Research Article

Received: 15 February 2013 Revised: 23 April 2013 Accepted: 21 May 2013 Published online in Wiley Online Library

Rapid Commun. Mass Spectrom. 2013, 27, 1801–1806

Isotopic evidence of limited exchange between Mediterraneanand eastern North Atlantic fin whales

Joan Giménez*,†, Encarna Gómez-Campos, Asunción Borrell, Luis Cardonaand Alex AguilarDepartment of Animal Biology and Biodiversity Research Institute (IRBio), Faculty of Biology, University of Barcelona, Av.Diagonal, 643 (08071), Barcelona, Spain

RATIONALE: The relationship between stocks of fin whales inhabiting the temperate eastern North Atlantic and theMediterranean Sea is subject to controversy. The use of chemical markers facilitates an alternative insight into populationstructure and potential borders between stocks because the two areas present dissimilar isotopic baselines.METHODS: Baleen plates, composed of inert tissue that keeps a permanent chronological record of the isotopic value ofbody circulating fluids, were used to investigate connectivity and boundaries between the stocks. Values weredetermined by continuous flow isotope ratio mass spectrometry.RESULTS: Stable isotopes confirm that, while the two subpopulations generally forage in well-differentiated grounds,some individuals with characteristic Atlantic values do penetrate into the Mediterranean Sea up to the northernmostlatitudes of the region. As a consequence, the border between the two putative subpopulations may be not as definiteas previous acoustic investigations suggested. The discriminant function obtained in this study may assist researchersto use baleen plate isotopic data to assign the origin of fin whales of uncertain provenance.CONCLUSIONS: This study strengthens the stock subdivision currently accepted for management and conservationwhile recognizes a low level of exchange between the Mediterranean and temperate eastern North Atlantic subdivisions.Copyright © 2013 John Wiley & Sons, Ltd.

(wileyonlinelibrary.com) DOI: 10.1002/rcm.6633

Fin whales make wide-range movements and their migrationtypically spans thousands of kilometres, traits that would inprinciple hinder the occurrence of demographic subdivisionswithin a given ocean basin. However, in the North AtlanticOcean fin whales have long been known to actuallysubdivide into subpopulation units, with little individualinterchange, and which for management purposes arecommonly denominated ’stocks’. In 1966, Jonsgård[1] wasthe first to comprehensibly investigate such structuring and,after considering the apparent differences in the trajectory ofthe catch per unit effort of various localities where the specieshad been exploited, the iodine values of the oil extracted fromthe captured individuals and their mean body size, heinferred the existence in the basin of at least six stocks. Later,evidence from further and more refined catch per unit effortseries, differences in age at sexual maturation and the resultsof marking programs led the International Whaling

* Correspondence to: J. Giménez, Department of ConservationBiology, Estación Biológica de Doñana – Consejo Superiorde Investigaciones Científicas (EBD-CSIC), AméricoVespucio s.n. (41092), Isla de La Cartuja, Sevilla, Spain.E-mail: joan.gimenez@csic.es

† Present address: Department of Conservation Biology,Estación Biológica de Doñana – Consejo Superior deInvestigaciones Científicas (EBD-CSIC), Américo Vespucios.n. (41092), Isla de La Cartuja, Sevilla, Spain.

Rapid Commun. Mass Spectrom. 2013, 27, 1801–1806

180

Commission (1977)[2] to slightly modify Jonsgård’s proposaland to agree a structuring of the North Atlantic into sevenmanagement subdivisions.

One of these subdivisions embraced the temperate watersof the eastern North Atlantic comprised between the BritishIsles, France, the Iberian Peninsula and northern Africa upto the 19�N line. Although marking with internal tags wasconducted off NW Spain in the past, all tags were recoveredin the same whaling grounds and thus did not provideevidence for stock structure. As a consequence, the rationalefor that subdivision relied on a parallel decline in catchper unit of effort observed by Jonsgård[1] between the BritishIsles and the Iberian Peninsula during the 1920s, a fact thatwas accepted as evidence of connectivity between these areas.At that time, and despite absence of any supportingevidence for connectivity, the fin whales inhabiting theMediterranean Sea were straightforwardly incorporatedinto the ’British Isles-France-Iberian Peninsula-northernAfrica’ stock. However, this was modified when laterresearch showed that adult fin whales and calves werepresent year round in the western Mediterranean[3] and thatindividuals from the Mediterranean Sea and the westernNorth Atlantic differed both genetically[4,5] and in theirorganochlorine pollutant concentrations and profiles,[6]

intrinsic markers which are frequently used to differentiatepopulations. The Mediterranean Sea was thus considered anew subdivision, with the Gibraltar Straits as the borderseparating from the adjoining Atlantic stock. Despite thepersistence of some uncertainties about the actual

Copyright © 2013 John Wiley & Sons, Ltd.

1

Figure 1. Sampling locations and important areas in theMediterranean Sea and Atlantic Ocean (triangle = this study;black dots = Bentaleb et al.[12]).

J. Giménez et al.

1802

subdivisions,[3] this demographic structure has been adoptedas the basis for management and conservation by theInternational Whaling Commission,[7,8] ACCOBAMS,[9] andthe International Union for the Conservation of Nature,[10]

among other organizations.However, the genetic studies warned that the isolation

between the Mediterranean Sea and Atlantic stocks wasnot complete and estimated the exchange between them atabout two females per generation, without clarifying whethersuch exchange was unidirectional or bidirectional.[5]

This appeared to be confirmed by satellite tagging, becausefrom eight whales successfully tagged in the north-westernMediterranean Sea one crossed the Straits of Gibraltartowards the Atlantic and moved up to central Portugal,[11,12]

and by acoustic recordings that showed that whalesproducing songs attributable to the north-eastern NorthAtlantic subpopulation were detected in the south-westernMediterranean Sea.[13] However, this last result does notdemonstrate an actual exchange between Atlantic andMediterranean stocks, but just that the border between themis not the Straits of Gibraltar. Actually, whales are observedevery year crossing through the Straits of Gibraltar in bothdirections[14,15] and the prevalence of Atlantic immigrantsinto the south-western Mediterranean is also true for othergroups of marine vertebrates.[16,17]

Chemical markers may facilitate an alternative insight intopopulation structure and potential borders between stocks. Inparticular, stable isotope values in tissues are known to reflectthe environment in which individuals obtain their food.[18,19]

Here we use baleen plates, an inert tissue that keeps apermanent chronological record of the isotopic value ofbody circulating fluids,[18,20,21] to investigate connectivity andboundaries between the stocks inhabiting the Mediterraneanand the temperate waters of the eastern North Atlantic.The two areas present dissimilar isotopic baselines, the d15Nand d13C values in the NW Iberian Peninsula being higher thanin the Mediterranean Sea,[22–24] thus providing the necessarydifferentiation. The results will not only be useful to gaugethe degree of exchange between putative subpopulations themain focus of the present study, but could provide the basisfor the assignment of origin to individual whales in the future.

EXPERIMENTAL

Sample collection and analysis

The stable isotope data used for this research originatedfrom two different sources: (i) the information providedby Bentaleb et al.[12] from ten baleen plates (BP1–BP10),corresponding to nine fin whales stranded in theMediterranean Sea during the period 1975–2002 (seven fromthe northern-western basin and two from the south-westernbasin), and (ii) the analysis of further baleen plates from fiveindividuals caught off north-western Spain (Caneliñaswhaling station, identified as A–E, Fig. 1), during the whalingseason of 1985 (July to October). Because stable isotope valuesare known to fluctuate along the longitudinal axis of thebaleen plate following seasonal changes in area of residenceand/or feeding regimes,[18,20] in both cases each plate wassubsampled at regular intervals along the longitudinal axis

wileyonlinelibrary.com/journal/rcm Copyright © 2013 John Wile

to incorporate into the analysis the expected variationoccurring throughout the biological cycle.

For storage and analytical procedures (that were almostidentical to those of the present study) in the first set of baleenplates, see Bentaleb et al.[12] In the case of the second set, thebaleen plates were stored dry until analysis. Before sampling,they were cleaned of surface oils and adhered materialusing a steel palette knife, steel wool and a chloroform/methanol solution (2:1), and subsequently subsampled with amicromilling device at 1 cm intervals, including the uneruptedsection beneath the gum. Forty-one subsamples were obtainedfrom each baleen plate. Approximately 0.3 mg of powderedbaleen plate was weighed into tin capsules (3.3 � 5 mm) andcombusted at 1000 �C in a continuous flow isotope ratio massspectrometer (Flash 1112 IRMS Delta C Series EA; ThermoFinnigan, Bremen, Germany). The analyses were performed atthe Centres Científics i Tecnològics of the University of Barcelona,Barcelona, Spain.

Stable isotope abundances, expressed in delta notation (d),where the relative variations of stable isotope values areexpressed in permil (%) deviations from the predefinedinternational standards, were calculated as:

dX ¼ Rsample=Rstandard� �� 1� �� 1000

where X is 13C or 15N, and Rsample and Rstandard are the13C/12C and 15N/14N ratios in the sample and standard,respectively. The standards were Vienna Pee Dee Belemnite(V-PDB) calcium carbonate for carbon and atmospheric nitrogen(air) for nitrogen. International isotope secondary standardsof known d13C values from the International Atomic EnergyAgency (IAEA, Vienna, Austria), namely polyethylene (IAEACH7, d

13C = –31.8%), graphite (USGS24, d13C = –16.1%) andsucrose (IAEA CH6, d

13C = –10.4%), were used for calibrationat a precision of 0.2%. For nitrogen, international isotopesecondary standards of known d15N values, namely (NH4)2SO4

(IAEA N1, d15N = + 0.4% and IAEA N22, d15N = +20.3%) and

KNO3 (IAEA NO3, d15N = +4.7%), were used for calibration

at a precision of 0.3%.

y & Sons, Ltd. Rapid Commun. Mass Spectrom. 2013, 27, 1801–1806

Figure 2. d13C and d15N signatures on baleen plates of finwhales from two different regions. Solid lines (SEAc), dottedlines (Convex Hull Area): (a) two groups (Atlantic andMediterranean whales), (b) three groups (considering BP1 asanother group).

Limited exchange between Mediterranean and Atlantic fin whales

Statistical analysis

Initial statistical screening showed that variances of the d13Cand d15N values between individual baleen plates were nothomogenous according to the Levene test. Moreover, in theMediterranean individuals, the number of subsamplesanalyzed was highly dissimilar between individuals. As aconsequence, comparison using the full dataset of samplesand including the ’individual’ factor as a variable to controlfor pseudoreplication was not possible. Therefore, thecomparison between whales from the different areas wasbased on the mean of all d13C and d15N values from eachspecimen, a procedure that was moreover expected to smooththe seasonal variability likely to exist within the plate. Indoing so, the mean values from each group of whales werenormally distributed according to the Lilliefors test and werehomoscedastic according to the Levene test. A t test was usedto compare the two datasets of baleen mean values.A visual inspection of the raw baleen plate isotope data

suggested that Mediterranean and Atlantic individualsseparated into two independent clusters, with the onlyexception of individual BP1 from Bentaleb et al.[12] occupyingan intermediate position (Fig. 2). Linear discriminant analysiswas used to investigate statistical assignment of thiscontroversial individual to one origin group. The comparisonbetween the isotopic niches of the two putativesubpopulations was carried out by standard ellipses analysis(SEAc) performed using SIBER (Stable Isotope BayesianEllipses in R[26]) as a measure of the mean core populationisotopic niche. The standard ellipse of a set of bivariate datawas calculated from the variance and covariance of the dataand contained approximately 40% of the data. SEAc wasconsidered to be appropriate when analyzing niche widthsbetween groups because it is unbiased with respect to samplesize, thus allowing robust comparison among datasets ofdifferent sample size.[26] Differences in isotopic niche spacebetween two different groups may indicate differences inthe type of prey eaten or differences in the area where theyforage. Convex Hull Area method[26] (polygon around themost extreme data points on the isotope bi-plot) was alsoused to consider the entire variability in the stable isotopevalues. SEAc and Convex Hull Area method allowed usto assess the degree of overlap between datasets. In theseanalyses, the input data were the isotopic values of all baleenplate subsamples instead of the mean values from the baleenplates. SEAc and Convex Hull area were performed using theR statistical computing package. The statistical program SPSS15.0 was used for the other tests.

180

RESULTS

The stable isotope values fluctuated along the longitudinalaxis of baleen plates. However, the pattern of variation washighly variable among individuals, both for the d13C andd15N values. Comparison of mean values between thetwo datasets revealed that whales from the Atlantic wereenriched in both 15N and 13C as compared with those fromthe Mediterranean (t = 4.49, df = 13, p <0.001 for d13C andt = 6.68, df = 13, p <0.001 for d15 N, nMediterranean = 5,nAtlantic = 10 for both stable isotope ratios). Furthermore,the magnitude of the differences between the two datasets

Copyright © 2013Rapid Commun. Mass Spectrom. 2013, 27, 1801–1806

matched the magnitude of the differences between Atlantic[24]

and Mediterranean[25] krill (Meganyctiphanes norvegica) (Fig. 3),thus confirming that they were not caused by dissimilarities inlaboratory procedures.

However, a closer look of the data biplot (Fig. 2(a), Table 1)revealed a 7.77% overlap between the convex hull area of thetwo datasets, but not in the standard ellipses area.Interestingly, all the Mediterranean samples overlapping withthe Atlantic dataset came from a single individual (BP1) thatstranded at the core of the north-western Mediterraneanforaging area (Fig. 1). The discriminant analysis successfullyclassified all the samples as Atlantic or Mediterranean, exceptthose from whale BP1. The resulting discriminant functionwas X = –3.74 + (1.84d15N + 0.7d13C) and the statisticsthat this function produced for the eastern North Atlantic

wileyonlinelibrary.com/journal/rcmJohn Wiley & Sons, Ltd.

3

Figure 3. Stable isotope ratios in fin whales and krill. Atlantic fin whales (whitetriangles), Mediterranean fin whales (black triangles), Atlantic Krill (whitecircles) and Mediterranean Krill (black circles). Krill samples are corrected forthe baleen plate enrichment factor determined by Borrell et al.[24] Error barsshow standard deviation.

Table 1. Origin, mean, minimum and maximum values of d15N and d13C measured on baleen plates. A–E: Caneliñas (Spain),BP1, BP2, BP9: Toulon (France), BP3–BP7: Port La Nouvelle (France), BP8, BP10: Málaga (Spain)

Reference Baleen

d15N (%) d13C (%)

Origin Mean � sd Min. Max. Mean � sd Min. Max.

This study A/B/C/D/E Eastern North Atlantic 9.92 � 0.5 8.57 10.76 –17.31 � 0.46 –18.48 –15.91Bentaleb et al.[12] BP1 Mediterranean Sea 9.43 � 0.25 8.9 9.95 –18.04 � 0.22 –18.55 –17.75

BP2- BP10 Mediterranean Sea 7.37 � 0.51 6.32 8.68 –18.20 � 0.39 –19.32 –16.98All baleens (BP) Mediterranean Sea 7.55 � 0.77 6.32 9.95 –18.19 � 0.39 –19.32 –16.98

J. Giménez et al.

1804

population were: centroid (mean): 2.41; standard deviation:0.99; ranges: –0.38 to 4.26, and for the Mediterraneanpopulation: centroid (mean): –2.92; standard deviation: 1.00;ranges: –5.03 to –0.66. Accordingly, when the analysis wasrepeated with whale BP1 excluded, the Atlantic andMediterranean whales did not exhibit any overlap in theirstable isotopic values either in the convex hull or in thestandard ellipses area (Fig. 2(b)).

DISCUSSION

The present study clearly shows that isotopic values, both ford15N and d13C, were higher in the Atlantic individuals than inthose from the Mediterranean Sea. In the case of d15N thiscould be explained by the two subpopulations feeding atdifferent trophic levels, because the nitrogen stable isotopeincreases at each trophic level.[19] This effect should bediscarded because the main prey of fin whales in both areasis almost exclusively Meganyctiphanes norvegica (for theAtlantic Ocean[1,24,27]; for the Mediterranean Sea[3,23,28]).Therefore, this difference can be more reasonably attributed

wileyonlinelibrary.com/journal/rcm Copyright © 2013 John Wile

to different isotopic baselines between the two areas. Grahamet al.[22] produced marine carbon and nitrogen isoscapes forthe Atlantic Ocean based on a meta-analysis of publishedplankton d13C and d15N values and, according to their maps,both d15N and d13C are higher in the northeast Atlantic thanin the Mediterranean Sea, thus matching the differencesfound here. This scenario is further supported by the isotopicvalues in other taxa such as squids[29] or determined directlyin samples ofM. norvegica from the two areas (for the AtlanticOcean[24] and for the Mediterranean Sea[25]) which, afterhaving been corrected for the baleen plate enrichmentfactor determined by Borrell et al.,[22] also matched the resultshere obtained (Fig. 3). Nevertheless, differences betweenthe Atlantic and the Mediterranean are larger and moreconsistent for d15N than for d13C values, both forM. norvegica[12,24,25] and whales (this study).

The only exception to this general rule was onewhale analyzed by Bentaleb et al.[12] that stranded in theMediterranean (BP1) and whose isotopic values matchedbetter the Atlantic than the Mediterranean baselines. Becausethis whale had been sampled about 15 years before theother Mediterranean sampled individuals, Bentaleb et al.[12]

y & Sons, Ltd. Rapid Commun. Mass Spectrom. 2013, 27, 1801–1806

Limited exchange between Mediterranean and Atlantic fin whales

180

proposed that these higher d15N values might reflect atemporal change in the Mediterranean d15N baseline.However, in our statistical analyses the discriminant functionassigned this controversial individual with reliability to theAtlantic subpopulation. Moreover, the convex hull and thestandard ellipses analyses performed to define trophic nichesimilarly matched it to the Atlantic subpopulation (Fig. 2).Further, if this particular individual is examined in moredetail it can be seen that the most recently formed part ofthe baleen plate had the most depleted value of 15N in thewhole plate and, indeed, that value fell within the typicalvalues found in the Mediterranean individuals. Thissuggested that the newly formed layers in the baleen platewere in the process of acquiring the Mediterranean signature,indicating a recent transit into Mediterranean waters. As aconsequence, all evidence indicates that BP1 was indeed anAtlantic individual that migrated into the MediterraneanSea and stranded soon after on the coast of France.Two individuals (BP8 and BP10) which stranded on the

coast of Malaga, i.e. in the south-western Mediterranean,matched the isotopic values of Mediterranean whalesalthough the values of one of them (BP10) were close to theAtlantic dataset. It has been proposed that fin whales visitingthis area would indeed be part of the Atlantic subpopulationbecause the acoustic parameters detected by archival bottom-mounted audio recorders matched those attributable to thenorth-eastern North Atlantic subpopulation,[13] so if thesetwo individuals actually originated from the Atlantic stockthey would have had to be foraging in the MediterraneanSea for at least 2 years, the approximate period recorded inthe baleen plates analysed.Thus, the information previously available and the results

here presented all concur to confirm the existence of twodifferentiated subpopulations occurring in the temperateeastern Atlantic Ocean and the Mediterranean Sea, althoughthe border between them may be not as definite as theacoustic investigations suggested.[13] Thus, the collectiveevidence of at least some individuals with stable isotopicvalues characteristic of the Atlantic found in thenorthernmost western Mediterranean Sea, the results fromgenetic studies pointing to the existence of some limitedexchange,[5] and the movement of one individual tagged witha satellite mark in the Mediterranean that crossed the Straitsof Gibraltar and reached the Atlantic coast of centralPortugal,[11,12] all confirm the occurrence of recurrentexchange between the subpopulations inhabiting these twowater masses.The actual distribution ranges are in both cases difficult to

determine. The Mediterranean subpopulation is known tomainly feed in the Ligurian Sea and in the northern zone ofthe Balearic Islands during the summer but afterwards it isthought that it would disperse around the southernMediterranean with individuals conducting during thewinter sporadic incursions to de Gulf of Cadiz, the centralcoast of Portugal or even further north. The ranges of thetemperate eastern North Atlantic subpopulation are moreuncertain, particularly because the very own identity andcomposition of the subpopulation is unclear. The regionwitnessed a severe whaling period during 1921–1927 thatresulted during the few years of exploitation in the catch ofover 6000 individuals.[30] The Gulf of Cadiz, whereobservational records from nineteenth century open-boat

Copyright © 2013Rapid Commun. Mass Spectrom. 2013, 27, 1801–1806

whalers show that the species was originally veryabundant,[31] sustained the bulk of the catch. Afterwards, finwhales almost vanished from the area; subsequent whalingoperations there focused on the sperm whale, with onlymarginal catches of fin whales and, even today, after sevendecades have passed from the last removals, the densityappears to be extremely low.[14,15] However, further north,off the coast of Galicia (NW Spain), whaling was conductedon a clearly more robust subpopulation until 1985, when aglobal moratorium on commercial whaling was establishedby the International Whaling Commission.[30] The distincttrajectory of the subpopulations occupying the two temperateeastern North Atlantic areas has been taken as suggestive ofthem being independent stocks, with the one occupying theGulf of Cadiz having been wiped out by the massiveremovals made in the 1920s.[32] The few individuals that arenowadays seen in the area or crossing the Gibraltar Straitsare thought to be either the negligible remains of the originallocal subpopulation of the Gulf of Cadiz or stragglers fromother neighbouring subpopulations.

Results from this study have proved the previouslyaccepted separation between Atlantic and Mediterranean finwhale subpopulations, but also confirmed that some Atlanticindividuals wander into the Mediterranean Sea and thattherefore the subpopulation borders are not as strict aspreviously thought.[13] This is of relevance to the conservationand management of the species. The discriminant functionobtained in this study may assist researchers to use baleenplate isotopic data to assign the origin of fin whales ofuncertain provenance. Further research is needed to moreprecisely determine the degree of connectivity between thesubpopulations and the actual location of their boundaries.Stable isotope studies conducted in combination withgenetics, particularly on fin whales sampled at the GibraltarStraits and neighbouring areas from where potentialstragglers may stem from, may assist in establishingdemographic structure, as has been the case with otherbalaenopterid species.[33]

AcknowledgementsThe baleen plates analysed in the present study wereprovided by the Environmental Tissue Bank of the Universityof Barcelona. Funding for the isotope analyses was providedby the Fundació Barcelona ZOO. Special thanks are due toIsabel Afán and David Aragonés from Laboratorio deSistemas de Información Geográfica y Teledetección, EstaciónBiológica de Doñana, CSIC (LAST-EBD) for their advice andhelp with the map.

REFERENCES

[1] Å. Jonsgård. Biology of the North Atlantic fin whaleBalaenoptera physalus (L.): Taxonomy, distribution, migrationand food. Hvalradets Skrifter. 1966, 49, 1.

[2] International Whaling Commission. Report of the WorkingGroup on North Atlantic Whales. Reports of the InternationalWhaling Commission. 1977, 27, 369.

[3] G. Notarbartolo di Sciara, M. Zanardelli, M. Jahoda,S. Panigada, S. Airoldi. The fin whale Balaenoptera physalus(L. 1758) in theMediterranean Sea.Mammal. Rev. 2003, 33, 105.

wileyonlinelibrary.com/journal/rcmJohn Wiley & Sons, Ltd.

5

J. Giménez et al.

1806

[4] M. Bérubé, A. Aguilar, D. Dendanto, F. Larsen,G. Notarbartolo di Sciara, R. Sears, J. Sigurjónsson, J. Urban-R,P. J. Palsbøll. Population genetic structure of NorthAtlantic, Mediterranean Sea and Sea of Cortez fin whales,Balaenoptera physalus (Linnaeus 1758): analysis ofmitochondrial and nuclear loci. Mol. Ecol. 1998, 7, 585.

[5] P. J. Palsbøll,M. Bérubé, A. Aguilar, G. Notarbartolo di Sciara,R. Nielsen. Discerning between recurrent gene flow andrecent divergence under a finite-site mutation modelapplied to North Atlantic and Mediterranean sea finwhale (Balaenoptera physalus) populations. Evolution2004, 58, 670.

[6] A. Aguilar, A. Borrell, P. J. H. Reijnders. Geographical andtemporal variation in levels of organochlorine contaminantsin marine mammals. Mar. Environ. Res. 2002, 53, 425.

[7] International Whaling Commission. Report of the JointNAMMCO/IWC Scientific Workshop on the Catch History,Stock Structure and Abundance of North Atlantic FinWhales, Reykjavík, 23–26 March 2006. J. Cetacean Res.Manage. 2007, 9(suppl), 451.

[8] International Whaling Commission. Report of the FirstIntersessional RMP Workshop on North Atlantic FinWhales. J. Cetacean Res. Manage. 2009, 11(suppl), 425.

[9] Report of the Joint ACCOBAMS/Pelagos Workshop on Fin Whalesin the Mediterranean Sea, (Eds: S. Panigada, G. Donovan,C. Guinet), Monaco, 12–13 November, 2005.

[10] R. Reeves, G. Notarbartolo di Sciara. The status anddistribution of cetaceans in the Black Sea and MediterraneanSea. IUCN Centre for Mediterranean Cooperation, Malaga,Spain, 2006.

[11] C. Cotté, C. Guinet, I. Taupier-Letage, B. Mate, E. Petiau.Scale-dependent habitat use by a large free-rangingpredator, the Mediterranean fin whale. Deep-Sea Res.(1 Oceanogr. Res. Pap.). 2009, 56, 801.

[12] I. Bentaleb, C. Martin, M. Vrac, B. Mate, P. Mayzaud,D. Siret, R. de Stephanis, C. Guinet. Foraging ecology ofMediterranean fin whales in a changing environmentelucidated by satellite tracking and baleen plate stableisotopes. Mar. Ecol. Prog. Ser. 2011, 438, 285.

[13] M. Castellote, C. W. Clark, M. O. Lammers. Fin whale(Balaenoptera physalus) population identity in the westernMediterranean Sea. Mar. Mamm. Sci. 2011, 28, 325.

[14] P. Gauffier, P. Verborgh, E. Andreu, R. Esteban, B. Medina,P. Gallego, R. de Stephanis. An update on fin whales(Balaenoptera physalus) migration through intense maritimetraffic in the Strait of Gibraltar. Paper SC/61/BC6 presentedto the International Whaling Commission ScientificCommittee, May 2009, Madeira, Portugal, 2009.

[15] P. Gauffier, M. Moral Cendón, A. Blasi, E. Carpinelli,C. Jiménez-Torres, J. Giménez, R. Esteban, R. de Stephanis,P. Verborgh. Winter presence of large cetaceans in the Straitof Gibraltar, 26th Annual Conference of the EuropeanCetacean Society, March 2012, Galway, Ireland, 2012.

[16] E. Gómez-Díaz, J. González-Solís, M. Peinado, R. D. M. Page.Phylogeography of the Calonectris shearwaters usingmolecular and morphometric data. Mol. Phylogenet. Evol.2006, 41, 322.

[17] M. Revelles, C. Carreras, L. Cardona, A. Marco,F. Bentivegna, J. J. Castillo, G. de Martino, J. L. Mons,M. B. Smith, R. Ciro. Evidence for an asymmetrical sizeexchange of loggerhead sea turtles between theMediterranean and the Atlantic through the Straits ofGibraltar. J. Exp. Mar. Biol. Ecol. 2007, 349, 261.

wileyonlinelibrary.com/journal/rcm Copyright © 2013 John Wile

[18] D. M. Schell, S. M. Saupe, N. Haubenstock. Naturalisotope abundances in bowhead whale (Balaena mysticetus)baleen: markers of aging and habitat usage. Ecol. Stud.1989, 68, 260.

[19] S. D. Newsome, M. T. Clementz, P. L. Koch. Using stableisotope biogeochemistry to study marine mammal ecology.Mar. Mamm. Sci. 2010, 26, 509.

[20] K. A. Hobson, F. F. Riget, P. M. Outridge, R. Dietz, E. Born.Baleen as a biomonitor of mercury content and dietaryhistory of North Atlantic minke whales (Balaenopteraacutorostrata): combining elemental and stable isotopeapproaches. Sci. Total Environ. 2004, 331, 69.

[21] S. H. Lee, D. M. Schell, T. L. McDonald, W. J. Richardson.Regional and seasonal feeding by bowhead whales Balaenamysticetus as indicated by stable isotope ratios. Mar. Ecol.Prog. Ser. 2005, 285, 271.

[22] B. S. Graham, P. L. Koch, S. D. Newsome, K. W. McMahon,D. Aurioles. Using isoscapes to trace the movements andforaging behavior of top predators in oceanic ecosystems, inIsoscapes: Understanding Movement, Pattern, and Process onEarth Through Isotope Mapping, (Eds: J. B. West, G. J. Bowen,T. E. Dawson, K. P. Tu), Springer Science + BusinessMedia B.V., 2010, pp. 299–318.

[23] M. Quevedo, R. Svanbäck, P. Eklöv. Intrapopulation nichepartitioning in a generalist predator limits food webconnectivity. Ecology 2009, 90, 2263.

[24] A. Borrell, N. Abad-Oliva, E. Gómez-Campos, J. Giménez,A. Aguilar. Discrimination of stable isotopes in fin whaletissues and application to diet assessment in cetaceans.Rapid Commun. Mass Spectrom. 2012, 26, 1596.

[25] L. Cardona, I. A. de Quevedo, A. Borrell, A. Aguilar.Massive consumption of gelatinous plankton byMediterranean apex predators. PloS one 2012, 7, e31329.

[26] A. L. Jackson, R. Inger, A. C. Parnell, S. Bearhop. Comparingisotopic niche widths among and within communities:SIBER–Stable Isotope Bayesian Ellipses in R. J. Anim. Ecol.2011, 80, 595.

[27] A. Aguilar. Fin whale, Balaenoptera physalus, in Encyclopediaof Marine Mammals, (2nd edn.), (Eds: F. Perrin, B. Würsig,J. G. M. Thewissen). Elsevier-Academic Press, Amsterdam,2009, pp. 433–437.

[28] G. Relini, L. Orsi Relini, A. Siccardi, F. Fiorentino, G. Palandri,G. Torchia, M. Relini, C. Cima, M. Cappello. Distribuzione diMeganyctiphanes norvegica e Balaenoptera physalus in MarLigure all’inizio della primavera. Biol. Mar. Medit. 1994, 1, 89.

[29] J. Navarro, M. Coll, C. Somes, R. J. Olson. Trophicniche of squids: Insights from isotopic data in marinesystems worldwide. Deep-Sea Res. II. 2013. DOI:10.1016/j.dsr2.2013.01.031.

[30] C. Sanpere, A. Aguilar. Modern whaling off the IberianPeninsula during the 20th Century. Rep. Int. Whal. Commn.1992, 42, 723.

[31] A. Aguilar, A. Borrell. Open-boat whaling on the Straits ofGibraltar ground and adjacent waters. Mar. Mamm. Sci. 2007,23, 322.

[32] P. J. Clapham, A. Aguilar, L. T. Hatch. Determining spatialand temporal scales for management: lessons from whaling.Mar. Mamm. Sci. 2007, 24, 183.

[33] E. W. Born, P. Outridge, F. F. Riget, K. A. Hobson, R. Dietz,N. �ien, T. Haug. Population substructure of North Atlanticminke whales (Balaenoptera acutorostrata) inferred fromregional variation of elemental and stable isotopicsignatures in tissues. J. Mar. Syst. 2003, 43, 1.

y & Sons, Ltd. Rapid Commun. Mass Spectrom. 2013, 27, 1801–1806