July2001] ShortCommunications 755

and female age in the primary reproductiveout- Department of Zoology, Uppsala University, put of Pied Flycatchers.Oecologia 126:339-344. Uppsala, Sweden. SHELDON,B.C., AND S. VERHULST.1996. Ecological WIEHN, J., AND E. KORPIM•KI. 1998. Resource levels, immunology: Costly parasite defenses and reproduction and resistanceto haematozoanin- trade-offs in evolutionary ecology. Trends in fections. Proceedingsof the Royal Society of Ecologyand 11:317-321. London, Series B 265:1197-1201. SIIKAM.,•KI, P., O. RATTI, M. HovI, AND G. F. BENNETT. WIEHN, J., E. KORPIM•KI, AND I. PEN. 1999. Haema- 1997. Association between haematozoan infec- tozoan infections in the Eurasian Kestrel: Effects tions and reproduction in the Pied Flycatcher. FunctionalEcology 11:176-183. of fluctuatingfood supply and experimentalma- STEARNS,S.C. 1992. The Evolution of Life Histories. nipulation of parental effort. Oikos 84:87-98. Oxford University Press,Oxford. WILLIAMS,J. B. 1997. Energeticsof avian incubation. SVENSSON,L. 1992. IdentificationGuide to European Pages 375-415 in Avian Energeticsand Nutri- Passerines.Fingraf AB, Stockholm,Sweden. tional Ecology (C. Carey, Ed.). Chapman and THOMSON, D. L., P. MONAGHAN, AND R. W. FURNESS. Hall, New York. 1998. The demands of incubation and avian clutch size. BiologicalReview 73:293-304. WIDEMO,F. 1989.Effect of blood parasiteson the Col- Received5 August2000, accepted25 January2001. lared FlycatcherFicedula albicollis. Honors thesis, Associate Editor: C. Blem

The 118(3):755-759, 2001

Diving Depths of

ALAN E. BURGER • BirdLifeSeychelles, P.O. Box 1310, Mont Fleuri, Seychelles

ABSTRACT.--Maximumdiving depths were mea- merskirchand Sagar1996, Weimerskirch and Cherel sured for shearwatersbreeding on Cousin Island, 1998, Keitt et al. 2000). More sophisticatedtime- Seychelles.Eighty-three percent of 23 Wedge-tailed depth-recorders(TDRs), which indicatetime spentat Shearwaters (Puffinus pacificus)dived, and their various depths and trace individual dives, have re- mean maximum depth was 14 m (SD = 23 m, range vealed muchof the underwaterforaging behavior of 1-66 m, N = 19). All Audubon's Shearwaters (P. lher- penguins, alcids, and cormorants (Kooyman 1989, minieri)dived, and their mean maximum depth was Croll et al. 1992, Wilson 1995, Watanuki et al. 1996), 15 m (SD = 12 m, range 6-35 m, N = 7). Thesedata but have not been applied to shearwaters.I report contradict the hypothesis that tropical shearwaters maximum depths attained by two tropical shearwa- should not specialize in underwater foraging. They ters, Wedge-tailed(Puffinus pacificus) and Audubon's are capableof exploiting deep prey unavailableto (P. lherminieri)shearwaters, breeding on Cousin Is- most other tropical .Five Puffinusspecies land, Seychelles(4ø20'S; 55ø40'E), and review data on (temperate and tropical) attained allometrically diving depths of other shearwaters.I examine the scaledmaximum depths comparableto thoseof pen- hypothesisthat tropical shearwatersshould not spe- guins and alcids. cialize in underwater foraging (Brown et al. 1978), It has long been known that shearwatersdive be- and discuss the role of diving in tropical shearwaters. neath the oceanto forage,using their feet and wings for propulsion (Brown et al. 1978, 1981), and show Methods.--Maximum-depth gauges were made anatomical adaptations for this mode of foraging from flexible plastic tubing with internal diameter (Kuroda 1954, Warham 1990). Simple depth gauges 0.8 mm, lined with a thin layer of icing sugar and measuring the maximum depths indicate some re- sealed at one end. Gaugeswere 70-120 mm long on markably deep dives attainedby shearwaters(Wei- Wedge-tailedShearwaters, and 70-90 mm long on Audubon'sShearwaters. As the gaugeis submerged, the increasingpressure forces water into the tube, • Presentaddress: Department of Biology,Univer- dissolving the sugar and leaving a record of the sity of Victoria, Victoria, BritishColumbia V8W 3N5, deepestdive (Kooyman et al. 1971, Burger and Wil- Canada. E-mail: [email protected] son 1988, Hedd et al. 1997). The equation provided 756 ShortCommunications [Auk, Vol. 118 by Burger and Wilson (1988) was used to calculate []Wedge-tailed 1 maximum dive depths. ß Audubon's • Cousin Island supportsbreeding populationsof -13,000 pairs of Wedge-tailed and 5,000-10,000 pairs of Audubon's shearwaters (Burger and Lawrencein press).At the time of this study (7-17 June 1999), Wedge-tailedShearwaters were return- ing nightly to nestcavities for courtship,but did not haveeggs or chicks.Audubon's Shearwaters breed all year round on CousinIsland and the statusof those 0 5 10 15 20 25 30 35 40 45 50 55 60 65 70 usedin the study was not known. Adult shearwaters Depth (m) sittingin or nearnest cavities were caughtand band- ed at night. Eachgauge was firmly tied to thebase of FIG. 1. Frequency distribution of maximum a singletail featherwith a thread (dental floss).Once depths attained by Wedge-tailedand Audubon's attached the gaugeswere surrounded by shearwaterson Cousin Island, Seychelles.X-axis la- and createdno impedimentsto the . Handling bels indicate the upper limit of each 5 m depth time was 10-15 min. Gaugesnot recoveredwould category. eventuallywork looseor be lostwhen the birdsmolt- ed. Eachbird was sampledonce. I made no attempt to collectfood samples,and none of the captured birds regurgitatedfood. ployment, althoughthe error with dives >20 m was Prolongeddeployment increases errors in these likely to be <10% (Burgerand Wilson 1988).There is devices(Burger and Wilson 1988).I includedgauges also a greaterprobability of recordingan exception- recoveredwithin two daysof deployment,and all ex- ally deep dive during a long trip. Those data are cept two (one for eachspecies) were recoveredafter comparedwith depths measuredin Cory's Shear- one day. I encounteredan unusual problem in the water (Calonectrisdiomedea) and White-chinned Pe- form of tiny ants that crawled inside the tubes and trel (Procellariaaequinoctialis), which share many removedthe sugar.Ants removedsugar unevenly, in similaritieswith Puffinusbut seemless morphologi- contrastto the sharpboundary created by water,and cally adaptedto diving (Warham1977, 1990). so with careful inspectionI was ableto rejectgauges All five Puffinus shearwaters demonstrated re- affectedby ants. markable diving abilities (Fig. 2). Their maximum Results.--Outof 23 undamagedgauges recovered diving depthsclustered close to the allometricequa- from Wedge-tailedShearwaters, 19 (83%) indicated tion derived from maximum diving depthsof pen- somediving activity (Fig. 1) and their mean maxi- guinsand alcids(maximum depth (meters)= 75.905 mum depthwas 14 m (SD = 23 m, range1-66 m). All M 0'316,where M is body mass in kilograms; Burger 7 gaugesrecovered from Audubon'sShearwaters in- 1991).Maximum depths of Calonectrisand Procellaria dicated diving, and the mean maximum depth was fell well below that regression.The diving abilitiesof 15 m (SD = 12 m, range 6-35 m). Most Wedge-tailed Puffinusshearwaters require more detailed study, us- Shearwaters remained within 20 m and most Au- ing TDR and activitydata-loggers, to confirmwheth- dubon'sShearwaters within 10 m of the surface(Fig. er deep diving forms a significantpart of their for- 1). aging routine. It will be fascinatingto discover Discussion.--Manyprocellariiform species dive to whether they show convergentanatomical, physio- captureprey, but mostspecies remain within 1-5 m logical, and behavioral adaptationsfor prolonged of the surface (Warham 1990, Prince et al. 1994, Hedd diving to thosebeing revealedfor penguins,alcids, et al. 1997),with the exceptionof the specialiseddiv- and cormorants. ing , Pelecanoididae(Prince and Jones1992, Kuroda(1954) regarded smaller species of Puffinus Chastel 1994, Zavalaga and Jahncke1997). Some as morphologicallymore specialized for diving than shearwatersof the genusPuffinus regularly use pur- most other shearwaters. Visual observations of small suit diving for foraging (Brown et al. 1978, 1981; shearwaters (Brown et al. 1978), including Audu- Warham 1990). They show adaptationsfor under- bon'sShearwater (Harris 1969),confirmed that they water swimming, including flattened tarsi and hu- dived, but this study is the first to confirm that div- meri, and shorter wings and higher wing-loading ing occursregularly (in all foragingtrips madein my than most otherpetrels (Kuroda 1954, Warham 1977, small sample), and that they are proficient, deep 1990).Maximum diving depthshave been measured divers. using gaugesin five speciesof Puffinus(Table 1). Keitt et al. (2000) speculated that shearwaters Some published depth records unavoidablycame might be most efficientat diving during wing molt, from prolonged foraging trips. There is a greater when the reduced wing area would produce suffi- chance that those gauges overestimate maximum cient propulsionbut less drag. None of the shear- depthswith repeatedsubmersion and prolongedde- waters in my sample showedany sign of primary July2001] ShortCommunications 757

Penguin-Alcidregresmon Puff'mus••S 0 • •v AU

Procellaria ß

ß Calonectns

1 1 10 Bodymass (kg)

FIG. 2. Puffinusshearwaters had maximum div- ing depths similar to those of alcids and penguins. This log-logplot of maximum diving depthsagainst body masscompares five speciesof Puffinusshear- waters (squares),including Audubon's(AU), Black- vented (BV), Sooty (SO), Short-tailed (ST), and Wedge-tailed(WT) shearwaters,with Cory'sShear- water (triangle) and White-chinned (dia- mond), and the allometric regressionof maximum depths predicted for penguins and alcids (Burger 1991).

wing molt and all appeared to have recently re- placed primaries. Maximum diving depthsare generallydetermined by allometricallyscaled physiological limits (Kooy- man 1989), whereas the depths of most foraging divesare determinedby distributionof prey.Typical foraging dives are much shallowerthan maximum limits (Kooyman 1989, Burger 1991, Wilson 1995). That applies to the Puffinusshearwaters; their mean maximum dives were generally far shallower than the overall maximum (Table 1). More accuratedepth profiles will emergewith deploymentof TDRs that show the depth distributionof all underwateractiv- ities, and not just the deepestdive per foraging trip. Brown et al. (1978) speculatedthat shearwaterspe- cies specialized for diving should be restricted to richer, cold, or cool-temperateseas. The sparsedis- tribution of prey and presenceof predatoryfish in the tropics was believed to favor shearwaterswith more efficient gliding flight rather than specialistdi- vers. Shearwatersspecialized for diving tend to have somewhatshorter wings and higher wing loading and hence rely more on flapping flight (Warham 1977, 1990), which is normally associatedwith high- ly productivetemperate and polar seas. My data do not support the hypothesisthat trop- ical shearwatersavoid diving in preferencefor sur- face foraging. Both Wedge-tailed and Audubon's shearwaterswere proficient, deep divers, and most (83%) Wedge-tailedand all Audubon'sshearwaters employeddiving on foraging trips. Diets of those 758 ShortCommunications [Auk, Vol. 118 speciesin Seychelleshave not beenrecorded, but Pa- pects of Feeding Ecology (W. A. Mon- cific Wedge-tailedShearwaters primarily take small tevecchi and A. J. Gaston, Eds.). Canadian schoolingfish and (Harrison et al. 1983),and Wildlife ServiceOccasional Paper 68. Audubon's Shearwaterstake planktonic larvae BURGER,A. E., AND A.D. LAWRENCE.2001. Census of and (Harris 1969). Depth distribution of Wedge-tailed and Audubon's shearwaters on likely prey in Seychellesis not known, nor is it Cousin Island, Seychellesusing call playback. known whether shearwaterswere restricting their Marine Ornithology. 29:in press. foraging to concentratedprey patches.Neither spe- BURGER,A. E., AND R. P. WILSON.1988. Capillary- cieswas restrictedto the most productivewater mas- tube depth gaugesfor diving :A review sesin the tropicalIndian Ocean(Bailey 1968, Pock- of their accuracyand applicability.Journal of lington 1979). Field Ornithology59:345-354. Both Wedge-tailed and Audubon's shearwaters CHASTEL,O. 1994. Maximum diving depths of Com- regularly feed at the surface(Harris 1969, Harrison mon Diving PetrelsPelecanoides urinatrix at Ker- et al. 1983, Warham 1990), as do most tropical sea- guelenIsland. Polar Biology14:211-213. birds (Ashmole and Ashmole 1967, Harrison '1990, CROLL, D. A., A. J. GASTON, A. E. BURGER,AND D. Ballanceet al. 1997). The shearwaters'diving abili- KONNOFF.1992. Foragingbehavior and physio- ties give them accessto additional, deeperprey in- logical adaptation for diving in Thick-billed accessibleto most other tropical seabirds. Even Murres. Ecology73:344-356. plunge-divingboobies and tropicbirdsseem restrict- HARRIS,M.P. 1969. Food as a factor controlling the ed to the upper 13 m (Le Corre 1997).More intensive breedingof Puffinuslherminieri. Ibis 111:139-156. researchis neededto elucidateforaging behavior of HARRISON, C. S. 1990. Seabirds of Hawaii: Natural tropical shearwaters,to confirmwhether they fill a History and Conservation.Cornell University similar pursuit-diving nicheto that occupiedby pen- Press, Ithaca, New York. guins, alcids,and cormorantsin cool-temperateand HARRISON,C. S., T. S. HIDA, AND M.P. SEKI. 1983. Ha- polar seas. waiian seabirdfeeding ecology.Wildlife Mono- Acknowledgments.--Thisstudy was funded by a graphs, no. 85. grant from the SecondDutch Trust Fund to BirdLife HEDD, A., R. GALES, N. BROTHERS,AND G. ROBERT- Seychelles.Additional support came from National SON.1997. Diving behaviourof the Shy Alba- Sciencesand Engineering ResearchCouncil Canada trossDiomedea cauta in :Initial findings and the University of Victoria. I thank Andrea and diver recorder assessment. Ibis 139:452-460. Lawrence and Ahtee Labont• for field assistance, HUIN, N. 1994.Diving depthsof White-chinnedPe- Nirmal Jivan Shah and Steve Parr for support and trels. Condor 96:1111-1113. discussion,and Harry Carter,David Lee,and Yutaka KEITT, B. S., D. A. CROLL, AND B. R. TERSHY. 2000. Watanuki for helpful comments. Dive depth and diet of the Black-ventedShear- water (Puffinusopisthomelas). Auk 117:507-510. LITERATU RE CITED KOOYMAN,G. L. 1989. Diverse Divers: Physiology and Behavior.Springer-Verlag, Berlin. ASHMOLE,N. P., AND M. J. ASHMOLE.1967. Compar- KOOYMAN, G. L., C. M. DRABECK,R. ELSNER,AND W. ative feeding ecologyof seabirds of a tropical oceanicisland. Bulletin of the PeabodyMuseum B. CAMPBELL.1971. Diving behavior of the Em- of Natural History 24:1-131. peror Penguin,Aptenodytes forsteri. Auk 88:775- 795. BAILEY,R. S. 1968. The pelagic distribution of sea- birds in the western . Ibis 110:493- KURODA,N. 1954. On the classificationand phylog- 519. eny of the order Tubinares, particularly the BALLANCE, L. T., R. T. PITMAN, AND S. B. REILLY. 1997. shearwaters(Puffinus). Published by the author, Seabirdcommunity structure along a productiv- Tokyo. ity gradient:Importance of competitionand en- LE CORRE,M. L. 1997.Diving depthsof two tropical ergetic constraint.Ecology 78:1502-1518. Pelecaniformes:The Red-tailed Tropicbird and BROWN, R. G. B., W. R. P. BOURNE, AND T. R. WAHL. the Red-footedBooby. Condor 99:1004-1007. 1978. Diving by shearwaters.Condor 80:123- MONTEIRO,L. R., J. A. RAMOS,R. W. FURNESS,AND A. 125. J. DEL NEVO. 1996. Movements, morphology, BROWN, R. G. B., S. P. BARKER,D. E. GASKIN, AND M. breeding, molt, diet and feeding of seabirdsin R. SANDEMAN. 1981. The foods of Great and the Azores. Colonial Waterbirds 19:82-97. Sootyshearwaters Puffinus gravis and P.griseus in POCKLINGTON,R. 1979. An oceanographicinterpre- eastern Canadian waters. Ibis 123:19-30. tation of seabird distributions in the Indian BURGER,A. E. 1991.Maximum diving depthsand un- Ocean.Marine Biology51:9-21. derwaterforaging in alcidsand penguins.Pages PRINCE, P. A., N. HUIN, AND H. WEIMERSKIRCH.1994. 9-15 in Studies of High-latitude Seabirds.1. Be- Diving depths of .Antarctic Science havioural, Energetic and Oceanographic As- 6:353-354. July 2001] Short Communications 759

-- PRINCE, P. A., AND M. JONES.1992. Maximum dive Tasmaniaand foraging in the Antarctic?Marine depthsattained by SouthGeorgia EcologyProgress Series 167:261-274. Pelecanoidesgeorgicus at Island, SouthGeor- WE/MERSK1RCH,H., AND P.M. SAGAR.1996. Diving gia. Antarctic Science4:433-434. depthsof SootyShearwaters Puffinus griseus. Ibis WARHAM,J. 1977. Wing loadings,wing shapes,and 138:786-794. flight capabilitiesof .New Zea- WILSON,R. P. 1995. Foraging ecology.Pages 81-106 land Journalof Zoology 4:73-83. in The PenguinsSpheniscidae (T. D. Williams, WARHAM,J. 1990. The Petrels: Their Ecology and Ed.). Oxford University Press,Oxford. BreedingSystems. Academic Press, London. ZAVALAGA, C. B., AND J. JAHNCKE.1997. Maximum WATANUKI,Y., A. KATO, AND Y. NAITO. 1996. Diving dive depthsof the PeruvianDiving-petrel. Con- performanceof male and female JapaneseCor- dor 99:1002-1004. morants. Canadian Journalof Zoology 74:1098- 1109. WEIMERSKIRCH,H., AND Y. CHEREL.1998. Feeding Received3 August2000, accepted20 January2001. ecologyof Short-tailedShearwaters: Breeding in AssociateEditor: D. Nettleship

The Auk 118(3):759-765, 2001

Visual Signalsfor Individual Identification:The Silent "Song"of Ruffs

DAVID B. LANK I'3 AND JAMESDALE 2 •Departmentof BiologicalSciences, Simon Fraser University, Burnaby, British Columbia V5A 1S6,Canada; and 2Departmentof Neurobiologyand Behavior, Cornell University, Ithaca, New York 14853-2702, USA

ABSTRACT.--Breedingmale Ruffs (Philomachus alone (Selous1906-1907), and it has long been as- pugnax)appear to communicateindividual identity sumedto function as a cue for individual identity for throughextreme variation in colorationand pattern Ruffs themselves(Hogan-Warburg 1966, van Rhijn of their .If variation evolved to 1983, 1991).Individual identificationbased on plum- provide sufficientinformation to signal individual age variationhas been demonstratedexperimentally identity, we might expect different plumage com- for just a few speciesof birds (Whitfield 1986,Watt ponentsto vary independently.We find that varia- 1986),including Ruffs (experimentsby A. SegreTer- tion in four plumagecharacteristics is largely inde- kel in van Rhijn 1991;D. B. Lank et al. unpubl.data). pendent. Previous studies produced conflicting Whereasmany speciesof birds identify individuals answersabout plumage-componentindependence, by voice (Stoddard 1996, Wiley 2000), male Ruff perhapsbecause they failed to separatetwo geneti- courtship and aggressivedisplays are completely cally distinct behavioralcategories of males, which silent. differ in plumage types, in their analysis.We pro- Did plumagevariation in Ruffs specificallyevolve posethat usingplumage variation to signalindivid- to facilitate individual variation? Is the functional ual identity, rather than voice (usedby most other design of plumage variation consistentwith that bird species)was favored by lengthy daytime male adaptivehypothesis? Characters specifically evolved display in open habitatsin closeproximity to receiv- to facilitate individual identification should have cer- ers. However, signaling associatedwith the unique tain properties(Beecher 1982, Dale 2000, Dale et al. dimorphismin this species'male mating behavior 2001).The mostfundamental is sufficientphenotypic might also have influencedthe evolutionof extraor- variation among individuals to facilitate discrimi- dinary plumagediversity in this species. nationby receivers.One simpleand powerful way to generatesuch variation is to have independently Breedingmale Ruffs (Philomachuspugnax) have the varying signalcomponents, each with high variance, mostvariably coloredand patternedfeather tracts of that combineto producemany differentphenotypes. any speciesof nondomesticatedbird. This extraor- We examine to what extent the most prominent dinary variationfacilitated study of sexualselection plumage characteristicsof breedingmale Ruffs vary by allowing an early studentto follow mating suc- independently.Previous analyseshave produced cessof individuals at leks using natural markings conflictingresults (Table 1; van Rhijn 1991). We re- visit that questionusing automatedand quantitative 3 E-mail: [email protected] measurementsof plumage characteristics,and by