11. sex determination of adult humboldt penguins using mosphometrics characters

8/6/2019 11. Sex Determination of Adult Humboldt Penguins Using Mosphometrics Characters

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Vol. 8,No. Sexing umboldtenguins [ 1031984). Becauseof a sharp decline in the wild population (Hays 1984),studiesof their ecologyand behavior are needed for developingeffectiveconservationplans. To achieve most of these studies, he ability to deter-mine the sex of individuals is essential or investigatingsex-specific e-havior (Davis 1988) or measuring certain reproductive parameters(CCAMLR 1994). Determining sex of captiveHumboldt Penguins n zoosis also mportant in order to maximize successfuleproduction in captivebirds (Cheney 1990, McGill and Perkins 1993, Steveson1993).Humboldt Penguins, ike most seabirdspecies, ack plumage charactersby which sexesmay be recognized. However, small differences in mor-phometric parameters reveal sufficient dimorphism to distinguishsexes(Murphy 1936:452,Scholten1987). Characters sed o determinesex npenguins ncludevent measurementsBoersma nd Davies1987), sexualbehavior (Davis 1988, Edgington 1989, Scholten 1992), morphometricdifferences in mated pairs (Edgington 1989) and temporal attendanceduring incubation (Kerry et al. 1993). Some of thesemethodshave beenused successfullyn the wild and in captivity,but only on reproductiveindividualsduring early parts of the breeding season.Cloacalexaminationhas been used in wild Adfilie Penguins (Pygoscelisdeliae,, ishman 1985,Sladen 1978), ChinstrapPenguins, Pygoscelisntarctica; ishman 1985)and captive Humboldt Penguins (Yamazakiet al. 1994). However, thistechnique requires trained researchers and specialized equipment tocomplete with minimal stress o the animal. Other methods,suchas chro-mosome analysis,hormone analysis,and laparoscopyare effective buttime-consumingand expensive (Edgington 1989).Sex determination by discriminant analysisof external measurementshas been used successfullyn the wild in severalpenguin species uch asMagellanicPenguin (Spheniscus agellanicus, colaroet al. 1983), Yellow-eyed Penguin (Megadyptes ntipodes,Darby and Seddon 1990), all pygos-celid penguins (Amat et al. 1993, Kerry et al. 1992, Williams 1990), LittleBlue Penguin (Eudyptulaminor novaehollandiae, ales1988), and others.Discriminant analysis uses morphometric differences between knownmale and female birds to calculate a function that predicts the sex ofunknown individuals. This technique is reliable, practical, fast, inexpen-sive,non-invasive, nd can be used outside of the breeding season.The objectivesof this studywere (1) to determine discriminant unc-tion(s) using external measurementswith which to determine the sex ofwild adult Humboldt Penguins at Punta SanJuan, Peru and (2) to testthe applicabilityof these functions on captiveHumboldt Penguins.

MATERIALS AND METHODS

Measurements f wild penguins.--BetweenSeptember 1992 and June1993, the bodies of 223 dead adult Humboldt Penguinswere recoveredfrom the port of San Juan de Marcona, 3 km north of Punta San Juan(1522'S,7512'W), a 54-ha guano bird reserveon the southerncoastofPeru. This reserve holds one of the largest populations of HumboldtPenguins n the country (Hays 1984). The birds were accidentally aught


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104] c. B. ZavalagandR. Paredes j. Field rnithol.Winter 1997and drowned in the nets of small boats n the courseof normal fishingoperationsbasedat Punta SanJuan along 50-60 km of the coast (within5 km offshore).Thus, the penguinscaughtmay originate rom Punta SanJuan as well as from neighboring colonies such as Sombrerillo, San Ni-colils, and San Fernando.Immediatelyafter collection,carcasses ere weighed o the nearest100g with a 10-kg Pesolaspring balance. Head and bill were measuredwithvernier calipers o the nearest0.1 mm and the flipper wasmeasuredwitha ruler to the nearest 0.1 cm. The measurementsncluded: total lengthof the head (LH) from supraoccipitalo the tip of the bill; width of thehead (WH) in a creviceust posterior o the bulge behind the eyes;billlength (BL) from the edge of implantationof feathers o the tip of theculmen;bill depth (BD) measured orso-ventrallyt the nostrils nd flip-per length (FL), maximum lattenedchord, from the humero-radialjointto the tip of the flipper (Fig. 1). The sex of each individual was deter-mined by gonad examination after dissection.Discriminant functions were derived from the measurements takenfrom the 223 carcassesanalysis ample). These data were analyzedbystepwisediscriminant unction analysiswith the SPSS/PC + 4.0.1 statis-tical package (Norusis 1990). The Wilks' lambda ratio was used as a cri-terion for variable selection.All other statistical nalysiswere carried outusing the SYSTAT5.0 statistical ackage Wilkinson 1991).To test the accuracy f our results,we measured 4 breedingwild pen-guins of known sex (validation sample). These animalswere banded andmeasuredbetween 1992 and 1994 at Punta San Juan as part of a long-term studyof the breeding ecologyof this species. he sex of thesebirdswas dentified from their position during copulation.Body masswasexcluded from the discriminantanalysis ecause herewas a significantamount of seasonal ariability (CV = 13.6%). Also, themajority of dead penguins were wet and their lungs were full of water(due to drowning) at the time of weighing, which would bias this mea-surement Table 1). These penguinswere 4.8% heavier han a sampleof288 living penguins of known sex (the sex of these individualswasdeter-mined from the discriminant unction reported below) weighedat thesame ime at Punta SanJuan (males: -- 4711.06 g, SE -- 31.55, range-- 3450-6000, n = 165; females: = 4047.39 g, SE -- 35.15, range =2950-5400, n = 123; pooled: = 4427.62 g, SE = 30.42, range = 2950-6000, n -- 288). These differences were significant (z-test, z = 98, P 0.05 in all tests)with some overlap between sexes. norder to determine a discriminant function, we established the same cri-

FIGURE . Variablesmeasuredo sexadult Humboldt Penguins. L = bill length;BD = billdepth;LH = length of the head;WH = width of the head;FL = flipper length.


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Vol. 68, No. I SexingHumboldtPenguins [105


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106] C. B. Zavalagaand R. Paredes Field Ornithol.Winter 1997


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Vol.8, o. Sexingumboldtenguins [ 107teria used by Kerry et al. (1992) for discriminant analysis: 1) characterswere not linear combinations of each other; (2) correlation coefficientsbetween characteristics used for the final discriminant function were lessthan 0.60; and (3) the variance-covariancematriceswere not significantlydifferent (Box's M-statistic = 6.02; F = 1.98; P = 0.1140).Measurementsf captive enguins.--to test the efficiencyof the discrim-inant functions for determining the sex of captive Humboldt Penguins,we evaluated measurements of 35 birds of known sex. These birds weremeasuredduring May 1995 by the bird keepersat the Metro WashingtonPark Zoo, Portland, Oregon, USA. The sex of these individualswas de-termined by genetic karyotyping.

RESULTS

Determination f sexof wild penguins.--Themeasurementsf 223 deadadult Humboldt penguins (112 males and 111 females) are presented nTable 1. Maleswere significantly arger than females (z-test,P 0.05) forall morphometriccharacters Table 1). Givensomeoverlappingmale andfemale distributions of each univariate character, the interception pointbetween both curveswasdetermined from the analysis ample,obtainingthe following values or sex separation:LH = 13.09, WH = 4.94, BL =6.31, BD = 2.42, FL = 15.29 (all measurements in cm). If the measure-ment of some of thesevariableswashigher than its respectivecutoff valuethe penguin wasclassified s a male, if lower as a female, and if equal thesex could not be determined. The percentageof cases orrectlyclassifiedfor the validationsamplewere 91%, 89%, 88%, 78% and 70% for BL,BD, LH, WH and FL, respectively.Following the criteria of Kerry et al. (1992), only WH and BL weresignificantly electedby the stepwise iscriminantanalysisWilks' Lambda= 0.321, X2 = 250.03, df = 2, P 0.001). On the basisof Wilks' Lambdavalues and the number of casescorrectly classified, he inclusion of theother variableswasnot justified. By usingWH and BL simultaneously, eobtained the following unstandardizeddiscriminant unction:D = -38.60 + 3.36(WH) + 3.48(BL), (1)

If D 0 the penguin was classified s male and if D 0 the penguinwasclassified s female. By usingthis function,we correctlysexed94%of the wild penguins n the analysis ample:103 of 111 females (93%)and 106 of 112 males (95%) were correctly identified.When we applied the discriminant unction to the validation sample(39 males,35 females),we correctlyclassified 7% of the birds,with twomales and no femalesbeing misclassified.The classificationccuracy f the analysis ample n -- 223, 94%) andthe validationsample (n = 74, 97%) were similar,suggestingminimalsamplingbias.The sampleswere combinedand a new functionbasedonthe larger samplesizewasderived.This secondunstandardizedunctionalsoaccurately iscriminated etween he sexes Wilks' Lambda = 0.3132,X2 = 341.31, df -- 2, P 0.001):


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C. B. Zavalaga and R. Paredes J. FieldOrnithol.Winter 1997108]20

18

16

14

o -4 -3 -2

FIGURE 2. Distribution of discriwild Humboldt penguins rc

D -- -3tAgain, if D waspositive

-1 0 1 2 3 4Discriminant scores

finant scoresof males filled bars) and females open bars)m Punta San Juan, Peru.

.98 + 3.16(WH) + 3.69(BL) (2)he bird was a male, if negative, a female. Thisfunction correctlyclassified 5% of the penguins.The slightlyhigher ac-curacy and the larger sample size used to derive function 2 suggest twould be the mostuseful unction. The averageof the discriminantscores

(group centroid) for femaleswas - 1.50 and for males 1.45. No birds withscoreshigher than 0.69 (males) or with scoresbelow -1.17 (females)were misclassified Fig. 2). Thus, for greatest accuracy,we recommendthat sex of individualswhose discriminantscore falls within this rangeshould not be identified.Determination f sexof captive opulation.--Except or bill length, cap-tive penguins were significantly arger than wild birds (t-test, P < 0.05)for all measurements.Bill depth showed he highest difference, captivebirds having 18% thicker bills than wild penguins.On the other hand,except for the length of the head, there were significantdifferencesbe-

tween sexes n all measurements t-test, P < 0.05), males being largerthan females (Table 2).We obtained poor sex discriminationof captivebirds using equation


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Vol. 8,No. Sexing umboldtenguins [ 109TABLE . Morphometric data of captiveHumboldt Penguins Spheniscusumboldti) eld inthe Metro WashingtonPark Zoo. Range s given n parentheses. odymass s in grams,other measurements are in cm.

t-testMales (n = 19) Females (n = 16) Pooled (n = 35)Variable +_ SE +_ SE -+ SE t PBodymass 4802.6 _+ 100.5 4328.0 + 92.6 4585.7 _ 79.2 3.42


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110] c. B. ZavalagandR. Paredes J.Field rnithol.Winter 1997number of birds is required in a short period of time. In addition, birdscannot be sexed reliably using head measurements uring the molt dueto the depositionand depletionof fat asocurrs n other penguinspecies(Boersma 976, Cooper 1978). In thesecaseswe recommend o use theequation D = -6.31 + BL as criterion of sex discriminationbecause hebill length wasone of the simplestmeasurement o take on living birdsand the number of cases orrectlyclassified91% of successfulllocation)was higher than other univariate characters.The discriminant function reported in this paper to sex wild adultHumboldt Penguins s an easy, ast, inexpensive,and minimally stressfultechnique.However,studiesof other penguin species BostandJouventin1990,Duffy 1987,Gales1988,Gandiniet al. 1992,Kerry et al. 1992,Murieet al. 1991), gulls (Evanset al. 1995), and petrels (van Franeker and terBraak 1993) havenoted geographic ariation n morphometry.Thus, geo-graphicvariation may nvalidate he function'sapplicability o populationsother than the one from which it was derived. Sex identification by ex-ternal measurements f other wild populationsof Humboldt Penguinsmust be interpreted with caution until a sample of known sex animalscan be developed to act as a control.It was not appropriate to apply the two-variablediscriminant functionderived rom wild penguinsat Punta SanJuan to sex captivebirdsbecausethere were differences n sizeof the head betweencaptiveand wild birds.The extent by which captivebirds differ from wild onesmaybe significant.Also,Humboldt Penguinsheld in the Metro WashingtonPark Zoo exhib-ited overgrownbills, not so much in length as n depth. We observed hesame pattern in 30 captiveHumboldt Penguinsheld in the Parque deLas LeyendasZoo in Lima, Peru. The causesof this extra depositionofmaterial are unknown. It may be nutrition-related or due to the absenceof bill abrasion rom digging, fighting or swimming,which is normal inwild penguins.However,we obtained83% successfulllocation f captivebirds using the univariate unction D = -6.31 + BL obtained from wildbirds, as bill length was similar betweenwild and captivebirds. Thus, ifthe meansand variancesof the bill length are similar betweenwild pen-guinsat Punta SanJuan and other captivepopulationsof Humboldt Pen-guins,the use of this function may be accomplished.

ACKNOWLEDGMENTS

We are deeply grateful to William Alderete for his help in the collectionand dissection fdead penguins.We thank CynthiaCheneyand the bird keepersat the WashingtonPark Zoo,Portland, Oregon, for providingmeasurements f captiveHumboldt penguins.The sex ofthesebirdswasdetermined by genetickariotyping n the Daniel F. and Ada L. Rice Conser-vation Biologyand ResearchCenter, Brookfield, llinois carrild out the karyotypeof thesebirds. Mike Cullen, Mike Schwartz, an Stirling, Patricia Majluf, and Juan Carios Riverosimproved earlier drafts of this manuscript.To all of these,we are sincerelygrateful. Also,wewould ike to thank Miguel Camposand Professoraime Garcia (Departmentof Physics ndMathematics, Universidad Peruana Cayetano Heredia) for advice on multivariate statisticalanalysis. his work wassupportedby a grant from Wildlife ConservationSociety o the au-thors. Fishing data and dead penguinswere recovered rom the port of Punta SanJuan


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Vol. 8,No. Sexing umboldtenguins [ 111through the ArtisanalFisheriesMonitoring Program,Punta SanJuan project, by a grant toDr. P. Majluf from Wildlife ConservationSociety.

LITERATURE CITED

AGNEW,D.J. 1992. Can we use discriminant function analysis o sex penguins prior tocalculating n index of a morphometric haracteristic?p. 259-272, in Selected apers,1992 (SC-CAMLR-SSP/9). CCAMLR, Hobart, Australia.AMAX, . A., J. VTNUEkA, ND M. FERRER. 993. Sexing Chinstrap Penguins (Pygoscelisnt-arctica)by morphologicalmeasurements. olonialWaterbirds16:213-215.BOERSMA,. D. 1976. An ecological nd behavioral tudyof the Galapagos enguin.LivingBird 15:43-93. 1991. Statusof wild and captivepenguin populations.Trends n Ecol. and Evol. 6:381-382.

, ANDE. M. DAXqES. 987. Sexing monomorphicbirds by vent measurements. uk104:779-783.CCAMLR. 1994. CCAMLR Ecosystem onitoring Program:standardmethods or monitor-ing parametersof predatory species.Committee for the Conservationof Antarctic Ma-rine Living Resources, obart, Australia.BOST,CH-A, AND P.JOtWrNTTN.1990. Evolutionaryecologyof GentGo Penguins Pygoscelispapua). Pp. 85-112, in L. S. DavisandJ. T. Darby,eds.Penguinbiology.AcademicPressInc., San Diego, California.CHENEY, . A. 1990. Spheniscusenguins:an overviewof the world captivepopulation.Spheniscusenguin Newsietter3:12-17.COO'ER,. 1978. Moult of the black-footed enguin. nternational Zoo Yearbook18:22-27.DARY,J.T., ANDP.J. SEDDON. 990. Breedingbiologyof Yellow-eyed enguins Megadyptesantipodes). p. 45-62, in L. S. Davisand J. T. Darby, eds. Penguin biology.AcademicPress nc., San Diego, California.DAXqS, . S. 1988. Coordination of incubation routinesand mate choice n Adelie Penguins(Pygoscelisdeliae).Auk 105:428-432.DUFFY, .C. 1987. Ecological mplicationsof intercolonysize-variationn Jackass enguins.Ostrich 58:54-57.EDGINGTON,. G. 1989. Behavioural nd morphological exingof the Humboldt Penguin(Spheniscusumboldti).SpheniscidPenguin Newsletter1:14-20.EvANs,D. R., P.M. CAVANAGH,. W. FRENCH, NDB. G. BLODGET. 995. Identifying he sexof Massachusettserring Gulls by linear measurements.. Field Ornithol. 66:128-132.FARAIN, ., AND R. SHINE. 1993. Patternsof sexual size dimorphism n seabirdsof theSouthern Hemisphere. Oikos 68:139-145.FITZPATRICK,. C., C. G. GUEP,A,ANDT. L. KING. 1988. Sex determination n gray gulls,Larus modestus,singexternal measurementsnd discriminant nalysis. stud.Oceanol.7:71-74.GALES, . 1988. Sexingadult Blue Penguins y externalmeasurements. otornis35:71-75.GANDINI,P.A., E. FeERE, NDT. M. HOLIK. 1992. Implicanciasde lasdiferencias n el tamafiocorporal entre coloniaspara el uso de medidasmorfomtricascomo mtodo de sexadoen Spheniscusmagellanicus. l Hornero 13:211-213.GLAHN, . F., ANDR. B. McCoY. 1995. Measurements f winteringDoubled-crested ormo-rants and discriminantmodelsof sex.J. Field Ornithol. 66:299-304.I-lys, C. 1984. The humboldt penguin in Peru. Oryx 18:92-95.KRy, K. R., D. J. AGNEW,. R. CkARr, ANDG. D. ELSE.1992. Use of morphometricpa-rameters or the determination of sex of Adlie penguins.Wildl. Res. 19:657-664.--, J. R. CkAP,,E, ANDG. D. ELSE. 1993. Identification of sex of Adlie penguins romobservationsf incubatingbirds.Wild. Res.20:725-732.LSHMAN, . S. 1985. The comparative reedingbiologyof Adelie and ChinstrapPenguins,Pygoscelisdeliae nd P antarctica t Signy sland,SouthOrkney Islands. bis 127:84-99.LORENTSEN, -H., AND N. ROv. 1994. Sex determination of antarctic petrels Thalassoicaantarctica y discriminantanalysis f morphometriccharacters. olar Biol 14:143-145.


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112] C. B. ZavalagandR. Paredes J.Field rnithol.Winter 1997MCGILL,P., NDG. PERKINS.993. Humboldt PenguinSSP eport. SpheniscusenguinNews-letter 6:2-4.Mumv,J.O., L. S. D^vIs,D I. G. McLF_x. 1991. Identifying he sexof FiordlandCrestedPenguinsby morphometriccharacters. otornis 38:233-238MURPHY, R. C. 1936. Oceanic birds of South America, Vol. 1. The American Museum ofNatural History, New York.NoRusIs,M.J. 1990. SPSS dvanced tatistics ser'sguide. SPSS nc., Chicago.SCHOLTEN,.J. 1987. Breedingbiologyof the Humbolt penguin,Spheniscusumboldti, tEmmen Zoo. International Zoo Yearbook 26:198-204

1992. Choice of nest-site nd mate in Humboldt Penguins Spheniscusumboldti).Spheniscus enguin Newsletter5:3-13ScOIRO,J. A., M. A. I-MLL,AND . M. XIMINEZ.1983. The MagellanicPenguin (Spheniscusmagellanicus):exingadultsby discrininant nalysis f morphometriccharacters.Auk100:221-224SLaDEN, .J.L. 1978. Sexingpenguins y cloacascope.nternationalZoo Yearbook 8:77-80.STFWSON,. 1993. 1993 meetingof the EEP PenguinTAG. SpheniscusenguinNewsletter6:10-12.VAN FP,qFKR,. A., D C. J. F TF BmK. 1993. A generalizeddiscriminant or sexingFulmarine Petrels from external measurements. Auk 110:492-502.YAMAZAKI,Y., A. YAMATO, A. YAMADA, AND K. NISHIWAKI. 1994. Sex determination of Hum-boldt Penguins Spheniscusumboldti) sing an original designed estraint.PenguinConservation 7:7-11.WIIKNSON,. 1991. SYSTAT: he system or statistics. ystat, nc., Evanston, llinois.WILLLXMS,. D. 1990. Annualvariation n breedingbiologyof the Gentoopenguin,Pygoscellspapua, at Bird Island,SouthGeorgia. Zool. Lond. 222:247-2581995. The Penguins:Spheniscidae. xford UniversityPress,New York.Received 23 Jan. 1996; accepted 24 Apr. 1996.

SEVENTY-FIFTH ANNIVERSARY MEETINGASSOCIATION OF HELD ORNITHOLOGISTS

The Association f Field Ornithologists ill hold its 75th anniversarymeeting ointly withthe AmericanBirding Associationn SanJosfi,CostaRica, 21-28 Jul. 1997, hostedby theAssociacitn rnitoltgicade CostaRica.Scienticpaper sessions,ymposia, orkshops, nd fieldtripsare planned.There will be a focuson conservation nd research n CostaRicaand post-meeting trips to major field stations or researchers nd educators. ravel and per diemfunds are being sought or Latin American participants.Likely symposiumopics ncludeConservationof New World Psitticines,Bird Sound Recording,Raptor Migration betweenthe Americas, Bird Observatories,and Birds in Environmental Education for IndigenousPeoples.Registrationwill begin 10 Feb. 1997. Call for papers:ScottK. Robinson, llinoisNatural History Survey, 607 E. Peabody Dr., Champaign, IL 61820 (217-333-6857;[email protected]), nd Rafael Campos Ramierez (fax 506-494-3346). For informa-tion aboutsymposiasuggestionsor additional opicswelcome):CharlesD. Duncan, nstitutefor Field Ornithology,Universityof Maine at Machias,Machias,ME 04654 (207-255-1358);[email protected]).egistrar:Carol Wallace, American Birding Association,P.O. Box 6599, ColoradoSprings,CO 80934-6599 800-850-2473 r 719-578-1614;ax 719-578-1480;[email protected]).

11. sex determination of adult humboldt penguins using mosphometrics characters

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