Sexual dichromatism in mediterranean storm petrels Hydrobates pelagicus melitensis. We propose the use of a non-invasive technique for sexing the Mediterranean subspecies of the European storm petrel Hydrobates pelagicus melitensis. We found that this subspecies shows sexual dimorphism in rump band length and wing length. We found that storm petrels can be sexed using discriminant analysis and/or the product of wing length * rump band length. Fast and cheap sex identification methods can improve conservation programs and population studies of this species

Albores-Barajas, Y.V.

Griffiths, K.

Massa, B.

Soldatini, C.

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Sexual Dichromatism In Mediterranean Storm Petrels Hydrobates Pelagicus Melitensis

We propose the use of a non-invasive technique for sexing the Mediterranean subspecies of the European storm petrel Hydrobates pelagicus melitensis. We found that this subspecies shows sexual dimorphism in rump band width and wing length.  Fast  and cheap sex identification methods can improve conservation programs and population studies of this species

Albores Barajas, YV

Griffiths, K

MASSA, Bruno

Archivio istituzionale della ricerca - Università di Palermo

SEXUAL DICHROMATISM IN MEDITERRANEANSTORM PETRELS HYDROBATES PELAGICUS MELITENSISDICROMATISMO SEXUALEN EL PAÍÑO EUROPEO HYDROBATES PELAGICUS MELITENSISY. V. ALBORES-BARAJAS* 1, B.MASSA2, K. GRIFFITHS3 and C. SOLDATINI1SUMMARY.—Sexual dichromatism in mediterranean storm petrels Hydrobates pelagicus melitensis.We propose the use of a non-invasive technique for sexing the Mediterranean subspecies of theEuropean storm petrel Hydrobates pelagicus melitensis. We found that this subspecies shows sexualdimorphism in rump band length and wing length. We found that storm petrels can be sexed usingdiscriminant analysis and/or the product of wing length * rump band length. Fast and cheap sexidentification methods can improve conservation programs and population studies of this species.Key words: Hydrobates pelagicus, non-invasive techniques, sex identification.RESUMEN.—Dicromatismo sexual en el paíño europeo Hydrobates pelagicus melitensis.Proponemos el uso de una técnica no invasiva para sexar la subespecie mediterránea del paíño euro-peo Hydrobates pelagicus melitensis. El tamaño de la banda del obispillo y la longitud del ala muestranun claro dimorfismo en esta subespecie. Los resultados obtenidos muestran que el paíño europeo pue-de ser sexado utilizando el análisis discriminante, o bien el producto de la longitud del ala por el tama-ño de la banda del obispillo. Un método que permite identificar el sexo de forma rápida y económica, yque puede mejorar los programas de conservación y los estudios poblacionales de esta especie.Palabras clave: identificación sexual, paíño europeo, técnicas no invasivas.Ardeola 57(2), 2010, 333-3371 Deptartment of Environmental Science. University Ca’ Foscari of Venezia.Campo della Celestia, Castello 2737/b. I-30122 Venezia, Italy.2 Deptartment SENFIMIZO (Bird Ringing Unit), University of Palermo.Viale Scienze 13, I-90128 Palermo, Italy.3 Institute of Biomedical and Life Sciences Graham Kerr Building.University of Glasgow, Glasgow G12 8QQ. UK.* Corresponding author: yalbores@unive.itINTRODUCTIONIn studies of population dynamics, age andsex are vital components (Nisbet, 2001). Sexidentification can be a difficult task in manybird species particularly if they are not sexual-ly dimorphic. The availability of moleculartechniques for sexing birds has had a great im-pact on our understanding of avian behaviour,ecology and evolution (Lessells and Mate-man, 1996; Kalmbach et al., 2009). Accuratesex identification can help ensure the successof conservation programmes during captivebreeding, reintroductions and populationmonitoring (Lessells and Mateman, 1996).Molecular sex identification has also shownhow birds can change the sex ratio of theiroffspring in response to resource availability(Ellegren et al., 1996; Nager et al., 1999).Molecular sex identification has threedisadvantages. The first is the economicalcost, a limiting factor for some ecologicalstudies. The second is that sex identificationis required instantly for some experimentaland behavioural studies. The last one is thedisturbance caused to the individual to takethe blood or feather samples. It is faster andless invasive to take some morphometricsthan a blood sample from the vein. It is pos-sible to avoid these problems in several birdspecies by using biometrical differences todetermine sex. In the case of some species,such as cassin’s auklets Ptychoramphusaleuticus (Nelson, 1981), and cory’s shear-water Calonectris diomedea (Bretagnolleand Lequette, 1990), where the plumage ismonomorphic, a pair can be captured andthe relative size of the bill and tarsus can beused to identify sex (Nelson, 1981; Bretag-nolle and Lequette, 1990). In the present studywe have used the biometrics of plumagecharacteristics as a non-invasive method toidentify the sex of the mediterranean stormpetrel, Hydrobates pelagicus melitensis, ataxon distinguished both morphologicallyand genetically (Lalanne et al., 2001; Cagnonet al., 2004) which appears to show nosexual dimorphism. Results were corrobo-rated by blood sampling and molecular sexidentification.MATERIAL AND METHODSThe mediterranean storm petrel colony inMarettimo Island, Italy, has been monitoredsince 1985, with about 6,000 individualsringed (Lo Valvo and Massa, 2000; Sanz-Aguilar et al., 2009; Sanz-Aguilar et al.,2010). In 2008 and 2009 we captured 46storm petrels and measured wing length, tothe nearest 0.1 mm with a wing rule; tarsus,from themiddle of midtarsal joint to distal endof tarsometatarsus; head plus bill, bill depthand width and rump band length (fig. 1), tothe nearest 0.01 mm using Vernier callipers.Individuals were chosen from previously se-lected nests that were followed during mostof the breeding season. Birds were capturedwhile on the nest. From these 46 individualswe obtained blood samples. Blood spots,which were preserved by drying onto piecesof filter paper were then stored in separatelabelled eppendorf tubes until analyses werecarried out.DNA for sex identification was extractedfrom the dried blood spots using QiagenDNeasy® Blood and Tissue Kit following theArdeola 57(2), 2010, 333-337ALBORES-BARAJAS, Y. V., MASSA, B., GRIFFITHS, K. and SOLDATINI, C.334FIG. 1.—Wemeasured the visible part of the rumpband length for sexing storm petrels.[Medida de la parte visible de la longitud de labanda del obispillo para sexar los paíños euro-peos.]recommended protocol. PCR amplificationof selected regions of the sex linked CHDgene was performed using primers 2550F5’GTTACT GAT TCG TCTACGAGA –3’(Fridolfsson and Ellegren, 1999) / 2757R 5’AAT TCC CCT TTTATT GAT CCA TC –3’(R. Griffiths pers. com.). A reaction volumeof 10ul was used with 1ul of genomic DNAas the template, 2ul 5x GoTaq® Flexi Buffer(Promega) 2mM MgCl2 (Promega), 200uMof each dNTP, (Promega) and 0.4U GoTaq®DNApolymerase (Promega). PCRwas carriedout using a Biometra Thermocycler, with thefollowing reaction conditions: initial dena-turing step of 94 °C for 2 mins, followed by30 cycles of 49 °C for 1 min, 72 °C for 1 minand 94 °C for 45 secs. Final annealing andextension temperatures of 49 °C for 1min and72 °C for 5 mins. PCR products were sepa-rated by gel electrophoresis using 2% agarosestained with ethidium bromide.A t-test was carried out to test whetherbiometrics were a good predictor of the sexof an individual based on the known sexes ofthese birds determined frommolecular analy-sis. We also compared the single biometricsbetween sexes. A discriminant analysis wascarried out entering all the biometrics taken(head+bill, rump, tarsus, wing length and billlength). We selected the variables with a Pvalue < 0.05 and entered those in the model.We used SPSS 13 to carry out the analysis.RESULTSWe sexed 46 individuals using moleculartechniques of which 21 were females and25 were males. Sexes were confirmed usingknown sex individuals from studies in theAtlantic population as positive controls. Usingmorphometrics we found that females havea longer rump band than males (table 1). Wealso confirmed the larger size of females incomparison with males. There were no sig-nificant differences in either head plus billlength or tarsus measurements. To sex with a95% confidence interval, we used the productwing length*rump band length (females:2042.08 ± 45.17, 95% confidence interval =1948.15 – 2136.02; males: 1781.87 ± 45.71,95% confidence interval = 1687.53-1876.21).The discriminant analysis correctly sexed80.9% of the individuals, selecting wing-length (F1,41 = 29.9 P < 0.001) and rump(F1,41 = 8.41 P < 0.01); the discriminantfunction was D = 0.402*wing-length +0.294*rump –55.35.Ardeola 57(2), 2010, 333-337SEXUAL DICHROMATISM IN MEDITERRANEAN STORM PETRELS 335TABLE 1Mean ± Standard Error for different biometrics and rump according to sex. P values for differencesbetween biometrics are indicated in the last column. In bold significant values.[Media ± Error Estandard de varios parámetros biométricos y obispillo, de acuerdo con el sexo. Losvalores de la P se indican en la última columna. En negrita los significativos.]Males Range Females Range t PWing 125.24 ± 0.42 122-130 128.6 ± 0.43 124-134 291.75 0.001Tarsus 23.8 ± 0.17 22-25-4 23.5 ± 0.18 22.1-24.9 0.171 0.41Head+bill 32.6 ± 0.21 30.2-34.5 32.7 ± 0.24 30.5-34.9 –0.27 0.81Rump 14.2 ± 0.34 11.2-16.9 16.0 ± 0.36 13.5-19.6 40.72 0.001DISCUSSIONThe analysis was done based on individu-als that were sexed genetically. We decidednot to assign the sex to the partner becauseoccasionally three different individuals wereobserved in the same nest over several days(unpublished data), probably because in ourstudy site the nests were very close. Due tothe peculiarity of the colony inMarettimo, wecannot assume the same would happen inother colonies where storm petrels nest onindividual burrows.When biometrics can be taken for bothmembers of the pair, discriminant analysiscan be a reliable method for sexing individu-als (Hamer and Furness, 1991; Henderson,1991; Granadeiro, 1993; Palomares et al.,1997; Phillips and Furness, 1997), but in thecase of storm petrel, biometrics do not con-sent a good discrimination except for winglength. Other Procellariiformes species canbe sexed using vocalizations (e.g.: Ristow andWink, 1980); however, for storm petrels it isa difficult task, as they do not emit calls whenthey are captured.The results obtained in this study show thatfor sexing storm petrels, the use of wing lengthand rump band length together may increasethe probability to separate sexes. Thus, the dif-ference that we have reported in rump bandlength is an original contribution to identifysexes in this monomorphic species. Plumagepatterns in storm petrels show that a whiterump band is highly contrasted against theblack of the rest of the feathers, and this couldindicate the sex of an individual to otherstorm petrels, especially under low light con-ditions, in addition to the olfactive signals(de Leon et al., 2003). Discriminant analysisprovided a lower percentage of birds sexedcorrectly, but it is still a valid method whensex determination does not have to be 100%accurate.This is the first reliable method that hasbeen discovered for sexing storm petrels usinga visual, non-invasive technique. Using thismethod the probability of correct sexing in-dividuals is very high (81%) and in the caseof both parents present at the nest evenhigher. Furthermore using only two biometricmeasures, would speed up measuring opera-tion reducing disturbance due to handlingthe birds. It would be interesting to confirmif this sexual difference is also present in theAtlantic subspecies H. p. pelagicus, which issmaller than the Mediterranean (Lalanne etal., 2001; Cagnon et al., 2004). The abilityto accurately determine sex will provideopportunities to examine possible inter- andintrasexual differences in the behaviour andecology of adults. Some adult storm petrelscan be sexed while in the field, reducing lo-gistical problems, the costs incurred usinglaboratory analysis, and furthermore speedingup data collection, data analysis and also pos-sibly affect policy implementation.ACKNOWLEDGEMENTS.—We are grateful to R.Griffiths for commenting on an earlier draft of thismanuscript, and R. Galici for some statistical sug-gestions. This project was funded by the Assesso-rato Regionale Agricoltura e Foreste to the BirdRinging Unit of the University of Palermo.BIBLIOGRAPHYBRETAGNOLLE, V. and LEQUETTE, B. 1990. Struc-tural variation in the call of Cory’s shearwater(Calonectris diomedea, Aves, Procellariidae).Ethology, 85: 313-323.CAGNON, C., LAUGA, B., HEMERY, G. andMOUCHES,C. 2004. Phylogeographic differentiation ofstorm petrels (Hydrobates pelagicus) based oncytochrome b mitochondrial DNA variation.Marine Biology, 145: 1257-1264.DE LEON, A., MÍNGUEZ, E. and BELLIURE, B. 2003.Self-odour recognition in European storm-petrelchicks. Behaviour, 140: 925-933.ELLEGREN, H., GUSTAFSSON, L. and SHELDON, B. C.1996. Sex ratio adjustment in relation to pater-Ardeola 57(2), 2010, 333-337ALBORES-BARAJAS, Y. V., MASSA, B., GRIFFITHS, K. and SOLDATINI, C.336nal attractiveness in a wild bird population. Pro-ceedings of the National Academy of Sciencesof the United States of America, 93: 11723-11728.FRIDOLFSSON, A. K. and ELLEGREN, H. 1999. Asimple and universal method for molecularsexing of non-ratite birds. Journal of AvianBiology, 30: 116-121.GRANADEIRO, J. P. 1993. 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Predict-ing the sex of Parasitic Jaegers by DiscriminantAnalysis. Colonial Waterbirds, 20: 14-23.RISTOW, D. and WINK, M. 1980. Sexual dimor-phism of Cory’s shearwater. Il Merill, 21: 9-12.SANZ-AGUILAR, A., MASSA, B., LO VALVO, F.,ORO, D., MÍNGUEZ, E. and TAVECCHIA, G. 2009.Contrasting age specific recruitment and sur-vival at different spatal scales: a case study withthe European storm petrel. Ecography, 32: 1-10.SANZ-AGUILAR, A., TAVECCHIA, G., MÍNGUEZ, E.,MASSA, B., LO VALVO, F., BALLESTEROS, G. A.,BARBERA, G. G., AMENGUAL, J. F., RODRÍGUEZ,A., MCMINN, M. and ORO, D. 2010. Recaptureprocesses and biological inference inmonitoringburrow-nesting seabirds. Journal of Ornitholo-gy, 151: 133-146.[Recibido: 01-12-2009][Aceptado: 12-03-2010]Ardeola 57(2), 2010, 333-337SEXUAL DICHROMATISM IN MEDITERRANEAN STORM PETRELS 337

Sexual dichromatism in Mediterranean storm petrels Hydrobates pelagicus melitensis.

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Sexual Dichromatism In Mediterranean Storm Petrels Hydrobates Pelagicus Melitensis

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