remains unusual. In terrestrial envi- the Antarctic (Jouventin and Robin 1983), and ronments, only two specieshave been shown the South Indian (Lequette et al. 1989). to locate their food by smell: the Kiwi (Apteryx These studies used a standardized method un- australis;Wenzel 1971) and the Turkey Vulture der artificial conditions (rafts) and showed that (Cathartesaura; Stager 1964). Some others have olfactory capacities are partly related to phy- shown good capacities under artificial condi- logeny and anatomy. Feeding ecology, partic- tions, including honeyguides(Indicator indicator ularly diet and feeding techniques,also play a and 1.minor; Stager 1967) and Black-billedMag- role in olfactory ability (Lequette et al. 1989). pies (Picapica; Buitron and Nuechterlein 1985). Seabirdsusing olfaction employ searchpatterns In contrast, there is evidence that at least 22 that seem to depend on wind conditions procellariiform speciesmay use olfactionwhen (Hutchison and Wenzel 1980, Hutchison et al. foraging (reviewed in Lequette et al. 1989). The 1984). Nonetheless, important questions re- existence of such a widespread ability and the main unsolved. First, can we extend the results extreme development of olfactory structures obtained under the artificial conditions of the (Wood Jones1937, Cobb 1960,Bang 1966, 1971, standardized method to natural feeding situa- Bang and Cobb 1968) make this unique tions? Second, are there specific searchbehav- among birds, and may explain its successin iors in those specieswhich do rely on olfactory exploiting the pelagic environment. Very few cuesand, if so, how are they related to wind? laboratory studieshave been conducted(Wen- We report the results of field experiments de- zel 1967, Wenzel and Sieck 1972, Jouventin signed to answer these questions,and provide 1977). Our present knowledge comes mainly new data for 15 speciesof procellariiforms. We 285 286 VERH•DENAND JOUVENTIN [Auk, Vol. 111 give details about the behavior of olfactoryfor- represent the main feeding area of most procellari- aging, and describethe role olfaction plays in iforms, unlike coastal waters where most previous the foraging strategiesof these . studies have been conducted. This choice also per- mitted the exclusion of larids that may attract other seabirds(including procellariiforms) to the yacht (Ha- STUDY AREA AND METHODS ney et al. 1992). We operated only when the boat was Two series of experiments were conducted from sailing close (+ 40ø) to the wind at speedsvarying from 5.3 to 9.7 knots in order to create a linear odor August 1991 to March 1992 on board a 36-m yacht during a cruise from the American to the African trail behind us. Immediately after closing the box, sector of the (35-64•S, 70øW-10øE). birds flying within a radius of 300 m around the yacht Whole cod-liver oil was used as an odor stimulus since were identified to speciesand counted for 10 min. it has been shown to be attractive in previous field Each period was divided into five circular counts of studies of procellariiforms. 2 min each to reduce the risk of counting the same Fine-scaleexperiment.--The odor stimulus was pre- several times. The highest count for eachspecies sented for 15 min by spreading 0.5 L on the ocean in a unit period was retained to compensatefor po- surface,thereby creating isolated surface slicks. Ex- tential underestimates.We separatedbirds flying up- periments were attempted only when the yacht was wind in our wake (within 45ø on either side of the anchored near the shore (500-1,000 m) of an open vesselaxis) from thoseflying in other directions.Con- bay in order to allow prolonged observations,and trol conditions were based on a 10-min count prior only when the wind was blowing from land to the to opening the box, and another count (also for 10 mouth of the bay so as to enhance the diffusion of min) 50 min after the closing of the box. We con- the odor towards the open ocean. Under these con- ducted a total of 26 trials, including 10 around the ditions, the slick tended to float away from the boat ScotiaSea and Drake Passage,and 16 during a cruise (maximum distance 100 m) and closely resembled in the South Atlantic from Tierra del Fuego to Cape Town. slicks frequently observed at sea (oily material orig- inating from dead , excreta, krill swarms) Comparisons.--Inboth experiments, we compared where many birds feed. Each bird sighted within 50 groupsof birds (e.g. having vs. not having olfactory m of the slickwas identified to specieswith binoculars capacities),experimental conditions (control vs. test), and followed by eye until it left the spot. Each bird and bird distributions (observed vs. expected) using was counted as a single event, including those that chi-square statistics (when n > 5 in all classes) or sometimesapproached repeatedly. Directions of ap- G-test(when n < 5 at leastin one class).Contingency proach were recordedas upwind approachesif they tests(chi-square with Yate's correction or G-test) were occured within 45 ø on either side of the wind source, applied to 2 x 2 tables.Our basicnull hypothesiswas and as indifferent approach if they did not. Flight that birds were distributed in proportion to the num- heightswere measuredwith graduatedbinoculars and ber of classesthat were compared. assignedto one of three classes(<1 m, 1-6 m, >6 m). Special behaviors such as landing or feeding on the RESULTS slick also were recorded. Control conditions consisted of a period of 15 min before spreadingthe oil, during Fine-scaleexperiment.--When confronted with which all the birds present within 50 m of the future a simulatedfeeding situation(oil slick),the four location of the slick were identified and counted. We speciesthat had previously been shown to re- also took into accountbirds present within 500 m of spond positively with the standard method (Gi- the spotduring the sameperiod. Ambient conditions on the ocean surface, such as wind direction and ve- ant [Macronectesgiganteus], Antarctic Ful- locity, as well as wave direction and height, were mar [Fulmarusglacialoides], Cape Pigeon [Daption recorded at the beginning of each trial (control + capense]and Wilson's Storm-Petrel [Oceanites odor test). oceanicus])also showed a positive response;their We conducted 16 experiments in several locations: frequency of occurrence(32.8%) and total num- CapeHorn and Diego RamirezIslands (3 tests);South- bers (n = 65) around slicks were, respectively, Shetlands (6 tests); and Western Antarctic Peninsula 5 and 13 times those recorded in the sameplace (7 tests).These locations were chosen for the presence free from oil (frequency = 6.2%, n = 5). This of procellariiform and nonprocellariiformspecies that distribution is significantly different (X 2 = 29.4, we had already tested in previous work using the P < 0.001) from that expectedif birds were not standard method (Lequette et al. 1989). attracted to the slick. Large-scaleexperiment.--The odor stimulus (0.2 L) was kept in an airtight metal box (diameter 12 cm, Three speciesknown as indifferent to odors height 19 cm) fixed on the back of the yacht and was (Kelp [Larus dominicanus],Antarctic Tern releasedin the air for 50 min after opening the box. [Sternavittata] and Imperial Shag [Phalacrocorax Trials were conductedin pelagic waters becausethey atriceps])showed no interest in oil slicks.Their April1994] ProcellariiformForaging and Olfaction 287 frequencies of occurrence (25%) and numbers TABLE1. Flight features(percent) of two groups of (n = 22) around slicks were close to those ob- speciesdiffering in their olfactory capaci- ties and way of approaching an oil slick: (group 1) served under control conditions (frequency = attracted by odor (Daption capense,Fulmarus glaci- 20.8%, n = 16). This distribution does not differ aloides,Macronectes giganteus, Oceanites oceanicus); from that expected by chance (X 2 = 0.21, P = (group 2) indifferent to odor (Larus dominicanus, 0.64). Opposite reactions of the two groups of Phalacrocoraxatriceps, Sterna vittata ). species (X • = 41.8, P < 0.001) in a simulated Attracted group Indifferent group feeding context are not only due to phyloge- (4 species, (3 species, netic divergencesbetween procellariiformsand n = 65) n = 23) other seabirds:two large procellariiforms, the Direction Grey-headed Albatross (Diomedeachrysostoma) Upwind 100.0 4.4 and the Black-browed Albatross (D. melanophris) Other 0.0 95.4 also showed no reaction to odor stimulus (14 Height compared to 38 for control). < 1 m 98.4 0.0 Proportions of birds approaching the slicks 1-6 m 1.6 17.4 against the wind and from the other three di- >6 m 0.0 82.6 rections in group 1 (specieswith olfactory ca- pacities)tended to reversein group 2 (G = 82.01, P < 0.001), the former approaching exclusively proportion of positive counts remained un- upwind, whereas the latter approached more changedunder control and test conditions(Ta- often from other directions (Table 1). In both ble 2). Downwind, however, the total number groups, observed proportions differed signifi- and mean number of species per count in- cantly from those expectedif bird arrivals were creasedtwofold, the mean number of birds per uniform with respect to wind direction (G = count increased threefold, and the proportion 91.96, P < 0.001, and G = 6.63, P = 0.001, re- of positive counts increased by 44% when an spectively). odor plume was diffused in the wake (Table 2). Use of air layers when approaching the odor Responsesto odor tests varied according to source was different in the two groups (Table familiesand groups(Table 3). Taken collective- 1), as shown by reversed proportions in the ly, members of the family Diomedeidae (Di three height classes(G = 96.10, P < 0.001). Spe- omedeachlororhynchos, D. chrysostoma,D. epo cies using olfactory cues (group 1) almost al- mophora,D. exulans,D. melanophris)tended to be ways approachedvery closeto the oceansurface more frequent and more numerous in the wake (< 1 m), whereas the others (group 2) tended to when the odor was presented,but this must be fly above 6 m, in proportions that differ from interpreted with caution, since 83% of all in- thoseexpected by chance(G = 75.04, P < 0.001, dividuals were of a single species (D. melano and G = 16.71, P < 0.001, respectively). The phris). The same tendency was observed for different flight behaviors observed in the two members of the Oceanitidae, where five species groups are not only a consequenceof phylo- (Fregettagrailaria, F. tropica, Garrodia nereis, genetic differences since two albatrosses(see Oceanitesoceanicus, Pelagodroma marina) dis- above)approached the slicksexactly as did non- procellariiformsof the group 2. Speciesthat useolfactory cues arrived first on T^llLE 2. Distribution of 24 procellariiform species the slicksslightly more often than others (56.2 flying in wake (downwind) and around (other di- rections) a sailing yacht, depending on presence vs. 43.7%, n = 16 trials), although the difference (test) or absence (control) of an odor plume in the was not statistically significant (P • 0.05). A wake (n = 26 trials). possible influence of wind speed on bird re- sponse is hinted at (although not statistically Other Downwind directions significant) by an increasing number of birds on the slicks and a reduction in delay of arrival Con- Con- with increasingwind speed (Pearson'sr = 0.34, trol Test trol Test P = 0.20, and r = -0.30, P = 0.20, respectively). Total species 9 19 21 21 Large-scaleexperiment.--Around the yacht Mean species/count 1.0 2.1 2.3 2.4 (except downwind), the total number of species, Mean birds/count 3.5 11.3 6.3 5.7 Percent counts with birds 52 96 88 96 mean number of species,birds per count, and 288 VEPa4•DmANI• JOVVEI, ITII, I [Auk, Vol.

TABLE3. Number and frequency of occurrence(percent in parentheses)of 24 procellariiform speciesflying around versus behind a sailing yacht that was (test) or was not (control) diffusing an odor stimulus in its wake (26 trials). Distributions compared using chi-square test (when n >_ 5 in all classes)or G-test (when n < 5 at least in one class).

Birds around Birds behind Taxon (no. species) Control Test Control Test P Diomedeidae (5) 14 (32) 17 (28) 4 (12) 14 (36) 0.04 Fulmarines (3) 8 (20) 16 (16) 16 (24) 39 (28) >0.05 Prions (4) 45 (28) 15 (28) 1 (4) 4 (12) 0.03 Others (7) 61 (48) 57 (52) 19 (24) 43 (40) 0.01 Oceanitidae (5) 34 (44) 28 (40) 8 (20) 19 (40) 0.05 played a similar reaction. Members of the fam- wake of the vesselwhen odor was presented. ily comprisedabout 60% of the Prionsand allies (Halobaenacaerulea, Pachyptila species tested and showed more varied reac- belcheri,P. desolata,P. vittata),however, clearly tions than other families; fulmarine avoided the wake, but less so when the odor (Macronectesgiganteus, Fulmarus glacialoides, Dap- was present. Members of the "other" group tion capense)typically were ship followers and (Procellariaaecquinoctialis, P. cinerea,Pterodroma were more numerous both around and in the incefta,P. mollis,Puffinus gravis, P. griseus,Calo- nectrisdiomedea) were the most commonly ob- servedaround the yacht (out of the wake) under TABLE4. Review of olfactory capacitiesof 43 pro- control and test conditionsand, clearly, began cellariiform speciestested in field: (yes) attracted following when the odor began to spread.This by odors;(no) not attractedby odors;(?) insufficient data or opposite reactions in different tests.Num- was mainly due to a single species(P. gravis), bers in parentheses refer to: (1) Crossin in Wenzel which accounted for 60% of total numbers, 1980; (2) Grubb 1972; (3) Hutchison and Wenzel whereas two species (Procellariacinerea and C. 1980; (4) Jouventin and Robin 1983; (5) Hutchison diomedea)showed no reaction. et al. 1984; (6) Miller 1942; (7) Lequette et al. 1989, and (8) this study. When pooled together irrespective of family or group, the eight speciesknown to use olfac- Diomedeidae tion when foraging (Macronectesgiganteus, Ful- Diomedeachlororhynchos, no (8); D. chrysostoma,no marusglacialoides , Daption capense, aec- (8), D. epomophora,no (8); D. exulans,no (7, 8); D. me- quinoctialis,Puffinus gravis, P. griseus,Fregetta lanophris,yes ? (8); D. nigripes,yes (3, 6); Phoebetria tropica,Oceanites oceanicus) were more frequent palpebrata,no (7). in the wake of the boat under test conditions Procellariidae than expected by chance (45.2 vs. 25%, n = 73), Macronectesgiganteus, yes (7, 8); M. halli, yes (7); and to a lesser extent under control conditions Fulmarusglacialis, yes (3, 5); F. glacialoides,yes (4, 7, 8); Daptioncapensis, yes (4, 7, 8); Pagodromanivea, yes (4); (35.7 vs. 25%, n • 56). The remaining 16 species Pterodromaincerta, yes ? (8); P. mollis,yes ? (8); Halo- (see Table 4 for speciesnames) were uniformly baenacaerulea, no (8); Pachyptilabelcheri, no (8); P. de- distributed around the vessel under control solata, no ? (8); P. salvini, no (7); P. turtur, no (7); P. conditions (18 vs. 25% in the wake, n = 34). vittata, no ? (8); Procellariaaecquinoctialis, yes (7, 8); P. They tended to cluster in the wake when the cinerea,no (8); Calonectrisdiomedea, no (8); Puffinusbul- leri, yes (3); P. creatopus,yes (3); P. gravis,yes (2, 8); P. odor was presented (35 vs. 25% in the wake, n griseus,yes (3, 8); P. puffinus,yes (3); P. tenuirostris,yes = 57), but less so than species listed above. (3). Moreover, at least 4 (Diomedeachrysostoma, D. Oceanitidae exulans,Pachyptila desolata, and P. vittata) of 10 Fregettagrailaria, yes ? (8); F. fropica,yes (7, 8); Gar- species that followed only in the odor plume rodianereis, yes ? (8); Halocyptenamicrosonia, yes (3); belong to genera that are insensitive to odors. Oceaniresoceanicus, yes (2, 4, 7, 8); Oceanodromafurcata, The number of birds in the wake was signif- yes (3); O. homochroa,yes (3); O. leucorrhoa,yes (3); O. ntelania,yes (3); O. tethys,yes (7); Pelagodromamarina, icantly correlated with the wind speed when yes (8). the odor was present (Pearson's r = 0.42, n = 25, P < 0.05), but the correlation was not sig- Pelecanoididae nificant when the odor was absent (r = 0.32, n Pelecanoidesgeorgicus, no (7); P. urinator,no (7). = 25, P > 0.10). This suggeststhat the influences April 1994] ProcellariiformForaging and Olfaction 289 of wind alone,and probablyof the vesselitself, but not of procellariiforms generally. Two al- on these followers can be excluded. batrossesreacted similarly to nonprocellari- iforms, showing no responseto odor and ap- proaching with a high flight unrelated to wind DISCUSSION direction. Similar specific olfactory behavior, independent of phylogeny, is also observedin Confirmationof previousstudies.--The seven American forest vultures (Houston 1984). The speciestested previously (Lequette et al. 1989) Turkey Vulture, a speciesthat has proven ol- showed exactly the sameresponse to oil slicks factoryability when foraging, flies exclusively as to test rafts. Those for which olfaction has at low heights just above the canopy(< 100 m), been demonstrated were attracted, whereas the whereasa speciesinsensitive to odors,the King other specieswere indifferent to the olfactory Vulture (Sarcorhamphuspapa), always flies much stimulus. This confirms that identical odor stim- higher (>300 m). In vultures, as well as in pro- uli inducethe sameeffects when presented,even cellariiforms, the speciesthat useolfaction con- in a different manner, to members of the same verge in their flight pattern. They fly in the species. However, under control conditions layer of air where odorousmolecules are likely birds tended to respond more to rafts than to a to diffusethe most.This mayrepresent the most seawaterarea alone. This suggeststhat raftsmay efficient strategy for localizing food by smell. cause a visual bias that does not exist with slicks. This particular flight pattern does not seem to Moreover, rafts do not resembleany potential depend on anatomical constraints. Procellari- prey and do not allow any food intake by birds. iform speciesas different in their body size and However, the oil slickswe spreadon the surface flight style as Giant Petrels and storm-petrels had the same appearance as natural slicks and are capable of adopting the same flight pattern provided feeding opportunities; at least one when searchingfor an odor source.Species that species,the Wilson's Storm-Petrel,repeatedly use olfaction also were more strongly attracted fed at slicks(27 of 35 trials) by pecking oily when wind speed increased,probably because drops from the surface (one bird was observed odorousmolecules diffused farther (Sutton 1953) pecking 246 times within 8 rain). and, thus, were likely to be detectedby more A specialflight for localizingodor sources.--Field birds. In previous work (Lequette et al. 1989), studies (Grubb 1972, Hutchison and Wenzel we saw some procellariiforms, particularly 1980, Jouventin and Robin 1983, Hutchison et storm-petrels, appearing around a test raft, al- al. 1984, Lequetteet al. 1989) have shown spe- thoughthey had beentotally absentover a great cies that rely on olfaction when searchingfor distance (radius >1 km) before the odor was food to approachthe odor sourcefrom down- released.From the present study, we estimate wind. Our experiments corroborate this result a maximum recruitment distance of about 8 km for both coastaland pelagic waters. We even for a storm-petrel flying at a speedof 30 km/h found this pattern to be exclusive in the first (Pennycuick 1989) and arriving in the wake of experiment, probably becausethere was no vi- the vesseljust after the 50 min of odor presen- sual cue (as with rafts) that could have attracted tation (for a mean boat speed of 7.8 knots and birds from all directions. Species that were a mean wind speedof 14.8 knots). This estimate, guided by olfaction toward oil slicksbehaved although ignoring some important factors re- as describedby Hutchison and Wenzel (1980) lated to the diffusion and degradationof odor for procellariiformsapproaching a raft, with zig- molecules in this environment, increases the zag crosswind excursionsbecoming narrower effectivedistance of odordetection by birdspre- as birds came closer to the source of the stim- viously estimated (several hundreds of meters) ulus. The samestrategy for localizing an odor by Waldvogel (1989) on a chemical basis. source is seen in insectsresponding to airborne These results lead to the conclusion that a pheromone cues (Kennedy and Marsh 1974). specificsearching behavior existsin those pro- However, our tests also revealed a new feature cellariiformsthat use olfactorycues when for- of approach flights; speciesknown to use ol- aging. This behavior is closely related to the faction approachedexclusively in the air layer direction, height, and speed of odor diffusion just above the surface,whereas other species by wind. flew higher. This style of flight is actually a Olfactory capacitiesand systematics.--Re- special feature of speciessearching for odors sponses to odor tests differ among families, 290 VEPa4EYr•ENAND JOUVENTIN [Auk, Vol. 111 groups,and speciesfor a given experiment,but poor (<400 m, n = 27) compared to that (37.6%) they also can differ between experiments for a observedwith good visibility (> 10 km, n = 30; given family, group, or species.All membersof X • = 21.8, P < 0.001) indicate that recruitment the Oceanitidae showed positive reactions to is basedpartly on visual cues.Some species,like odors, whereas prions showed no or very little albatrosses,may be attractedby flocksof birds interest in odors, whatever the experiment. flying over a food sourceor in the wake of a Thus, we confirm the existence of well-devel- boat, as happens with other seabirds(Haney et oped olfactory capacitiesin the former family al. 1992).These flocksare likely to be initiated and its absencein the latter group. Conclusions by and composedof speciesthat use olfaction, are less firm in those taxa where differences since these latter tend to arrive first at food- appear between experiments. The fulmarines, related odors (first experiment). It is also likely for example,usually orient toward odor sources that visual foragers recognize birds that are ac- (Hutchison and Wenzel 1980, Jouventin and tively searching for odors, since they display Robin 1983, Hutchison et al. 1984, Lequette et specific flight patterns. This idea is strongly al. 1989, this study), but this was not obvious supported by observationson King Vultures in our secondexperiment where their numbers (Houston 1984), which have no functional sense increased twofold all around the vessel when of smell, but are able to locate carcassesby the odor was presented. We think this can be watching the flight behavior of sympatricTur- explained by birds attracted by odors being key Vultures, which possesswell-developed ol- counted both in and out of the wake because factorycapacities. In this case,the visually ori- of the tendencyobserved in fulmarinesto circle ented speciesusually arrives after the species many times around a food source once it has guided by odors, and becomesdominant in been located.This suggeststhat flight patterns feeding interactions becauseof its larger size may be different before and after locating the (Koster and Koster-Stoewesand 1978). odor source. If so, this should be considered in Olfactoryforaging and evolution.--In procellar- interpreting the resultsof experimentslike ours. iiforms, smaller speciesshow more obvious ol- Results obtained with albatrosses raise fur- factorycapacities (e.g. storm-petrels),arrive first ther questions since two species (the Black- at odor sources,and are dominated in feeding browed Albatrossand Grey-headed Albatross) interactions. The largest species(e.g. albatross- were not attractedby odorswhen they are test- es) tend to arrive later, are dominant, and ap- ed near their colonies (first experiment), but pear to be mostlyvisual foragers.Olfactory for- showed positive reactions in pelagic waters aging in both vultures and procellariiforms (second experiment). The same occurs with a seemsto be restricted to small speciesthat com- true olfactory forager, the Antarctic Fulmar, pensate for their low resourceholding potential which does not react to odors near its breeding by detecting food from a great distance,and by cliffs (Jouventin and Robin 1983), but shows a moving only to thosefood sourcesthat are cer- strong attraction in other situations with the tainly available.Arriving first on a food source same (Lequette et al. 1989) or with different is a great advantagefor small specieswhen the methods (this study). Such differential re- risk of displacementby larger speciesis high. sponsesin pelagic speciesdo not occur in ol- Selection of olfactory capacityin small species factorily foraging species that feed both in as a responseto competition has not been sug- coastal and pelagic waters, such as Wilson's gestedpreviously. Several studieshave tried to Storm-Petreland Giant Petrels.Perhaps a mech- identify the forcesselecting for large olfactory anismexists, comparable to echolocationin bats, bulbs in birds, but Healy and Guilford (1990) which mainly usesthis sensorycapacity in feed- stated that their conclusions must be taken with ing context. caution. They examined the relationship be- Direct or indirectuse of odors.--In pelagic wa- tween the size of olfactory bulbs in 124 species ters, albatrossesreact to odorsin the sameway of 17 orders and a number of ecological vari- as speciesthat are indifferent to odors;they are ables cited in other studies.After removing the more numerous in the odor trail despite their effect of body and brain size, and controlling apparent lack of olfactory capacities.This sug- for the effect of , only the timing of gests that something other than olfaction may activity(nocturnal or diurnal) wasfound to have be involved in recruitment of birds within the a significant influence. Healy and Guilford diffusion range of the odorant. The low pro- (1990) concluded that this validated their basic portion (14.7%) of followers when visibility is hypothesisthat olfaction in birds has been se- April1994] ProcellariiformForaging and Olfaction 291 lected as a generalized responseto compensate corhamphuspapa use a sense of smell to locate for reduced effectiveness of vision under low- food? Ibis 126:67-69. light conditions. However, when examined at HUTCHISON,L. V., ANDB. H. WENZEL. 1980. Olfactory the family level, their results were not signifi- guidancein foragingby procellariiforms.Condor 82:314-319. cantin procellarids.Several species of this group, HUTCHISON, L. V., B. H. WENZEL, K. E. STAGER,AND B. suchas the Snow Petrel (Pagodromanivea), have L. TEDFORD. 1984. Further evidence for olfac- both large olfactory bulbs (Bang 1966) and a tory foraging by Sooty Shearwatersand North- diurnal activity (Bretagnolle 1988). We suggest ern Fulmars. Pages78-89 in Marine birds: Their that olfaction in procellariiforms, as well as in feeding ecology and commercial fisheries rela- several other taxa (Cathartidae, Indicatoridae), tionships (D. N. Nettleship, G. A. Sanger, and P. may have evolved as a response to environ- F. Springer,Eds.). Canadian Wildlife ServiceSpe- ments where food is patchily distributed and cial Publication, Ottawa. provides no visual cues that could be used for JOUVENTIN,P. 1977. Olfaction in Snow Petrels.Con- dor 79:498-499. detection, whatever the light conditions. JOUVENTIN,P., ANDP. ROBIN. 1983. Olfactory exper- iments on some Antarctic seabirds. Emu 84:46- ACKNOWLEDGMENTS 48. KENNEDY,J. S., AND D. MARSH. 1974. Pheromone- We are grateful to J. L. Etienne for organizing the regulated anemotaxisin flying moths. Science expedition and providing the opportunity to conduct 184:999-1001. these experimentsonboard his yacht Antarctica.We KOSTER, F., AND H. KOSTER-STOEWESAND. 1978. Ko- thank V. Bretagnolle,P. Duncan and H. Weimerskirch nigsgeierBeobachtungen im Tayrona-National- for helpful suggestionson an earlier draft of the park im Norden Kolumbiens, Sudamerika. Z. manuscript.K. E. Stager,J. A. Waldvogel and an anon- Koeln. Zoo 21:35-41. ymous referee gave commentsthat greatly improved LEQUETTE,B., C. VERHEYDEN,AND P. JOUVENTIN. 1989. the paper. French National Television (Channel FR3), Olfaction in subantarctic seabirds:Its phyloge- the Elf Foundation,and FrenchMinistry of Education netic and ecologicalsignificance. Condor 91:732- gave financial support to this project. 735. MILLER,L. 1942. Some tagging experiments with LITERATURE CITED Black-footed Albatrosses. Condor 44:3-9. PENNYCUICK,C.J. 1989. Bird flight performance: A BANG,B.G. 1966. The olfactory apparatusof tube- practicalcalculation manual. Oxford Univ. Press, nosedbirds (procellariiforms).Acta Anat. 65:391- New York. 415. STAGER,K. E. 1964. The role of olfaction in food BANG,B.G. 1971. 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