the latin american journal of aquatic · pdf filethe latin american journal of aquatic mammals...

ISSN 1676-7497

THE LATIN AMERICAN

JOURNAL OF AQUATIC

MAMMALS

Vol. 6, No. 2

December 2007Published by

Instructions for Authors are available at the website:http://www.solamac.org

Subscription rates for libraries and non-members of SOLAMAC are US$ 60.

LAJAM is distributed free of charge to members of SOLAMAC and SOMEMMA.

Copyright SOLAMAC.

The Latin American Journal of Aquatic Mammals is abstracted or indexed in:Cambridge Scientific Abstracts - ASFA 1 and Oceanic Abstracts - (http://www.csa.com); NISCSouth Africa (www.nisc.co.za); OneFish (http://onefish.org/id/161082); Zoological Record(http://www.biosis.org/products_services/zoorecord.html).

Exchange information:Universidade Estadual do Norte Fluminense Darcy RibeiroCentro de Biociências e Biotecnologia - BIBLIOTECAAvenida Alberto Lamego, 2000, Parque CalifórniaCampos dos Goytacazes, 28013-602 RJ BRAZILPhone/Fax: 55+ (22) 2726 1628E-mail: [email protected]

THE LATIN AMERICAN JOURNAL

OF AQUATIC MAMMALS

(LAJAM)

Volume 6

Number 2

DECEMBER

2007

RIO DE JANEIRO

LAJAM Rio de Janeiro v.6 n.2 p.121-208 December 2007

ISSN 1676-7497

The Latin American Journal of Aquatic Mammals

The Latin American Journal of Aquatic Mammals is published twice a year (June and December) in Rio deJaneiro, Brazil, by SOLAMAC (Latin American Society of Specialists in Aquatic Mammals) and SOMEMMA(Mexican Society for the Studies of Marine Mammals). Print run: 800 copies.

Financial support:

The Latin American Journal of Aquatic Mammals – LAJAM – Vol. 1, n.1 (2002) – Rio de Janeiro: Sociedade Latino-americana de Especialistas em Mamíferos Aquáticos – SOLAMAC, 2002 – Semestral ISSN 1676-7497

1. Mamíferos aquáticos – América Latina – Periódicos I. Sociedade Latino-americana de Especialistas em Mamíferos Aquáticos.

CDD 599.5098

Cover drawing

José Vázquez Mazzini

Graphic project

Lia Ribeiro ([email protected])

Printed in Brazil

U.S. MARINEMAMMAL

COMMISSION

Editor-in-chief

Nélio B. Barros([email protected])

Portland State University,Portland, USA

Assistant Editor

Daniel M. Palacios([email protected])

National Oceanic and AtmosphericAdministration, Pacific Grove, CA, USA

Managing Editor

Salvatore Siciliano([email protected])

Fundação Oswaldo Cruz,Rio de Janeiro, Brazil

Associate Editors

Alexandre N. ZerbiniNational Oceanic and Atmospheric

Administration, Seattle, USA

Enrique A. CrespoCentro Nacional PatagónicoPuerto Madryn, Argentina

Koen Van WaerebeekPeruvian Centre for Cetacean

Research, Pucusana, Peru

Jorge Urbán RamírezUniversidad Autónoma de BajaCalifornia Sur, La Paz, Mexico

Marie-F. Van BressemCetacean Conservation Medicine

Group, Starnberg, Germany

Editorial Board

Carlos Alvarez-FloresOkeanus Consultores en Conservación

y Desarrollo Marino, Ensenada, Mexico

Julio ReyesAreas Costeras y Recursos Marinos

Pisco, Peru

Mônica MuelbertFundação Universidade Federal do

Rio Grande, Rio Grande, Brazil

Carlos OlavarriaCentro de Estudios del

Cuaternario, Punta Arenas, Chile

Lilián Flórez-GonzálezFundación Yubarta

Cali, Colombia

Paul G. KinasUniversidade Federal do RioGrande, Rio Grande, Brazil

Christoph RichterQueen’s University,Kingston, Canada

Lorenzo Rojas-BrachoInstituto Nacional de Ecología

Ensenada, Mexico

Paulo César Simões-LopesUniversidade Federal de SantaCatarina, Florianópolis, Brazil

David Aurioles GamboaInstituto Politecnico Nacional,

La Paz, Mexico

Luciana MöllerMacquarie University

Sydney, Australia

Ricardo BastidaUniversidade Nacional de Mar del

Plata, Mar del Plata, Argentina

Diane GendronInstituto Politécnico Nacional

La Paz, Mexico

Luciano Dalla RosaUniversity of British Columbia

Vancouver, Canada

R. Natalie P. GoodallCentro Austral de InvestigacionesCientíficas, Ushuaia, Argentina

Fernando C. W. RosasInstituto Nacional de Pesquisas da

Amazônia, Manaus, Brazil

Luis A. PasteneInstitute of Cetacean Research

Tokyo, Japan

Rodrigo Hucke-GaeteUniversidade Austral de Chile,

Valdivia, Chile

Fernando Félix GrijalvaFundación Ecuatoriana para elEstudio de Mamíferos Marinos

Guayaquil, Ecuador

Marcos C. O. SantosUniversidade Estadual Paulista

“Júlio de Mesquita Filho”,Rio Claro, Brazil

Sheila M. SimãoUniversidade Federal Rural

do Rio de Janeiro,Seropédica, Brazil

Fernando TrujilloFundación Omacha,

Bogotá, Colombia

Mario A. CozzuolUniversidade Federal de MinasGerais, Belo Horizonte, Brazil

Silvana DansCentro Nacional Patagónico,Puerto Madryn, Argentina

John WangFormosa Cetus Research &

Conservation Group, Thornhill, Canada

Miriam MarmontelInstituto de Desenvolvimento

Sustentável Mamirauá, Tefé, Brazil

Vera Maria F. da SilvaInstituto Nacional de Pesquisas da

Amazônia, Manaus, Brazil

Mirtha LewisCentro Nacional PantagónicoPuerto Madryn, Argentina

Editor EmeritusEduardo R. Secchi

([email protected])Universidade Federal do Rio Grande - FURG

Rio Grande, Brazil

INSTRUCTIONS FOR AUTHORS

THE SCOPE

The Latin American Journal of Aquatic Mammals (LAJAM) will publish research on aquatic mammals in LatinAmerica, regardless of the nationality of the authors. Articles on techniques in which the region or nationalityof the authors is of no matter will also be accepted.

LANGUAGE

Manuscripts must be written in either “American” or “British” English; however, authors should be consistentalong the text. By using English as its official language, LAJAM will be more readily available, and of greaterrelevance, to the global aquatic mammal research community. Papers should normally be in the passivevoice unless an opinion needs to be clearly attributed to the authors. The abstract must also be written inEnglish, with an additional version in either Portuguese or Spanish also provided. It is recognized that Englishmay not be the first language for most authors. Therefore, the Editorial Board will work with the authors toensure that the paper is written in good English.

TYPES OF MANUSCRIPT

Articles report results of original research. They should normally not exceed 30 pages of text (Title page,Abstract, Keywords, Introduction, Materials and methods, Results, Discussion, Acknowledgements,References).

Notes are brief reports of original research. They should normally not exceed 14 pages of text. They may beorganized like articles, with formal headings, or preferably more simply (no headings except forAcknowledgements and References).

Reviews must address topics of general interest or current importance to the Latin American aquatic mammalresearch community. They should be synthetic in nature (i.e. summarize the topic), rather than present largeamounts of detailed information. Reviews will be considered for publication only after invitation by, oragreement with, the Editors.

Comments are short critiques of papers previously published in LAJAM. Authors of the original paper beingdiscussed will be invited to reply to these critiques.

Short Communications are brief reports of 1 or 2 paragraphs dedicated to inform about unusual sightings,strandings, incidental captures or other issues. Proof of species identification (such as photographs or detailedsketches of prominent or conspicuous features) must be provided.

FORMAT

Manuscripts should be typed in A4 paper, with double line spacing and all margins set to 2.5cm (1in). All textshould be typed using Times New Roman font of size 12. Headings should be in bold (e.g. Introduction). Ifadditional sub-headings are required, these should appear in italics (e.g. Data analysis).

PAGE NUMBERING should start at the Title page, with the page numbers appearing centred at the bottom of each page.

TITLE PAGE: should contain a concise and informative title, and a list of authors’ names and addresses. Thecorresponding author should be indicated, and an email address for that author, if available, should also beprovided. Keywords (in English) should also be stated.

ABSTRACT PAGE: Should contain an abstract in English, as well as a version in either Portuguese or Spanish.Abstracts should not exceed 350 words.

BODY OF THE MANUSCRIPT: Should contain the Introduction, Materials and methods, Results, Discussion,Acknowledgements, and References.

Please be brief in the Acknowledgements.

REFERENCES should be formatted according to the following examples:

DEMASTER, D.P., EDWARDS, E.F., WADE, P. AND SISSON, J.E. (1992) Status of dolphin stocks in the eastern tropicalPacific. Pages 1038-1050 in MCCULLOUGH, D.R. AND BARRETT, R.H. (Eds) Wildlife 2001: Populations. ElsevierScience Publishers Ltd., London.

DI BENEDITTO, A.P., RAMOS, R. AND LIMA, N.R. (2001) Os golfinhos: Origem, Classificação, Captura Acidental, HábitoAlimentar. 1.ed. Porto Alegre: Editora Cinco Continentes. v.1. 152 pp.

FERNANDEZ, S.P. (1992) Composicion de edad y sexo y parametros del ciclo de vida de toninas (Tursiops truncatus) varadasen el noroeste del Golfo de Mexico. M.Sc. Thesis. Insituto Tecnologico y de Estudios Superiores de Monterrey, CampusGuaymas. Guaymas, SON, Mexico. 109 pp.

GERPE, M., RODRÍGUEZ, D., MORENO, V.J., BASTIDA, R.O. AND DE MORENO, J.E. (2002) Accumulation of heavy metalsin the franciscana (Pontoporia blainvillei) from Provincia Buenos Aires, Argentina. The Latin American Journal ofAquatic Mammals 1 (special issue 1): 95-106.

LEATHERWOOD, S. AND REEVES, R.R. (Eds) 1990. The Bottlenose Dolphin. Academic Press, San Diego, CA, USA. 653 pp.

PALACIOS, D.M. AND MATE, B.R. (1996) Attack by false killer whales (Pseudorca crassidens) on sperm whales(Physeter macrocephalus) in the Galápagos Islands. Marine Mammal Science 12(3): 582-587.

SILVA, K.G. (2004) Os pinípedes no Brasil: ocorrências, estimativas populacionais e conservação. Ph.D. Thesis. FundaçãoUniversidade Federal do Rio Grande. Rio Grande, RS, Brazil. 242 pp.

Important note: abstracts can be quoted (just like personal communications can) and placed in footnotes. Theformat should be as follows:

Dalla Rosa, L., Secchi, E. R., Kinas, P. G., Santos, M. C. O., Zerbini, A. N. and Bassoi, M. (1999) Photo-identificationand density estimation of humpback whales in Antarctic waters. Page 43 in Abstracts, XIII Biennial Conference onthe Biology of Marine Mammals, 28 November – 3 December, Maui, HI, USA.

Only month and year are compulsory for conference dates in the reference. Full date (including days) ispreferable if available.

Citations of reports that are not peer-reviewed (i.e., “grey literature”) but can be obtained from a particularsource (e.g., NOAA, UNEP, IUCN, UNEP) should be included in the list of References; however, those thatare not readily available (e.g., Working documents, contract reports) should be presented as footnotes.

References containing more than two authors should appear in the text as, for example, Di Beneditto et al.(2001). When more than one reference is cited at a time, references should appear in chronological order (e.g.DeMaster et al., 1992; Palacios and Mate, 1996; Dalla Rosa et al., 1999; Di Beneditto et al., 2001; Gerpe et al.,2002). References from same year by an author should be cited as Vaz-Ferreira (1975a,b).

TABLES: Each table should be presented on a separate page, with the table caption placed at the top of thepage. Tables should be cited in the text as Table 1, Table 2, etc. Authors should try to ensure that as manytables as possible do not exceed 8.5cm in width, when printed in Times Roman 8pt (or similar). The maximumpermitted width of any table is 17.5cm.

FIGURES: Each figure should be presented on a separate page, with the figure caption placed at the bottom ofthe page. Figures should be cited in the text as Figure 1, Figure 2, etc.

PHOTOGRAPHS AND ARTWORK: The inclusion of photographs in a paper is very expensive. Therefore we onlypublish photographs that are an essential part of the paper (for example, photographs that would serve toconfirm the identification of a species which is extremely difficult to be positively identified at sea). Highquality black and white photographs are recommended. Color print photos will be at the authors’ expenses.

Whenever possible, please submit photographs and/or artwork in electronic format (e.g. .bmp, .tif). Tabulatedx,y data files should also be provided for graphs. This will allow, where necessary, graphs to be plotted in ourstandard style using Excel 8.0. Artwork is expensive. Where possible, single column artwork (width 8.5cm) ispreferred. The maximum allowable width is 17.5cm. Lettering should be in Arial, Helvetica or a similar font(10pt).

EQUATIONS: Authors are asked to submit equations created in either Microsoft Equation EditorÓ (the defaultsupplied with several word-processing packages, including Microsoft WordÓ and WordPerfectÓ) or its upgradecalled MathTypeÓ.

CETACEAN NAMES: Please use approved IWC (International Whaling Commission) common names in the text.For the sake of cultural values, regional names can be used if the international name is referred to at leastonce. Scientific names must be quoted after the first time the common name is mentioned. Afterwards itshould be left up to the authors and at the editor’s discretion (for instance, papers on taxonomy may need toquote scientific names several times). Scientific names must be placed in parentheses after the common name.

CAPITALS: examples are given below:

Area (when referring to official Area names – e.g. Area I, Franciscana Management Area, etc.), Sector, Division,Antarctic, South Atlantic Ocean, Northern Hemisphere, Scientific Committee, Table 1, Fig. 1, Chairman, Vice-Chairman, Blainville’s beaked whale and Commerson’s dolphin (i.e. where named after a person);

but

western South Atlantic, sub-committee, sub-Antarctic, humpback whale, bottlenose dolphin, etc.

NUMBERS, DATES, MAP REFERENCES: In the text numbers under 10 should be spelled out where used individually.Figures should be used for a sequence of quantities and in reference to percentages (where % rather thanpercent is used):

e.g. three humpback whales but 3% of humpback whales; 1 fin whale, 4 Bryde’s whales and 9 southern rightwhales were observed.

Numbers with four or more figures should have no spaces: e.g. 1328; 9369234; 1540.5

Decimal points should be indicated by full stops, not commas. Zeros should be included: e.g. 0.86

There should be no space between numbers and abbreviated units: e.g. 114cm, 16kgDates should be in the form: 12 March 1996 not April 14, 1977

Map references should be in the form: 32º05’S, 52º08’W or 32º05’00"S, 52º08’55"W

HYPHENS: should be used in compound adjectives preceding a noun, e.g. age-specific survival rates, length-specificmodel. But not where part of the compound adjective consists of a numeral, e.g. 8cm long testis, 35ppm water.

ABBREVIATIONS: Where the last letter of an abbreviation is the same as the last letter of the full word then no fullstop is necessary:

Capital abbreviations do not require full stops: e.g. IWC, FMA, MSYR, 25°S, CV, SD, SE etc.

Metric units are required. However, two widespread nautical units (i.e. knots and nautical miles) will beallowed. Commonly used abbreviations for quantities have no full stop: e.g. 10cm, 15m, 3nm, 15kt, etc.

Scientific names (e.g. Pontoporia blainvillei) must be originally written in full but may subsequently beabbreviated (e.g. P. blainvillei).

If a personal communication is used, abbreviate as ‘pers. comm.’.

ITALICS: Should be used for: references to titles of books and periodicals (e.g. Moby Dick); names of vessels (e.g.Ary Rongel, Atlântico Sul); Scientific names of plants and animals (e.g. Coprosma foetidissima); foreign words orabbreviations not part of everyday English (e.g. et al., i.e., e.g.); trade names (e.g. Serramalte).

QUOTATIONS: Use single quotation marks. Double quotation marks are only to be used for a quote within aquote. Within a quotation, follow the style and punctuation of the original. If omitting a section, indicate bythree full stops ‘…’. If interpolating a word or phrase please use square brackets [Editors’ italics].

EQUATIONS, MATHEMATICAL REFERENCES: Ensure that superscripts and subscripts are easily discernible. Clearlydistinguish between: the letter l and the number 1 (e.g. by underlining the letter); and the letter O and thenumber 0. Use italics for letters indicating parameters, e.g. y = a + bx

COPYRIGHT

Author(s) of a manuscript accepted for publication in LAJAM are automatically agreeing to have the copyrightof the manuscript transferred to SOLAMAC.

AUTHOR’S DECLARATION FORM

The corresponding author of a manuscript submitted to LAJAM should complete a copy of this declarationand enclose it with the submitted manuscript.

SUBMISSION OF MANUSCRIPTS

Manuscripts should be submitted electronically via e.mail to [email protected]. Files larger than 1.5MBshould be compressed or fragmented in different files. Manuscripts should be written using Microsoft Word©

or sent as a rich text format (.rtf) file. A printed copy of the Author’s Declaration Form, signed by thecorresponding author, should be mailed to:

THE MANAGING EDITOR

The Latin American Journal of Aquatic Mammals (LAJAM)Fundação Oswaldo Cruz – FIOCRUZ

Escola Nacional de Saúde Pública – ENSPDepartamento de Endemias, Laboratório de Ecologia

Rua Leopoldo Bulhões, 1480 - térreoManguinhos, Rio de Janeiro, RJ 21041-210, Brazil

Manuscripts will be reviewed by two referees, which will usually, but not necessarily, be members of LAJAM’sEditorial Board.

There are no page charges for articles published in LAJAM. Copy of the articles will be available for theauthors only in electronic format (e.g. .pdf).

Spanish and Portuguese versions of the Instructions for Authors can be obtained from SOLAMAC’s website(www.solamac.net).

LAJAM 6(2): 127-137, December 2007 ISSN 1676-7497

1 Laboratorio de Ecología, Comportamiento y Mamíferos Marinos - Museo Argentino de Ciencias Naturales “Bernardino Rivadavia”(CONICET), Av. Ángel Gallardo 470, C1405DJR, Buenos Aires. Argentina.

2 Estación Hidrobiológica de Puerto Quequén (MACN – CONICET), Quequén, Buenos Aires, Argentina.3 Acuario de Buenos Aires. Argentina.* Corresponding author, e-mail: [email protected] or [email protected] / 54-11-4984 6670 int 159 or 211.

INCIDENTAL MORTALITY OF FRANCISCANA DOLPHIN (PONTOPORIA BLAINVILLEI)IN ARGENTINA

HUMBERTO L. CAPPOZZO1, 2, *; MARIA F. NEGRI1; FABIÁN H. PÉREZ1;

DIEGO ALBAREDA3; FLORENCIA MONZÓN

2. AND JAVIER F. CORCUERA2.

ABSTRACT: La Plata River dolphin or franciscana, Pontoporia blainvillei, is an endemic small cetacean of the Southwest Atlanticcoast. It is threatened all along its distribution by a sustained high level of incidental mortality in fisheries. Here we assesslevels of franciscana bycatch in Argentine waters between 1997 and 2003. We surveyed 18 localities along the coast of theBuenos Aires Province, between General Lavalle (35°06’S, 57°08’W) and Bahía Blanca (Puerto Rosales-Ingeniero White harbour:38°47’S, 62°16’W). We recorded data on incidental mortality, fishing gears and fishing effort through 209 personal interviewswith fishermen. We estimated annual mortality, fishing effort and catch per unit of effort (CPUE) for each locality andperiod of time. Mortality was caused by gillnets and trawling gears, purse seine nets and shrimper gears. The total mortalityestimated for 1997-2000 was 354 dolphins/year (95% CI = 318-392) and 307 dolphins/year (95% CI = 273-343) for 2002-2003.In the entire survey, CPUE of the northern coast of Buenos Aires Province (Bahía Samborombón and Cabo San Antonio) wassignificantly higher than CPUE for the southern coast (from Mar del Plata to Bahía Blanca estuary). In addition, CPUE of thenorthern coast decreased significantly throughout the years. This study suggested that even though the gears or fleet behaviourchanged locally, Buenos Aires Province evidenced an overall mortality relatively constant during the survey. If we considera minimum of 400 dolphins killed each year in fishing gear and the estimated population values of 15000 individuals for theArgentine coast; mortality represent more than 2% of the Argentine franciscana population, suggesting that it would besubject to decline. Trends in mortality need to be periodically monitored in this area in order to articulate programs ofconservation for the species.

Resumen: El delfín del Río de la Plata o Franciscana, Pontoporia blainvillei, es un pequeño cetáceo endémico de la costa delAtlántico Sudoccidental. A lo largo de toda su distribución se encuentra amenazado por un alto nivel sostenido de mortalidadincidental en pesquerías. En este trabajo, se determinaron los niveles de captura incidental en aguas argentinas entre 1997 y2003. Se relevaron 18 localidades de la costa de la Provincia de Buenos Aires, entre General Lavalle (35°06’S, 57°08’W) y BahíaBlanca (Puerto Rosales-Ingeniero White: 38°47’S, 62°16’W). Se registró información de mortalidad incidental, artes de pesca yesfuerzo pesquero a través de 209 encuestas personales con pescadores. Se estimó mortalidad anual, esfuerzo pesquero ycaptura por unidad de esfuerzo (CPUE), para cada localidad y período de tiempo. La mortalidad fue ocasionada por redesagalleras y de arrastre, redes de cerco y camaroneras. La mortalidad total estimada para 1997-2000 fue de 354 delfines/año (CI95% = 318-392) y 307 delfines/año (CI 95% = 273-343) para 2002-2003. Durante todo el período de estudio, la CPUE de la costanorte de la provincia de Buenos Aires (Bahía Samborombón y Cabo San Antonio) fue significativamente más alta que la CPUEde la costa sur (desde Mar del Plata hasta el estuario de Bahía Blanca). Asimismo, la CPUE de la costa norte disminuyósignificativamente a través de los años. Este estudio sugirió que aún cuando las artes de pesca y el comportamiento de la flotacambiaron localmente, la Provincia de Buenos Aires evidenció una mortalidad total relativamente constante durante el períodode estudio. Si consideramos un mínimo de 400 delfines muertos por año en artes de pesca y los valores poblacionales estimadosde 15000 individuos para la costa argentina; la mortalidad representa más de 2% del stock de franciscanas de Argentina,sugiriendo que la población en este país sería vulnerable a declinar. Es necesario monitorear periódicamente las tendencias demortalidad y es urgente obtener información sobre la identidad de los stocks en esta área a fin de articular programas deconservación para la especie.

Keywords: Franciscana, Pontoporia blainvillei, incidental mortality, gillnet fisheries, southwest Atlantic Ocean.

Introduction

La Plata River dolphin or franciscana (Pontoporiablainvillei) is an endemic small cetacean frequentlycaught in fishing nets in the southwest Atlantic coast.The species occurs from southeastern Brazil (18°25’S;Siciliano, 1994) to, Golfo Nuevo, northern Patagonia(42°35’S, 64°48’W) (Crespo et al., 1998) and inhabits acoastal marine habitat, usually in waters up to 30m deepand approximately 25 to 30nm from shore (Praderi etal., 1989; Pinedo et al., 1989; Monzón and Corcuera,1991). Incidental capture of this species occurs all along

its geographical distribution (Corcuera, 1994; Secchi etal., 1997; Rosas et al., 2002). The bycatch in gillnets hasbeen reported in the Buenos Aires area since the mid1980s (Pérez Macri and Crespo, 1989). The southern areaof Buenos Aires Province (from Puerto Quequén-Necochea to Carmen de Patagones) was monitoredbetween 1988 and 1994 where an overall fishing-relatedmortality of 237 individuals per year (CI 95%: 208-269)was estimated (Corcuera, 1994), while the northern area(from Tigre, La Plata River Estuary, to Mar del Plata,Atlantic Ocean) was monitored in 1998 where an overallmortality of 228 individuals per year (CI 95%: 200-260)

128 H.L.CAPPOZZO et al.

LAJAM 6(2): 127-137, December 2007

was estimated (Corcuera et al., 20004). Previous studieshave shown that, in Argentina, artisanal vessels fromsmall fishing camps located along the coasts of BuenosAires Province pose more of a threat to franciscana thanthose based at large fishing harbours (Corcuera et al.,1994). Nevertheless, Bordino and Albareda (2004)5

estimated an annual mortality of about 410 dolphins inthe northern Buenos Aires Province and in 651 for theentire artisanal fleet in Buenos Aires.

Franciscana abundance was estimated recently at 14234individuals from aerial surveys for the Argentine coast(Crespo et al., 20066).

According to previous studies in the southern area, andcurrent data, some harbours show changes in thefishing gears so incidental mortality might differbetween years in each locality (Cappozzo et al.,19997; Corcuera et al., 20004). The aim of this studywas to estimate an annual incidental mortality offranciscana dolphin in waters off Buenos AiresProvince for the period 1997-2003.

Material and Methods

Fieldwork

We conducted three surveys between August 1997and March 2003 and interviewed 209 fishermenalong 18 localities in the Buenos Aires Province(Figure 1).

We considered as a fishing camp a non-permanentsettlement along the coast formed by fishermenwith 3-10 meter-long vessels dedicated to artisanalfishing, located farther from any harbour.

Data concerning fishing activities, such as fleet size,fishing gear, net length, mesh size and length offishing season, as well as an approximate numberof dolphins bycaught by different gears wereobtained by interviewing fishermen from alllocalities (Figure 1 and Table 1). The interviewswere conducted by one or two researchers twiceor three times per fishing season surveyed (atthe beginning, middle and end of each one). Theinformation obtained was also confirmed andcompleted with data recorded by the CoastGuard of Argentina (Prefectura Naval Argentina).

We have only considered the fishing vessels that wereoperating at the moment of the study.

Previous studies in southern Buenos Aires Provincehave used this method to obtain data on marinemammal incidental mortality (Pérez Macri and Crespo,1989; Corcuera et al., 1994; Crespo et al., 1994; Cappozzoet al., 19997). Nevertheless, in recent studies onboardobservers were implemented in order to validate theincidental mortality estimation by interviews (Bordinoand Albareda, 20045).

Between August 1997 and February 2000, 15 localitieswere monitored along the coast of Buenos Aires Provincewhere a high mortality had been previously detected.

4 Corcuera, J.F., Monzón, F., Cornejo, I., Pérez, J.E., Beilis, A., Gingarelli, M., Albareda, D. and Arias, A. (2000) Mortalidad de Pontoporiablainvillei en el norte de la Provincia de Buenos Aires. DT 25 in Report of the Third Workshop for Coordinated Research and Conservationof the Franciscana Dolphin (Pontoporia blainvillei) in the Southwestern Atlantic.

5 Bordino, P. and Albareda, D. (2004) Incidental mortality of Franciscana dolphin Pontoporia blainvillei in coastal gillnet fisheries in northernBuenos Aires, Argentina. Paper SC/56/SM11 presented at the International Whaling Commission Meeting, Sorrento, Italy, July 2004, 7pp.

6 Crespo, E. A., Pedraza, S. N., Grandi, M. F., Dans, S. L., Garaffo, G. (2006) Estimación de abundancia de Franciscana (Pontoporia blainvillei)en aguas argentinas e implicancias para su conservación. Page 15 in Abstracts, I Reunión Internacional sobre el Estudio de los MamíferosAcuáticos SOMEMMA-SOLAMAC, 5-9 November, Mérida, México.

7 Cappozzo, H. L., Monzón, F., Pérez, J. E. and Corcuera, J. F. (1999) Mortality of La Plata River Dolphin, Pontoporia blainvillei, in SouthernBuenos Aires Province, Argentina (1998): Big changes that change nothing. Page 52 in Abstracts, 13th Annual Conference of the EuropeanCetacean Society, 5-9 April, Valencia, Spain.

Figure 1: Study area with location of harbours (h) and fishing camps (fc)where dolphin mortality has been recorded along the coast of Buenos AiresProvince, Argentina. Northern area: 1- General Lavalle (h), 2- San Clementedel Tuyú (h), 3- Las Toninas (fc), 4- Santa Teresita (fc), 5- Mar del Tuyú (fc),6- Aguas Verdes (fc), 7- La Lucila del Mar (fc), 8- San Bernardo (fc), 9- Marde Ajó (fc), 10- Villa Gessell (fc); Southern area: 11- Mar del Plata (h), 12-13Quequén-Necochea (h), 14- Claromecó (fc), 15- Monte Hermoso (fc), 16-Villa del Mar (fc), 17- Puerto Rosales (h), 18- Ingeniero White (h).

INCIDENTAL MORTALITY OF FRANCISCANA DOLPHIN (PONTOPORIA BLAINVILLEI) IN ARGENTINA 129

LAJAM 6(2): 127-137, December 2007

Ta

ble

1:

Lo

cali

ties

(fi

shin

g c

am

ps fc

an

d h

arb

ou

rs h

) w

her

e fr

an

cisc

an

a m

ort

ali

ty h

as

bee

n s

tud

ied

alo

ng

Bu

eno

s A

ires

Pro

vin

ce c

oa

st i

n t

he

per

iod

19

97

-20

00

an

d2

00

2-2

00

3,

nu

mb

er o

f co

ast

al

ves

sels

per

fis

hin

g g

ear,

nu

mb

er o

f in

terv

iew

ed v

esse

ls a

nd

su

rvey

ed d

ay

s.

Ref

eren

ces

(FA

O f

ish

ing

gea

r co

des

): S

et g

illn

ets

(bG

NS

: b

ott

om

, m

GN

S:

mid

-wat

er),

Bo

tto

m t

raw

ls (

TB

B),

Mid

-wat

er t

raw

ls (

TM

), T

rap

s (F

IX),

Han

d d

red

ges

(D

RH

),L

on

gli

nes

(L

L),

Dri

ftn

ets

(GN

D),

Han

dli

nes

(L

HP

), O

ne-

bo

at o

per

ated

pu

rse

sein

es (

PS

1),

Tw

o-b

oat

op

erat

ed p

urs

e se

ines

(P

S2)

, S

hri

mp

tra

wls

(T

MS

), n

ot

spec

ifie

d (

NS

).

1997

-200

0 20

02-2

003

L

oca

liti

es

Gea

rs t

hat

ca

use

d m

ort

alit

y

(N o

f v

esse

l)

Gea

rs t

hat

did

no

t ca

use

mo

rtal

ity

(N

of

ves

sel)

To

tal

coas

tal

ves

sels

N o

f in

terv

iew

ed

ves

sels

N o

f su

rvey

ed

day

s

Gea

rs t

hat

cau

sed

m

ort

alit

y

(N o

f v

esse

l)

Gea

rs t

hat

did

n

ot

cau

se

mo

rtal

ity

(N

of

ves

sel)

To

tal

coas

tal

ves

sels

N

of

inte

rvie

wed

v

esse

ls

N o

f su

rvey

ed

day

s

1 G

ener

al L

aval

le (

h)

bG

NS

(3)

, TB

B

(13)

-

16

16

11

- -

- -

-

2 S

an C

lem

ente

del

T

uy

u (

h)

bG

NS

(6)

, TB

B

(12)

-

18

18

13

bG

NS

(3)

, TB

B (

2)

NS

(10

) 15

3

1

3 L

as T

on

inas

(fc

) b

GN

S (

3)

LH

P (

1)

3 3

7 b

GN

S (

2)

LL

(1)

2

2 3

4 S

anta

Ter

esit

a (f

c)

bG

NS

(4)

L

HP

(4

) 4

4 8

bG

NS

(2)

L

L (

2)

3 2

1

5 M

ar d

el T

uy

ú (

fc)

bG

NS

(4)

L

HP

(3)

4

4 7

bG

NS

(2)

, TB

B (

1)

LL

an

d L

HP

(2)

4

3 1

6 A

gu

as V

erd

es (

fc)

bG

NS

(1)

-

1 1

3 -

- -

- -

7 L

a L

uci

la d

el M

ar

(fc)

b

GN

S (

1)

- 1

1 5

bG

NS

, mG

NS

, TM

-

1 1

1

8 S

an

Ber

nar

do

(fc

) b

GN

S (

3)

TB

B (

1), L

HP

(2)

3

3 7

bG

NS

(2)

, mG

NS

(2

), T

BB

an

d T

M (

2)

- 2

2 1

9 M

ar d

e A

jó (

fc)

bG

NS

(5)

T

BB

(1)

, LH

P (

3),

LL

(1)

, GN

D (

1)

5 5

8 b

GN

S (

3), m

GN

S

(1),

TM

(1)

-

3 3

1

10

Vil

la G

esel

l (f

c)

- -

- -

- b

GN

S (

2), m

GN

S

(2),

TM

(2)

L

L (

1)

2 2

1

11

Mar

del

Pla

ta (

h)

bG

NS

(10

), P

S1

and

PS

2 (8

0)

- 90

19

3

bG

NS

, mG

NS

, TB

B

and

TM

(58

)

FIX

(2)

, LH

P (

3)

and

PS

1 an

d

PS

2 (7

0)

85

38

17

12

13

Qu

equ

én -

N

eco

chea

(h

) b

GN

S (

4)

TB

B a

nd

TM

(18

) 22

7

9 b

GN

S a

nd

TB

B (

3)

NS

(6)

9

6 3

14

Cla

rom

ecó

(fc

) b

GN

S (

5)

TB

B a

nd

FIX

(4)

9

3 5

bG

NS

(10

) F

IX a

nd

DR

H

(5)

15

9 16

15

Mo

nte

Her

mo

so

(fc)

b

GN

S (

12)

NS

(18

) 30

11

6

b

GN

S (

9)

FIX

, LH

P

and

TB

B (

44)

53

14

3

16

Vil

la d

el M

ar (

fc)

TM

S (

2)

NS

(5)

7

3 5

bG

NS

(9)

-

9 9

1

1718

- P

uer

to R

osa

les

- In

gen

iero

Wh

ite

(h)

bG

NS

(3)

, TM

S

(53)

-

56

13

5 b

GN

S (

59)

and

TM

S

(1)

- 60

5

3

T

OT

AL

22

4 45

26

9 11

1 10

2 16

9 94

26

3 99

53


LAJAM 6(2): 127-137, December 2007

Catch per Unit of Effort (CPUE) was estimated for allgears within each locality. The CPUE was calculated asthe mortality (M) of the locality divided by the fishingeffort (FE) of the same place.

CPUE= (M / FE) * 1000

CPUE CI were obtained by dividing the CI of M by theFE recorded for the respective year and locality(Corcuera et al., 1994).

In order to estimate the total mortality and CPUE forthe Buenos Aires Province, we pooled data from 1997-1998 and 1998-2000, as the information of Mar delPlata harbour was available only from 1997-1998. Forthe northern coast (localities 1-9) we computed themean mortality estimated for the period 1997-1998and 1998-2000.

Additionally, the estimated M and CPUE of eachsurveyed period and area (northern and southern coast)were compared with a non-parametric test as KruskalWhalis, considering only the localities consistentlymonitored.

Results

Table 1 shows the localities surveyed, whether they wereworking as a fishing harbour or fishing camps for theperiod 1997-2000 and 2002-2003, the number of coastaloperating vessels, the number of vessels interviewed,the gears used and whether there was franciscanabycatch in any one of them, and for how long eachlocality was surveyed.

In the localities surveyed, mortality was caused at leastin one period, by bottom and mid-water gillnets, bottomand mid-water trawls, shrimpers and purse seines(Table 1).

From the 263 vessels operating in the study area in 1997-2000, 89 operated with bottom gillnet and/or trawlinggears (see Table 1), 80 fished with purse seines, 55 usedshrimper and the remaining 45 vessels operated withother fishing gears not involved in Franciscanaincidental mortality (e.g. long lines, handlines, sportfishing lines, and traps).

From the 263 vessels operating in the study area in 2002-2003, 162 operated with bottom and mid-water gillnetand trawling gears, one used shrimper gears and theremaining 94 vessels operated with others fishing gearsnot involved in franciscana incidental mortality, suchas longlines, handlines, purse-seines nets and traps(Table 1).

Mortality estimates

For each locality and period surveyed, the estimatedmortality, fishing effort and catch per unit of effort areshown in Tables 2, 3 and 4 respectively, in comparisonwith data of 1992-1993 from Corcuera (1994).

These localities include five fishing harbours: GeneralLavalle (fishing location 1), San Clemente del Tuyú (2),Mar del Plata (11), Quequén-Necochea (12-13) andPuerto Rosales-Ingeniero White (17-18); and 10 fishingcamps: Las Toninas (3), Santa Teresita (4), Mar delTuyú (5), Aguas Verdes (6), La Lucila del Mar (7), SanBernardo (8), Mar de Ajó (9), Claromecó (14), MonteHermoso (15) and Villa del Mar (16) (Figure 1).

Between September 2002 and March 2003, the localitiesmonitored were 14 including four fishing harbours(localities 2, 11, 12-13 and 17-18) and 10 fishing camps(localities 3-5, 7-10, 14-16) (Figure 1, Table 1).

We interviewed 110 fishermen in 1997-2000 and 99 in2002-2003 who were present in the harbours and fishingcamps. We have considered localities between GeneralLavalle (1) and Villa Gessell (10) as the Northern Coastand localities between Mar del Plata (11) and PuertoRosales-Pto. Ingeniero White (17-18) as the Southern Coast.

We assumed that the bycatch rate of franciscana estimatedfor monitored boats was the same as for unmonitoredones in the same locality for the same fishing gear.

Analysis Methods

We estimated the Fishing Effort (FE), the annualMortality (M) and the Capture per Unit of Effort (CPUE)in each locality.

To calculate the gillnet fishing effort (FE) of a localitywe used the following variables: number of boats (N),mean number of days of active fishing operations (D),and total length of gillnets used during the fishingseason by a single boat, in km (K). The formula appliedto obtain FE is:

FE = N*D*K

The shrimper is a different sort of gear in which a funnel-shaped net with walls and anchors is set at a stationarytide and is recovered before the next stationary tide (Crespoet al., 1994). To calculate FE for the bottom shrimpers atIngeniero White-Puerto Rosales and Villa del Mar we used:

FE = N*m*C

where m is months of active fishing operations and C isnumber of nets.

Because in some localities the recorded data wereobtained from partial surveys, we adjusted each meanof M and its confidence intervals (CI) to account for boththe number of boats and fishing season days notmonitored as a straight proportional correction. M CIwere calculated for each estimate using a Poisson model(Zar, 1996) following Corcuera et al. (1994) in order toallow comparisons with previous studies:

Upper M CI = χ2(0.025, 2(c+1))2

Lower M CI = χ2(0.975, 2c) 2

where c is number of animals bycaught.


LAJAM 6(2): 127-137, December 2007

Bahía Samborombón

This area includes two of the localities surveyed thatcaused incidental mortality: General Lavalle and SanClemente del Tuyú. All the 34 vessels operating inBahía Samborombón were interviewed in 1997-2000.Most of the fishermen used bottom trawls (Table 1). In2000 only three boats from General Lavalle and sixfrom San Clemente del Tuyú were operating withgillnets that were set for three months, from Octoberto December. According to our interviews each vesselsets 300-700 metres of net with a mesh size of 16cm.Their target species was the white croacker(Micropogonias furnieri).

During 2002-2003, the black drum (Pogonias cromis) wasalso targeted in gillnet fisheries with mesh sizes of 27and 30cm operating from San Clemente del Tuyú.

In General Lavalle mortality estimates were always

low, but the fishing effort increased from 1997-1998 to1998-2000.

San Clemente del Tuyú showed the highest mortalitylevels of all sampled periods. In 1998-2000 it wascaused by the only three vessels operating withbottom gillnets. The fishing effort was nearly the sameduring 1997-2000, but the CPUE was quite different.From six vessels causing this high mortality, the onecausing the greatest incidental catch (64%) is nolonger using this gear but changed to longline. Onthe other hand, in 2002-2003 the fishing effortincreased almost three times compared to theprevious periods and the catch per unit of effortdecreased.

Cabo San Antonio

Cabo San Antonio is an extensive coast only small

1992-1993 1997-1998 1998-2000 2002-2003

LOCALITIES M CI min

CI max

M CI min

CI max

M CI min

CI max

M CI min

CI max

1 General Lavalle - - - 1.00 0.03 5.57 3.00 0.60 9.50 - - -

2 San Clemente del Tuyu - - - 58.00 44.40 74.98 94.00 75.90 115.00 127.50 106.35 151.65

3 Las Toninas - - - 21.00 13.00 32.10 16.00 9.10 26.00 4.00 1.09 10.24

4 Santa Teresita - - - 27.00 17.79 39.28 21.00 13.00 32.10 7.50 3.13 15.10

5 Mar del Tuyú - - - 16.20 9.15 25.94 19.50 11.80 30.30 8.00 3.45 15.77

6 Aguas Verdes - - - 5.25 1.91 12.37 - - - - - -

7 La Lucila del Mar - - - 3.50 0.85 9.51 4.00 1.10 10.20 12.00 6.20 20.96

8 San Bernardo - - - 14.00 7.65 23.49 26.00 17.00 38.10 19.00 11.44 29.67

9 Mar de Ajó - - - 49.00 36.25 64.78 25.00 16.20 36.90 17.00 9.91 27.22

10 Villa Gesell - - - - - - - - - 6.00 2.20 13.06

11 Mar del Plata - - - 15.00 8.40 24.74 - - - 42.50 30.70 57.35

12 13

Quequén - Necochea 4.70 1.40 11.00 - - - 13.00 6.90 22.20 0.00 0.00 3.69

14 Claromecó 34.00 23.50 47.50 - - - 7.50 3.10 15.10 3.33 0.77 9.27

15 Monte Hermoso 91.50 73.70 112.30 - - - 30.00 20.20 42.80 11.78 6.05 20.68

16 Villa del Mar 14.00 7.70 23.50 - - - 1.00 0.00 5.60 0.00 0.00 3.69

17 18

Puerto Rosales - Ingeniero White

85.50 68.30 105.70 - - - 83.00 66.10 102.90 48.00 35.39 63.65

TOTAL 229.70 200.77 261.19 209.95 182.09 239.87 343.00 307.66 381.29 306.61 273.15 342.81

Table 2: Mortality (M) detected in the periods 1992-1993, 1997-1998, 1998-2000 and 2002-2003 in each locality, see Map and text for details.

The 95% confidence limits intervals are shown.


LAJAM 6(2): 127-137, December 2007

fishing camps including: Las Toninas, Santa Teresita,Mar del Tuyú, Aguas Verdes, La Lucila del Mar, SanBernardo and Mar de Ajó. Although the number ofsmall vessels using gillnets in the entire area wassimilar along the periods, the fishing camp of AguasVerdes no longer operates since 1998 and there wereslight differences per locality. The fishing ground ofthese small fishing camps overlapped with those ofneighboring localities. Fishermen used exclusivelygillnet and trawling gears and targeted several species(sharks, teleosts, rays) setting approximately 200m ofnet/day of a mesh size of 12, 14 or 15cm. They weregenerally active in spring and summer and the catchwas usually sold to tourists. Although incidentalcatches of franciscana decreased during the surveys,mortality for the entire area was high between 1997and 2000, with more than 100 dolphins incidentallycaught each year. However, in 2002-2003 it was lower.Effort was lower in 1998-2000 in comparison to theprevious survey (1997-1998). In contrast, the fishingeffort was higher in 2002-2003 despite the fewernumber of vessels. Mortality levels have shown to behigher in Mar de Ajó, followed by Santa Teresita, andSan Bernardo in 1997-2000. On the other hand, in2002-2003, San Bernardo showed the highest mortalityfollowed by Mar de Ajó and La Lucila del Mar. TheCPUE of the entire area decreased throughout theyears.

Mar del Plata

This is an important harbour with a large fleet of up to90 artisanal vessels in 1997-1998. Most of them operatedwith purse-seine nets, and only some of them withgillnets. At this harbour mortality was associated withpurse-seines, where nets were operated by two co-operating vessels being the mackerel (Scomberjaponicus) and anchovies (Engraulis anchoita) their targetspecies (see Table 1). The fishing season was short, fromOctober to November. During 2002-2003, 85 vesselswere recorded in the harbour, most of them (see Table1) operating with gillnets targeting sharks, which wereresponsible for the incidental mortality of franciscana.In contrast, in this last period, no bycatch wererecorded in purse seine nets. The mortality increasedbecause of the great increase of gillnets fishing effort.

Puerto Quequén - Necochea

During 1998-2000, 82% of the coastal vessels (n = 18,see Table 1) were operating with bottom and mid-watertrawling and no franciscana was killed in this kind ofgear. There were only four vessels operating withgillnets targeting sharks which set 2500m of net/dayduring spring months. Thirteen dolphins were killedin 1998-2000 but no dolphin was caught by the ninevessels recorded during the 2002-2003 survey.

FISSHING EFFORT

LOCALITIES 1992-1993 1997-1998 1998-2000 2002-2003

1 General Lavalle - 9.30 63.00 -

2 San Clemente del Tuyu - 137.50 129.00 384.00

3 Las Toninas - 70.80 67.38 72.00

4 Santa Teresita - 26.25 59.94 114.00

5 Mar del Tuyú - 15.75 57.32 64.50

6 Aguas Verdes - 19.00 - -

7 La Lucila del Mar - 15.75 23.60 63.00

8 San Bernardo - 45.00 31.50 105.00

9 Mar de Ajó - 115.80 54.44 79.80

10 Villa Gesell - - - 162.00

11 Mar del Plata - 450.00 - 2550.00

12 13

Quequén - Necochea 1215.00 - 445.20 1000.00

14 Claromecó 724.50 - 63.00 160.00

15 Monte Hermoso 178.40 - 180.00 1344.00

16 Villa del Mar 187.50 - 94.50 108.00

17 18

Puerto Rosales - Ingeniero White 2038.50 - 6720.00 2160.00

TOTAL 4343.90 905.15 7988.88 8366.30

Table 3: Fishing effort detected in the periods 1992-1993, 1997-1998, 1998-2000 and 2002-2003 in each locality, see Map and textfor details.


LAJAM 6(2): 127-137, December 2007

Claromecó

In this small fishing camp there were 4-5 small vessels10-meter long operating with traps and hand dredgesduring the entire survey. The other 5-10 boats 5-meterlong were all working with gillnets for small sharks (asthe narrownose smooth-hound Mustelus schmitti),setting 150m of net/day of 9-10.5cm of mesh size. Theestimated bycatch decreased from 34 to 3 dolphins peryear, throughout the survey. The CPUE of 2002-2003showed a decrease of more than 80% compared to the1998-2000 survey.

Monte Hermoso

Twelve and nine boats used gillnets with mesh size of10-22cm in 1998-2000 and 2002-2003, repectively.Although FE increased almost 7.5 times franciscanamortality decreased considerably from 1998-2000 to2002-2003.

Villa del Mar

Franciscana mortality was also low in this fishing camp.

Incidental catch was reported in the 1998-2000 period.In the last surveyed period, two vessels fished withgillnet, setting 350m of net/day but no mortality wasreported.

Ingeniero White and Puerto Rosales

Ingeniero White is a large fishing harbour inside theBahía Blanca estuary. Puerto Rosales is a small fishingcamp with only three boats operating with gillnets in1998-2000. This small harbour is close to Ingeniero Whiteand their fishing ground overlap.

The fishing gear that caused mortality in IngenieroWhite-Puerto Rosales, during the 1998-2000 survey, wasthe shrimper bottom trawl, operating with 12 nets/day.In 2002-2003, the fleet was composed by 60 vesselsfishing with gillnet gears except one of them that useda shrimper. The estimated mortality decreased throughtime.

Global mortality in the study area

The global M and CPUE for the northern and southerncoasts of each period are shown in Figure 2, compared

1992-1993 1997-1998 1998-2000 2002-2003

LOCALITIES CPUE CI min CI max CPUE CI min CI max CPUE CI min CI max CPUE CI min CI max

1 General Lavalle - - - 107.50 88.2 129.96 47.62 35.00 63.10 - - -

2 San Clemente del Tuyu

- - - 421.80 382.5 464.04 728.68 676.70 783.80 332.03 276.95 394.92

3 Las Toninas - - - 296.61 263.80 332.35 237.46 208.30 269.70 55.56 15.14 142.24

4 Santa Teresita - - - 1028.60 966.3 1093.0 350.35 314.70 389.10 65.79 27.46 132.41

5 Mar del Tuyú - - - 1028.60 966.3 1093.0 340.20 305.00 378.30 124.03 53.54 244.42

6 Aguas Verdes - - - 274.40 243.0 308.97 - - - - - -

7 La Lucila del Mar - - - 222.20 193.9 253.4 169.49 145.00 197.00 190.48 98.41 332.70

8 San Bernardo - - - 311.10 277.5 347.7 825.40 770.00 883.70 180.95 108.95 282.57

9 Mar de Ajó - - - 423.10 465.4 383.8 459.22 418.20 503.20 213.03 124.12 341.10

10 Villa Gesell - - - - - - - - - 37.04 13.59 80.62

11 Mar del Plata - - - 33.30 23.15 46.90 - - - 16.67 12.04 22.49

12 13

Quequén - Necochea

3.90 1.10 9.00 - - - 29.20 19.40 41.70 0.00 0.00 3.69

14 Claromecó 46.90 32.50 65.60 - - - 119.05 98.60 142.40 20.83 4.80 57.91

15 Monte Hermoso 512.90 413.20 629.40 - - - 166.67 142.40 194.00 8.76 4.50 15.39

16 Villa del Mar 74.70 40.80 125.30 - - - 10.58 5.14 19.04 0.00 0.00 34.16

17 18

Puerto Rosales - Ingeniero White

41.94 30.22 56.70 - - - 12.35 6.56 21.60 22.22 16.38 29.47

TOTAL 52.88 39.27 68,76 231,95 202,64 263,32 42,93 30,70 57,35 36.65 32.65 40.98

Table 4: Catch per unit of effort (CPUE) X 1000 of franciscanas, detected in the periods 1992-1993, 1997-1998, 1998-2000 and 2002-2003in each locality, see Map and text for details.

The 95% confidence limits intervals are shown.


LAJAM 6(2): 127-137, December 2007

with data from 1992-1993 (Corcuera, 1994).

The total mortality estimated for the 1997-2000 periodin bottom gillnets, purse-seines and bottom trawls was354 dolphins per year (95% CI = 318-392) for the BuenosAires Province (Northern Coast: 204, 95% CI = 177-234;Southern Coast: 150, 95% CI = 127-175). The total CPUEfor this period was 42 (95% CI = 38-47).

During 2002-2003 period the estimated total mortalitywas 307 dolphins per year (95% CI = 273-343; NorthernCoast: 201, 95% CI = 174-231; Southern Coast: 106, 95%CI = 86-128). The total CPUE for this period was 37(95% CI = 33-41).

For both surveyed period, CPUE of the northern coastwas significantly higher than CPUE for the southerncoast (Kruskal Wallis test, 1997-2000: H=8.68, p=0.0032;2002-2003: H=9.82, p=0.0017). In addition, CPUE of thenorthern coast of 1997-2000 was significantly higher thanfor 2002-2003 (Kruskal Wallis test, H=7.55, p=0.0060)

and for the southern area CPUE values weresignificantly lower in 2002-2003 (Kruskal Wallis test,H=3.97, p=0.0465).

Discussion and Conclusions

We surveyed 62% of the coastal vessels includingbottom gillnet, shrimpers, trawling and purse seine nets.Mortality levels were related to the fishing effort andthese values change with the fleet behaviour, mostly inthe fishing camps, as the number of vessels and effectivefishing days change among years (Tables 1 and 3).

Highest mortality was estimated for San Clemente delTuyú. Therefore, Bahía Samborombón is an area todevelop further studies in order to verify whether thispattern in which very few vessels are responsible formost of the captures is true or not. Thus, the largest partof mortality could be mitigated by means of changing

Figure 2: Mortality, as dolphins captured incidentally per year, and CPUE measured along the northern and southern coast of theBuenos Aires Province for each period surveyed. Data from 1992-1993 are taken from Corcuera (1994).


LAJAM 6(2): 127-137, December 2007

the fishing grounds of a few vessels.

Although the fishing season was shorter and the amountof gears per boat was lower, the mortality levels andthe number of boats at Cabo San Antonio area remainedconstant from 1997 to 2000. Fishermen of this area statedthat they were facing two problems: the presence of theSouth American sea lion (Otaria flavescens) causingimportant damages on their nets (Crespo et al., 1994)and the presence of vessels from the Mar del Plataharbour operating in their fishing grounds. In 2002-2003,the mortality decreased by 35% but the fishing effortincreased more than that in the previous periods.

The mortality estimated for the southern area was lowerin 1997-2000 as compared to previous estimations of1992-1993 (Table 3, Corcuera et al., 1994) with CPUEvalues significantly lower in 2002-2003. The collapse ofshark fisheries (Chiaramonte, 1998) around the fishinggrounds near Necochea and Puerto Quequén area hasled fishermen to move to the fishing grounds furtheroffshore and to replace gillnets by bottom trawls. Thus,the lower CPUE levels in gillnets might be a result offishing gears set further offshore.

From Mar del Plata harbour operates the most importantfishing fleet along the coast. The increased in fishingeffort showed during the last years probably causedmost of the franciscana mortality, but additionalmonitoring is necessary.

Claromecó used to be a fishing camp with high reportedfranciscana bycatch (Corcuera, 1994), but the currentestimation suggests a decrease (Table 3). This might bedue to the collapse of the shark fishery that caused highfranciscana mortality in the early 1990s. Fishermen whocontinued operating with gillnets were using smallermesh sizes (18-36cm for Corcuera, 1994 vs 9-10.5cm inthis study) which is suspected to be less harmful tofranciscana (e.g. Praderi et al., 1989). In addition, asobserved in Cabo San Antonio, damage to fishing gearcaused by South American sea lions have forcedfishermen to reduce fishing effort.

Monte Hermoso showed lower mortality and CPUElevels than those estimated for the 1992-1993 period(Tables 3 and 4). There were no changes in fishinggrounds, so the decrease in mortality values might berelated to changes in the gillnet mesh size (10cmcompared with the 22cm of mesh size used earlier,Corcuera, 1994). Fishermen had the same problems asthose from Cabo San Antonio because of the presenceof the South American sea lion severely damaging theirnets and the presence of vessels from Mar del Platawhose fishing grounds overlap those of local fishermen.

Corcuera (1994) estimated for Villa del Mar that 6 vessels

caused a mortality of 14 dolphins (95% CI = 8-24) with gillnetgears. In this study, the bycatch of only one franciscana wasrecorded in a shrimper and none in gillnets.

At Ingeniero White and Puerto Rosales harbours themortality levels remain high (Table 3), although thesurvey effort in the last period was low and beyond thechanges in the fishing gears that alternate from shrimpersto gillnets (Table 1). Artisanal fisheries still prove to be apotential threat to the conservation of franciscana in thisharbour as shown by our results from 1997-2000 and theestimations of Corcuera (1994) for the 1992-1993 period.

The global mortality for the northern coast of BuenosAires Province seems not to show important changes inthe estimated mortality (Figure 2). However, the CPUElevel of that area in 1997-2000 was significantly higherthan 2002-2003, possibly as a result of a higher FE thatwas not followed by a linear mortality during the lastsurveyed period.

Additionally, the CPUE on the southern coast wassignificantly lower than that of the northern coast in bothsurveyed periods (Figure 2).

As in other parts of the world, there is a tendency ofunderreporting dolphin bycatch in Argentina. Becauseof that, our figures should be considered a minimummortality of franciscana in this region. Nevertheless, ifwe compare values obtained in this study with resultsof onboard observations (Bordino and Albardeda, 20045)we obtain a similar mortality rate: those authorsestimated a mortality of 175 dolphins/year for theperiod 2002-2003 vs. 195 (95% CI = 169-224) estimatedfor the same period in this study in the northern area(excluding Villa Gessell). Consequently, both methods(onboard observations and interviews) allowed us toobtain a similar result. However, the mortalityestimation from the entire Province does showdifferences with Bordino and Albareda (20045) as theseauthors extrapolated the northern mortality estimationsto the southern coasts, considering them similar.

Mortality levels could be important at each localpopulation or stock and the conservation policy mustbe implemented locally. It is urgent to obtain data aboutfranciscana stock identity in order to articulate programsof conservation for the species.

Franciscana shows a continuous presence along thecoastal area of Buenos Aires Province (Corcuera, 1994).Recent studies conducted by Lázaro et al. (2004) and Ottet al. (2005)8 described a substantial geographicheterogeneity in its distribution, particularly in thesouthern Buenos Aires Province, suggesting this areashould be considered separately. Moreover, Mendez etal. (2007) suggest that the franciscana population in

8 Ott, P.H., Freitas, T.R.O., Secchi, E.R., Lázaro, M., Bastida, R., Di Beneditto, A.P.M., Zanelatto, R.C., Bordino, P., Vicente, A.F.C.,Ramos, R.M.A. and White, B.N. (2005) Estructura populacional de Toninha (Pontoporia blainvillei) baseada na análise de DNA mitocondriale nuclear. DT Nº 3 in Abstracts, V Taller para la Coordinación de la Investigación y Conservación del delfín Franciscana (Pontoporiablainvillei) en el Atlántico Sudoccidental, 28-30 November, Mar del Plata, Argentina.


LAJAM 6(2): 127-137, December 2007

northern Buenos Aires is the most isolated populationin Argentina and their results support the currentscheme of larger recognized Franciscana ManagementAreas (FMA), but argue for a finer-scale subdivisionwithin Northern Buenos Aires region (FMA IV).

The International Whaling Commission ScientificCommittee (Donovan and Bjørge, 1995) has noted thatincidental mortality estimates of 1% per year of anestimated population size are sufficient to concern overthe status of small cetacean population and the catchesof 2% per year may not be sustainable.

This study suggests that, even though the gears orfleet behaviour changed locally, the overall mortalityin the Buenos Aires Province was relatively constantduring the surveyed periods, considering the areasconsistently monitored and therefore feasible of beingcompared.

A maximum estimated annual mortality of nearly 400individuals corresponds to more than 2% of the stockof Argentina, suggesting that the population offranciscana in this country may be vulnerable. Takinginto account that some species under pressure ofextensive bycatch increase their growth rate (Caswellet al., 1998), the current effect of incidental mortalityby artisanal fisheries on the sustainability offranciscana stock of southern Buenos Aires Provinceremain uncertainty until more population data becomeavailable.

Argentina is lacking and needs a policy for themanagement of fisheries that include the bycatch of non-target species (Crespo et al., 1994, 1997, 2000). Thus,identification of alternative fishing grounds and gearsare of great importance. An education program focusedto show and disseminate these alternatives to thefishermen communities should be developed. All theseefforts should be urgently focused on the areas with highmortality, that is, those centered on San Clemente delTuyú-Cabo San Antonio, Necochea-Puerto Quequénand Monte Hermoso-Bahía Blanca estuary.

Acknowledgments

This project was founded by grants to HLC fromFundación Antorchas, Proyecto A-13672/1-3 fromArgentina (survey at southern coast) and to JFC andFM from ONG Yaqu Pacha from Germany (survey atnorthern coast). We (HLC) obtained additionalfinancial support from the Convention of MigratorySpecies (CMS) and Fundación Vida SilvestreArgentina. We thank E. Crespo, A. Schiavini for theiruseful comments and suggestions to improve themanuscript. We thank Eduardo Secchi, AlexandreZerbini, Nelio Barros and an anonymous referee fortheir helpful comments on the manuscript. We thankP. Bordino, G. Chiaramonte, L. Tamini, J. E. Perez, A.Averbuj, A. J. Alarcos, M. Iurman, E. Bocci and F.Romeo for their help at field work. We also thank the

Bertazzo family from Monte Hermoso for theirhospitality and information about those fishing camps.This study was possible by the help given by fishermenand skippers from fishing vessels along the BuenosAires Province coast. Logistical support given by IADO(Instituto Argentino de Oceanografía from BahíaBlanca), Cintia Piccolo (Director of IADO) and itstechnical personnel (Sr. Camilo Bernardez and Sr.“Beto”) help us during the Bahía Blanca survey. Wethank Prefectura Naval Argentina for allowing us tocarry on this research along the coast. This is a scientificcontribution of the Estación Hidrobiológica de PuertoQuequén on its 80th anniversary.

References

ALBAREDA, D.A. AND ALBORNOZ, N. (1994) Mortalidad defranciscanas en la pesquería artesanal de San Bernardo y Marde Ajó - Prov. De Buenos Aires- Argentina. Pages 54-61 inPINEDO, M.C. E A.S. BARRETO (Eds), Anais do 2° Encontro sobrecoordenação de pesquisa e manejo da franciscana,Florianópolis, SC, Brazil.

CASWELL, H., BROULT, S., READ, A.J. AND SMITH, T.S. (1998) Harborporpoise and fisheries: an uncertainty analysis of incidentalmortality. Ecological Applications 8: 1226-1238.

CHIARAMONTE, G.E. (1998) Shark fisheries in Argentina. Marineand Freshwater Research 49: 601-609.

CORCUERA, J.F. (1994) Incidental mortality of franciscanadolphin in Argentine waters: the threat of small fishing camps.Pages 291-294 in PERRIN, W.P., DONOVAN, G.P. AND BARLOW, J.(Eds) Gillnets and Cetaceans. Report of the InternationalWhaling Commission (Special Issue 15), Cambridge, U.K.

CORCUERA, J.F., MONZÓN, F., CRESPO, E., AGUILAR, A. AND RAGA,J. (1994) Interactions between marine mammals and the coastalfisheries of Necochea and Claromecó. Pages 283-290 in PERRIN,W.P., DONOVAN, G.P. AND BARLOW, J. (Eds) Gillnets and Cetaceans.Report of the International Whaling Commission (Special Issue15), Cambridge, U.K.

CRESPO, E.A., CORCUERA, J.F. AND LÓPEZ CAZORLA, A. (1994)Interactions between marine mammals and fisheries in somecoastal fishing areas of Argentina. Pages 269-281 in PERRIN,W.P., DONOVAN, G.P. AND BARLOW, J. (Eds) Gillnets and Cetaceans.Report of the International Whaling Commission (special issue15), Cambridge, U.K.

CRESPO, E.A., PEDRAZA, S.N., DANS, S.L., KOEN ALONSO, M., REYES,L.M., GARCIA, N.A., COSCARELLA, M AND SCHIAVINI, A.C.M. (1997)Direct and indirect effects of the highseas fisheries on themarine mammal populations in the northern and centralPatagonian Coast. Journal of the Northwest Atlantic FisheryScience 22: 189-207.

CRESPO, E.A., HARRIS, G. AND GONZÁLEZ, R. (1998) Group sizeand distribution range of the franciscana, Pontoporia blainvillei.Marine Mammal Science 14(4): 845-849.

CRESPO, E.A., KOEN ALONSO, M., DANS, S.L., GARCÍA, N.A.,PEDRAZA, S.N., COSCARELLA, M.A. AND GONZÁLEZ, R. (2000)Incidental catch of dolphins in mid-water trawls for southernanchovy of Patagonia. Journal of Cetacean Research andManagement 2(1):11-16.


LAJAM 6(2): 127-137, December 2007

DONOVAN, G.P. AND B JØRGE, A. (1995) Dall’s porpoise,Phocoenoides dalli - Introductory remarks. Pages 378-380 inBJØRGE, A. AND DONOVAN, G.P. (Eds.) Biology of the Phocoenids.Report of the International Whaling Commission (special issue16), Cambridge, U.K.

LÁZARO, M., LESSA, E.P. AND HAMILTON, H. (2004) Geographicgenetic structure in the franciscana dolphin (Pontoporiablainvillei). Marine Mammal Science 20(2): 201-214.

MENDEZ, M., ROSENBAUM, H.C. AND BORDINO, P. (2008)Conservation genetics of the franciscana dolphin in NorthernArgentina: population structure, by-catch impacts, andmanagement implications. Conservation Genetics 9(2): 419-435.

MONZÓN, F. AND CORCUERA, J.F (1991) Franciscana Pontoporiablainvillei (Gervais and d´Orbigny, 1844). Pages 16-22 inCAPPOZZO, H.L. AND JUNÍN, M. (Eds.) Estado de conservación delos mamíferos marinos del Atlántico sudoccidental. Informes yestudios del Programa de Mares Regionales del PNUMA No 138.

PÉREZ MACRI, G. AND CRESPO, E.A (1989) Survey of thefranciscana, Pontoporia blainvillei, along the Argentine coast,with a preliminary evaluation of mortality in coastal fisheries.Occasional papers IUCN SSC 3: 57-63.

PINEDO, M.C., PRADERI, R. AND BROWNELL, JR., R.L. (1989) Reviewof the biology and status of the franciscana Pontoporia blainvillei.

Pages 46-51 in PERRIN, W.F., BROWNELL, R.L., ZHOU, K. AND LIU, J.(Eds) Biology and conservation of the river dolphins. IUCN-Species Survival Commission, Occasional papers IUCN SSC 3.

PRADERI, R., PINEDO, M.C. AND CRESPO, E.A. (1989) Conservationand Management of Pontoporia blainvillei in Uruguay, Braziland Argentina. Pages 52-56 in PERRIN, W.F., BROWNELL, R.L.,ZHOU, K. AND LIU, J. (Eds) Biology and conservation of the riverdolphins. IUCN-Species Survival Commission, Occasionalpapers IUCN SSC 3.

ROSAS, F.C.W., MONTEIRO FILHO, E.L.A. AND OLIVEIRA, M.R. (2002)Incidental catches of franciscana (Pontoporia blainvillei) on thesouthern coast of São Paulo State and the coast of Paraná State,Brazil. The Latin American Journal of Aquatic Mammals 1(1): 161-167.

SECCHI, E.R., ZERBINI, A.N., BASSOI, M., DALLA ROSA, L., MOLLER,L.M. AND ROCHA-CAMPOS , C.C. (1997) Mortality offranciscanas, Pontoporia blainvillei, in coastal gillnetting insouthern Brazil: 1994-1995. Report of the InternationalWhalingCommission 47: 653-658.

SICILIANO, S. (1994) Review of small cetaceans and fisheryinteractions in coastal waters of Brazil. Report of the InternationalWhaling Commission 15: 241-250.

ZAR, J.H. (1996) Biostatistical analysis. 3rd Edition. Prentice-HallInc. Upper Saddle River, NJ , USA. 662 pp.

Received 23 January 2006. Accepted 30 November 2007.


1 Programa de Pós-graduação em Biologia Animal IB/UFRGS, Porto Alegre, RS, Brazil; Museu de Ciências Naturais/FZBRS. Av.Salvador França, 1427, Porto Alegre, 90690-000, RS, Brazil.

* Corresponding author, e-mail: [email protected] Genetics Department, IB/UFRGS, Porto Alegre, RS, Brazil.

THE ONTOGENY OF SHAPE DISPARITYIN THREE SPECIES OF OTARIIDS (PINNIPEDIA: MAMMALIA)

DANIELA SANFELICE1,* AND THALES R. O. DE FREITAS2

Abstract: We compared skull ontogenies in three otariid species to identify evolutionary novelties and to understand theirrelationships with diversity. The species studied were Arctocephalus australis, Callorhinus ursinus and Otaria byronia. We analyzedevolutionary changes in three parameters of developmental trajectories of skull shape: shape at the outset of ontogeny, allometricpattern, and the amount of change undergone over the course of ontogeny, which depends on its duration (the length of theontogenetic vector) and on the rate of development. Initial shapes were always very different among the species and the distancesbetween shapes increased with time, independently from size. Furthermore, when the complete samples were considered, allthe ontogenetic trajectories were significantly different concerning the directions of the allometric vectors during ontogeny.Ontogenetic trajectories also differed significantly among almost all compared pairs, except for the trajectories of males of A.australis and C. ursinus. However, these differences are expected by chance (considering the range of angles within each sample).A similar pattern was found when the subadults were compared in pairs of species, as well as adult males of A. australis and O.byronia. The correlation found between ontogenies of juveniles was expected by chance, with exception of C. ursinus and O.byronia. The ontogenetic trajectory of C. ursinus is the shortest and that of O. byronia is the longest, with the latter being near thetriple of the former. A. australis has an intermediary length of ontogenetic trajectory. Considering all three species, disparityincreased significantly over ontogeny since the disparity of the adults is near double that between juveniles. However, thepattern of disparity did not change considerably during ontogeny. For any ontogenetical stage, O. byronia is the species thatmost contributed to the disparity of the group, followed by C. ursinus. Finally, ontogenies examined herein are clearly notconstrained (almost every developmental parameter of shape that could evolve was observed) and perhaps the differences inpatterns have additive effects in the differentiation of the ontogenies.

Resumo: Objetivou-se comparar as ontogenias do crânio de três espécies de Otariidae para identificar novidades evolutivas naforma a fim de entender as relações destas com a diversidade. As espécies estudadas foram Arctocephalus australis, Callorhinusursinus and Otaria byronia. Analisaram-se mudanças evolutivas em três parâmetros das trajetórias de desenvolvimento daforma dos crânios: forma no início do desenvolvimento, padrão alométrico e a quantidade de mudanças - que depende daduração (tamanho do vetor ontogenético) e da taxa das mudanças. As formas iniciais mostraram-se sempre diferentes entretodas as espécies e as distâncias entre as formas aumentou com o tempo, independentemente do tamanho. Em acréscimo, aoconsiderar-se toda a amostra, todas as trajetórias mostraram-se significativamente diferentes no que concerne às direções dosvetores alométricos. As trajetórias ontogenéticas diferiram significativamente entre praticamente todos os pares comparados,exceto para as trajetórias de machos de A. australis e C. ursinus. Estas espécies não se revelaram mais diferentes do que seriaesperado ao acaso (considerando a distribuição dos ângulos em cada amostra). Um padrão similar foi encontrado quando ossubadultos foram comparados entre pares de espécies e também quando foram comparados machos adultos de A. australis e deO. byronia. As correlações entre as ontogenias dos juvenis das três espécies enfocadas tampouco diferiram mais entre si do queo esperado ao acaso, excetuando-se entre os juvenis de C. ursinus e O. Byronia. A trajetória ontogenética de C. ursinus é a maiscurta e a de O. byronia a mais longa (quase o triplo daquela de C. ursinus). A. australis apresenta um tamanho de trajetóriaintermediário. Quando as três espécies foram analisadas conjuntamente, verificou-se um aumento da disparidade ao longo daontogenia (a disparidade dos adultos foi praticamente o dobro daquela entre os juvenis) e o padrão de disparidade não sealtera significativamente ao longo da ontogenia. Para qualquer estágio ontogenético, O. byronia é a espécie que mais contribuipara a disparidade do grupo examinado, seguida de C. ursinus. Finalmente, as trajetórias examinadas aqui claramente não sãoconstringidas e talvez a diferença entre os padrões apresente efeitos aditivos na diferenciação das ontogenias.

Keywords: Otariidae, ontogeny, skull, disparity, geometric morphometrics.

Introduction

Disparity and taxonomic diversity provide insights intothe expansion and contraction of variety, and therelationship between these two aspects of diversity alsohave important implications for evolutionarymechanisms. Disparity is measured as the total varianceamong forms in morphological space (proportional tothe mean squared distance among forms) (Foote, 1993).This quantity is a measurement of the range ofmorphologies in a given sample of organisms, as

opposed to diversity, which is expressed in terms ofnumber (and sometimes ranking) of taxa.

The concept of biological and ecological diversity isfamiliar. It can be assessed by a variety of indices,usually depending upon the number of taxa present ina given sample. A related concept is the absolutemorphological variety of a group, its variance in shapeor the amount of morphological space that it occupies(Foote, 1992). On the other hand, the concept of disparityrefers to how much the members of a group oforganisms are morphologically different from each

140 D.SANFELICE AND T.R.O.FREITAS

LAJAM 6(2): 139-154, December 2007

other, and then geometric morphometry provides a veryobjective assessment for these differences (Foote, 1992).

Furthermore, variation and disparity are similar termsrelated to the concept of variety, where disparitygenerally means the variety among a group. Disparityis the outcome of evolutionary processes and variationis the variety of individuals within a homogeneousgroup. Thus, it is the raw material to evolutionaryprocesses (Zelditch et al., 2004).

The objective of this work is to compare ontogenies toidentify divergent developmental features in the shapeof the otariid skull with the purpose of understandingtheir relationships with diversity. The species studiedwere Arctocephalus australis Zimmermann, 1783,Callorhinus ursinus Linnaeus, 1758 and Otaria byroniaBlainville, 18203. Thus, we present a comparative studyof the ontogeny of the skull of the two Otariidae speciesmore frequently found on the coast of Rio Grande do Sulstate, Brazil (A. australis and O. byronia). Callorhinus ursinusis also included because it is supposedly the extant otariidmore closely related to the ancestral of this family (Bertaet al., 2006). In this context, we analyzed evolutionarychanges in three parameters of developmental trajectoriesof skull shapes: (1) shape at the outset of ontogeny,defined here as the starting point of the vectorrepresenting the ontogeny of shape; (2) allometric patternand the direction of allometric vector in shape and space,and (3) the amount of change undergone over the courseof ontogeny, which depends on the duration (the lengthof the ontogenetic vector) and rate of development.

That approach is justified by the fact that the study ofdisparity is a primordial step to understand howevolutionary novelties interact in those groups, whichis particularly interesting considering the rapid (andpoorly understood) radiation and speciation of theextant Otariidae (Demeré et al., 2003).

In addition, the shape disparity between differentdevelopmental stages was compared to check if thedisparity level decreases during ontogeny (presence ofnovelties), which could indicate non-additive interactionsbetween novelties (Zelditch et al., 2003a).

The selected focus was skull shape because these ontogeneticseries are easily available and these data are especially wellsuited to studies of disparity (Zelditch et. al, 2003a). Inaddition, shape underlies the general statistical theory ofmodern shape analysis, the Procrustes distance. In fact,traditional morphometrics presents a major analyticproblem caused by discrete characters: units of the sameapparent magnitude are not necessarily equivalent (Zelditchet al., 2003a). However, any two samples that are separatedby one unit of Procrustes distance differ from each other bythe same amount as any other taxa. This aspect is importantwhen the goal is to quantify the degree of difference among

morphologies, especially when it concerns non-additivity of the interacting causes of disparity.Otherwise, this distance can be traced directly to themodifications in the place of homologous landmarks—the change in those locations is directly proportional tothe difference in shape (Zelditch et al., 2003a).


Sampling

Our samples comprise cross-sectional ontogenetic seriesof the skull of three otariid species: A. australis (n=76),C. ursinus (n=51) and O. byronia (n=84) (Appendix 1).We used the number of growth layer groups depositedin the dentine of the bisected canine as our estimate ofchronological age (Schiavini, 1992) and the sutural agesto determine the ontogenetic stages (juvenile, subadultsand adults) (Sivertsen, 1954). The analyses wereperformed considering species, sex and sutural agegroups (juveniles, subadults and adults).

Our analyses were based on landmarks, discrete pointsthat were recognizable and homologous on all species(and specimens) at different ages, in the study (Figure 1).The landmarks were chosen to provide the mostcomprehensive coverage of that view of the skull.Consistency of relative position, repeatability andcoplanarity of the landmarks were also considered in theselection of these points. All landmarks were digitalizedby one of the authors (D. Sanfelice). After that, thespecimens were superimposed using the GeneralizedLeast-Squares Procrustes superimposition (GLS).

Defining Morphological space and measuring morphologicaldiversity

The approach here is to ordinate forms in amultidimensional morphospace and to basemorphological differences on the array of points inmorphospace (Cherry et al., 1982). Consequently,disparity is measured as the sum of univariate variancesof all dimensions in morphospace, which is proportionalto the mean squared Euclidean distance among pointsin morphospace (Van Valen, 1974).

The partial disparity is analogous to a variance, where thesquared distances are taken relative to the overall centroidrather to the centroid of the subgroup. This permits accessto the disparity contributions of subgroups. This has allowedmorphological disparity analysis to address an issue thathas long been addressed with taxonomic diversity data -concerning the relative contributions of different subgroupsto overall morphological disparity. The method of disparitypartitioning allows an assessment of the relativecontributions of different taxa to the morphologicaldisparity of the larger group containing them.

3 Our use of the specific name byronia follows Drehmer (2005), Gardner and Robbins (1995) and ICZN Opinion 1962 (2000).

THE ONTOGENY OF SHAPE DISPARITY IN THREE SPECIES OF OTARIIDS 141

LAJAM 6(2): 139-154, December 2007

Estimation and Comparisons among the Initial Shapes

The initial shape is estimated from the regression equation,which predicts the expected shape at each size or age. Here,we predicted the mean shape for each species at age zero.The sexes were pooled together considering that juvenileswere not dimorphic in shape (Sanfelice and Freitas, 2008).Subsequently, the residuals from the regression wereadded to the predicted form, yielding a sample of shapesat each stage. Each individual specimen contributed withonly one residual (i.e. the deviation of that individual fromthe predicted shape). To compare shapes, multivariateanalysis of the variance (MANOVA) was performed andpairwise comparisons tested the differences betweengroups two-by-two. Otherwise, an experiment-wise errorrate of 0.05 was maintained by dividing the number ofunplanned comparisons (three) to obtain the critical a valueof 0.016 (Bonferroni Correction). The misclassification rateof the discriminant function was also analyzed. Thestatistical significance of the pairwise differences was testedby a resampling-based F-test. The MANOVA and themisclassification rate were performed with CVAGen6j;pairwise F-tests were run in Two-Group6h. Theseprograms belong to the Integrated MorphometricsPrograms (Sheets, 2000) and they are freely availableelectronically at http://www.canisius.edu/;sheets/morphsoft.html.

Comparisons of the Allometric Trajectories

These parameters were assessed by multivariateregression of the partial warp plus the uniformcomponent scores (dependent variable representingshape) on a measurement of geometric scale (the

logarithm of the centroid size). For each speciesseparately, the full set of shape variables was regressedon the independent variables considered. We assumed alinear relationship between shape and size since theseestimates were based on linear regression.

Estimates and Comparisons between Allometric Patterns

The vector of allometric coefficients that describesmorphogenesis is calculated using the multivariateregression of shape on size, as detailed above. To comparethese vectors by multivariate analyses, we calculated theangle between them (the cosine of that angle is the vectorcorrelation between the two ontogenetic trajectories ofshape). That cosine was calculated as the inner productof vectors of allometric coefficients, normalized to theunit length. Thus, if two vectors pointed in the samedirection, the angle between them would be equal to zeroand the cosine would be 1. Since it would be too strict toconsider an angle of 0 as the null hypothesis, here thenull hypothesis states that the angles between species areno larger than we would expect from the variation withina single species or group (some variation is expectedbecause individuals of the same species do not haveidentical ontogenies of shape). The subject here is whetheror not the uncertainty of the estimation of each speciestrajectory (due to sampling) is very large, making itimpossible to reject the null hypothesis of any significantdifference. To estimate the range of angles within eachspecies in congruence with the datasets (and thus tocalculate the imprecision of the trajectory due tosampling) we estimate the residuals from the multivariateregression in a way that each individual gives a multi-

Figure 1. Landmarks shown on the ventral view of the skull of a juvenile of Otaria byronia. Descriptions of each landmark are given inAppendix 2.


LAJAM 6(2): 139-154, December 2007

dimensional set of residuals describing its deviation fromthe expected shape at its size. Thus, a pair of bootstrapsets was constructed for species that will be used tocalculate the angle between the trajectories inconsideration. These pairs were constructed byresampling residuals (with replacement) and wererandomly assigned to expected values of shape (derivedfrom the original regression model) at values of thelogarithm of centroid size (detected in the original data).This bootstrap approach is no more than a multivariateextension of the known procedure to estimation ofuncertainties of regression slopes by resampling thecovariance structure among variables (Efron & Tibshirani,1993). Finally, the angles between the trajectories derivedfrom the two within-species bootstrap sets were estimatedand this procedure was repeated N times to produce adistribution of within-species angles. In the present study,we employed N=100. Since sample sizes were differentamong the species, the two bootstrap sets constructedfrom the species with largest sample size matched samplesizes of the two species in comparison (i.e. one set has thelargest sample size of that species, while the other hasthe smallest sample size of the other species). The twobootstrap sets obtained from the data of the species withthe smallest sample size have that sample size, since abootstrap larger than the original data set cannot beconstructed. If the interspecific angle exceeded the 95th

percentile of the within-species range of angles, theinterspecific difference was considered to be statisticallysignificant. The multivariate regressions were performedusing Regress6k and the comparisons betweenontogenetic trajectories were carried out usingVecCompare, both programs freely available in the IMPseries (Sheets, 2000).

Estimations and Comparisons between the Lengths ofOntogenetic Trajectories

The length of the ontogenetic trajectory of shape is afunction of the rate of shape change and the duration ofdevelopment. To estimate this length, the Procrustesdistance between the average shape in the juvenile stageand the shape at maximum body size was calculated.Confidence limits were placed on this measurement bybootstrap, considering the variability among individualsat the same size and the uncertainty of the regression.That is, the residuals estimated from the regression weredrawn with replacement at random and were added tothe expected shape, generating a bootstrap data set foreach species. In the sequence, the same regression modelwas fitted to the bootstrapped sets and the size correctionwas carried out on these sets. The result was a bootstrapset for each species that incorporated the uncertainty ofregression. These calculations were performed byDisparityBox6g, another freely available program in theIMP series (Sheets, 2000).

Measurement of the Level of Disparity

The level of disparity was calculated according to Zelditch

et al. (2003a) for the different ontogenetical stages in eachspecies and sexes (adults) and among species. To test thesignificance of differences in levels of disparity, we usedthe bootstrapping procedure explained in the previoussection, since the analyses presented here were based onstandardized data and the tests should take into accountthe uncertainties of the regression. Considering that oneof the difficulties found in calculating the level ofdisparity was the differences in shape related todifferences in size (allometry) and its influence on thedisparity, the level of disparity was studied with andwithout correction for size. Therefore, we fitted aregression model to the data, determining the residualsand producing size-standardized data set. In the studywithout size correction, we measured disparity withcorrection to the mean size of each subsample and withcorrection using the same size for the two samples. ThePartial Disparity, which is the contribution to disparityof each subsample analyzed, was calculated usingDisparity Box6g (Sheets, 2000).

Analysis of the Pattern of Disparity

The dimensions and the distribution of shapes along theseries where shapes are most disparate were describedby principal components analysis, using the softwarePCAGen6n (Sheets, 2000). Such examinations arerelevant because distinct ontogenetic stages may havethe same level of disparity but present a differentpattern, which hide the dynamic nature of disparity(Zelditch et al, 2003b). The patterns were examined foreach subsample separately with the aim of finding onebiological explanation to the direction of dominantvariation within shape space (in addition to the fact thatthe morphospace resultant is different from sample tosample). The significance of the principal componentswas tested by Anderson´s test.

The sub-samples compared were: juveniles (specimenswith sutural age between 9 and 10, including newborn andanimals between 0 or 1 year of age), subadults (specimenswith sutural ages between 11 and 18) and adults (specimenswith sutural ages superior to 18). The adults were separatedby sex, due to the dimorphism in the adult shape.

Results and Discussion

Comparisons among the Initial Shapes

All pairwise F-tests among species showed statisticallysignificant differences in the initial shape (p=0.01), evenafter Bonferroni corrections for three comparisons(p=0.05). In addition, no specimens (n= 47) wereincorrectly classified by the discriminant function. Thepairwise distances between means are presented (Tables1 and 2), suggesting a labile aspect in the initial shape ofthe otariid skull.

Performing the same analysis for the otherontogenetic phases, we detected that the differencestend to increase during ontogeny and that size doesnot have a great influence in the amount of difference.


LAJAM 6(2): 139-154, December 2007

We compared shapes with different standardizations(e.g. standardized by the minimum size of allspecimens, by the maximum size of all the females, bythe maximum size of all the males, by the range of sizeof the females of each correspondent species or evenstandardized by the range of size of the males of eachcorresponding species).

Allometric Patterns

When complete samples were considered, all theontogenetic trajectories were significantly differentconcerning the directions of the allometric vectorsduring ontogeny. Here, the allometric patterns for eachsex were presented separately, since patterns are distinctbetween males and females of the same species(Sanfelice and Freitas, 2008). Ontogenetic trajectoriesdiffered significantly among almost all compared pairs,except for the trajectories of males of A. australis and

C. ursinus. The differences presented by this group areexpected by chance considering the range of angleswithin each sample (Table 3). A similar pattern wasobserved when the subadults were compared betweenpairs of species, as well as for adult males of A. australisand O. byronia. Differences observed in juveniles wereexpected by chance (correlation between ontogenies inthat phase was equal to one), with exception of C. ursinusand O. byronia, where angles ranged from 38.2° to 40.7°in females and from 38.1° to 48.8° in males. The mostdivergent trajectories found were those of C. ursinus andO. byronia for both sexes.

Table1. Procrustes distances among the average initial shapes ofArctocephalus australis, Callorhinus ursinus and Otaria byronia.

All pairwise differences are statiscally significant forthe Bonferroni-adjusted value of α=0.05.

Table 2. Procrustes distances among the average shapes of Arctocephalus australis, Callorhinus ursinus and Otaria byronia.

All pairwise differences are statiscally significant for the Bonferroni-adjusted value of α=0.05.Distance is the Partial Procrustes Distance; 95% CI is the confidence interval; St. minimum is thePPD when the samples were standardized to the respective smallest size.

Table 3. Comparisons among ontogenetic trajectories of Arctocephalusaustralis, Callorhinus ursinus and Otaria byronia. Vector correlationsare above the diagonal, angles (in degrees) are below the diagonal.

Angles statistically significantly different from 0° arein bold.

A. australis C. ursinus O. byronia

A. australis 0 0.0685 0.1003

C. ursinus 0 0.1444

O. byronia 0

�


A. australis - 0.766044 0.785857

C. ursinus 40 - 0.758134

O. byronia 38.2 40.7 -

�


A. australis - 0.772734 0.786935

C. ursinus 39.4 - 0.658689

O. byronia 38.1 48.8 -

A. australis x C. ursinus DISTANCE 95% CI ST. MINIMUM 95% CI

JUVENILES 0.0685 0.0577-0.0861 0.0719 0.0628-0.0821

SUBADULTS 0.0647 0.058-0.08 0.0592 0.0551-0.0674

ADULT FEMALES 0.0673 0.0552-0.0793 0.0543 0.0478-0.065

ADULT MALES 0.0497 0.0444-0.0567 0.0573 0.909-0.1153

A. australis x O. byronia DISTANCE 95% IC ST. MINIMUM 95% IC

JUVENILES 0.0996 0.930-0.1125 0.1063 0.0989-0.1233

SUBADULTS 0.1444 0.1353-0.1528 0.1373 0.1299-0.1464

ADULT FEMALES 0.1387 0.1288-0.1459 0.142 0.1345-0.1488

ADULT MALES 0.1683 0.1578-0.1795 0.1662 0.1532-0.1747

C. ursinus x O. byronia DISTANCE 95% IC ST. MINIMUM 95% IC

JUVENILES 0.1445 0.1355-0.1566 0.1406 0.1356-0.1487

SUBADULTS 0.1842 0.1683-0.1989 0.16 0.1491-0.1703

ADULT FEMALES 0.1859 0.1747-0.1969 0.1717 0.1615-0.1807

ADULT MALES 0.1921 0.1839-0.2014 0.1745 0.1652-0.1841


LAJAM 6(2): 139-154, December 2007

It may appear that the three species examined weremore similar than expected by chance (i.e. the correlationis higher than zero) but they differed significantly (i.e.the correlations were lower than one). Additionally, thedifferences in the ontogenetic transformations of shapewere visually conspicuous between sexes and overallbetween species (Figure 2).

Lengths of Ontogenetic Trajectories

The ontogenetic trajectory of C. ursinus was theshortest, while the longest was observed for O. byronia.Arctocephalus australis had an intermediary length ofontogenetic trajectory. In the three species, the femaleshad the longest trajectories, but the confidence intervalsof lengths of trajectories overlapped between the sexesof the same species. On the other hand, the lengthswere significantly different between species(considering the sex pooling together or separately)(Table 4).

Shape disparity

In A. australis the disparity increased gradually andthe disparity between the two sexes was the smallestin the adults, especially when we corrected for size(Table 5). The disparity between juveniles andsubadults was nearly four times higher in C. ursinusthan in A. australis, but the level of disparity betweenthe different ontogenetic stages was more or lessconstant (the disparity between adults was nearly four

times higher in C. ursinus that it was observed for A.australis) (Table 5). In the sea lion O. byronia (thespecies with a high level of disparity between malesand females) the high level of disparity was foundrelatively early in ontogeny, between juveniles andsubadults (Table 5 and 6). The subadults versus adultfemales presented the smallest disparity inmorphology. In addition, it was observed that thedisparity between the juveniles and the otherontogenetic stages was extremely striking, increasinggradually (Table 5). Moreover, standardization wasnot effective due to the small difference in sizeobserved among the stages compared in the samespecies (Tables 5 and 6). For the sample comprisingall three species, disparity increased significantlythroughout ontogeny, since the disparity of the adultsis near double the disparity found between juveniles(Table 7). Otherwise, for any ontogenetical stage, O.byronia is the species that most contributed to thegroup disparity, followed by C. ursinus (Table 8).

Comparing the two species of fur seals, the level ofdisparity is nearly static over the course of ontogeny,especially in females (but with some increment whenwe analyzed the disparity applying the sizecorrection). In males we observed a decrease indisparity (Table 8). When A. australis and O. byroniawere compared, the level of disparity increased earlyin ontogeny, but after the subadult stages it wasalmost stable. The disparity between C. ursinus and

Figure 2. Ontogenetic transformations in shape. Each diagram depicts the regression of shape on log-transformed centroid size as aCartesian transformation using the thin-plate spline.


LAJAM 6(2): 139-154, December 2007

O. byronia was high and constant during thedevelopment, with a very inconspicuous increment inthe early ontogeny. In addition, this level was almosttwo times higher in adults of both sexes when the sizecorrection was performed. The disparity between thesea lion and the other two species was similar,considering the range of the confidence intervals (andwhen the size correction was not applied).

Pattern of shape disparity

When we considered the three species together, thepattern of disparity did not show a considerably changeduring ontogeny (Figure 3). In the variance of juvenileshape, two significant components were found: the firstseparate the fur seals species from the sea lion species(Figure 3A). Otaria byronia, which presents high scoresin that component, is differentiated from those with lowscores by the great extension of the palate (and byconsequence, the shorter choanes), the deepening of the

braincase, and the comparison of the braincase with therostrum. The second component describes theenlargement of the rostrum and the forwarddisplacement of the choanes, but the most conspicuouspattern of changes in shape explained by this componentis the postero-distal expansion lateral and posterior tothe braincase. Arctocephalus australis had the lowest scoresin that component and C. ursinus the highest. In subadults,the first principal component is responsible for theenlargement of the rostrum and the mastoid processregion, and the second principal component expressedthe enlargement of the posterior region of the bone palate.

In adults of both sexes, the enlargement in length andwidth is expressed largely by the first principalcomponent (except in the condyle region), and thesecond principal component is related to changes in theposterior regions of the bone palate (females) ormodifications in the posterior regions of the alveolarprocess (males).

SPECIES ALL SPECIMENS (95% CI ) � (95% CI) � (95% CI )

A. australis 0.0099 (0.0084-0.0119) 0.0084 (0.0066-0.0106) 0.0062 (0.0052-0.0075)

C. ursinus 0.0053 ( 0.0040 – 0.00078) 0.0059 (0.0033-0.0081) 0.0038 (0.0020-0.0067)

O. byronia 0.0184 (0.0163-0.0217) 0.0162 (0.0131-0.0230) 0.0134 (0.0106-0.0167)

Table 4. Lengths of ontogenetic trajectories in units of Procrustes distance for Arctocephalus australis, Callorhinus ursinus and Otaria byronia.

The confidence intervals are in parentheses.


JUVENILES X SUBADULTS 0.00023 (0.00027-0.00077)

0.0017 (0.0009-0.0034)

0.00117 (0.00069-0.00264)

0.0028 (0.0012-0.0064)

0.00415 (0.00320-0.00077)

0.0111 (0.0087-0.0218)

JUVENILES X ADULT FEMALES 0.00212 (0.00178-0.00280)

0.0051 (0.0038-0.0076)

0.00163 (0.00116-0.00289)

0.0035 (0.0026-0.0055)

0.00592 (0.00520-0.00830)

0.0145 (0.0123-0.0261)

JUVENILES X ADULT MALES 0.00227(0.00186-0.003)

0.0071 (0.0058-0.0104)

0.00316 (0.00239-0.00450)

0.0063 (0.0050-0.0084)

0.00934 (0.00740-0.01289)

0.0197 (0.0165-0.0300)

SUBADULTS X ADULT FEMALES 0.00116 (0.00091-0.00197)

0.0016 (0.0013-0.0025)

0.00116 (0.00091-0.00197)

0.0016 (0.0013-0.0025)

0.00033 (0.00029-0.00076)

0.0008 (0.0006-0.0016)

SUBADULTS X ADULT MALES 0.00139 (0.00112-0.00208)

0.0034 (0.0023-0.0048)

0.00128 (0.00101-0.00243)

0.0018 (0.0010-0.0041)

0.00172 (0.00128-0.00274)

0.0030 (0.0024-0.0042)

ADULT FEMALES X ADULT MALES 0.00037 (0.00038-0.00081)

0.0013 (0.001-0.0027)

0.00128 (0.00105-0.00151)

0.0019 (0.0012-0.0034)

0.00146 ( 0.00108-0.00253)

0.0025 (0.0019-0.0040)

FEMALES X MALES 0.00011 (0.00015-0.00045) 0.00035 (0.00025-0.001) 0.0005 (0.00041-0.00133)

Table 5. Level of disparity among ontogenetic and/or sex groups of Arctocephalus australis, Callorhinus ursinus and Otaria byronia.

The values in the first line of each case are the unstandarized levels of disparity and the values in the second line are thecorresponding level with the samples standardized with respect to size. The numbers in parentheses are the confidenceintervals.


LAJAM 6(2): 139-154, December 2007

In this context, we could observe that those earlyontogenies (allometric patterns) were similar, with earlystages overlapping in shape space. By contrast, subadultscompose a confuse age group that could, sometimes,affect the clarity of the results with its heterogeneity andhigh variance. In fact, it is important to highlight thatmean shape of female and male subadults was close tothe significance level (p=0.055) in O. byronia, whichincreased the heterogeneity of this subgroup.

Ontogenies examined herein were clearly notconstrained: almost every developmental parameter ofshape that could evolve was observed. The speciesdiffered in the initial and later shape of the skull, in thelength of the ontogenetic trajectories, and in theallometric pattern. Thus, we observed a complexscenario where it was difficult to establish a relationshipbetween the developmental processes with the

phylogeny, mainly because we had sampled only threespecies. It may be possible that if all species in the familywere examined we would have been able to determinethe causal relations between ontogeny and phylogenyin otariids. Thus, it would be very interesting to analyzethe relevance of evolution and development in thehistory of otariids. Since the species did not conservethe same ontogenetic trajectory, their evolution cannotbe explained only by a heterochronic hypothesis.

The strongest differences in the repatterning of theallometry occur in the later ontogeny, but C. ursinus andO. byronia are extremely different during the entire process.The observed result where the disparity is higher whenall the species are pooled together was logical. Similarly,the high partial contribution to disparity by the sea lion iscongruent with all the other results regarding thecomparisons between shapes in these species.

Table 6. Level of disparity (distance-based disparity based on the group means, working with all loaded groups-bootstrapped sizecorrection between males and females) between males and females of Arctocephalus australis, Callorhinus ursinus and Otaria byronia.

The numbers in parentheses are the confidence intervals.

Table 7. Shape disparity, measured as the square root of the average of the squared distances between the mean shape of each speciesand the centroid of Arctocephalus australis, Callorhinus ursinus and Otaria byronia. Confidence intervals are obtained by resampling.

In the first line the disparity is presented without correction for size and in the second line the level of disparity is corrected for size,using a different size for each subsample.

GROUPS JUVENILE DISPARITY

95TH PERCENTILE

OF THE WITHIN-

SPECIES RANGE

SUBADULT DISPARITY

95TH

PERCENTILE OF

THE WITHIN-SPECIES

RANGE

� ADULT DISPARITY

95TH

PERCENTILE OF

THE WITHIN-SPECIES RANGE

� ADULT DISPARITY

95TH

PERCENTILE OF

THE WITHIN-SPECIES

RANGE

All species

0.00603 0.006

0.0054-0.0073 0.0056-0.012

0.0098 0.0089

0.0089-0.0113 0.0074-0.0108

0.0097 0.0116

0.00885-0.01074 0.0102-0.0138

0.01128 0.0123

0.0104-0.0124 0.0109-0.0145

A. australis

x C.

ursinus

0.00266 0.0026

0.0022 -0.004 0.0016 to 0.0046

0.0021 0.0015

0.0016-0.0032 0.0010-0.0032

0.0027 0.0038

0.00175-0.00352 0.0028-0.0065

0.00124 0.0022

0.001-0.0017 0.0016-0.0037

A. australis

x O. byronia

0.00497

0.056

0.0043-0.0071

0.0042-0.0112

0.0104

0.0104

0.0095-0.0115

0.0094-0.0119

0.0096

0.01

0.00878-0.01075

0.0081-0.0132

0.01417

0.0134

0.0126-0.0162

0.0105-0.0167

C. ursinus x

O. byronia

0.01047 0.0099

0.0095-0.0125 0.0086-0.0156

0.0169 0.0147

0.0146-0.0198 0.0113-0.0187

0.0172 0.0210

0.01551-0.01989 0.0159-0.0261

0.01846 0.0212

0.0168-0.0208 0.0184-0.0243


Standandized for the minimum size

0.0172 (0.0105-0.0376) 0.0214 (0.0171-0.0542) 0.0753 (0.0539-0.1212)

Standardized for the maximum size of the females

0.0129 (0.0098-0.0282) 0.0165 (0.0110-0.0389) 0.0246 (0.0154-0.0381)

Standardized for the maximum size of the males

0.0119 (0.0082-0.0239) 0.0154 (0.0122-0.0406) 0.0224 (0.0153-0.0376)

Standardized for the range of size of the females

0.0058 (0.0045-0.0076) 0.0061 (0.0036-0.0088) 0.0150 (0.0123-0.0194)

Standardized for the range of size of the males

0.0046 (0.0037-0.0060) 0.0079 (0.0051-0.0115) 0.0098 (0.0083-0.0123)


LAJAM 6(2): 139-154, December 2007

PARTIAL DISPARITY SE PD WITH SIZE

CORRECTION

SE

Aa 0.00053 0.00143 0.00072 0.00115

Cu 0.00236 0.00136 0.00216 0.00123

JUVENILES

Ob 0.00314 0.00150 0.00314 0.00104

Aa 0.00089 0.00259 0.00101 0.00217

Cu 0.00307 0.00246 0.00242 0.00231

SUBADULTS

Ob 0.00587 0.00262 0.00544 0.00218

Aa 0.00072 0.00256 0.00071 0.00325

Cu 0.00327 0.00271 0.00439 0.00263

ADULT �

Ob 0.00574 0.00232 0.00648 0.00356

Aa 0.00136 0.00344 0.00108 0.00343

Cu 0.00279 0.00274 0.00370 0.00327

ADULT �

Ob 0.00713 0.00271 0.00747 0.00343

Table 8. Contributions to the disparity for each species, with and without size correction.

Aa=Arctocephalus australis; Cu=Callorhinus ursinus; Ob=Otaria byronia; PD= PartialDisparity; SE=Standard error.

Concomitantly with the allometric repatterning, thelengths of the ontogenetic trajectories are alsodifferent; thus, complex changes are acting in theevolving ontogenies of these otariid species.However, the impact of each evolutionary patternon disparity (counterbalance or amplification) isdifficult to design without modeling hypotheticalontogenies.

The hypothesis of amplification predicts that theinteraction among several novelties enhancesdisparity above the level we would anticipate fortheir separate effects while the hypothesis ofcounterbalancing predicts that the interaction amongseveral novelties diminishes the impact of combinednovelties. The most probable one is the occurrenceof amplifications, since the ontogeny is notconstrained and we did not fince evidence ofcounter-balancing in the disparity, which tended toincrease during ontogeny.

Acknowledgements

Work by D. Sanfelice was partially supported by afellowship of Coordenadoria de AperfeiçoamentoPessoal (CAPES), Conselho Nacional deDesenvolvimento Científico e Tecnológico (CNPq),Fundação de Amparo à Pesquisa do Rio Grande doSul (FAPERGS) and by the Society for MarineMammalogy. We thank E. A. Crespo, A. Lebas, J.Patton, D. Long, L. H. Cappozzo, P. C. Simões-Lopesand GEMARS for access to the scientific collections;L. R. de Oliveira for access to the ages of somespecimens of Arctocephalus australis; D. M. M. M.

Schiller and E. A. Crespo for the help in the ageanalysis and L. A. Valério and E. Quadros for thehelp with the figures.

References

BERTA, A., SUMICH, J.L. AND KOVACS, K.M. (1999) Marine Mammals– Evolutionary Biology. Academic Press, New York. 547 p.

CHERRY, L.M., CASE, S.M., KUNKEL, J.G., WYLES, J.S. AND WILSON,A.C. (1982) Body shape metrics and organismal evolution.Evolution 36: 914-933.

DEMERÉ, T.A., BERTA, A. AND ADAM, P. (2003) Pinnipedimorphevolutionary biogeography. Bulletin American Museum ofNatural History 279: 32-76.

DREHMER, C.J. (2005) Variação geográfica em Otaria byronia (deBlainville, 1820) (Pinnipedia, Otariidae) com base namorfometria sincraniana. Ph.D. Thesis. Universidade Federaldo Rio Grande do Sul. Porto Alegre, RS, Brazil. 202 p.

EFRON, B. AND TIBSHIRANI, R.J. (1993) An introduction to thebootstrap. Chapman and Hall, New York. 436 p.

FOOTE, M. (1992) Rarefaction analysis of morphological andtaxonomic diversity. Paleobiology 18: 1-16.

FOOTE, M. (1993) Discordance and concordance betweenmorphological and taxonomic diversity. Paleobiology 19: 185-204.

GARDNER , A.L. AND ROBBINS , C.B. (1999) Case 3058.Arctocephalus F. Cuvier, 1826 and Callorhinus Gray, 1859(Mammalia, Pinnipedia): proposed conservation by thedesignation of Phoca pusilla Schreber, [1775] as the typespecies of Arctocephalus; and Otaria Péron, 1816 andEumetopias Gill, 1866: proposed conservation by thedesignation of Phoca leonina Molina, 1782 as the type speciesof Otaria. Bulletin of Zoological Nomenclature 56: 136-141.


LAJAM 6(2): 139-154, December 2007

Fig

ure

3.

Pri

nci

pa

l co

mp

on

ents

an

aly

sis

of

sha

pe

po

oli

ng

all

sp

ecie

s to

get

her

. (A

) ju

ven

ile

sha

pes

; (B

) su

ba

du

lt s

ha

pes

; (C

) a

du

lt f

ema

les

sha

pes

; (D

) a

du

lt m

ale

s sh

ap

es.

Th

ed

iffe

ren

ce b

etw

een

lo

w a

nd

hig

h s

core

s o

n e

ach

ax

is i

s p

lott

ed a

s d

efo

rma

tio

ns

usi

ng

th

e th

in-p

late

sp

lin

e te

chn

iqu

e. C

ircl

es=

Arc

toce

ph

alu

s au

stra

lis,

Sq

ua

res=

Cal

lorh

inu

s u

rsin

us,

Dia

mo

nd

= O

tari

a by

ron

ia.


LAJAM 6(2): 139-154, December 2007

INTERNATIONAL COMISSION OF ZOOLOGICAL NOMENCLATURE.OPINION 1962 (2000) Arctocephalus F. Cuvier, 1826 andCallorhinus Gray, 1859 (Mammalia, Pinnipedia): proposedconservation by the designation of Phoca pusilla Schreber,[1775] as the type species of Arctocephalus; and Otaria Péron,1816 and Eumetopias Gill, 1866: proposed conservation by thedesignation of Phoca leonina Molina, 1782 as the type speciesof Otaria. Bulletin of Zoological Nomenclature 57: 193-195.

SANFELICE, D. AND FREITAS, T.R.O. (2008) A comparativedescription of dimorphism in skull ontogeny of Arctocephalusaustralis, Callorhinus ursinus and Otaria byronia (Pinnipedia:Otariidae). Journal of Mammalogy 89: 336-346.

SCHIAVINI, A.C., LIMA, M.M AND BATALLÉS, L.M. (1992) Growthstructures of maxillary canines of the Southern fur seal(Arctocephalus australis). Marine Mammals Science 8: 89-93.

SHEETS, D.H. (2000) Integrated Morphometric Softwares (IMP) –Mathworks, MATLAB6. The Mathworks, Natick, Mass. http:/

/www.canisius.edu/~sheets/morphsoft.html.

SIVERTSEN, E. (1954) A survey of the eared seals (family Otariidae)with remarks on the Antarctic seals colected by M/K “Norvegia”in 1928-1929. Det Norske Videnskaps-Akademi 36: 1-76.

VAN VALEN, L. (1974) A natural model for the origin of somehigher taxa. Journal of Herpetology 8: 109-121.

ZELDITCH, M.L.; SWIDERSKI, D.L., SHEETS, D.H., AND FINK, W.L.(2004) Geometric Shape Analysis for Biologists: A Primer.Academic Press, NY.

ZELDITCH, M.L.; LUNDRIGAN, B.L.; SHEETS, D.H. AND THEODORE,G. JR. (2003a) Do precocial mammals develop at a faster rate?A comparison of rates of skull development in Sigmodonfulviventer and Mus musculus domesticus. Journal of EvolutionaryBiology 16:708-720.

ZELDITCH, M.L.; SHEETS H.D. AND FINK, W.L. (2003b) Theontogenetic dynamics of shape disparity. Paleobiology 29: 139-156.


LAJAM 6(2): 139-154, December 2007

APPENDIX 1

LISTING OF THE SPECIMENS EXAMINED

Coll. N°= Collection Number; CS= Centroid Size in units of centroid size (cm); CCB= Skull Total Length (condylo-basal length); Sut. Age= Sutural Age; Age= age in years.Institution Acronyms: AMNH= American Museum of Natural History (New York, USA); CAS= California Academyof Sciences (San Francisco, USA); CNP= Centro Nacional Patagónico (Puerto Madryn, Argentina); FCIEN= Facultadde Ciencias (Montevideo, Uruguay); GEMARS= Grupo de Estudos de Mamíferos Marinhos (Porto Alegre, Brazil);LAMAMA= Laboratorio de Mamíferos Marinos (Puerto Madryn, Argentina); MACN= Museu Argentino de CienciasNaturales Bernardino Rivadavia (Buenos Aires, Argentina); MCN= Museu de Ciências Naturais da FundaçãoZoobotânica do Rio Grande do Sul (Porto Alegre, Brazil); MZV= Museu de Zoologia de Vertebrados (Montevideo,Uruguay); MVZ= Museum of Vertebrate Zoology (Berkeley, USA); NMNH= National Museum of Natural History(Washington D.C.); UAM= University of Alaska Museum; UFSC= Universidade Federal de Santa Catarina(Florianópolis, Brazil); UMICH= University of Michigan (Ann Arbor, USA). (*) Pictures by Dr. Sylvia Brunner(Alaska University Museum); (#) Information available only upon request.

Arctocephalus australis

Coll. Nº Sex CS CCB Sut. Age AgeFCIEN A 21 DS 4 � 23.59 15.73 10 1MCN 2834 � 25.18 15.97 9 1MCN 2682 � 26.51 16.12 9 0MCN 2692 � 26.88 16.22 9 0MCN 2457 � 25.52 16.26 10 1MCN 2647 � 26.94 16.42 10 1MCN 2839 � 25.28 16.71 10 1MCN 2702 � 26.13 16.77 9 0UFSC 1147 � 29.28 16.85 9 1MCN 2500 � 27.27 17.02 9 1UFSC 1272 � 29.67 17.23 10 #MCN 2684 � 28.69 17.35 10 1MCN 2638 � 27.18 17.57 10 2MCN 2537 � 28.96 17.59 9 3UFSC 1111 � 29.54 17.67 9 #MCN 2650 � 26.48 16.46 12 2MZV 435 � 25.45 17.1 10 1UFSC 1096 � 29.72 17.13 11 #MCN 2634 � 28.37 17.35 9 1MACN 20570 � 26.77 17.4 11 -UFSC 1283 � 28.33 17.51 11 #MCN 2628 � 26.60 17.84 13 1UFSC 1282 � 27.76 17.89 11 #MCN 2529 � 29.68 17.98 12 1MCN 2606 � 29.34 18.12 13 3UFSC 1135 � 35.67 22 8 -UFSC 1156 � 34.22 22 18 #UFSC 1143 � 36.93 22.2 19 #UFSC 1157 � 37.28 22.4 19 #UFSC 1153 � 35.75 22.54 18 -UFSC 1142 � 38.02 22.7 19 #UFSC 1158 � 39.12 23 26 #UFSC 1163 � 40.79 23 29 #UFSC 1063 � 36.64 23.2 25 -UFSC 1160 � 39.53 23.2 18 #UFSC 1170 � 38.36 23.4 29 #UFSC 1154 � 37.66 23.5 20 #UFSC 1169 � 38.43 24 21 #MCN 2688 � 43.94 24.24 24 10


LAJAM 6(2): 139-154, December 2007

FCIEN 1584 � 18.93 13.19 9 -FCIEN 434 � 21.62 14.49 9 0UFSC 1139 � 24.68 15.11 9 #MCN 533 � 23.68 15.14 9 -MCN 2694 � 23.18 15.43 9 1MCN 2690 � 23.51 15.44 9 0FCIEN 433 � 23.16 15.57 12 0MACN 25192 � 23.36 15.73 9 -MCN 1531 � 23.41 16.06 9 1UFSC 1137 � 24.81 16.11 10 -MCN 247 � 26.24 16.19 9 1MCN 2636 � 26.48 16.4 10 0UFSC 1141 � 28.27 16.56 9 -MCN 2683 � 25.95 16.9 9 1UFSC 1131 � 29 17.04 9 -MCN 2639 � 28.07 16.17 13 1UFSC 1040 � 28.57 17.48 11 #MACN 28261 � 25.16 17.73 11 -MCN 2644 � 28.51 17.75 13 4MZV 1517 � 31.63 18.2 16 4MCN 2625 � 27.88 - 12 2MZV 1523 � 30.43 19.19 29 -FCIEN AL961 � 33.36 20 - -FCIEN 1538 � 30.83 20 30 14MCN 2523 � 37.36 20 28 -MCN 2833 � 34.41 20 28 10MZV 1532 � 31.61 20.11 32 -MCN 2614 � 34.92 20.3 27 14MZV 1552 � 31.59 20.32 30 7MZV 1580 � 31.07 20.5 39 -MCN 2699 � 35.29 21.13 28 9FCIEN 1527 � 30.91 21.19 25 -FCIEN 336 � 31.72 21.72 29 11FCIEN 1529 � 32.07 21.73 23 -FCIEN 1550 � 37.01 24.39 26 11UFSC 1133 � 35.33 29.54 19 #

Callorhinus ursinus

Coll. Nº Sex CS CCB Sut. Age AgeMZV 114107 � 214.542 12.93 9 0MZV 115223 � 342.167 19.28 10 3CAS 22829 � 266.568 13.2 9 -CAS 2323 � 254.386 13.55 9 0CAS 26753 � 269.104 15.37 9 -CAS 4655 � 296.989 16.93 9 2CAS 3845 � 233.996 19.85 15 4MZV 115218 � 332.438 18.44 14 3MZV 115224 � 323.052 19.12 16 4MZV 35085 � 331.588 18.95 16 3CAS 3070 � 336.563 17.81 11 2CAS 3696 � 384.514 19.26 15 -CAS 4656 � 371.644 20.83 14 5CAS 4468 � 404.831 20.71 15 4CAS 3151 � 469.817 24.65 20 -CAS 545 � 425.393 28.37 29 9UMICH 114794 � 278.803 18.87 - -UMICH 114793 � 280.559 18.81 - -NMNH* 285726 � 364.135 23.06 33 -NMNH* 285653 � 387.057 24.04 28 -NMNH* 285665 � 419.181 25.33 30 -NMNH* 47080 � 405.045 24.98 19 -


LAJAM 6(2): 139-154, December 2007

MZV 43 � 343.644 24.01 26 -NMNH* 285684 � 398.729 22.07 31 2NMNH* 285694 � 387.280 23.72 20 4NMNH* 285697 � 402.634 23.65 27 3CAS 23153 � 406.728 12.85 9 -CAS 23831 � 211.166 13.66 9 0CAS 23145 � 211.166 13.58 9 -CAS 23829 � 210.265 13.2 9 0CAS 23835 � 235.537 13.94 9 -CAS 26760 � 239.410 14.4 9 -CAS 23832 � 236.604 14.16 11 0MZV 115227 � 296.393 16.85 11 2CAS 2322 � 307.635 16.36 11 1CAS 4185 � 293.647 19.58 12 3CAS 4682 � 292.519 17.03 12 -CAS 4235 � 296.029 19.51 23 5CAS115228 � 304.093 18.01 23 7CAS 21497 � 381.839 20.18 34 -CAS 23101 � 306.776 16.59 24 -CAS 2329 � 386.688 19.51 19 6CAS 4564 � 370.351 18.73 18 7CAS 1894 � 305.949 19.25 25 7CAS 2402 � 341.551 19.15 28 -CAS 3081 � 320.004 18.06 21 10CAS21243 � 343.078 18.3 30 -UAM 11492* � 290.226 17.92 20 -UAM 11497* � 312.306 19.44 25 -NMNH 286143* � 299.077 18.62 22 6AMNH 3800* � 270.482 17.16 18 -

Otaria byronia

Coll. Nº Sex CS CCB Sut. Age AgeFCIEN 1202 � 220.856 15.11 9 0CNP 115 � 257.928 15.49 9 0MACN 30236 � 246.002 16.88 9 -LAMAMA 62 � 236.171 17.16 9 -LAMAMA 115 � 243.689 17.55 9 0LAMAMA 134 � 274.455 18.43 10 0MACN 125 � 295.501 21.14 9 -MACN 20595 � 309.940 22.23 14 2LAMAMA 555 � 332.540 23.95 - -LAMAMA 31 � 358.622 24.73 14 3MACN50.52 � 363.366 24.85 13 3LAMAMA 24 � 356.799 25.05 13 2CENPAT 160 � 364.590 25.24 16 -MCN 2610 � 462.272 25.88 15 5MACN 21743 � 364.699 26.1 15 -LAMAMA 487 � 397.021 26.21 17 -LAMAMA 105 � 352.305 26.32 15 5UFSC 1161 � 375.044 26.43 13 2LAMAMA 270 � 355.093 26.55 14 0LAMAMA 43 � 400.319 26.86 15 5MACN 25.45 � 403.084 27.15 15 4MCN 2525 � 427.622 27.35 14 5UFSC 1168 � 395.835 28.64 15 2MACN 20420 � 447.971 29.29 15 4LAMAMA 337 � 412.758 29.69 15 7GEMARS 667 � 540.036 32 17 -LAMAMA 90 � 329.387 25.73 22 3UFSC1152 � 379.361 26.56 15 1MZV 28 � 525.993 29.67 23 7


LAJAM 6(2): 139-154, December 2007

LAMAMA 60 � 412.408 30.49 20 6MACN 20583 � 542.353 30.98 26 8MZV 87001 � 571.605 31.88 36 -LAMAQ 1134 � 497.132 31.9 23 -LAMAQ 1140 � 479.440 32 21 7MCN 2990 � 552.200 32.27 33 9MACN 41226 � 478.253 32.4 26 -GEMARS 171 � 532.548 32.45 36 #GEMARS 353 � 524.341 32.52 26 #MCN 2505 � 558.594 32.95 20 7MCN 2696 � 569.611 33.15 27 6MZV 1181 � 543.199 33.43 21 9UFSC 1171 � 538.996 33.5 36 -MCN 2460 � 576.586 33.58 30 14GEMARS 284 � 519.106 33.84 30 #MACN 20168 � 446.280 34.34 32 -GEMARS 658 � 543.883 34.39 31 -CENPAT 111 � 158.295 9.98 9 0MACN 21740 � 230.889 14.99 9 0LAMAMA 70 � 250.979 16.53 9 0MACN 21737 � 322.395 20.69 17 -MACN 21741 � 148.127 9.58 9 0MACN 10.30 � 157.847 12.21 9 0LAMAMA 237 � 297.321 20.89 12 2FCIEN 1196 � 282.251 22.4 15 -LAMAMA 483 � 338.476 22.59 16 -MACN 21738 � 337.451 22.69 16 -LAMAMA 240 � 316.188 22.89 15 3FCIEN 332 � 335.863 22.9 15 3LAMAMA 243 � 339.389 23.44 15 7LAMAMA 127 � 326.419 23.94 16 6LAMAMA 251 � 326.602 24.12 16 -LAMAMA 33 � 340.558 24.21 15 6LAMAMA 536 � 330.940 25.25 15 -LAMAMA 303 � 367.634 25.32 17 3MACN 20573 � 340.015 25.33 15 -MCN-M 2691 � 446.209 25.5 17 7LAMAMA 61 � 371.000 25.12 29 10MACN 25138 � 335.881 25.28 23 5MACN 90.03 � 392.383 25.33 23 11LAMAMA 478 � 351.266 25.34 - -MACN 20578 � 367.904 25.67 23 -LAMAMA 89 � 377.546 25.83 30 -LAMAMA 88 � 369.004 25.87 29 10MCN 2701 � 449.707 25.96 22 8MACN 20576 � 375.854 26.31 27 -MACN 20596 � 443.583 26.7 28 12MCN 2462 � 385.647 26.9 20 13MCN 2703 � 470.011 27.48 24 9MACN 13.11 � 409.025 27.8 27 9MZV 1188 � 465.070 30.48 17 11MACN 20572 � 352.886 26.75 29 -GEMARS 428 � 533.254 33. 53 36 #


LAJAM 6(2): 139-154, December 2007

APPENDIX 2

ANATOMICAL DESCRIPTION OF THE LANDMARKS

1 Anteriormost point of the pre-maxilla tuberosity 2 Antero-lateral extremity of third incisive alveolus 3 Anteriormost point of incisive foramen 4 Lateral extremity of canine alveolus 5 Anteromedial point of first post-canine alveolus 6 Anteriormost point of the maxilla-palatine suture 7 Point that label the direction change of the maxilla-palatine suture 8 Posteriormost point of the root at the lateral limit at bone palate of zigomatic process of the maxilla 9 Posteriormost point of sixth post-canine alveolus10 Posteriormost point of palatine extension of maxilla (“pterygoid” process of the maxilla)11 Posteriormost point of interpalatine suture12 Point that label the direction change of the posterior border of palatine13 Posteriormost extremity of oval foramen14 Lateral extremity of jugal-esquamosal suture15 Medial extremity of the contact between the glenoid fossa and the ectotympanic16 Anteriormost extremity of the anterior aperture of carotid canal17 Antero-lateral corner of mastoid process18 Posteriormost point of the condiloid foramen19 Posteriormost point of occipital condyle20 Anteriormost point of foramen magnum

Received 18 March 2007. Accepted 30 November 2007.


1 Universidade Federal do Amazonas - UFAM, Manaus, AM, Brazil.2 Universidade Federal do Amazonas - UFAM, Departamento de Morfologia - ICB, Laboratório de Histologia, Manaus, AM, Brazil.3 Instituto Nacional de Pesquisas da Amazônia - INPA, Laboratório de Mamíferos Aquáticos, Caixa Postal 478, Manaus, AM,

69011-970, Brazil.* Corresponding author, e-mail: [email protected]

AGE ESTIMATION IN GIANT OTTERS (PTERONURA BRASILIENSIS)(CARNIVORA: MUSTELIDAE) USING GROWTH LAYER GROUPS IN CANINE TEETH

GABRIEL DA CRUZ DE OLIVEIRA1, JOSÉ FERNANDO MARQUES BARCELLOS2 AND FERNANDO CÉSAR WEBER ROSAS3

ABSTRACT: The canines of six giant otters Pteronura brasiliensis (5 males and 1 female) from the zoological collection of theNational Institute of Amazonian Research (INPA) were analyzed for age estimation. Of these, two were from known-ageindividuals of 2 and 5 years. Ages were read counting the Growth Layer Groups (GLGs) observed in thin sections (30μm) ofdecalcified teeth. GLGs were present in the dentine but were not conspicuous; age estimates were only reliable when countedin the cementum. Periodicity of GLGs and age estimates were calibrated with the known-age individuals. Results revealed anannual deposition pattern of GLGs in the cementum of giant otter canines, and no apparent differences were found in the GLGpatterns observed between males and females, or between captive and free-ranging individuals. The youngest and oldest giantotters analyzed were 2 and 20 years old, respectively. These results suggest that the longevity of captive giant otters is around20 years. The age determination technique applied here proved to be useful for age estimation in giant otters and can contributeas a powerful tool for future studies on the population dynamics of P. brasiliensis, which is currently classified as endangered.

RESUMO: Dentes caninos de cinco machos e uma fêmea de ariranha depositados na Coleção de Mamíferos do Instituto Nacionalde Pesquisas da Amazônia foram analisados para estimativa de idade nesta espécie. Desses, dois eram animais de idadeconhecida, com idades de 2 e 5 anos. As idades foram lidas contando-se o número de camadas de crescimento (GLGs) observadasem secções finas (30μm) de dentes. Embora se observem GLGs na dentina, essas não são conspícuas. Estimativas confiáveis deidade puderam ser feitas somente no cimento. O padrão de deposição dos GLGs e as idades estimadas no cimento dos caninosde ariranha foram calibrados com os animais de idade conhecida e os resultados revelaram um padrão de deposição de umGLG por ano. Não foram encontradas diferenças no padrão de deposição dos GLGs entre machos e fêmeas e tampouco entreanimais cativos e de vida livre. A mais jovem e a mais velha das ariranhas analisadas nesse estudo tinham 2 e 20 anos,respectivamente. Esses resultados sugerem que a longevidade de ariranhas cativas está próxima dos 20 anos de vida. A técnicade determinação de idade aqui utilizada revelou ser útil para estimativa de idade em ariranhas e pode contribuir como umavaliosa ferramenta para futuros estudos de dinâmica populacional dessa espécie ameaçada de extinção.

KEYWORDS: Teeth, age, growth layers, Pteronura brasiliensis, giant otter.

Introduction

The giant otter (Pteronura brasiliensis) is currentlyclassified by The World Conservation Union as an“endangered species” (IUCN, 2006). However, virtuallynothing is known about the population dynamics of thisspecies and its longevity is still controversial in theliterature. According to Staib (2005), the longevity offree-ranging giant otters is 11 years, while for captiveanimals the reported longevity is 20 years (F.Brandstätter, pers. comm.).

Age composition is a vital parameter to assess thedynamics of any mammalian population (Scheffer &Myrick, 1980), especially when dealing with threatenedspecies. Growth Layer Groups (GLGs) observed in thedentine and cementum of mammalian teeth are widelyused to estimate age in odontocete cetaceans (Perrin &Myrick, 1980; Hohn et al., 1989). According to Klevezal(1996), the methods used to estimate age in mammalsalso include counting GLGs in the dentine andcementum of teeth. In carnivores, however, countingcementum layers is the most widely used method forage determination (Klevezal, 1996). Cementum layerswere used to estimate age in river otters (Lontracanadensis) (Tabor & Wight (1977), Eurasian otters (Lutra

lutra) (Heggberget, 1984), and sea otters (Enhydra lutris)(Bodkin et al., 1997). According to Bodkin et al. (1997),variation in the GLGs deposited in the cementum occursamong and within species and may be caused byphysiological (reproduction, estivation or nutrition) orenvironmental (temperature or daylight) factors.Therefore, the periodicity of cementum layers in giantotter teeth has to be tested and validated with known-age individuals.

According to Sykes-Gatz (2005), field biologists andinstitutions that hold giant otters in captivity are in needof accurate information regarding the age of sexualmaturity, body weight/length relationships and growthcurves, which can only be obtained after establishing areliable method for age determination. Therefore, themain objective of this study was to test the ageestimation technique using thin teeth sections from giantotters in order to verify its efficiency in this species.


One upper canine tooth (Figure 1) was extracted fromeach of the five giant otter skulls deposited in theMammal Collection of the National Institute of

156 G.C.OLIVEIRA, J.F.M.BARCELLOS AND F.C.W.ROSAS

LAJAM 6(2): 155-160, December 2007

Amazonian Research (INPA). These five individualswere all captive males that had been kept in the INPAfacilities up to their deaths (Table 1). One of the captivemale otters (named Ticuna) was donated to INPA bythe Cousteau Society team in 1982, when it wasalready an adult animal. This otter died 10 years later,in August 1992 (Table 1). The other captive animalswere wild-caught otters by riverine people, whocapture otter pups to sell as pets to tourists in theAmazon region. These otters were confiscated byIBAMA, the Brazilian Institute of the Environmentand Natural Resources and taken to the INPAfacilities to be raised. Their age when they arrived incaptivity (based on size and weight), the time spentin captivity, their total length at death, and theestimated age (counting the GLGs in the cementum)are presented in Table 1. Additionally, one uppercanine tooth was analyzed from a free-ranging femalegiant otter (see Table 1), which was found dead inBalbina hydroelectric lake in February 2002 (Rosas andde Mattos, 2003).

Bodkin et al. (1997) consider a known-age sea otter asbeing an individual less than one year old based onlyon its weight. We used a similar criterion to defineknown-age giant otters in this study.However, we took into account not only theweight, but also the size of the otters whenthey arrived at INPA. Only otters estimatedto be #6 months old were considered to beof known age.

All the teeth analyzed in this study were keptdry and maintained at air temperature untilthey were prepared for age estimation. Theage estimation technique applied followedthe method described by Hohn et al. (1989)and Rosas et al. (2003), with somemodifications as follows.

Decalcification and sectioning

After the extraction, all external and internalpulp cavity tissues were removed by boilingthe teeth. The most external lateral portionsof the teeth were then removed using adiamond saw (Isometâ) in order to allow foran easier and better decalcification process.After that, the teeth were left in a 10%formaldehyde solution for 24 hours andsubsequently decalcified in RDO®, acommercial decalcifying agent.

While in RDO, the teeth were periodicallymonitored in order to avoid over-decalcification, which precludes reliable GLGcountings. Insufficient decalcification time, onthe other hand, will damage the microtomeblades and prevent acquiring intact sections.

The decalcified teeth were then sectioned

longitudinally using a freezing microtome followingthe labial-lingual plane. Section thickness was adjustedto 30μm and only central or close-to-center sections,which presented at least 50% of the pulp cavity, wereselected for age estimation.

Staining

The thin sections were left in Harris’ hematoxilin for 3to 5 minutes and then washed in running water forapproximately 5 minutes to remove the excesshematoxilin, as recommended by Rosas et al. (2003).Afterwards, they were put in a 1% sodium boratesolution to increase the contrast between layers andthen washed in running water for 10 minutes,according to Molina and Oporto (1993).

Slide mounting and growth layer readings

The stained sections were placed into a 1:1 mixture ofglycerin and distilled water for 5-10 minutes and thentransferred to 100% glycerin for over 5 hours. Thesections were then mounted between microscope slidesand coverslips, and sealed with Entellan®.

Figure 1. Upper canine tooth of giant otter (Pteronura brasiliensis). The scale is incentimeters.

AGE ESTIMATION IN GIANT OTTERS 157

LAJAM 6(2): 155-160, December 2007

Both the dentine and cementum of the giant otter teethsections were observed for GLGs under a transmittedlight microscope. However, it was only possible todetermine a reliable age in the cementum. Age readingswere carried out counting GLGs following themethodology described by Hohn et al. (1989). At leastfive readings were performed on each tooth sectionwith a minimum interval of 3 days between readings.Age was estimated without access to biometric andbiological data, thereby avoiding reader bias.Assuming that reading skill increases with time(Pinedo and Hohn, 2000), the estimated age was takenas the last reading. Age estimations were calibratedusing deposition rates in teeth from the known-ageindividuals, allowing the identification of theperiodicity of GLG deposition in giant otter teeth.

Results

Decalcification time of giant otter teeth varied from 13hours for younger individuals up to a maximum of 23hours for older adults, with a mean decalcification timeof 17.5 hours. No age estimates could be carried out inthe dentine due to a lack of conspicuousness of GLGs inthis part of the teeth. However, the GLGs were readilyobserved in the cementum. Two major types of layerswere identified: one thick unstained layer followed byone thin stained layer (Fig. 2). There was no differencebetween the GLG deposition observed in captive giantotters and the free-ranging individual analyzed. Norwere there differences observed between the GLGpatterns in males when compared with the patternpresented by the female analyzed. The results revealedthat age estimates corroborate the real ages of theknown-age individuals. Nevertheless, due to theramified layers sometimes observed in the giant otters‘teeth, it is important to follow the GLGs throughout thetooth root in order to avoid counting these ramifiedlayers as two different annual layers. The agreementbetween the ages estimated by GLG counting and thoseof known-age animals, allowed us to assume that GLGs

in the cementum of giant otter teeth follow an annualdeposition. The youngest and oldest individuals in oursample were 2 and 20 years old, respectively (Figures2a and 2c). Worn, missing and broken teeth wereobserved in the 20 year-old giant otter, suggesting thatthis is an advanced age for P. brasiliensis.

Discussion

According to Heggberget (1984), the possibilities ofageing European otters (Lutra lutra) from their externalcharacteristics are very limited because of their rapidgrowth. This is also true for the giant otter, asobservations of captive P. brasiliensis show that one-yearold animals are very difficult to distinguish from olderindividuals based on their size (F. Rosas, pers. obs.).According to Klevezal (1996), counting cementum layersis the standard when ageing carnivores, and this wasthe methodology used by Tabor and Wight (1977),Heggberget (1984) and Bodkin et al. (1997) to estimateages in river otters, Eurasian otters and sea otters,respectively. Although the former authors do notmention anything about dentine layers in the otterspecies they work with, the reason for not using them isprobably due to the lack of conspicuousness of thedentine layers, as observed here for giant otters.

Different methods have been used to prepare otters‘ teethfor age estimation, and all of them used thin sections,varying from 14 to 30μm, which were decalcified andstained in buffered formic acid, nitric acid and inhydrochloric acid, and stained in PapanicolauHematoxylin Stain Solution or Giemsa solution (Taborand Wight, 1977; Heggberget, 1984; Bodkin et al., 1997).The methodology applied in the present study with giantotters followed the method largely used for odontocetecetaceans (Hohn et al., 1989), which also proved to beuseful for giant otter age estimates in the cementum ofcanine teeth. However, we use Harris‘ hematoxylin, assuggested by Rosas et al. (2003), instead of Mayer‘shematoxylin as recommended by Hohn et al. (1989).Harris‘ hematoxylin is much more efficient in staining

ANIMAL

IDENTIFICATION SEX ORIGIN ESTIMATED AGE

WHEN ARRIVED IN

CAPTIVITY (YEARS)

TOTAL LENGTH

(IN cm) AT DEATH TIME IN

CAPTIVITY (YEARS)

ESTIMATED AGE

FROM GLGS (YEARS)

Ticuna M Wild-caught Adult (age unknown) 155 10 20

Kiwá M Wild-caught 0.4* 157 5 5

Sammy M Wild-caught 0.5* 160 1.5 2

Frank M Wild-caught ?? 163 0.6 2

Kiwi M Wild-caught ?? 149 3 6

Balbina #1 F Found dead in the wild --- 150 --- 2

Table 1. Characteristics of the giant otters used in this study.

* Those otters which arrived at INPA with ages equal to or less than 0.5 year old were considered as known-age individuals.


LAJAM 6(2): 155-160, December 2007

thin sections, reducing the time of staining from 20-30minutes when using Mayer‘s hematoxylin, to 3-6 minuteswhen using Harris‘ hematoxylin. Additionally, Harris‘

hematoxylin sections last longer when compared toMayer‘s hematoxylin sections, which usually becomefaded a few months after preparation.

Figure 2. Tooth sections of giant otters showing the growth layer groups in the cementum. A known-age otter of two years of age (A),a known-age otter of five years of age (B), and a twenty year-old otter (C).

AGE ESTIMATION IN GIANT OTTERS 159

LAJAM 6(2): 155-160, December 2007

The validation of age estimated by counting GLGs inteeth is of primary importance, as the ability toaccurately estimate age is fundamental to study the agestructure in populations, as well as age-specificmeasures of reproduction, growth or survival (Bodkinet al., 1997). Despite not having any known-age animalsin their samples, the annual periodicity of the cementumlayers was determined by Tabor and Wight (1977) byanalyzing the ovary scars of river otters (Lontracanadensis), while Heggberget (1984) analyzed skulldevelopment in the European otter (Lutra lutra).However, the best validation of age estimates can beobtained when the sample contains known-agespecimens, as presented by Bodkin et al. (1997) for thesea otter (Enhydra lutris), and in this study for giant otters(Pteronura brasiliensis).

The complexity and difficulties in estimating age in otters‘cementum layers were presented by Bodkin et al. (1997),who analyzed the accuracy of age estimations betweenthree independent readers and compared their ageestimates with the age of known-age sea otters. Accordingto those authors, despite the fact that the differences werenot very evident when grouping the otters in age classes,they may contain large errors when estimating the ageof individual sea otters. However, according to Pinedo& Hohn (2000), estimated age accuracy tends to increasewith time, as readers‘ skills increase with experience. Thedifficulties observed by Bodkin et al. (1997) may also bedue to the fact that those authors used premolar sea otterteeth, while other age estimate studies in otters, includingthe present one, used the canines, which in carnivoresare conical (Fig. 1) and bigger than the premolars, makingage estimates easier.

The worn canine teeth, which can usually causeproblems when estimating age in the dentine (Rosas etal., 2003), did not become a problem in this study as ageestimates were performed in the cementum layers, andnormally cementum is less subjected to resorption(Klevezal, 1996).

According to Brandstätter (2005), the oldest giant otterin captivity died at the age of 17 years, but its twinbrother was still alive in 2005. Recent informationobtained in May 2008 revealed that this animal is stillalive and is 20 years old now (F. Brandstätter, pers.comm.), which is exactly the age of the oldest giant otteranalyzed in the present study. Considering the wornteeth observed in that individual, it is reasonable toassume that this is an advanced age for giant otters,which is probably very close to the longevity of thespecies. Nonetheless, for most species, longevity ofcaptive animals is not necessarily representative of thelongevity of free-ranging individuals. This seems to bethe case of giant otters, for which the longevity of free-ranging animals is estimated to be around 11 years basedon photo-identified otters (Staib, 2005).

Although the results presented here were based on asmall number of animals, they do show that the pattern

of GLGs observed in giant otter teeth is valuable forage estimation, as described for other species of otters(Tabor and Wight, 1977; Heggberget, 1984; Bodkin etal., 1997). Therefore, by using this method it is possibleto relate features of the giant otter life cycle to anabsolute time scale, thus greatly increasing theirimportance in understanding the population dynamicsof the species.

According to the results obtained, age estimates in thedentine of giant otter teeth using the thin section methodhere applied are not recommended due to the lack ofdefinition of GLGs in this structure. However, GLGsare very conspicuous and deposited on an annual basisin the cementum of giant otter canines as shown byknown-age animals, providing accuracy in determiningthe absolute age in this species. According to Klevezal(1996), absolute age can also provide valuableinformation to estimate an individual’s growth rate, andspecific characteristics of reproduction and feeding. Inaddition, future age estimates from giant otter teethdeposited in museums and zoological collections willprovide the establishment of growth curves for thespecies, as well as to determine with a higher degree ofprecision the age of sexual maturity in P. brasiliensis,which still needs to be defined.

Acknowledgements

We thank Kesä K. Lehti and Nélio Barros who kindlyrevised the English version of the manuscript. Dr. AletaHohn and an anonymous referee provided critical andinsightful comments on the manuscript. We also thankIngrid Karoline Albuquerque Ferreira who helped uswith the teeth photographs. This work was partiallyfunded by Conselho Nacional de DesenvolvimentoCientífico e Tecnológico (CNPq) by means of a grant toGabriel da Cruz de Oliveira (“Programa de IniciaçãoCientífica/UFAM/INPA”).

References

BODKIN, J.L.; AMES, J.A.; JAMESON, R.J.; JOHNSON, A.M. ANDMATSON, G.M. (1997) Estimating age of sea otters withcementum layers in the first premolar. Journal of WildlifeManagement 61 (3): 967-973.

BRANDSTÄTTER, F. (2005) Maximum age of giant otters incaptivity. Friends of the Giant Otter 12: 5.

DUPLAIX, N. (1980) Observations on the ecology and behaviourof the giant otter Pteronura brasiliensis in Suriname. RevueEcologique (Terre Vie) 34: 495-620.

HEGGBERGET, T.M. (1984) Age determination in the Europeanotter Lutra lutra. Zeitschrift für Säugetierkunde 49: 299-305.

HOHN, A.A., SCOTT, M.D., WELLS, R.S., SWEENEY, J.C. ANDIRVINE, A.B. (1989) Growth layers in teeth from known-age,free-ranging bottlenose dolphins. Marine Mammal Science5(4): 315-342.


LAJAM 6(2): 155-160, December 2007

IUCN (2006) 2006 IUCN Red List of Threatened Species.<www.iucnredlist.org>. Downloaded on 17 April 2007.

KLEVEZAL, G.A. (1996) Recording structures of mammals.Determination of Age and Reconstruction of Life History. A.A.Balkema Publishers, Rotterdam, The Netherlands, 274 pp.

MOLINA, D.M. AND OPORTO, J.A. (1993) Comparative study ofdentine staining techniques to estimate age in the Chileandolphin, Cephalorhynchus eutropia (Gray, 1846). AquaticMammals 19(1): 45-48.

PERRIN, W.F. AND MYRICK, A.C. (Eds) (1980) Age Determination ofToothed Whales end Sirenians. Reports of the International WhalingCommission (special issue 3). Cambridge, U.K., 229 pp.

Pinedo, M.C. and Hohn, A.A. (2000) Growth layer patterns inteeth from the franciscana, Pontoporia blainvillei: Developing amodel for precision in age estimation. Marine Mammal Science16(1): 1-27.

ROSAS, F.C.W., BARRETO, A.S. AND MONTEIRO FILHO, E.L.A. (2003)Age and growth of Sotalia guianensis (Cetacea, Delphinidae)

on the coast of Paraná State, southern Brazil. Fishery Bulletin101(2): 377-383.

ROSAS, F.C.W. AND DE MATTOS, G.E. (2003) Natural deaths ofgiant otters (Pteronura brasiliensis) in Balbina hydroelectric lake,Amazonas, Brazil. IUCN Otter Specialist Group Bulletin 20(2): 62-64.

SCHEFFER, V.B. AND MYRICK, A.C. (1980) A review of studies to1970 of growth layers in the teeth of marine mammals. Pages51-63 in PERRIN, W.F. AND MYRICK, A.C. (Eds) Age Determinationof Toothed Whales and Sirenians. Reports of the InternationalWhaling Commission (special issue 3). Cambridge, U.K.

STAIB, E. (2005) Eco-etologia del lobo de río (Pteronura brasiliensis)en el sureste del Perú. Sociedad Zoologica de Francfort Peru.Lima, Peru, 195 pp.

SYKES-GATZ, S. (2005) International Giant Otter Studbook.Zoologischer Garten Dortmund, Dortmund, Germany, 120pp.

TABOR, J.E. AND WIGHT, H.M. (1977) Population status of riverotter in Western Oregon. Journal of Wildlife Management 41(4):692-699.

Received 23 July 2007. Accepted 30 November 2007.


1 Museu Oceanográfico Prof. “Eliézer C. Rios”, Fundação Universidade Federal do Rio Grande, Rio Grande, RS, 96200-970, Brazil.E-mail: [email protected].

2 Department of Zoology and Marine Mammal Research Unit, Fisheries Centre, University of British Columbia, Room 247, AERL, 2202Main Mall, Vancouver, B.C. V6T 1Z4, Canada.

ACTIVITY bUDGETS AND dISTRIBUTIONOF bOTTLENOSE dOLPHINS (TURSIOPS TRUNCATUS)IN THE PATOS LAGOON eSTUARY, sOUTHERN BRAZIL

PAULO H. MATTOS1, LUCIANO DALLA ROSA1,2 AND PEDRO F. FRUET1

Abstract: The common bottlenose dolphin, Tursiops truncatus, is one of the world’s best known cetaceans. However, there arefew studies on the activity budgets and distribution of this species along the Brazilian coast. This study aimed at describing andquantifying the behavioral activity of T. truncatus in the Patos Lagoon Estuary, Rio Grande do Sul state, southern Brazil (ca.32o09’S, 52o05’W). The study area was divided into three sub-areas according to the proximity to the estuary mouth. The behavioraldata were gathered every 5 minutes following a focal group sampling approach. A total of 34 boat surveys were conductedbetween December 2001 and January 2003, totaling 66.95h of direct observation and 672 records of behavioral activities. Thefirst 15 minutes of each group encounter were discarded to avoid the influence of the boat approach on dolphin behavior. Themost observed behavior was feeding (37.64%), followed by traveling (29.17%), travel-feeding (21.87%), socializing (5.8%), milling(4.33%) and resting (1.19%). There was not a significant difference among the frequencies of commonly observed behaviors:feeding, traveling and travel feeding (p>0.05, t-test for proportions). Dependence between activity and season was detected insubareas I and II (p<0.001; Pearson’s X2), as well as an association between activity and sub-areas (p<0.001; Pearson’s X2).Regarding group size, 56.41% of the activities recorded were carried out by groups of 1 to 3 dolphins, 31.63% from 4 to 6,10.25% from 7 to 10, and 1.71% by groups with more than 10 individuals. This study confirmed the importance of the PatosLagoon Estuary as an area for bottlenose dolphins to conduct their daytime activities, in particular feeding.

Resumo: O boto ou golfinho nariz-de-garrafa, Tursiops truncatus, é um dos cetáceos mais bem conhecidos no mundo. Entretanto,existem poucos estudos sobre a atividade comportamental e distribuição desta espécie ao longo da costa brasileira. O objetivo destetrabalho foi descrever e quantificar os comportamentos de T. truncatus no Estuário da Lagoa dos Patos, Rio Grande do Sul, Brasil(32°09’S, 52°05’W). A área de estudo foi dividida em três subáreas de acordo com a proximidade da desembocadura do estuário. Osdados comportamentais foram registrados a cada 5 minutos seguindo a metodologia de amostragem de grupo focal. Um total de 34saídas foram conduzidas entre dezembro de 2001 e janeiro de 2003, totalizando 66,95h de observações diretas e 672 registros deatividades comportamentais. Os primeiros 15 minutos de cada grupo encontrado foram descartados a fim de evitar qualquer influênciada aproximação da embarcação no comportamento dos animais. O comportamento mais observado foi alimentação (37,64%), seguidopor deslocamento (29,17%), deslocamento com alimentação (21,87%), socialização (5,8%), milling (4,33%) e descanso (1,19%). Nãohouve diferença significativa entre as freqüências de comportamento mais comuns: alimentação, deslocamento e deslocamento comalimentação (p>0.05, teste t para proporções). Detectou-se uma dependência entre o tipo de atividade e a estação do ano nas subáreasI e II (p<0,001, Pearson’s X2), assim como uma associação entre o tipo de comportamento e a subárea (p<0,001, Pearson’s X2). Comrespeito ao tamanho do grupo, 56,41% das atividades registradas foram realizadas por grupos de 1 a 3 indivíduos, 31,63% de 4 a 6,10,25% de 7 a 10 e apenas 1,71% por grupos com mais de 10 indivíduos. Este estudo confirma a importância do Estuário da Lagoa dosPatos como área para os botos executarem suas atividades diurnas, em especial a alimentação.

Keywords: common bottlenose dolphin, Tursiops truncatus, activity budget, behavioral ecology, distribution, group size, Brazil.

Introduction

The common bottlenose dolphin (Tursiops truncatus) isfound in temperate and tropical waters worldwide. Thespecies is common in pelagic as well as coastal waters,where they are often found in bays and tidal creeks, andare even known to travel up rivers (Leatherwood et al.,1983a; Rice, 1998; Cubero-Pardo, 2007). The existence ofseveral nearshore populations and some long-term studieshas made T. truncatus one of the best known cetaceans,with described coastal and offshore forms or ecotypes(Leatherwood et al., 1983a; Segura et al., 2006) which differin physiology, morphology, and ecology (Duffield et al.,1983; Hersh and Duffield, 1990; Mead and Potter, 1990).

In Brazilian waters, the common bottlenose dolphin hasbeen reported from the northeastern (Alves Júnior et al.,1996) to the southern (Simões-Lopes, 1991; Castello and

Pinedo, 1977) coasts. In the state of Rio Grande do Sul,southern Brazil, bottlenose dolphins are commonly foundin coastal waters, forming small populations or sub-populations associated with river and estuary mouths(Möller et al., 1994). However, there have been few studieson their behavior along the Brazilian coast (Pryor andLindbergh, 1990; Möller, 1993). Bottlenose dolphins inthe Patos Lagoon estuary, southern Brazil, form a smalland resident population estimated at 83 dolphins (95%CI: 72-90; Dalla Rosa, 1999). A previous study on thebehavioral activities of this population showed thatdolphins used the area for all activities, especially feeding,and usually concentrated near the estuary mouth in smallgroups of up to 5 individuals (Möller, 1993).

The opportunistic feeding habits of T. truncatus aredemonstrated by its use of various foraging strategies(Shane, 1990). Bottlenose dolphins feed upon a wide

162 P.H.MATTOS, L. DALLA ROSA AND P.F.FRUET

LAJAM 6(2): 161-169, December 2007

Figure 1. Map of the study area in the Patos Lagoon estuary. Romannumbers indicate the three sub-areas.

3 DNPVN (1941) Enchentes de maio de 1941. Diretoria Nacional de Portos e Vias de Navegação. Relatório Técnico, Porto Alegre.

variety of fish, including small rays and sharks, as wellas cephalopods (squid and octopus), and occasionallyshrimp (Leatherwood, 1975; Barros and Odell, 1990;Mead and Potter, 1990; Cockcroft and Ross, 1990).Whereas this wide range of feeding habits has led, alongwith social interactions, to the documentation of severaltypes of behavioral events, their activity budgets aregenerally described in terms of four major categories:feeding, traveling, socializing and resting (Shane et al.,1986). Studies on behavioral ecology lead to a betterunderstanding of habitat use and of the potential impactsof habitat degradation and incidental mortality. This isparticularly important for the management of smallcoastal populations of cetaceans. In this paper, we presentnew information on activity budgets and distribution ofbottlenose dolphins in the Patos Lagoon estuary.


The Patos Lagoon estuary (31°50’S, 52°20’W; Figure 1)is a nursery area for several commercially importantspecies of fish from this region, including Micropogoniasfurnieri, Cynoscion guatucupa, Paralonchurus brasiliensis

and Menticirrhus americanus (Chao et al., 1985; Vieira andScalabrin, 1991; Vieira, 2006). Located along the coastalplain of Rio Grande do Sul state, in southern Brazil,Patos Lagoon is the largest choked lagoon in the world(Kjerfve, 1986) and is characterized by industrial andartisanal fisheries, tourism, port activities and oilrefinery, fertilizer and fish processing plants (Taglianiet al., 2003). The Patos Lagoon is connected to theAtlantic Ocean through a narrow channel (0.5-3km),which is secured by two rock-jetties at the estuary mouth(Seeliger et al., 1997). Marine water influx at this mouthcan reach 1.3m s-1, and freshwater discharge after longperiods of rain can result in currents of up to 1.7-1.9m s-

1 (DNPVN, 1941)3. The marine water intrusion is favoredduring periods with higher temperatures, lowerprecipitation and southwesterly winds, leading tohigher salinity values in the estuary. Increasedfreshwater runoff and lower salinity values are observedduring periods of high precipitation or prevailingnortheasterly winds (e.g. Möller and Castaing, 1999).Mean water temperature ranges from about 25o C inJanuary (warmest month) to 12o C in July (coldestmonth) (Laboratório de Tartarugas e MamíferosMarinhos-FURG, unpublished data).

The study area was divided into three sub-areasaccording to the proximity to the mouth of the estuary,being sub-area I closest and sub-area III more distantfrom the entrance. Sub-area I comprises approximately10km2, sub-area II 20km2 and sub-area III about 10km2

(Figure 1). On occasion surveys extended to theadjacent coastal waters up to about 3km north andsouth of the estuary mouth.

Thirty-four boat surveys were conducted fromDecember 2001 to January 2003. We used a 5.5maluminum boat with a 50hp outboard engine. Thesurvey design followed a zig-zag transect from northto south along the study area to increase the chance ofencountering dolphin groups. Behavioral data werecollected following the Focal Group Samplingapproach (Altmann, 1974), in which the behavior of afocal group, characterized by the presence of at leastone animal with identifiable natural markings, wasrecorded every 5 minutes. Approximately 51.5% of theindividuals of the Patos Lagoon population showconspicuous long-lasting marks (Dalla Rosa, 1999)facilitating the use of this methodology.

A group was defined as any number of dolphinsobserved in apparent association, moving in the samedirection, within 30m of any individual in the groupand often, but not always, engaged in the same activity(see Shane, 1990). When a group was sighted, weslowly approached the group to minimize disturbanceand recorded the time, sub-area, group size andgeographic position using a hand-held GPS.

ACTIVITY BUDGETS AND DISTRIBUTION OF BOTTLENOSE DOLPHINS IN THE PATOS LAGOON ESTUARY, SOUTHERN BRAZIL 163

LAJAM 6(2): 161-169, December 2007

Figure 2. Activity budgets of bottlenose dolphins in the Patos Lagoon estuary, by sub-area.

Four major behavioral categories were considered in thisstudy: feeding, traveling, socializing and resting (Shane,1990). Feeding was characterized by the lack of directionalmovement. The animals generally surfaced and doveasynchronously while the entire group remained looselyaggregated over an area of several meters. Traveling wascharacterized by directional movement of a group,moving as a unit. Resting was characterized by low levelsof activity during which almost no forward movementof the animals occurred. A resting animal slowly rose tothe surface with its head and dorsal fin breaking the watersimultaneously. Socializing animals surfaced together ina tight aggregation and often remained at or near thesurface for several minutes. During this time, animalsexhibited prolonged body contact, often in the form ofslaps of the flukes or pectoral fins of one animal againstthe body of another.

Two additional categories included activities that didnot fit well into the behaviors described above: millingand travel-feeding. Milling involved frequent changesin heading with movements generally lackingcomponents of the other types of behavior (Shane, 1990).An association of traveling with feeding, travel-feedingwas characterized by animals moving consistently inone direction while foraging and feeding regularly.Although this category could potentially be consideredjust feeding, we deemed that its frequency of occurrenceand distinctive characteristics warranted a separateclassification (e.g. Bearzi, 2005).

The first 15 minutes of each group encounter werediscarded to avoid the influence of the boat approachon dolphin behavior. Observation periods were dividedinto three periods: 09:00-12:00h; 12:01-15:00h and 15:01-18:00h. Encounter rates of groups per hour of searchingeffort were calculated in order to adjust for unequaleffort in the sub-areas, allowingus to verify area use by seasonand by time of the day.

The Pearson’s X2 test (Zar, 1984)was used to investigateassociations among the type ofbehavior, season and sub-area.The t-test for difference ofproportions (Zar, 1984) wasused to verify if the frequenciesof the observed behavioralcategories were significantlydifferent. All tests wereperformed using a 5% level ofsignificance.

Results

Activity budgets

A total of 672 behavioral recordswere obtained during 66.95h ofdirect observation of dolphin

groups. Feeding was the most frequently observedactivity (37.64%), followed by traveling (29.17%), travel-feeding (21.87%), socializing (5.8%), milling (4.33%) andresting (1.19%). There was no significant differencebetween feeding, traveling and travel-feeding frequencies(t-test for proportions, p>0.05).

An association was observed between the activity andthe sub-areas (p<0.001; Pearson’s X2). All behavioralcategories were observed in sub-area I, where feedingwas the most frequent, followed by traveling (n=551;Figure 2). Greater total effort was spent in sub-area Ithan in sub-areas II and III, partly as a consequence ofhigher encounters rates in this area (see Table 1). Only101 behavioral observations were recorded in sub-areaII, where travel-feeding was the most frequent activity(36.63%). The number of observations in sub-area III wastoo small to be statistically analyzed (Figure 2).

An association between activity and season was detectedin sub-areas I and II (p<0.001; Pearson’s X2). Allbehavioral categories were observed during summer,when feeding and traveling were the most frequentactivities (n=218; Figure 3). During fall, travel-feedingwas the most frequently observed activity, whereasresting was not observed. Winter was the season withthe highest relative frequency of feeding, followed bytraveling and travel-feeding (n=124; Figure 3). Travelingwas the most frequent activity in spring, followed byfeeding (Figure 3). There was no significant differencebetween traveling and socializing during this season (t-test for proportions, p>0.05; Figure 3).

Regarding the distribution of activities according tothe daytime periods, most observations were madein the morning (09:00-12:00h; n=304), probably dueto increased survey effort. Feeding was the mostfrequent activity during this period (Figure 4).


LAJAM 6(2): 161-169, December 2007

SUB-AREA GROUPS EFFORT (h) ENCOUNTER RATE

I 102 29.02 3.51

II 11 26.01 0.42

III 4 11.54 0.34

Season

Summer 35 16.04 2.18

Fall 34 11.47 2.96

Winter 23 13.38 1.72

Spring 25 25.68 0.97

Daytime

09:00-12:00h 59 41.16 1.43

12:01-15:00h 40 19.21 2.08

15:01-18:00h 18 6.20 2.90

Table 1. Encounter rates (groups per hour) of bottlenose dolphinsin the Patos Lagoon estuary by sub-area, season and daytime period.

Figure 3. Activity budgets of bottlenose dolphins in the Patos Lagoon estuary, by season.

During the 12:01-15:00h period, we observed anincrease in both feeding and travel-feeding relative tothe other periods (n=210; Figure 4). Feeding andtraveling were the most frequent activity observedbetween 15:01h and 18:00h (n=158; Figure 4).

Distribution and Group Size

Bottlenose dolphins were present in the study area inall but one of the 34 surveys. A total of 117 groupswere recorded between the Porto Novo of the city ofRio Grande and the mouth of the estuary, includingadjacent areas. Most sightings occurred in sub-area I(Table 1; Figure 5).

The average group size was 4.05 dolphins (SD = 2.10).Group size frequencies were 25.63% for pairs, 20.66%for trios, 30.58% for groups of 4 to 6,9.91% for 7 to 10, and 2.48% for largergroups. Lone individuals accountedfor 10.74% of the sightings. Groupslarger than 4 individuals were themost common in sub-area I (29%),followed by pairs and trios (20.9%each), while pairs and trios were mostcommon in sub-areas II and III,respectively. Larger groups (>4) werealso the most common during springand summer (44 and 37.14%,respectively). Pairs predominatedduring fall (33.3%) and trios duringwinter (36.3%).

Discussion

Several techniques are available forrecording animal behavior. Mann

(1999) presents a review on behavioral samplingmethods for cetaceans and points out the potentialbiases of each method. According to this author, thefocal-group sampling is not recommended because ittends to bias towards most common or conspicuousbehaviors, therefore overestimating their relativeimportance in a group. Also, the focal-groupmethodology (Altman, 1974) was proposed for groupsin which all individuals were continuously visiblethrough the sampling period, and when theseconditions were not met, this method should only beapplied for individuals or pairs. Keeping in mind theselimitations, we still chose to use this approach forseveral reasons. Groups, as we defined them, tend tobe relatively small in our study area and engage in thesame activity, minimizing the potential biasesmentioned above. In addition, alternative methods alsopresent difficulties. In particular, individuals that arevisually identifiable from natural markings within areasonable distance tend to be older and possibly males(e.g. Wilson, 1995); therefore using an individual-follow protocol would bias sampling towards this ageand sex classes. Difficulties in distinguishing amongunmarked animals would also potentially biassampling methods such as scan sampling (Mann, 1999),where individuals should be sampled sequentially.And finally, for comparative purposes, we preferredto use the same method used in a previous study inthe same area (see Möller, 1993). Once sampling wasconcluded, we compared the behavioral frequenciesbetween groups of 1-2 individuals and groups of 3 ormore individuals to verify if there was any evidencethat the most common activities could have beenoverestimated in the larger groups, as suggested above.However, feeding actually decreased in larger groups,traveling and travel-feeding frequencies were similarand socializing and milling increased, suggesting thatthis type of bias was likely not important.

Effort refers to searching effort only.


LAJAM 6(2): 161-169, December 2007

Figure 4. Activity budgets of bottlenose dolphins in the Patos Lagoon estuary, by daytime period.

Figure 5. Distribution of the first activity recorded for each bottlenose dolphin group along the study area. Note that sampling ofbehavioral activities was not possible for all recorded dolphin groups.

Feeding was the most commonactivity recorded in sub-area I.Möller (1993) also observed ahigher amount of feeding inthis sub-area, although with alower relative frequency whichwas similar to socializing. Thisis not surprising because sub-area I comprises a narrow andsteep channel with fastcurrents at the estuary mouth.Bottlenose dolphins seem toprefer narrow channels andfeatures such as steep slopes,uneven bottom substrates andtidal eddies, which are knownto attract or concentrate fish(Wilson et al . , 1997). Byfunctioning as a bottleneck for fish moving throughthis kind of habitat, these features may help dolphinsto take advantage of prey concentration, improvingtheir foraging efficiency (Hastie et al., 2004). The rockyformation of the jetties in sub-area I may also attractfish that commonly associate with rocks. Informationon prey distribution and biomass would certainlyimprove our understanding of the behavior anddistribution of bottlenose dolphins in the study area,and should therefore be pursued in future studies.

Similar frequencies of socializing were observed inall sub-areas in our study, as opposed to a higherfrequency of socializing observed by Möller (1993),and limited to sub-area I. Despite the constant trafficof cargo ships and fishing boats in the channel of sub-area I, resting was only observed on flat and shelteredwaters that are present on the northeastern sector ofthis sub-area, adjacent to the channel. This findingcorroborates the observations on resting made byMöller (1993).


LAJAM 6(2): 161-169, December 2007

Activity budgets also changed seasonally in sub-areas Iand II. The higher relative frequency of feeding inwinter, which was also observed by Möller (1993), andthe predominance of travel-feeding in fall might berelated to increased energy requirements in cold waters(Shane, 1990), lower prey densities in the study area ora change in diet. Pinedo (1982) reported a great amountof Sciaenidae fish in the stomach contents of bottlenosedolphins stranded along the coast near the Patos Lagoonestuary. The white croaker, Micropogonias furnieri,accounted for nearly 80% of the absolute frequency ofprey in the stomachs (Pinedo, 1982). However, thesample size was small and did not represent all seasons.Therefore, no conclusions can be drawn regardingseasonal variation in feeding preferences of thispopulation and how it might affect their activities. Fromobservations on surface feeding behavior, it is suggestedthat the cutless fish, Trichiurus lepturus, and the mullet,Mugil platanus, may also be important seasonal preyspecies. The Patos Lagoon estuary is a highly seasonalenvironment, with fish abundance and assemblagechanging across the seasons (Ramos and Vieira, 2001).Specifically, fish abundance decreases drastically duringthe cold months, which could force the dolphins tospend more time feeding and foraging (e.g. Bearzi et al.,1999). The highest frequency of socializing observed inthe spring is likely due to an increase in the frequencyof mating interactions. Considering that the gestationperiod in this species is approximately 10 to 12 monthslong (Wells et al., 1987), this would explain the highestincidence of calves in the study area at the end of thespring and beginning of the summer (Fruet, 2008).Möller (1993) did not conduct surveys in spring;however socializing was the most frequently observedactivity in the summer in her study. The few records ofresting in our study were made in the spring andsummer months, in contrast with the previous study,where resting was more frequent in the fall. However,the low number of resting observations should not beinterpreted as an indication that this activity was notimportant in the study area. Given that our observationperiods were limited to daylight hours, resting couldbe underestimated. Experiments with bottlenosedolphins in captivity suggest that resting at the surfacemay occupy between 50 and 70% of the nighttime inadults (Lyamin et al., 2007), and telemetry data alsoindicate that wild bottlenose dolphins might engage inthis activity predominantly at night (Mate et al., 1995).

Differences in activity budgets over the course of theday were not as marked as seasonal and spatialdifferences, at least for the most commonly observedactivities. Feeding frequencies were relatively constantthroughout the day, while Möller (1993) found a steadyincrease in feeding over the course of the day. Bottlenosedolphins in South Africa (Tayler and Saayman, 1972;Saayman et al., 1973) and Texas (Shane, 1977; Shane etal., 1986) fed more frequently in the early morning andlate afternoon, possibly in response to the diurnal

patterns of prey. We observed a slight increase intraveling and especially travel-feeding in the earlyafternoon, with similar frequencies remaining in the lateafternoon. Möller (1993) also observed a higherfrequency of traveling in the beginning of the afternoon.Resting was more frequent in the morning, and it wasnot observed in the evening. Möller (1993) reportedresting during the three periods, with a higher frequencyin the morning, and bottlenose dolphins in Argentinaalso rested in the morning (Würsig and Würsig, 1979).

During the present study, bottlenose dolphins werefound all over the study area; however a preference forthe region between the jetties in sub-area I was observed(Fig.5), similarly to previous studies in the area (Möller,1993; L. Dalla Rosa, unpublished data). Commonbottlenose dolphins tend to aggregate inside or near theentrances to estuaries, lagoons and bays (Leatherwoodand Reeves, 1983b; dos Santos and Lacerda, 1987;Ballance, 1992; Fertl, 1994; Wilson et al., 1997; Cortese,2000; Garrison and Yeung, 2001; Read et al., 2003), oftenconcentrating in areas of fast tidal current (Irvine et al.,1981; Shane, 1980, 1990; Harzen, 1998). Therefore, lowerencounter rates in sub-areas II and III were expected.We suspect, however, that they were lower than usual.

The 2002/03 warm El Niño event (McPhaden, 2004) thatoccurred during this study resulted in higherprecipitation indices in the Patos Lagoon and salinityvalues below the average of the previous thirteen years(Laboratório de Ictiologia/Fundação UniversidadeFederal do Rio Grande, unpublished data). Salinityvalues in the Patos Lagoon estuary vary according toprecipitation and wind-driven circulation (e.g. Calliari,1980; Costa et al., 1988), affecting the abundance anddistribution of marine fish species (Garcia et al., 2001)that are prey for the bottlenose dolphins. High salinityvalues in the inner portions of the estuary lead toincreased marine fish abundance and thus have thepotential to attract foraging dolphin groups further intothe estuary. We assume low salinity values anddecreased fish abundance would have the oppositeeffect, particularly in sub-areas II and III.

We must point out that we investigated the distributionof bottlenose dolphins only near the mouth of the PatosLagoon estuary. As they also travel along the coastline,in both southward and northward directions, it wouldbe important to carry out a larger-scale study toinvestigate the home range and core areas of thispopulation.

The structure and composition of dolphin groups isbased on the age, gender, kinship and reproductivecondition of the individuals (Wells, 1991; Krützen et al.,2003; Parsons et al., 2003; Möller, 2006). Group size andcomposition in bottlenose dolphins varies amongdifferent populations. In the west coast of Florida, theaverage group size is about 10 animals (Scott andChivers, 1990), while in California group sizes of about18 (Hansen, 1990) and 9 (Bearzi, 2005) individuals have


LAJAM 6(2): 161-169, December 2007

been reported. In the present study, the average groupsize was very similar to that reported by Dalla Rosa(1999) for the same area (4.44 individuals) and byCampbell et al. (2002) for a Central American population,where 3.8 individuals were recorded. Flores andFontoura (2007) reported a group size of 5.4 individualsin Baía Norte, Santa Catarina State, Brazil, for thisspecies.

In conclusion, this study confirms the importance of thePatos Lagoon estuary for the population of bottlenosedolphins and demonstrates that the area next to themouth of the estuary is highly used by the dolphinsduring the daytime and throughout the year, providingthe necessary conditions for the accomplishment of vitalactivities such as feeding, socializing and resting.

Acknowledgements

We wish to thank Lauro Barcellos and the staff of theMuseu Oceanográfico “Prof. Eliézer C. Rios” for thelogistical support. Special thanks to Altemir Brás Pintofor driving the boat during all surveys and Juliana DiTullio for technical support. Two anonymous reviewersmade helpful comments and suggestions that greatlyimproved the manuscript. This work was supported byCompanhia Brasileira de Projetos e Obras (CBPO) andFundo Nacional do Meio Ambiente (FNMA).

References

ALTMANN, J. (1974) Observational study of behaviour: samplingmethods. Behaviour 49: 227-267.

ALVES JÚNIOR, T.T., ÁVILA, F.J.C., DE OLIVEIRA, J.A., FURTADO NETO,M.A.A. AND MONTEIRO NETO, C. (1996) Registros de cetáceospara o litoral do estado do Ceará, Brasil. Arquivo de Ciências doMar, Fortaleza, 30(1-2): 70-83.

BAILEY, H. AND THOMPSON, P. (2006) Quantitative analysis ofbottlenose dolphin movement patterns and their relationshipwith foraging. Journal of Animal Ecology 75: 456-465.

BALLANCE, L.T. (1990) Residence patterns, group organization,and surfacing associations of bottlenose dolphins in Kino Bay,Gulf of California, Mexico. Pages 267-283 in LEATHERWOOD, S.and REEVES, R.R. (Eds) The Bottlenose Dolphin. San Diego,California, Academic Press, Inc.

BALLANCE, L.T. (1992) Habitat use patterns and ranges of thebottlenose dolphin in the Gulf of California, Mexico. MarineMammal Science 8(3): 262-274.

BARROS, N.B. AND ODELL, D.K. (1990) Food habits of bottlenosedolphins in the southeastern United States. Pages 309-328 inLEATHERWOOD, S. and REEVES, R.R. (Eds) The Bottlenose Dolphin.San Diego, California, Academic Press, Inc.

BEARZI, M. (2005) Aspects of the ecology and behaviour of thebottlenose dolphins (Tursiops truncatus) in Santa Monica Bay,California. Journal of Cetacean Research Management 7(1): 75-83.

BEARZI, G., POLITI, E. AND NOTARBARTOLO DI SCIARA, G. (1999).Diurnal behavior of free-ranging bottlenose dolphins in theKvarneric (northern Adriatic Sea). Marine Mammal Science

15(4): 1065-1097.

CALLIARI, L.J. (1980) Aspectos sedimentológicos e ambientais daregião sul da Lagoa dos Patos . M.Sc. Thesis. FundaçãoUniversidade Federal do Rio Grande, RS, Brasil.

CAMPBELL, G.S., BILGRE, B.A. AND DEFRAN, R.H. (2002) Bottlenosedolphins (Tursiops truncatus) in Turneffe Atoll, Belize:occurrence, site fidelity, group size and abundance. AquaticMammals 28: 170-180.

CASTELLO, H.P. AND PINEDO, M.C. (1977) Botos na Lagoa dosPatos. Natureza em Revista 2: 46-49.

CHAO, L.H., PEREIRA, L.E. AND VIEIRA, J.P. (1985) Estuarine fishcommunity of the dos Patos Lagoon, Brazil. A baseline study.Pages 429-450 in Fish Community Ecology in Estuaries and CoastalLagoons: Towards an Ecosystem Integration. DR (R) UNAM Press,Mexico.

COCKCROFT, V.G., AND ROSS, G.J.B. (1990) Food and feeding ofthe Indian Ocean bottlenose dolphin off southern Natal, SouthAfrica. Pages 295-308 in LEATHERWOOD, S. and REEVES, R.R. (Eds)The bottlenose dolphin. Academic Press, San Diego, CA.

CORTESE, N.A. (2000) Delineation of bottlenose dolphin populationsin the western Atlantic Ocean using stable isotopes. M.Sc. Thesis,University of Virginia, 118 pp.

COSTA, C.S.B., SEELIGER, U. AND KINAS, P.G. (1988) The effect ofwind velocity and direction on the salinity regime in the PatosLagoon estuary. Ciência e Cultura 40: 909-912.

CUBERO-PARDO, P. (2007) Distribution and environmentalconditions related to the behavior in the bottlenose dolphin(Tursiops truncatus) and the spotted dolphin (Stenella attenuata)(Cetacea : Delphinidae) in Golfo Dulce, Costa Rica. Revista deBiologia Tropical 55: 549-557.

DALLA ROSA, L. (1999) Estimativa do tamanho da população debotos, Tursiops truncatus, do estuário da Lagoa dos Patos, RS, apartir da foto-identificação de indivíduos com marcas naturais e daaplicação de modelos de marcação-recaptura. M.Sc. Thesis,Fundação Universidade Federal do Rio Grande, Brasil. 104p.

DOS SANTOS, M.E. AND LACERDA, M. (1987) Preliminaryobservations of the bottlenose dolphin (Tursiops truncatus) inthe Sado estuary (Portugal). Aquatic Mammals 13(2): 65-80.

DUFFIELD, D.A., RIDGWAY, S.H., AND CORNELL, L.H. (1983)Hematology distinguishes coastal and offshore forms ofdolphins (Tursiops). Canadian Journal of Zoology 61: 930-933.

FERTL, D. (1994) Occurrence patterns and behavior of bottlenosedolphins (Tursiops truncatus) in the Galveston ship channel,Texas. Texas Academy of Science 46(4):299-317.

FLORES, P.A.C. AND FONTOURA, N.F. (2007) Ecology of marinetucuxi, Sotalia guianensis, and bottlenose dolphin, Tursiopstruncatus, in Baia Norte, Santa Catarina state, southern Brazil.The Latin American Journal of Aquatic Mammals 5(2): 105-115.

FRUET, P.F. 2008. Abundância, mortalidade em atividadespesqueiras e viabilidade da população de botos, Tursiopstruncatus, do estuário da Lagoa dos Patos, RS, Brasil. M.Sc.Thesis. Universidade Federal do Rio Grande, Brasil. 192p.

GARCIA, A.M, VIEIRA, J.P. AND WINEMILLER, K.O. (2001) Dynamicsof the shallow-water fish assemblage of the Patos Lagoonestuary (Brazil) during cold and warm ENSO episodes. Journalof Fish Biology 59(5): 1218-1238.


LAJAM 6(2): 161-169, December 2007

GARRISON, L. AND YEUNG, C. (2001) Abundance Estimates for AtlanticBottlenose Dolphin Stocks During Summer and Winter, 1995. NMFS/SEFSC report prepared and reviewed for the Bottlenose DolphinTake Reduction Team. Available from: NMFS-Southeast FisheriesScience Center, 75 Virginia Beach Dr., Miami, FL 33149.

HANSEN, L.J. (1990) California coastal bottlenose dolphins.Pages 403-420 in LEATHERWOOD, S. and REEVES, R.R. (Eds) TheBottlenose Dolphin. Academic Press, San Diego, California.

HARZEN, S. (1998) Habitat use by the bottlenose dolphin(Tursiops truncatus) in the Sado estuary, Portugal. AquaticMammals 24(3): 117–128.

HASTIE, G.D., WILSON, B. AND THOMPSON, P.M. (2004) Fine-scalehabitat selection by coastal bottlenose dolphins: applicationof a new land-based video-montage technique. CanadianJournal of Zoology 81: 469-478.

HERSH, S.L. AND DUFFIELD, D.A. (1990) Distinction betweenNorthwest Atlantic offshore bottlenose dolphins based onhemoglobin profile and morphometry. Pages 129-139 inLEATHERWOOD, S. and REEVES, R.R. (Eds) The Bottlenose Dolphin.Academic Press, San Diego.

IRVINE, A.B. SCOTT, M.D. WELLS, R.S. AND KAUFMANN, J.H. (1981)Movements and activities of the Atlantic bottlenose dolphin,Tursiops truncatus, near Sarasota, Florida. Fishery Bulletin79(4): 671-688.

KJERFVE, B. (1986) Comparative oceanography of coastal lagoons.Pages 63-81 in WOLFE, D.A. (Ed.). Estuarine variability.Academic Press, New York.

KRÜTZEN, M., SHERWIN, W.B., CONNOR, R.C., BARRÉ, L.M., DECASTEELE, T.M., MANN, J. AND BROOKS, R. (2003) Contrastingrelatedness patterns in bottlenose dolphins (Tursiops sp.) withdifferent alliance strategies. Proceedings of the Royal Society ofLondon Series B - Biological Sciences 270(1514): 497-502.

LEATHERWOOD, S. (1975) Some observations of feeding behaviorof bottlenose dolphins (Tursiops truncatus) in the Northern Gulfof Mexico and (T. gilli) off southern California, Baja California,and Nayarit, Mexico. Marine Fisheries Review 37(9): 10-16.

LEATHERWOOD, S., REEVES, R.R. AND FOSTER, L. (1983a) The SierraClub Handbook of Whales and Dolphins. San Francisco, SierraClub Books. 302p.

LEATHERWOOD, S. AND REEVES, R.R. (1983b) Abundance ofbottlenose dolphins in Corpus Christi Bay and CoastalSouthern Texas. Contributions in Marine Science 26:179-199.

LYAMIN, O., PRYASLOVA, J., KOSENKO, P. AND SIEGEL, J. (2007)Behavioral aspects of sleep in bottlenose dolphin mothers andtheir calves. Physiology & Behavior 92: 725-733.

MANN, J. (1999) Behavioral sampling methods for cetaceans:A review and critique. Marine Mammal Science 15(1): 102-122

MATE, B.R., ROSSBACH, K.A., NIEUKIRK, S.L., WELLS, R.S., IRVINE,A.B., SCOTT, M.D. AND READ, A.J. (1995) Satellite-monitoredmovements and dive behavior of a bottlenosed dolphin(Tursiops truncatus) in Tampa Bay, Florida. Marine MammalScience 11(4): 452-463.

MCPHADEN, M.J. (2004) Evolution of the 2002/03 El Niño.Bulletin of the American Meteorological Society 85: 677-695.

MEAD, J.G. AND POTTER, C.W. (1990) Natural history ofbottlenose dolphins along the Central Atlantic Coast of the

United States. Pages 165-195 in LEATHERWOOD, S. and REEVES,R.R. (Eds) The Bottlenose Dolphin. San Diego, California,Academic Press.

MÖLLER, L.M. (1993) Observações sobre o comportamento e aecologia do Boto, Tursiops truncatus, no Estuário da Lagoa dos Patos,RS, Brasil. Monografia de graduação, Fundação UniversidadeFederal do Rio Grande, Brasil, 32 p.

MÖLLER, L.M., SIMÕES-LOPES, P.C., SECCHI, E.R. AND ZERBINI, A.N.1994. Uso de fotoidentificação no estudo do deslocamento debotos, Tursiops truncatus (Cetacea, Delphinidae) na costa suldo Brasil. Proceedings of the 6th Meeting of South AmericanAquatic Mammals Specialists, Florianópolis, Santa Catarina,Brazil. p. 5-8.

MÖLLER, L.M., BEHEREGARAY, L.B., ALLEN, S.J. AND HARCOURT, R.G.(2006) Association patterns and kinship in female Indo-Pacificbottlenose dolphins (Tursiops aduncus) of southeasternAustralia. Behavioral Ecology and Sociobiology 61: 109-117.

MÖLLER, O.O. AND CASTAING, P. 1999. Hydrographicalcharacteristics of the estuarine area of Patos Lagoon (30°S,Brazil). Pages 83-100 in PERILLO, G.M.E., PICCOLO, M.C. AND PINOQUIVIRA, M. (Eds) Estuaries of South America: TheirGeomorphology and Dynamics. Springer-Verlag, Berlin.

PARSONS, K.M., DURBAN, J.W., CLARIDGE, D.E., BALCOMB, K.C.,NOBLE, L.R. AND THOMPSON, P.M. (2003) Kinship as a basis foralliance formation between male bottlenose dolphins, Tursiopstruncatus, in the Bahamas. Animal Behavior 66: 185-194.

PINEDO, M.C. (1982) Análise dos conteúdos estomacias de Pontoporiablainvillei (Gervais and D’Orbigny, 1844) e Tursiops gephyreus(Lahille, 1908) (Cetacea, Platanistidae e Delphinidae) na zonaestuarial e costeira de Rio Grande, RS, Brasil. M.Sc. Thesis,Fundaçao Universidade do Rio Grande, RS, Brazil. 95pp.

PRYOR, K. AND LINDBERGH, J. (1990) A dolphin-human fishingcooperative in Brazil. Marine Mammal Science 6(1): 77-82.

RAMOS, L.A. AND VIEIRA, J.P. (2001) Composição específica eabundância de peixes de zonas rasas dos cinco estuários doRio Grande do Sul, Brasil. Boletim do Instituto de Pesca, SãoPaulo, 27:109-121.

READ, A.J., URIAN, K.W., WILSON, B. AND WAPLES, D.M. (2003)Abundance of bottlenose dolphins in the bays, sounds, andestuaries of North Carolina. Marine Mammal Science 19(1): 59-73.

RICE, D.W. (1998) Marine mammals of the world - Systematics anddistribution. Society of Marine Mammalogy. Special PublicationNo. 4.

SAAYMAN, G.S., TAYLER, C.K., AND BOWER, D. (1973) Diurnal activitycycles in captive and free-ranging Indian Ocean bottlenosedolphins (Tursiops aduncus Ehrenburg). Behavior 44: 212-233.

SEELIGER, U., ODEBRECHT, C. and CASTELLO, J.P. (1997) Subtropicalconvergence environments: the coast and sea in thesouthwestern Atlantic. Springer-Verlag, Berlim. 308pp.

SCOTT, M.D. AND CHIVERS, S.J. (1990) Distribution and herdstructure of bottlenose dolphins in the eastern tropical PacificOcean. Pages 387-402 in Leatherwood, S. and Reeves, R. R. (Eds)The Bottlenose Dolphin. San Diego, California, Academic Press.

SEGURA, I., ROCHA-OLIVARES, A., FLORES-RAMÍREZ, S. AND ROJAS-BRACHO, L. (2006) Conservation implications of the genetic andecological distinction of Tursiops truncatus ecotypes in the Gulfof California. Biological Conservation 133(3): 336-346.


LAJAM 6(2): 161-169, December 2007

Received 13 June 2007. Accepted 30 November 2007.

SHANE, S.H. (1977) The population biology of the Atlantic bottlenosedolphin, Tursiops truncatus, in the Aransas Pass area of Texas.M.Sc. Thesis, Texas A&M University, College Station, Texas.239 pp.

SHANE, S.H. (1980) Occurrence, movements and distributionof bottlenose dolphin, Tursiops truncatus, in Southern Texas.Fishery Bulletin 78(3): 593–601.

SHANE, S.H., WELLS, R.S. AND WÜRSIG, B. (1986) Ecology,behavior and social organization of bottlenose dolphin: AReview. Marine Mammals Science 2(1): 34-63.

SHANE, S.H. (1990) Behavior and ecology of the bottlenose dolphinat Sanibel Island, Florida. Pages 245-265 in LEATHERWOOD, S. andREEVES, R.R. (Eds) The Bottlenose Dolphin. San Diego, California,Academic Press.

SIMÕES-LOPES, P.C. (1991) Ecologia comportamental do delfin,Tursiops truncatus (Montagu, 1821), durante as interações com apesca artesanal de tainhas (Mugil spp) no sul do Brasil. Ph.D.Thesis, Pontifícia Universidade Católica, RS, Brasil, 199p.

TAGLIANI, P.R.A., LANDAZURI, H., REIS, E.G., TAGLIANI, C.R.,ASMUS, M.L. AND SÁNCHEZ-ARCILLA, A. (2003) Integrated coastalzone management in the Patos Lagoon estuary: perspectivesin context of developing country. Ocean & Coastal Management46: 807-822.

TAYLER, C.K. AND SAAYMAN, G.S. (1972) The social organizationand behavior of dolphins (Tursiops truncatus) and baboons

(Papio ursinus): Some comparisons and assessments. Annals ofthe Cape Provincial Museums (Natural History) 9(2): 11-49.

VIEIRA, J.P. (2006) Ecological analogies between estuarinebottom trawl fish assemblages from Patos Lagoon, Rio Grandedo Sul, Brazil and York River, Virginia, USA. Revista Brasileirade Zoologia 23(1): 234-247.

VIEIRA, J.P. AND SCALABRIN, C. (1991) Migração reprodutiva daTainha (Mugil platanus Günther, 1880) no sul do Brasil.Atlântica 13(1): 131-141.

WELLS, R.S., SCOTT, M.D. AND IRVINE, A.B. (1987) The socialstructure of free-ranging bottlenose dolphins. Pages 247-305in GENOWAYS, H.H. (Ed.) Current Mammalogy, New York 1: 519p.

WELLS, R.S. (1991) The role of long-term study in understandingthe social structure of a bottlenose dolphin community. Pages199-225 in PRYOR, K. AND NORRIS, K. (Eds) Dolphin SocietiesDiscoveries and Puzzles. University of California Press.

WILSON, B., THOMPSON, P.M. AND HAMMOND, P.S. (1997) Habitatuse by bottlenose dolphins: seasonal distribution and stratifiedmovement patterns in the Moray Firth, Scotland. Journal ofApplied Ecology 34: 1365-1374.

WÜRSIG, B. and WÜRSIG, M. (1979) Behavior and ecology of thebottlenose dolphin, Tursiops truncatus, in the South-Atlantic.Fishery Bulletin 77(2): 399-412.

ZAR, J.H. (1984) Biostatistical Analysis. Ed. Prentice Hall, Inc.,New Jersey, USA.


1 Peruvian Centre for Cetacean Research (CEPEC).* Corresponding author, e-mail: [email protected]. Avenida F. Mariátegui 129, Dpt. 403, Lima 11, Peru.2 Peruvian Centre for Cetacean Research (CEPEC), Museo de Delfines, Pucusana, Lima 20, Peru. E-mail: [email protected] Áreas Costeras y Recursos Marinos (ACOREMA), Calle San Francisco 253, 201-B, Pisco, Peru. E-mail: [email protected] Pro Delphinus, Calle Octavio Bernal 572-5, Lima 11, Peru.5 University of Exeter, Cornwall Campus, Center for Ecology and Conservation, Penryn, Cornwall TR10 9EZ, UK.6 Center for Tropical Marine Ecology, Fahrenheitstrasse 6, 28359, Bremen, Germany.

PREY OCCURRENCE IN THE STOMACH CONTENTS

OF FOUR SMALL CETACEAN SPECIES IN PERU

IGNACIO GARCÍA-GODOS1,*, KOEN VAN WAEREBEEK

2, JULIO C. REYES3,

JOANNA ALFARO-SHIGUETO4,5 AND MILENA ARIAS-SCHREIBER6

ABSTRACT: The diets of long-beaked common dolphins Delphinus capensis (n=117), dusky dolphins Lagenorhynchus obscurus(n=72), Burmeister’s porpoises Phocoena spinipinnis (n=69) and offshore common bottlenose dolphins Tursiops truncatus (n=22)were determined based on the analysis of the stomach contents collected from animals landed in ports along the Peruviancentral coast and from Marcona, in southern Peru, during 1987-1993. The number of prey ingested was obtained by countingthe number of fish otoliths and cephalopod mandibles (beaks). Only fish could be identified to species level. Long-beakedcommon dolphins fed mainly on Peruvian anchovy Engraulis ringens (70.0% by number), Panama lightfish Vincigerria lucetia(7.8%) and slimtail lanternfish Lampanyctus parvicauda (6.7%). Dusky dolphins consumed mainly anchovies (49.7%, 16.8%),slimtail lanternfish (23.6%, 0.1%), Inca scad Trachurus murphyi (17.1%, 0%) and mote sculpin Normanichthys crockeri (0%, 76.0%)off the central Peruvian coast and Marcona, respectively. In the same areas, Burmeister’s porpoises fed mainly on anchovy(88.9%, 77.6%), silverside Odontesthes regia (6.5%, 0%), mote sculpin (0%, 8.1%) and South Pacific hake Merluccius gayi (0.6%,7.9%). Offshore common bottlenose dolphins consumed mainly slimtail lanternfish (39.2%), barracuda Sphyraena sp. (13.5%)and Peruvian pilchard Sardinops sagax (13.3%). The diversity indices of the diet and temporal shifts in the main prey suggest anopportunistic feeding strategy for the four cetacean species studied, which take advantage of the locally most available epipelagicand mesopelagic schooling fish. Cluster analysis shows high similarity in their diets, with these four marine top predatorsbeing able to optimally exploit the high productivity of the Peruvian upwelling ecosystem.

KEYWORDS: small cetaceans; food; prey; habitat; feeding ecology, Peru, Southeast Pacific.

Introduction

The Peruvian upwelling system is one of the mostproductive ecosystems in the world (Ryther, 1969;Duffy, 1994; Bakun and Weeks, 2008), supporting a greatvariety of fish species and fisheries that provide foodfor humans and prime material for the animal feedindustry. Despite intense exploitation, our knowledgeof the trophic relationships within this ecosystem islimited (Pauly and Tsukayama, 1987), with the highestresearch efforts focused on the Peruvian anchovyEngraulis ringens.

The Peruvian anchovy is the most heavily exploitedmarine resource in Peru and its industrial fishery forfish meal and oil is the largest single species fishery inthe world (Whitehead et al. 1988, Jahncke et al. 2004;Bakun and Weeks, 2008). Over-exploitation in the early1970s, in combination with a severe El Niño eventcaused the collapse of anchovy populations and theirfishery, whose effects are experienced even decadesafter (Jordán, 1982; Jahncke et al., 2004). Together withthe anchovy its predators also collapsed; the mostconspicuous case was that of Peruvian guano-producing seabirds, whose populations declineddramatically (Duffy et al., 1984; Jahncke et al., 2004).Other marine predators, including small cetaceans,could also have been negatively affected by theanchovy collapse. However, no information is available

due to the lack of studies during those years.

Research on the exploitation of cetaceans by artisanaland industrial fisheries in Peru started in late 1984 byscientists of the Peruvian Centre for Cetacean Research(CEPEC) and associates (e.g. Read et al., 1988; VanWaerebeek and Reyes, 1990; García-Godos, 1993; VanWaerebeek et al., 1994a, b). The mortality of smallcetaceans caused by these fisheries in 1985 and 1994 wasestimated to range between 10000 and 17500 individuals(Read et al., 1988; Van Waerebeek and Reyes, 1994),including by-catch in gillnet and purse-seine operationsand animals taken directly with large-mesh gillnets orhand-thrown harpoons. Of the 32 cetacean speciesrecorded to date in Peru (Arias-Schreiber, 1996), thesetakes affected mainly four species: the dusky dolphinLagenorhynchus obscurus, the long-beaked commondolphin Delphinus capensis, the common bottlenosedolphin Tursiops truncatus (both offshore and inshoreforms sensu Van Waerebeek et al., 1990; Sanino et al.,2004) and the Burmeister’s porpoise Phocoena spinipinnis.These species have been protected by Peruvianlegislation since 1990, but with low impact on mortalityrates until 1996 when law enforcement wasimplemented more strictly after a massive publiccampaign for their conservation. Nowadays the fishery-related mortality of cetaceans may have declinedsignificantly, although a black market for dolphin meatpersists (García-Godos, 2007).

172 I.GARCÍA-GODOS, K.VAN WAEREBEEK, J.C.REYES, J.ALFARO-SHIGUETO AND M.ARIAS-SCHREIBER

LAJAM 6(2): 171-183, December 2007

Despite the intense exploitation of small cetaceans in thelate 1980s and early 1990s, there is only fragmentaryknowledge on the natural history of these species, withthe exception of the dusky dolphin (e.g Van Waerebeek,1992a,b; Van Waerebeek and Read, 1994; McKinnon,1994). Pauly and Tsukayama (1987) argued that the lackof knowledge of the diet of small cetaceans was a limitingfactor for designing a model for the management offisheries in the Peruvian-Chilean region. Here we presentan analysis of the diet of the four main small cetaceanspecies caught in fishing operations from central andsouthern ports of Peru over the past two decades, withthe focus on fish prey. Comparisons between their dietsare discussed as to define their respective ecological rolesin the Peruvian upwelling ecosystem.


Samples

Stomach contents of 280 small cetaceans landed byartisanal fishermen in the Peruvian ports of Ancón,Pucusana, Cerro Azul and San Juan de Marcona (furtherreferred to as Marcona) (Figure 1) were collected andexamined by the authors between 1987 and 1993. Thesamples from Marcona were collected by MAS duringport monitoring for the Punta San Juan Project (seeMajluf et al., 2002). The cetacean sample consisted ofstomach contents of long-beaked common dolphins(n=117), dusky dolphins (n=72), offshore commonbottlenose dolphins (n=22) and Burmeister’s porpoises(n=69). All prey items sampled from stomach contentsin the ports of Pucusana, Cerro Azul and Ancón werepooled as from single stocks named ‘centralcoast of Peru’, comprising a coastal strip ofca. 160km long (Figure 1). Indeed, the marineecosystem of the central coast of Peru ispractically homogeneous (Brainard andMcLain, 1987; Peña et al., 1989).Stomachs (fore, main and pyloric) of freshlylanded cetaceans were dissected at the localfish markets and their complete contents weresieved and washed over plastic containers.Hard items including otoliths and squid beakswere recovered. Otoliths were stored dry,while squid beaks were kept in 70% ethanol.All material and field data are deposited at theMuseo de Delfines, CEPEC, Pucusana. Wherepossible otoliths were morphologicallyidentified to species by the first authorfollowing García-Godos (2001) and referencecollections. Squid beaks could not be identifiedto species due to the lack of a referencecollection. However, pooled, they wereaccounted for in the general prey composition.Also because of their low occurrencecephalopods were not further analyzed, butwere considered as a single item in the inter-species cluster analysis of the diet (see below).

Data analysis

Samples were grouped by sampling periods determinedby the season and the year they were collected (the‘sampling period’). Main food parameters studiedincluded the ‘frequency of occurrence’ (FO), defined asthe percentage of occurrence (%FO) of a particular preyspecies in the sample of stomach contents for eachcetacean species, and the ‘prey composition by number’(% Num) as the percentage of the total number of allfish prey individuals for each cetacean species. Thenumber of individual fishes found in each stomach wasdetermined as the number of sagittae otoliths dividedby two (Frost and Lowry, 1980; McKinnon, 1994).To verify differences in the diet with respect toreproductive status of the cetaceans, the sample wasdivided into five categories: 1) immature females; 2)resting adult females; 3) reproductive females (pregnantor lactating); 4) sexually immature males; and 5) adultmales. Reproductive status was determined in the fieldbased on the macroscopic examination of gonads andother reproductive organs (Van Waerebeek, 1992a; VanWaerebeek and Read, 1994). The frequency distributionof reproductive status per species is shown in Table 1.Non-parametric statistics were used in the data analysisbecause of the heterogeneity of the sample and smallsample sizes of sub-groups. To determine differencesin the median percentage of prey consumption bynumber among seasons, reproductive status anddiversity (see below), Kruskal-Wallis (KW), Mann-Whitney (MW) and Chi–square tests (Siegel, 1956) wereapplied. Mann-Whitney test was also used to determineapparent bias in the sample, probably caused by a more

Figure 1. Sampling locations along the Peruvian coast

PREY OCCURRENCE IN THE STOMACH CONTENTS OF FOUR SMALL CETACEAN SPECIES IN PERU 173

LAJAM 6(2): 171-183, December 2007

intensive sampling in 1987. Spearman correlations werecomputed between the body length of cetaceans andboth the number of prey species and number ofindividual prey items.

The trophic niche breadth was estimated for each speciessampled using the Shannon and Wiener index ofdiversity (H) as defined by Krebs (1989). The logarithmicbase of this index is 2, therefore its units are bits and itranges from zero to infinite. For a better interpretationof this index we used its standardized form (H

std) which

ranges from zero to one (Krebs, 1989). To determine thelevel of similarity in the diet of the small cetaceansstudied we used the Simplified Morisita’s index ofsimilarity (Krebs, 1989).

For a graphical view of diet diversification in the smallcetacean community we ran a mean linkage hierarchicalcluster analysis (Krebs, 1989) using the Morisita’ssimplified similarity index and the pooled ratio of preyspecies for each cetacean species. The level of overlapbetween the general consumption by small cetaceansand the landings of the pelagic industrial fishery waspreliminarily estimated using the latter index. Fisherylandings were taken from the statistics published byÑiquen and Bouchón (1995).

Results

Long-beaked common dolphin

Food items of long-beaked common dolphins weremainly fish, comprising 98.7% of the prey (9828individuals), while the remainder was composed ofsquids and crustaceans. From the 20 fish prey speciesobserved, six were present in at least 10% of the pooledsample (Table 2). The Peruvian anchovy Engraulisringens was the most important prey (70%), followedby the Panama lightfish Vinciguerria lucetia (7.76%) andthe slimtailed lanternfish Lampanyctus parvicauda(6.66%). The Peruvian anchovy was the most frequentlyconsumed prey (81.51% FO), followed by silversideOdontesthes regia (17.65% FO), Peruvian pilchardSardinops sagax (15.97% FO), Inca scad Trachurus murphyi(15.97% FO), South Pacific hake Merluccius gayi (14.29%FO) and squids (11.76% FO). No statistical differencewas found in prey composition by number between 1987and the whole period sampled (MW= 185.00, P>0.6),

however significant differences existed in theconsumption of anchovy (KW= 14.042, P<0.05, df= 6)and silverside (KW= 24.498, P<0.01, df= 6) among sevensampling periods with more than five stomach contentscollected. For 1987, differences were found amongseasons for anchovy (KW= 9.541, P<0.05, df= 3),slimtailed lanternfish (KW= 17.86, P<0.001, df= 3),pearly lanternfish Myctophum nitidulum (KW= 13.23,P<0.01, df= 3) and Panama lightfish (KW= 18.416,P<0.001, df= 3). The largest amount of anchovyconsumed in 1987 was during summer and winter, whilemesopelagic species like lightfish and slimtailedlanternfish showed higher consumption during autumnand spring of that year (Table 2).

Among reproductive status, no statistical differenceswere found in the median number of prey species (KW=2.469, P=0.65, df= 4), in the number of prey consumed(KW= 2.021, P>0.7, df= 4) nor the median percentage ofanchovy (KW= 4.527, P>0.3, df= 4). The body length ofdolphins was positively related to the number of preyspecies (r= 0.243, n=84, P<0.05) and the number of prey(r= 0.283, n=84, P<0.01).

The standardized Shannon-Wiener index of diversity(H

std) obtained for the pooled sample was 0.397 (mean=

0.199, S.D.= 0.156, n= 14). No statistical differences inthe diversity of the diet were found among all samplingperiods (x2=7.600, P>0.8, df= 13; using H

max as expected

value: x2=9.952, P>0.5, df=13). A higher diversity of dietwas observed when different prey other than anchovydominated the diet. During 1987, when mesopelagic fishdominated the diet, H

std was higher, 0.472 and 0.453 in

autumn and spring, respectively (Table 2).

Dusky dolphin

The diet of the dusky dolphin in the central coast of Peru(n= 49, Table 3) consisted almost exclusively of fish, with14 prey species (1815 prey individuals), the remainder(0.11%) were squids. Anchovy was the main preyconsumed by number (49.70%), followed by the slimtaillanternfish (23.61%), Inca scad (17.06%), and Panamalightfish (3.52%), among other species. Anchovy wasalso the most frequent prey species (71.43% FO),followed by Inca scad (57.14% FO), pilchard Sardinopssagax (20.41% FO), silverside (16.33% FO) and slimtaillanternfish (12.24% FO).

Table 1. Categories of reproductive status in the sample of Peruvian small cetaceans examined for this study.

SPECIES REPRODUCTIVE STATUS

D.capensis L. obscurus T. truncatus P.spinipinnis

� - immature 22 4 2 3

� - resting adult 3 3 2 3

� - reproductive 5 8 1 7

� - immature 35 3 3 15

� - adult 19 18 9 13


LAJAM 6(2): 171-183, December 2007

Ta

ble

2.

Per

cen

tag

e b

y n

um

ber

(%

Nu

m.)

of

pre

y o

f lo

ng

-bea

ked

co

mm

on

do

lph

ins

lan

ded

in

cen

tral

Per

u.

% F

.O.

= F

req

uen

cy o

f o

ccu

rren

ce;

HS

td =

Sta

nd

ard

ized

Sh

ann

on

-Wie

ner

div

ersi

ty i

nd

ex;

ND

= N

ot

det

erm

ined

.

LO

CA

TIO

N

PU

CU

SA

NA

A

NC

ÓN

C

ER

RO

AZ

UL

PO

OL

ED

PR

EY

IT

EM

S

um

-8

7

Au

t-8

7

Win

-8

7

Sp

r-8

7

Au

t-8

8

Win

-8

8

Win

-8

9

Win

-9

0

Su

m-

91

S

um

-9

1

Win

-9

1

Su

m-

93

A

ut-

93

W

in-

93

%

F

O

%

Nu

m.

FIS

H

En

grau

lis

rin

gen

s 8

9.5

5

17

.35

9

5.3

9

41

.91

9

5.6

8

10

0.00

9

4.7

9

25

.93

3

.17

35

.59

8

5.5

9

32

.12

6

0.0

0

10

0.00

8

1.5

1

70

.00

Odo

nte

sth

es r

egia

1

.28

0.6

7

0

.22

5

1.2

5

61

.86

0

.19

7.8

6

1

7.6

5

3.4

8

Mer

lucc

ius

gay

i

1.02

0.

17

0.1

0

4

1.9

5

0.8

5

11

.88

6

7.8

8

14

.29

4

.42

Sar

din

ops

sagax

1.5

3

1.1

4

0.0

7 3

.24

3

.17

0

.19

0.7

1

1

5.9

7

0.7

9

Ser

iole

lla

vio

lace

a 2.

13

0.

06

1

.68

0

.12

Tra

chu

rus

mu

rph

y

6.1

8

4.5

9

0.7

0

1.0

0 0

.43

4

.17

74

.07

1

5.9

7

1.4

0

Sco

mbe

r ja

pon

icu

s

0.

14

1

.04

1

.68

0

.06

Pri

onot

us

step

han

ophr

is

0.6

1

0

.43

1

4.2

9

6

.72

0

.45

An

choa

nas

us

0.11

0.8

4

0.0

4

Sco

mbe

reso

x s

auru

s 0

.21

1

.20

5.8

8

0.3

7

Vin

cigu

erri

a lu

ceti

a

6.12

25

.87

7

.56

7

.76

Myct

ophu

m n

itid

ulu

m

0.21

8.

16

0.03

8

.11

9.2

4

2.5

8

Lam

pan

yct

us

par

vic

aud

a

56

.63

18

.76

7

.56

6

.66

Sphy

raen

a sp

.

0.1

0

0

.84

0

.03

Nor

man

ich

thy

s cr

ocke

ri

0

.03

11

.43

2.5

2

0.1

7

Ap

hos

por

osu

s

5

.71

0.8

4

0.0

8

Ophic

hth

ius

pac

ific

i

0.

03

0

.84

0

.01

ND

1

1

.02

0.2

7

2

.52

0

.10

ND

2

0

.03

0.8

4

0.0

1

Fa

m.

My

cto

ph

idae

0.6

5

1

.68

0

.19

CE

PH

AL

OP

OD

S

0.4

3

3.5

7

0.0

8

1.8

9

1.6

9

11

.76

0

.70

CR

US

TA

CE

AN

S

Eu

ph

ausi

acea

0.

73

0

.45

1

.68

0

.28

Ple

uro

nco

des

mon

odon

0.

14

2.

15

7

.56

0

.28

Sa

mp

le s

ize

7

6 3

6

17

8

2

1

1

1

8

2

1

1

3

5 1

17

HStd.

0.1

46

0

.45

3

0.0

90

0

.472

0

.068

0.0

74

0.1

83

0

.303

0

.24

7

0.1

57

0

.20

0

0.3

93

0.3

97


LAJAM 6(2): 171-183, December 2007

Ta

ble

3.

Per

cen

tag

e b

y n

um

ber

(%

Nu

m.)

of

pre

y o

f d

usk

y d

olp

hin

s la

nd

ed i

n c

entr

al P

eru

an

d M

arco

na.

CE

NT

RA

L C

OA

ST

PU

CU

SA

NA

C

ER

RO

AZ

UL

AN

CÓ

N

PO

OL

ED

CE

NT

RA

L C

OA

ST

MA

RC

ON

A

PO

OL

ED

MA

RC

ON

A

PR

EY

IT

EM

Su

m-8

7

Win

-87

Sp

r-8

7

Su

m-9

0S

um

-90

Su

m-9

1

% F

.O.

% N

um

. S

um

-92

Sp

r-93

% F

.O.

% N

um

.

FIS

H

En

grau

lis

rin

gen

s 45.2

1

93.6

6

47.1

4

62.7

4

12.3

3

94.7

4

71.4

3

49.7

0

15.7

6

98.6

5

95.6

5

16.7

9

Odo

nte

sthe

s re

gia

0.4

7

8.9

6

0.1

7

3.5

1

16.3

3

1.3

2

Mer

lucc

ius

gayi

0.4

7

1.7

5

6.1

2

0.1

7

0.9

8

43.4

8

0.9

7

Sar

din

ops

saga

x

2.2

0

19.8

1

0.5

1

20.4

1

2.7

5

Tra

chu

rus

mu

rphy

i 54.7

9

5.4

0

48.4

6

5.1

9

57.1

4

17.0

6

Sco

mbe

r ja

pon

icu

s

0.4

4

0.1

7

4.0

8

0.1

1

0.0

3

4.3

5

0.0

3

Pri

onot

us

step

han

ophr

is

0.0

3

8.7

0

0.0

3

Vin

cigu

erri

a lu

ceti

a

10.8

1

2.0

4

3.5

2

0.0

5

4.3

5

0.0

5

Myc

toph

um

nit

idu

lum

2.8

7

2.0

4

0.9

4

Lam

pan

yctu

s pa

rvic

auda

0.4

4

0.9

4

71.9

6

12.2

4

23.6

1

0.0

8

4.3

5

0.0

8

Sph

yrae

na

sp.

0.4

7

1.0

1

4.0

8

0.3

9

Nor

man

icht

hys

croc

keri

76.9

5

60.8

7

76.0

0

Aph

os p

oros

us

0.0

2

4.3

5

0.0

2

Mu

gil

cep

halu

s

0.4

7

2.0

4

0.0

6

Che

ilop

ogon

het

eru

rus

1.3

2

4.0

8

0.1

7

ND

1

0.1

7

2.0

4

0.0

6

ND

3

5.0

1

34.7

8

4.9

5

ND

4

0.3

7

4.3

5

0.3

7

ND

6

0.0

7

4.3

5

0.0

7

ND

8

0.0

5

4.3

5

0.0

5

ND

9

0.4

7

2.0

4

0.0

6

0.0

2

4.3

5

0.0

2

ND

13

0.0

3

4.3

5

0.0

3

CE

PH

AL

OP

OD

S

0.9

4

4.0

8

0.1

1

0.5

4

1.3

5

43.4

8

0.5

5

Sa

mp

le s

ize

13

10

4 13

7 3

49

20

3

23

HStd.

0.2

54

0.0

99

0.3

30

0.4

23

0.3

48

0.0

89

0.5

09

0.2

82

0.0

26

0.2

88

%

F.O

. =

Fre

qu

ency

of

occ

urr

ence

; H

Std

= S

tan

dar

diz

ed S

han

no

n-W

ien

er d

iver

sity

in

dex

; N

D =

No

t d

eter

min

ed.


LAJAM 6(2): 171-183, December 2007

Dusky dolphins landed at Marcona ate mainly fish withsome squid present in their diet. Fourteen prey species wererecorded (5,966 individuals). The mote sculpinNormanichthys crockeri was the main prey species consumed(76.00% by number), followed by anchovy (16.79%), amongother species. However, the anchovy was the most frequentspecies consumed (95.65% FO), followed by the mote sculpin(60.87% FO), hake (43.48% FO) and squids (43.48% FO).

There was no statistical difference between the percentageof prey by number consumed in 1987 and in later years(MW= 64.00, P>0.1), therefore all the samples were pooledfor further analysis. For the Peruvian central coast nodifference was found in the median consumption of anchovy(KW=7.712, P>0.1, df=4) between sampling periods, withimportant consumption of this prey in summer as in winter,but with some exceptions (Table 3). Similarly, there wereno significant seasonal differences in the consumption ofsilverside (KW= 5.824, P>0.2, df= 4) and slimtail lanternfish(KW= 6.968, P>0.1, df= 4), in contrast with Inca scad (KW=23.243, P<0.001, df=4) as it was absent during two samplingperiods. In Marcona there were significant differences inthe consumption of anchovy (MW= 51.00, P<0.05) and motesculpin (MW=51.00, P<0.05) between spring 1992 andsummer 1993, when one of the species predominatedby number in each period, respectively.

No statistical differences were found in the central coastamong reproductive status with respect to the number

of prey (KW= 6.287, P>0.1, df= 4) and species consumed(KW= 4.010, P>0.4, df= 4), nor in the number of anchovy(KW= 2.452, P>0.6, df= 4) and Inca scad (KW= 6.869,P>0.1, df= 4) consumed. No relationship existed betweenthe number of prey species (r

s= 0.05, n= 42, P>0.7) and

the number of individual fish consumed (rs = 0.084, n=

42, P>0.6) with respect to the body length of the dolphin.

The standardized Shannon-Wiener index (Hstd

) of diversityfor the pooled sample of the central coast was 0.509 (mean= 0.257, SD= 0.126), while for Marcona this index was 0.29.No statistic differences were detected in the diversity ofthe diet among sampling periods (x2= 1.174, P>0.9, df= 5)and the combined diversity H

std for the two areas sampled

was 0.474 (mean = 0.284, SD= 0.145).

Offshore common bottlenose dolphin

The diet of offshore common bottlenose dolphins wascomposed exclusively of fish, accounting for 1157individuals representing 21 prey species, including theslimtail lanternfish (39.89% by number), followed bybarracuda Sphyraena sp. (13.71%), Peruvian pilchard(13.53%) and the lumptail sarobin Prionotus stephanophrys(9.75%), among other species (Table 4). The slimtaillanternfish was also the most frequently consumedspecies (45.45% FO), followed by pilchard (40.91%), Incascad (31.82%) and anchovy and barracuda, both with22.73% FO, amongst other species (Table 4).

Table 4. Percentage by number (% Num.) of prey of offshore common bottlenose dolphins landed in central Peru.

LOCATION

PUCUSANA ANCÓN CERRO

AZUL

POOLED PREY ITEM

Sum-87 Sum-88 Aut-89 Win-89 Spr-89 Aut-90 Sum-92 Spr-87 % F.O. % Num.

FISH

Engraulis ringens 0.93 3.57 100.00 22.73 4.13

Odontesthes regia 2.44 4.55 0.09

Merluccius gayi 21.05 81.82 13.64 7.56

Sardinops sagax 15.17 3.57 41.99 1.43 40.91 13.53

Trachurus murphyi 6.19 33.93 5.19 31.82 4.48

Scomberesox saurus 0.93 4.55 0.26

Scomber japonicus 0.62 4.55 0.18

Lampanyctus parvicauda 18.27 44.64 4.76 85.24 4.55 45.45 39.89

Sphyraena sp. 30.96 13.33 22.73 13.71

Mugil cephalus 0.31 4.55 0.09

Prionotus stephanophrys 48.05 4.55 9.75

Stellifer minor 7.14 4.55 0.35

Galeichthys peruvianus 97.56 4.55 3.51

Labrisomus philippii 1.79 4.55 0.09

ND 1 4.33 9.09 1.23

ND 2 33.33 4.55 0.09

ND 9 1.79 4.55 9.09 0.18

ND 10 1.24 9.09 0.35

ND 11 3.57 4.55 0.18

ND 12 9.09 4.55 0.18

ND 14 66.67 4.55 0.18 Sample size 7 4 4 1 3 1 1 1 22

HStd. 0.578 0.458 0.328 0.153 0.037 0.215 0.206 0.627

% F.O. = Frequency of occurrence; H

Std = Standardized Shannon-Wiener diversity index; ND = Not determined.


LAJAM 6(2): 171-183, December 2007

There was no statistical difference between the numberof prey consumed in 1987 and the rest of samples (MW=198.00, P=0.3), therefore all samples were pooled. Nosignificant differences existed among sampling periodswith respect to the mean number of slimtail lanternfish(KW= 1.272, P>0.7, df= 3), anchovy (KW= 4.35, P>0.2,df= 3), pilchard (KW= 1.75, P>0.6, df= 3) and Inca scad(KW= 1.87, P=0.6, df= 3).

The mean number of prey consumed (KW= 6.286, P>0.15,df= 4) and the number of prey species (KW= 3.527, P>0.4,df= 4) did not vary significantly among dolphins ofdifferent reproductive status. Neither were differencesnoted (KW tests, df=4) in the mean consumption ofslimtail lanternfish (P>0.2), pilchard (P>0.4), Inca scad(P>0.35) nor anchovy (P>0.2) among reproductive status.No significant relationship was apparent between the size(body length) of the dolphin and the number of preyspecies consumed (r

s = 0.24, P>0.3, n= 18), nor the number

of individuals eaten (rS =0.18, P>0.45, n=18).

The standardized Shannon-Wiener index of diversity(H

std) obtained for the pooled sample was 0.627 (mean=

0.29, SD= 0.20). There were no statistic differencesbetween sampling periods with respect to Shannon-Wiener indices (x2=1.918, P> 0.95, df= 7; with H

max as

the expected value: x2= 1.942, P>0.95, df= 7).

Burmeister’s porpoise

The diet of the Burmeister’s porpoise in the central coastof Peru was composed almost exclusively of fish(98.35%), represented by eight species and 1070individuals (Table 5). Anchovy was the main prey bynumber (88.88%) followed by silverside (6.53%),amongst other species (Table 5). Anchovy was presentin 90.38% FO of stomach contents, followed by silverside(9.62% FO) and hake (7.38% FO).

In Marcona the diet was largely composed of fish(94.78% by number) followed by squid. Fish accountedfor 762 individuals representing eight species. Anchovywas the main prey by number (77.61%), followed bythe mote sculpin (8.08%) and hake (7.96%). Anchovywas the most frequent prey (76.47% FO), followed bysquids (52.94% FO), hake (35.29% FO) and mote sculpin(23.53% FO).

There were no significant differences in the percentageby number of prey consumed in 1987 and the rest of thesamples from the central coast (MW= 22.00, P>0.29),therefore all samples could be pooled. The meanconsumption of anchovy (KW= 9.798, P>0.10, df=6) andof silversides (KW= 10.601, P>0.10, df= 6) did not varysignificantly. There were no statistical differences (MWtests) in the consumption of anchovy (P>0.4), hake(P>0.1), mote sculpin (P>0.8) and squids (P>0.2)between spring 1992 and summer 1993 in Marcona.

Porpoises of different reproductive status did notshow significant variation with respect to the numberof prey (KW= 6.526, P>0.15, df= 4) nor in the numberof prey species consumed (KW= 7.229, P>0.1, df= 4).

Ta

ble

5.

Per

cen

tag

e b

y n

um

ber

(%

Nu

m.)

of

pre

y o

f B

urm

eist

er’s

po

rpo

ises

lan

ded

in

cen

tral

Per

u a

nd

Mar

con

a.

% F

.O.

= F

req

uen

cy o

f o

ccu

rren

ce;

HS

td =

Sta

nd

ard

ized

Sh

ann

on

-Wie

ner

div

ersi

ty i

nd

ex;

ND

= N

ot

det

erm

ined

.

CE

NT

RA

L C

OA

ST

PU

CU

SA

NA

A

NC

ÓN

C

ER

RO

AZ

UL

PO

OL

ED

CE

NT

RA

L C

OA

ST

MA

RC

ON

A

PO

OL

ED

MA

RC

ON

A

PR

EY

IT

EM

Su

m-8

7 A

ut-

87

Win

-87

Sp

r-87

S

um

-88

Au

t-88

W

in-8

8 A

ut-

89

Win

-89

Su

m-9

1 S

um

-92

% F

.O.

% N

um

. S

pr-

92

Su

m-9

3 %

F.O

. %

Nu

m.

FIS

H

En

grau

lis

rin

gen

s 88.3

7

89.4

7 98.2

2

97.9

5

61.2

2

96.4

8 100.0

0

42.1

1

100.

00

50.0

0

31.2

5

90.3

8

88.8

8

70.6

5 87.7

7

76.4

7 77

.61

Odo

nte

sthe

s re

gia

4.6

5

37.4

1

1.4

1

35.7

1

9.6

2

6.5

3

Mer

lucc

ius

gayi

5.26

0.5

9

1.3

7

7.6

9

0.6

4

13.4

2

35.2

9 7.9

6

Sar

din

ops

saga

x

1.3

6

1.9

2

0.1

8

0.6

3

5.8

8

0.3

7

Tra

chu

rus

mu

rphy

i

5.26

0.5

9

0.35

5.7

7

0.3

7

An

choa

nas

us

0.5

9

68.7

5

3.8

5

1.1

0

Sci

aen

a de

lici

osa

0.6

8

1.

41

5.7

7

0.5

5

0.4

2

0.6

1

11.7

6 0.5

0

Sco

mbe

reso

x sa

uru

s

0.3

5

1.9

2

0.0

9

Oph

icht

hus

paci

fici

0.2

1

5.

88

0.1

2

Nor

man

icht

hys

croc

keri

8.1

8

7.9

5

23.5

3

8.0

8

ND

1

0.2

1

5.

88

0.1

2

CE

PH

AL

OP

OD

S

6.9

8

57.8

9

14.2

9

7.6

9

1.6

5

6.2

9

3.6

7

52.9

4 5.2

2

Sam

ple

siz

e 4

2 11

9

2 11

1

1 1

9 1

52

13

4 17

H

Std.

0.1

99

0.18

6 0.0

49

0.0

52

0.3

31

0.08

8

0.3

10

0.4

52

0.2

83

0.2

28

0.46

9 0.3

38

0.39

4


LAJAM 6(2): 171-183, December 2007

There were no differences among reproductive statuswith respect to number of anchovy (KW= 5.281, P>0.2,df= 4) nor in the percentage of anchovy consumed (KW=3.697, P>0.4, df= 4). While we found a significantrelationship between the number of prey consumed andthe porpoise’s body length (r

s =0.41, P=0.01, n=46), there

was no relation with the number of prey speciesconsumed (r

s=0.03, P>0.8, n=46).

The standardized Shannon-Wiener index (Hstd

) ofdiversity obtained for the pooled sample of the Peruviancentral coast was 0.23 (mean= 0.177, SD= 0.145, n= 11),while that obtained for Marcona was a higher 0.39 (n=2).There were no differences in indices calculated for everyperiod sampled (x2=3.501, P>0.95, df= 10; with H

max as

the expected value: x2= 1.699, P>0.99, df= 10).

Interspecific relations

The mean linkage cluster analysis applied to the ratioof contribution of the prey species to the pooled sampleof each cetacean studied, using the simplified Morisita’sindex (Figure 2) shows that the diet of the four cetaceanspecies is very similar, with overlapping trophic niches.The Burmeister’s porpoise and the long-beaked commondolphin are closest with a similarity of 0.965. This clusterjoins with the dusky dolphin at a similarity of 0.920 andwith the offshore common bottlenose dolphin at 0.873,Figure2.

The similarity matrix calculated for 1987 among D.capensis, L. obscurus and P. spinipinnis did not differgreatly from that obtained for the pooled samples,supporting the methodology used for the pooled data.

A high similarity index (0.915) was found between thegeneral diet of small cetaceans and the industrial fisheryof pelagic resources (Ñiquen and Bouchón, 1995),explainable because anchovy, the main targetof industrial fisheries in Peru, is also the mainprey of the most abundant small cetaceansspecies, in the same area. Since cetaceanmortality in the artisanal fishery occurs mainlyon the continental shelf (Van Waerebeek et al.,1997), it fully overlaps with the industrialfishery for anchovy.

DISCUSSION

Long-beaked common dolphin

Epipelagic schooling fish, mainly anchovy, wasthe main prey of long-beaked common dolphinsoff central Peru. Other prey were important onlyduring certain sampling periods and comprisedneritic (silverside), epipelagic (pilchard and Incascad), demersal (hake) and mesopelagic(lanternfish and lightfish) fish species. Theseresults are consistent with the findings for theBenguela Current, where common dolphinsforage over the shelf on both shallow and deep-water fish (Sekiguchi et al., 1992).

Anchovy schools off Peru are found over the shelf fromthe surface and 30 m depth at night and between 30-60m during the day (Jordán and Vildoso, 1965). Themesopelagic prey species found are associated with thedeep scattering layer and also show diel verticalmigrations from surface at night to 400-1000 m depthduring the day (Fitch and Brownell, 1968; Wisner, 1976;Robinson and Craddock, 1983). There is littleinformation on the depth at which this dolphin feeds,but daytime surface feeding (likely on anchovy) hasbeen observed by the authors off central and northernPeru. Gaskin (1982) suggested that common dolphins(Delphinus sp.) make deep dives for food at night andstay near the surface during the day.

El Niño-Southern Oscillation (ENSO) events exert a greatinfluence over pelagic resource fluctuations in the PeruCurrent (Arntz and Fahrbach, 1996) and thus over preyavailability. Anchovy was the main prey species overall,but it was not consumed by common dolphins duringall the periods sampled, when alternative prey formedthe bulk of the diet. For example, mesopelagic fishduring the 1987 El Niño, as well as silversides, hake andsculpins during different periods acquired highimportance temporally. This flexibility agrees with anopportunistic feeding behaviour related to local preyavailability. The low trophic niche breadth values,unexpected from any opportunistic feeding strategy, arethought to be an artifact produced by the highavailability of Peruvian anchovy, which is permanentand abundant during normal years (Pauly andTsukayama, 1987). Opportunistic feeding behaviourappears to be characteristic for common dolphinsaround the world, their stomach contents reflecting thelocal availability of resources (Klinowska, 1981). Offsoutheast South Africa long-beaked common dolphins

Figure 2. Mean linkage cluster analysis of the diet of four species of smallcetaceans from the Peruvian central coast


LAJAM 6(2): 171-183, December 2007

forage on the more available prey (Young and Cockcroft,1994; Sekiguchi et al., 1992). Neritic squids, engraulids,clupeids and mackerels were the main prey in theBenguela Current system (Sekiguchi et al., 1992), whileYoung and Cockcroft (1994) reported pilchard andmyctophids. In the California Current system the speciesfeeds mainly on clupeids, engraulids and hake (Norrisand Prescott, 1961; Heyning and Perrin, 1994). Ourresults for the Peruvian Current ecosystem are consistentwith these findings. On the other hand, short-beakedcommon dolphins, not typically associated with coastalupwelling areas, appear to feed on mesopelagic fish(myctophids), with epipelagic fish as alternative preyin the western North Pacific (Ohizumi et al., 1998; Chouet al., 1995) and mesopelagic fishes (Evans, 1980),carangids and squids (Pascoe, 1986) in the EnglishChannel. Prey differences between both species ofcommon dolphin appear to reflect their diverse habitat(Ohizumi et al., 1998). More productive coastalupwelling environments usually maintain a highbiomass of epipelagic schooling fish like anchovies andsardines, while mesopelagic diel migratory fish are moreabundant in oceanic waters (Mann and Lazier, 1996;Barnett, 1984).

A higher consumption of anchovy was observed mainlyduring winter, when anchovy disperses and reachesgreater depths (Jordán and Vildoso, 1965; Jordán, 1982).Young and Cockroft (1994) found diet differences inlong-beaked common dolphins of different sex, size andreproductive status off South Africa. However, suchdifferences were not found in the present study, possiblydue to sampling discontinuity.

Dusky dolphin

The diet of the dusky dolphin was composed mainlyof epipelagic schooling fish (anchovy, sculpins andscads) and mesopelagic fish (lanternfish and lightfish),with an important incidence of neritic fish (silverside)and some demersal fish (hake). Off central Peru duskydolphins foraged mainly on anchovy, while offMarcona they foraged on sculpins. McKinnon (1994)recorded 92.5% by weight of anchovy in central Peruin 1985-1986 besides Inca scad, hake and pilchard, butin contrast with the present study he found nomesopelagic species, which suggests changes in thefood supply or in the feeding habits. On the Atlanticcoast of South America, another engraulid is the mainprey of dusky dolphins which forage mainly in theafternoon (Würsig and Würsig, 1980; Crespo et al., 1994;Koen Alonso et al., 1998). Off South Africa the speciesfeeds at any time of the day on both pelagic and deepwater fishes such as mackerels, hake and lanternfishesin areas closer to shore and more on the shelf than other

cetacean species (Sekiguchi et al., 1992, 19957). Duskydolphins off Peru have been observed by the presentauthors feeding on anchovy during both night and day.Stomach contents suggest that they could also feed onmesopelagic fishes at night.

Latitudinal differences in the diet of dusky dolphinsbetween Marcona and Peru’s central coast suggest lowprey specialization. This becomes evident consideringthe high occurrence of anchovy in Marcona (96% FO)and its low percentage by number (17%), below motesculpins, which were completely absent from thecentral coast sample. Important landings of motesculpin, a subantarctic schooling fish, have beenreported in the area since 1991 (Quiroz et al., 1996).Coincidently, the southern distribution limit for theNorthern-Central stock of anchovy is situated at 14°S(Pauly and Tsukayama, 1987), i.e. near Marcona,where anchovy becomes scarce. Dusky dolphins thencould take advantage of the high availability ofsculpins in the area.

Diet composition and trophic niche breadth seemsinfluenced by different food supplies off the central coastand off Marcona, the result of the differentoceanographic conditions. Temporal differences in dietwere also detected on the central coast during years ofstrong influence of El Niño (e.g. in 1987). We concludethat dusky dolphins in Peruvian waters areopportunistic schooling fish feeders, foraging on themore abundant and available prey at determined areasand periods, replacing anchovies for sculpins, scads andlanternfishes according their availability.

Offshore common bottlenose dolphin

The main prey observed were mesopelagic myctophidfish with high diel migration. Van Waerebeek et al.(1990) found anchovy and lanternfish to be the mainprey of coastal and offshore Peruvian bottlenosedolphins, respectively. Considering the bathymetricdistribution of its main prey (Wisner, 1976; Fitch andBrownell, 1968), offshore common bottlenosedolphins in Peru are thought to feed from the surfacedown to at least 200m depth, but their diel behavioris unknown. However, inshore bottlenose dolphinscommonly forage during the day (authors, personalobservations).

The values of trophic niche breadth obtained for thisspecies are the highest of the four species analysed inthis study and are a reflection of a more varied diet,with six prey species consumed with more than 10%FO. This figure suggests that the offshore commonbottlenose dolphin is an opportunistic and flexiblefeeder with a wide trophic niche.

7 Sekiguchi, K., Best, P.B. and Klages, N.T.W. (1995) Foraging times of day for three Benguela dolphin species. Eleventh Biennal Conferenceon the Biology of Marine Mammals, Orlando, USA. (Abstract).


LAJAM 6(2): 171-183, December 2007

Burmeister’s porpoise

The main prey species of the Burmeister’s porpoise wasanchovy followed by silverside in the central coast andSouth Pacific hake and mote sculpin in Marcona. Byoccurrence, squids were important prey in Marcona. Thehigh amount of anchovy in the diet biased diversity indicesas a result of its high availability. However, an importantconsumption of other prey suggested an opportunisticfeeding behaviour on schooling fish and a high dietflexibility, consistent with conclusions from previous work(Reyes and Van Waerebeek, 1995). Porpoises caught offMarcona consumed less anchovy than those from thecentral coast, but instead consumed more hake, sculpinsand squids. Recent nuclear and mt-DNA analysis ofBurmeister’s porpoises (Rosa et al., 2005) indicatespopulation differences between Peruvian, Chilean andArgentinean individuals, while suggesting geneticheterogeneity also between northern and central Peru.Differences found in diet composition between central Peruand Marcona (separated by ca. 500km) may reflect differentfeeding habits between subpopulations.

Information gathered from bycatches in Peru indicates thatthe Burmeister’s porpoise is a neritic species. It has beensighted in both, protected bays and open waters relativelyclose to shore (Read et al., 1988; García-Godos, 1993; Reyesand Van Waerebeek, 1995; Van Waerebeek et al., 2002;Reyes, 2002). Insights obtained from stomach contentscollected in the present work confirm such a neritic habitat.Such field data allow a more accurate definition of habitatrange than that predicted indirectly from oceanographicinformation (e.g. Molina-Schiller et al., 2005). A similarinshore distribution has been observed in southern SouthAmerica where this species also prey on clupeids andgadids (Goodall et al., 1995a, b). On the basis of its prey,sightings and reports of specimens captured in shoreseines, Burmeister’s porpoise would be the second mostneritic forager of the Peruvian small cetaceans after theinshore common bottlenose dolphins (not sampled in thisstudy, but see Van Waerebeek et al., 1990). Despite this,the occurrence of Inca scad and other pelagic prey includesa subtle offshore component or adaptability to occasionalprey occurrence in its habitual environment.

Interspecific relations

The diet of all the species studied was highly related amongthem, conforming a cluster to a high similarity level of0.85 (Fig. 2). The long-beaked common dolphin comprisesthe first cluster with Burmeister’s porpoise at a similarityof 0.97, and not with dusky dolphin, contrary to expectationwhen considering that in Peru both dolphin species overlapconsiderably in distribution, and often form mixed schools(authors’ observations). However, their diets are still verysimilar, at a level of 0.875. The common bottlenose dolphinlogically showed the more distant diet because the samplebelongs to the large offshore population (Sanino et al. 2005).Likely the identification of cephalopods to species couldadd more detail to this cluster analysis than cephalopodsconsidered as a single item, although their contribution to

the diet was low.Although the diets of Burmeister’s porpoise and duskydolphin were relatively close off central Peru (simplifiedMorisitas’ Index = 0.780), they were distant in Marcona, at0.313 of the same index, explainable by a different habitatuse further south. The dusky dolphin off Peru shows mainlypelagic, not inshore, habits in relation to coastal waters (VanWaerebeek, 1992a,b), while Burmeister’s porpoise is mostoften sighted nearshore and often occupies, and apparentlyfeeds in, shallow waters of protected bays (Van Waerebeeket al., 2002). Despite this difference, both species feed onanchovy and mote sculpin off Marcona, but probably ondifferent components of these fish stocks.High similarity in diet between species translates in a lowlevel of diversification in feeding habits and broadly similarforaging strategies. This low diversification would berelated to the vast availability of anchovy off Peru (Jordán,1982; Pauly and Tsukayama, 1987) which can beconsidered a stabilizing factor for Peruvian small cetaceansunder ‘normal’ oceanographic conditions, keepinginterspecific competition for food low, in agreement withtheoretical models (Giller, 1984). However, the uncertaintyproduced by El Niño events off Peru (Arntz and Fahrbach,1996) sums a selection pressure that would compel smallcetaceans to keep an opportunistic feeding strategy.Despite the high similarity in the diets of these four highlysympatric small cetaceans studied, some differences infeeding habits can be noted. Burmeister’s porpoise feedscloser to shore than the other species and with a moredemersal foraging component. The distribution range ofdusky dolphin and long-beaked common dolphin largelyoverlaps off Peru, perhaps with some latitudinal differencesat their northern limits of distribution. Along the Peruviancoast the dusky dolphin distribution is strongly linked tocool waters and the species is thought to migrate southwardwhen a severe El Niño occurs (Van Waerebeek, 1992; García-Godos, 1993). Offshore bottlenose dolphins occur in deeperwater off Peru even beyond the continental slope, asreflected in a different diet based on mesopelagic fish.Peruvian anchovy has been exploited at a large scale sincethe 1960s and both overexploitation and fluctuations causedby El Niño have led to the collapse of anchovy predatorslike guano-producing seabirds (Arnzt and Farbach, 1996).Jahncke et al. (2004), using time series of wind stress, seasurface temperature, seabird population and anchovylandings from central and northern Peru between 1925 to2000, found that Peruvian guano-producing seabirdsreduced their consumption of the available anchovy in thesystem from 14.2% before the development of the fisheryto 2.2% afterwards, when fishery captured 85% of theavailable anchovy of the system. Together, overfishing andsevere El Niño events dramatically reduced the local seabirdpopulations, mainly during the collapse of the anchovyfishery (Duffy et al., 1984; Jahncke et al., 2004). The diet ofPeruvian guano-producing seabirds is mainly composedby anchovy and other pelagic species (Jahncke and Goya,1997; 1998), which suggests that seabirds are positionedtrophically very close to the studied small cetaceans. This


LAJAM 6(2): 171-183, December 2007

assumption allows us to suppose that small cetaceans couldbe similarly affected by the anchovy fishery and El Niño asseabirds were. Some evidence supports this hypothesis.Reyes and Van Waerebeek (1995) recorded strandings andemaciated Burmeister’s porpoises during the 1982-83 ElNiño, suggesting some related effects involved, while foodstress during the same event was recorded in dentinal layersof Peruvian dusky dolphins (Manzanilla, 1989). On the otherhand, the decrease in dolphin catches, as indicated bydecreased landings, during the 1991-92 El Niño may alsosuggest population movements (García-Godos, 1993),presumably southward as occurs with Peruvian guano-producing seabirds during El Niño events (Arntz andFahrbach, 1996).

Based on the relation of prey composition in cetaceanspecies and the Peruvian anchovy, we hypothesize thatstrong El Niño events would affect firstly and mostintensively inshore species and populations in coastalwaters of the Peru Current, i.e. Burmeister’s porpoises,followed by dusky dolphins and long-beaked commondolphins. Especially the latter species appears somewhatmore flexible in habitat and foraging. Offshore commonbottlenose dolphins are expected to cope considerablybetter than the other small cetaceans studied.

Acknowledgements

We are grateful to Mónica Echegaray, Karina Ontón andMarie-Françoise Van Bressem, for their support duringfield work. Field research was aided by grants to CEPECfrom the Leopold III Fonds voor Natuuronderzoek enNatuurbehoud, United Nations Environment Programme(UNEP), IFAW, IUCN Cetacean Specialist Group/ SpeciesSurvival Commission, Cetacean Society International (CSI)and the Whale and Dolphin Conservation Society (WDCS).IGG was supported by Wildlife Conservation Society(WCS) and Concejo Nacional de Ciencia y Tecnología ofPeru (CONCYTEC). Data processing and reporting wassupported by the International Whaling Commission (IWCVoluntary Fund for small cetacean research) accordingresearch proposal SC/52/SM34. We thank Kelly Robertson(SWFSC) and an anonymous reviewer for theirconstructive comments on the submitted paper.

References

ARIAS-SCHREIBER, M. (1996) Informe sobre el estado de conocimientoy conservación de los mamíferos marinos en el Perú. InformeProgresivo Instituto del Mar del Perú 38: 3-30.

ARNTZ, W. E. AND FAHRBACH, E. (1996) El Niño: Experimento Climáticode la Naturaleza. Fondo de Cultura Económica, México.

BAKUN, A. AND WEEKS, S.J. (2008) The marine ecosystem off Peru:What are the secrets of its fishery productivity and what might itsfuture hold? Progress in Oceanography 79:290-299.

BARNETT, M.A. (1984) Mesopelagic fish zoogeography in the centraltropical and subtropical Pacific Ocean: species composition andstructure at representative locations in three ecosystems. MarineBiology 82(2): 199-208.

BRAINARD, R.E. AND MCLAIN, M.C. (1987) Seasonal and interannualsubsurface temperature variability off Peru, 1952-1984. Pages 14-45 in PAULY, D. AND TSUKAYAMA, I. (Eds) The Peruvian Anchovetaand its Upwelling Ecosystem: Three Decades of Change. ICLARMStudies and Reviews 15. ICLARM, IMARPE, GTZ, Manila.

BROWNELL, R.L.JR. AND CLAPHAM, P.J. (1998) Burmeister’s porpoise Phocoenaspinipinnis (Burmeister, 1865). Pages 393-410 in RIDGWAY, S.H. AND HARRISON,R. (Eds), Handbook of Marine Mammals, Vol. 6. Academic Press, London.

CHOU, L.S., BRIGHT, A.M. AND YEH, S.Y. (1995) Stomach contents ofdolphins (Lissodelphis borealis and Delphinus delphis) from NorthPacific Ocean. Zoological Studies 34(3): 206-210.

CRESPO, E.A., NEPOMNASCHY, P., KOEN ALONSO, M. AND GARCÍA, N. (1994)Análisis preliminar de la dieta de mamíferos marinos sobre la basede contenidos estomacales y heces. Anales 4ta. Reunión de Trabajo deEspecialistas en Mamíferos Acuáticos de América del Sur: 75-88.

DUFFY, D.C., HAYS, C. AND PLENGE, M.A. (1984) The conservationstatus of Peruvian seabirds. Pages 245-259 in CROXALL, J.P. EVANS,P.G.H. AND SCHREIBER, R.W. (Eds) Status and conservation of the world’sseabirds. International Council for Bird Preservation, Cambridge.

EVANS P.G.H. (1980) Cetaceans in British waters. Mammalian Reviews10:1-52.

FITCH, J. AND BROWNELL, R. (1968) Fish otoliths in cetacean stomachsand their importance in interpreting feeding habits. Journal ofFishery Research Board of Canada 25(12): 2561-2575.

FROST, K.S. AND LOWRY, L.I. (1980) Feeding habits of the ribbon seal(Phoca fasciata) in the Bering Sea in spring. Canadian Journal ofZoology 58: 1601-1607.

GASKIN, D.E. (1982) The Ecology of Whales and Dolphins. HeinemannEducational Books Ltd. London.

GARCÍA-GODOS, A. (1993) Captura estacional de cetáceos menores en lacaleta de Ancón. Memoria del X Congreso Nacional de Biología: 273-279.

GARCÍA-GODOS, I. (2001) Patrones morfológicos del otolito sagitta dealgunos peces óseos del mar peruano. Boletín del Instituto del Mardel Perú 20: 1-83.

GARCÍA-GODOS, I. (2007) Revisión de las interacciones entre cetáceosy la pesquería marina peruana; perspectivas para la conservación delos cetáceos en Perú. Pages 77-82 in FÉLIX, F. (Ed) Memorias del Tallerde Trabajo Sobre el Impacto de las Actividades Antropogénicas enMamíferos Marinos en el Pacífico Sudeste. Bogotá, Colombia, 28-29de noviembre de 2006. CPPS/PNUMA. Guayaquil, Ecuador.

GOODALL, R.N.P., WÜRSIG, B., WÜRSIG, M., HARRIS, G. AND NORRIS, K.S.(1995a) Sightings of Burmeister’s porpoise, Phocoena spinipinnis, offsouthern South America. Pages 297-316 in BJØRGE, A. AND DONOVAN

G.P. (Eds) Biology of the Phocoenids. Report of the International WhalingCommission (special issue 16). Cambridge.

GOODALL, R.N.P., NORRIS, K.S., HARRIS, G., OPORTO, J. AND CASTELLO,H.P. (1995b) Notes on the biology of the Burmeister’s porpoise,Phocoena spinipinnis, off southern South America. Pages 317-347 inBJØRGE, A. AND DONOVAN G.P. (Eds) Biology of the Phocoenids. Reportof the International Whaling Commission (special issue 16). Cambridge.

GILLER, P.S. (1984) Community Structure and the Niche. Chapmanand Hall Ltd. London.

HEYNING, J.E. AND PERRIN, W.F. (1994) Evidence for two species ofcommon dolphins (Genus Delphinus) from the eastern NorthPacific. Contributions in Science 442: 1-35.

JAHNCKE, J. AND GOYA, E. (1997) Variación latitudinal y estacional enla dieta del guanay (Leucocarbo bougainvillii) y el piquero peruano(Sula variegata) en la costa peruana. Boletín del Instituto del Mar delPerú 16(1): 23-41.


LAJAM 6(2): 171-183, December 2007

JAHNCKE, J. AND GOYA, E. (1998) Las dietas del guanay y piqueroperuano como indicadoras de la abundancia y distribucion deanchoveta. Boletín del Instituto del Mar del Perú 17:15–34.

JAHNCKE, J., CHECKLEY, D.M. AND HUNT, G.L. (2004) Trends in carbonflux to seabirds in the Peruvian upwelling system: effects of wind andfisheries on population regulation. Fisheries Oceanography 13: 208-223.

JORDÁN, R. (1982) La anchoveta y su captura frente a las costas dePerú. Monografías Biológicas 2: 51-63.

JORDÁN, R. AND VILDOSO, A. (1965) La anchoveta (Engraulis ringensJ.). Conocimiento actual sobre su biología, ecología y pesquería.Informe del Instituto del Mar del Perú 6: 1-52.

KLINOWSKA, M.M. (1991) Dolphins, Porpoises and Whales of the World.The UICN Red Data Book. IUCN, Gland, Switzerland andCambridge, U.K.

KOEN ALONSO, M., CRESPO, E.A., GARCIA, N.A., PEDRAZA, S.N. ANDCOSCARELLA, M. (1998) Diet of dusky dolphins, Lagenorhynchus obscurus,in waters off Patagonia, Argentina. Fishery Bulletin 96(2): 366-374.

KREBS, C.J. (1989) Ecological methodology. Harper & Row,Publishers, New York, 654pp.

MAJLUF, P., BABCOCK, E.A., RIVEROS, J.C., ARIAS-SCHREIBER, M. ANDALDERETE, W. (2002) Catch and bycatch of seabirds and marinemammals in the small-scale fishery of Punta San Juan, Peru.Conservation Biology 16(5):1333-1343.

MANN, K.H. AND LAZIER, J.R.N. (1996) Dynamic of MarineEcosystems, Biological-physical Interactions in the Oceans.Blackwell Science, Massachusetts.

MANZANILLA, S.R. (1989) The 1982-1983 El Niño event recorded indentinal growth layers in teeth of Peruvian dusky dolphins(Lagenorhynchus obscurus). Canadian Journal of Zoology 67(9):2120-2125.

MCKINNON, J. (1994) Feeding habits of the dusky dolphin,Lagenorhynchus obscurus, in the coastal waters of central Peru.Fishery Bulletin 92(3): 569-578.

MOLINA-SCHILLER, D., ROSALES, S.A. AND DE FREITAS, T.R.O. (2005)Oceanographic conditions off coastal South America in relationto the distribution of Burmeister’s porpoise, Phocoena spinipinnis.The Latin American Journal of Aquatic Mammals 4(2):141-156.

NORRIS, K.S AND PRESCOTT, J.H. (1961) Observations of Pacificcetaceans of Californian and Mexican waters. University ofCalifornia Publications on Zoology 63(4): 291-402.

ÑIQUEN, M. AND BOUCHÓN, M. (1995) Información estadística de lapesquería pelágica en la costa peruana, 1981-1993. Informe delInstituto del Mar del Perú 107:1-66.

OHIZUMI, H., YOSHIOKA, M., MORI, K.,MIYASAKI, N. (1998) Stomachcontents of common dolphins (Delphinus delphis) in the pelagicwestern North Pacific. Marine Mammal Science 14(4): 835-844.

PASCOE, P.L. (1986) Size data and stomach contents of commondolphins, Delphinus delphis, near Plymouth. Journal of the MarineBiology Association, U.K. 66(2):319-322.

PAULY, D. AND TSUKAYAMA, I. (1987) On the implementation ofmanagement-oriented fishery research: The case of the Peruviananchoveta. Pages 1-13 in PAULY, D. AND TSUKAYAMA, I. (Eds) ThePeruvian Anchoveta and its Upwelling Ecosystem: Three Decades ofChange. ICLARM Studies and Reviews 15. IMARPE, GTZ,ICLARM, Manila.

PEÑA, N.J., MENDO, J. AND PELLÓN, J. (1989) Sexual maturity ofPeruvian anchoveta (Engraulis ringens), 1961-1987. Pages 132-142in PAULY, D., MUCK, P., MENDO, J. AND TSUKAYAMA, I. (Eds) ThePeruvian Upwelling Ecosystem: Dynamics and Interactions. ConferenceProceedings 18, ICLARM, IMARPE, GTZ, Manila.

QUIROZ, M., ZAMBRANO, M. AND CÁRDENAS, F. (1996) El recursocamotillo (Normanichthys crockeri) en la costa sur del Perú. Abril1995 a enero 1996. Informe Progresivo del Instituto del Mar del Perú46: 19-29.

READ, A.J., VAN WAEREBEEK, K., REYES, J.C., MCKINNON, J.S. ANDLEHMAN, L.C. (1988) The exploitation of small cetaceans in coastalPeru. Biological Conservation 46: 53-70.

REYES, J.C. (2002) Burmeister’s porpoise, Phocoena spinipinnis. Pages177-179 in PERRIN, W.F., WÜRSIG, B. AND THEWISSEN, J.G.M. (Eds)Encyclopedia of Marine Mammals, Academic Press, San Diego.

REYES, J.C. AND VAN WAEREBEEK, K. (1995) Aspects of the biology ofBurmeister’s porpoise from Peru. Pages 350-364.in Biology of thePhocoenids. BJØRGE, A. AND DONOVAN G.P. (Eds) Report of theInternational Whaling Commission (special issue 16). Cambridge.

ROBINSON, B.H. AND CRADDOCK, J.E. (1983) Mesopelagic fisheseaten by Fraser’s dolphin, Lagenodelphis hosei. Fishery Bulletin81(2): 283-289.

ROSA, S., MILINKOVITCH, M.C., VAN WAEREBEEK, K. BERCK, J., OPORTO,J., ALFARO-SHIGUETO, J., VAN BRESSEM, M.F., GOODALL, N. AND CASSENS,I. (2005) Population structure of nuclear and mitochondrial DNAvariation among South American Burmeister’s porpoises (Phocoenaspinipinnis). Conservation Genetics 6(3): 431 – 443.

RYTHER, J.H. (1969) Photosynthesis and fish production in the sea.Science 166: 72-76.

SANINO, G.P., VAN WAEREBEEK, K., VAN BRESSEM, M.-F. AND PASTENE,L.A. (2005) A preliminary note on population structure in easternSouth Pacific common bottlenose dolphins, Tursiops truncatus.Journal of Cetacean Research and Management 7(1): 65-70.

SEKIGUCHI, K., KLAGES, N.T.W. AND BEST, P.B. (1992) A comparativeanalysis of the diets of smaller odontocete cetaceans along thecoast of Southern Africa in Benguela Trophic Functioning. PAYNE,A.I.L., BRINK, K.H., MANN, K.H. AND HILBORN, R. (Eds) South AfricanJournal of Marine Science 12: 843-861.

SIEGEL, S. (1956) Nonparametric Statistics for the BehavioralSciences. McGraw-Hill Book Company, New York.

VAN WAEREBEEK, K. (1992a) Population identity and general biologyof the dusky dolphin Lagenorhynchus obscurus (Gray, 1828) in theSoutheast Pacific. Doctoral thesis, Institute for TaxonomicZoology, University of Amsterdam. 160pp.

VAN WAEREBEEK , K. (1992b) Records of dusky dolphinsLagenorhynchus obscurus (Gray, 1828) in the eastern South Pacific.Beaufortia 43(4): 45-61.

VAN WAEREBEEK, K. AND READ, A.J. (1994) Reproduction of duskydolphins Lagenorhynchus obscurus from coastal Peru. Journal ofMammalogy 75(4): 1054-1062.

VAN WAEREBEEK, K. AND REYES, J.C. (1990) Catch of small cetaceansat Pucusana port, central Peru, during 1987. Biological Conservation51: 15-22.

VAN WAEREBEEK, K. AND REYES, J.C. (1994a) Post-ban small cetaceantakes off Peru: a review. Report of the International WhalingCommission (special issue 15): 503-520.

VAN WAEREBEEK, K. AND REYES, J.C. (1994b) Interaction betweensmall cetaceans and Peruvian fisheries in 1988-1989 and analysisof trends. Report of the International Whaling Commission (specialissue 15): 495-502.

VAN WAEREBEEK, K., REYES, J.C., READ, A.J. AND MCKINNON, J.S. (1990)Preliminary observations of bottlenose dolphins from the Pacific coastof South America. Pages 143-154 in Leatherwood, S. and Reeves, R.R.(Eds) The Bottlenose Dolphin. Academic Press, San Diego.


LAJAM 6(2): 171-183, December 2007

VAN WAEREBEEK, K., VAN BRESSEM, M.F., FÉLIX, F., ALFARO-SHIGUETO,J., GARCÍA-GODOS, A., CHÁVEZ-LISAMBART, L., ONTÓN, K., MONTES, D.AND BELLO, R. (1997) Mortality of dolphins and porpoises in coastalfisheries off Peru and Southern Ecuador in 1994. BiologicalConservation 81: 43-49.

VAN WAEREBEEK, K., SANTILLÁN, L. AND REYES, J.C. (2002) An unusuallylarge aggregation of Burmeister’s porpoise Phocoena spinipinnis offPeru, with a review of sightings from Pacific South America. NoticiarioMensual Museo Nacional de Historia Natural, Chile 350: 3-8.

WISNER, L.R. (1976) The taxonomy and distribution of lanternfishes(Family Myctophidae) of the Eastern Pacific Ocean. NORDAReport 3. Office of Naval Research. St. Louis.

WHITEHEAD, P.J.P., NELSON, G.J. AND WONGRATANA, T. (1988) FAOspecies catalogue. Vol. 7. Clupeoid fishes of the world (SuborderClupeoidei). An annotated and illustrated catalogue of theherrings, sardines, pilchards, sprats, shads, anchovies and wolf-herrings. Part 2. Engraulididae. FA0 Fisheries Synopsis No. 125,Volume 7, Part 2:305-579.

WÜRSIG, B AND WÜRSIG, M. (1980) Behavior and ecology of the duskydolphin, Lagenorhynchus obscurus, in the South Atlantic. FisheryBulletin 77: 871-870.

YOUNG, D.D. and COCKCROFT, V.G. (1994) Diet of common dolphins(Delphinus delphis) off southern Africa: opportunism orspecialization? Journal of Zoology 234: 41-53.

Received 8 April 2006. Accepted 30 November 2007.


1Aquario de Ubatuba. Rua Guarani, 859. Ubatuba, São Paulo, Brazil. E-mail: [email protected] Instituto Argonauta para a Conservação Costeira e Marinha. Rua Guarani, 835. Ubatuba, São Paulo, Brazil.3 Fundação Pró-Tamar, Base Ubatuba. Rua Antonio Athanásio da Silva, 273. Ubatuba, São Paulo, Brazil.4Aquatic Animal Health Program, University of Florida, 2015 SW 16th Ave, Gainesville FL, 32610, USA.5 Jones, M.H., Otten, T., Smith, R. and Houck, J. (1988) Neonatal care of a stranded harbor porpoise, Phocoena phocoena. Pages 165-169 in

Abstracts, International Association of Aquatic Animal Medicine Annual Conference. 23-26 May. Orlando, FL, USA.

VETERINARY TREATMENT OF AN INJURED WILD FRANCISCANA DOLPHIN CALF(PONTOPORIA BLAINVILLEI, GERVAIS & D‘ORBIGNY, 1844)

PAULA BALDASSIN1,2; MAX RONDON WERNECK2,3; CARLA BEATRIZ BARBOSA1,2;

BERENICE MARIA GOMES GALLO2,3; HUGO GALLO

1,2 AND MICHAEL WALSH4

The Franciscana dolphin (Pontoporia blainvillei) is a smallcetacean endemic to the western South Atlantic Ocean,ranging from Espírito Santo, Brazil (18°25’S) to GolfoNuevo, Península Valdés, Argentina (42°35’S) (Kinas,2002). It appears to inhabit a narrow strip of coastalwaters between the surf line and the 30-m isobath. Itsconservation is of particular concern because of itsrestricted distribution and vulnerability to incidentalcapture in fishing gear (Reeves et al., 2003). Between 1997and 2001, 109 stranded animals, among which 28 livingcalves that could not be rescued, were observed in thecoastal region of São Paulo, Brazil (Santos et al., 2002).

Located in the north of São Paulo State, Brazil, theUbatuba Aquarium and Argonaut Institute for Costaland Marine Conservation have worked in therehabilitation of marine animals since 1996. Four otherfranciscana dolphin calves, including two males and twofemales, were treated in Ubatuba. One of these calveshad been caught in nets.

This case report describes the husbandry and medicalmanagement of an injured orphan female Pontoporiablainvillei calf entangled in a fishing net, and rescued bya diver in the shallow waters of São Sebastião, São Paulostate (23°21’20’’S) on 9 January 2006. Physical examinationand blood glucose test were performed on site by therescue team. Blood glucose level was 86 mg/dl and therespiratory rate was 5 breathes per minute. The animalwas transported to the Ubatuba Aquarium (23°26’13’’S)by car on foam transported dry and wet down with seawater for evaluation and rehabilitation. It was maintainedin a 1,000-L pool filled with sea water at 25oC and 35ppmsalinity, which was all changed after each feeding. Thecalf measured 76cm, weighed 5kg and had a bodytemperature of 36.4ºC. It presented with several abrasionson the rostrum. The umbilical cord was already detachedwith no signs of fetal folds. Teeth were partially eruptedand no hair was observed on the rostrum. Theseobservations suggest that the calf was about three monthsold. The teeth development indicated that it was alreadyable to consume small amounts of fish. Feces were greenin color, with a pasty consistency.

Heart rate and respiratory frequency were measuredevery 30 minutes. The heart rate ranged from 99 to 139per minute and the respiratory rate from 5 to 9 perminute. Respiration frequency increased initially after

handling but returned to normal shortly after release.The animal was alert but exhibited some abnormalswimming posture and appeared to be uncomfortableas evidenced by abdominal flexing and shivering. Thewater temperature was subsequently increased to 28ºCand the animal began swimming normally.

Prophylactic anti-microbial therapy was initiated witha daily intramuscular injection of 5mg/kg amikacinsulfate twice a day (Stoskopf, 1990). A milk replacerused at Sea World California and other marine parkswas prepared and the animal was fed every 1.5 h(Table 1) by bottle. The feeding frequency followedthe natural patterns known for dolphins, whichinclude nursing intervals between 30 min and 2 hourswith a 20-sec duration for each session (Jones et al.,19885; Sweeney, 1990). The rostrum lesions weretreated with a combination of Cicatrilex®, awaterproof ointment, and Quadriderm® (Gentamicin,Betamethasone, Tolnaftate and Iodoclorohidroxiquina).Three blood samples were collected from the central tailvein, with a 19 gauge butterfly and a 3-cc syringe (Table 2).

MILK COMPOSITION (1 LITER)

280g fish fillet (Sardina pilchardus)

50g zoologic 30/55

90g zoologic 33/40

1/2 tablet soy lecithin

7.25g glucose

62mg taurine

4.5g NaCl

1.2g (18.75g) dicalcium phosphate

25ml cod liver oil

550ml filtered tap water/milk without lactose

50ml milk cream without lactose

Table 1. Milk formula administered to the franciscana dolphin fromthis study, adapted from formula used at Sea World California(Young and Dalton, 1994*) but modified based on the oil available.

* Young, W. G. and Dalton, L. M. (1994) Treatment of a livestranded young Risso’s dolphin (Grampus griseus) Page 140in Abstracts, International Association of Aquatic AnimalMedicine Annual Conference. 11-14 May. Vallejo, CA, USA.

186 P.BALDASSIN et al.

LAJAM 6(2): 185-187, December 2007

Whole blood glucose was measured three times a day(morning, pre-feeding, afternoon and night), withAccu-Chek Advantage®. These ranged from 42 to82mg/dl and weren’t consistently maintained. Bloodglucose values showed large variation during thetreatment and in periods of low glycemia the animalshowed apathymild depression and slight tremblingwhich may also be related to the lower watertemperature. Glucose levels in milk weresubsequently increased and the blood glucose levelsstabilized. The increasing hematocrit and hemoglobinlevels indicated that the dolphins deterioratinghydration status. The level of eosinophils was initiallylow. A decrease in the frequency of eosinophils hasbeen observed in stressed cetaceans or when anti-inflammatory medications were given (Bossart andDierauf, 1990). The dolphin developed a leucopeniaindicative of a severe bacterial or viral infection anddied six days after rescue. Gross necropsy revealed afriable liver of light pink color and hyperemic lungsthat had diffusely scattered areas of emphysema inthe dorsal region. Histologically, the liver had mildto severe diffuse micro- and macro-vacuolization ofthe hepatocytes, indicative of diffuse vacuolarhepatopathy which can be related with nutritionaldisturb. The lungs showed mild congestion, edemaand hemorrhagic points, and thickened alveolar septa.There were numerous macrophages in the alveolarlumen and heterophils in the capillaries, indicatingacute interstitial pneumonia. Histological resultssuggest an infection process due to the association ofthe degenerative hepatic process with the lung and

intestinal compromised.

Management of neonatal cetaceans can becomplicated with clinical parameters changing veryrapidly. Immune compromise and exposure to newbacterial flora in the environment requires an increasein surveillance for current and developing pathogensduring the rehabilitation process. Additionaldiagnostic tests may include aerobic and anaerobicbacterial cultures, as well as yeast and fungal culturesfrom the respiratory system, gastric and rectum.Cytology from these systems is also recommended.Whenever possible, cultures and antibiotic sensitivitypatterns should be used to guide antibiotic choice andthe route of administration. Cytology may also helpto determine the site of involvement and help in thechoice of oral and parenteral antibiotics.

While initial CBC results indicated issues withdehydration as evidenced by an increasing hematocrit(Table 2) there is little published information on thenormal ranges for these parameters of this species inthe literature.

According to the IUCN (Cetacean Specialist Group,1996), francicana dolphins are listed as “DataDeficient”, meaning there is inadequate informationto make a direct, or indirect, assessment of its risk ofextinction based on its distribution and/or populationstatus. The current lack of information on Pontoporiablainvillei emphasizes the need to improve veterinaryhealth care, gather additional baseline information,and to implement and develop healthcare protocolsfor this species.

HEMOGRAM

09 JAN 2006 11 JAN 2006 13 JAN 2006

Erythrocytes (millions/mm3) 4.23 4.56 4.77

Hematocrit (%) 47 51 55

Hemoglobin (g/%) 15.5 16.3 17.7

MCV (µ3) 111.11 111.84 115.30

MCH (pg) 36.64 35.74 37.10

MCHC(%) 32.97 31.96 32.18

Leukocytes (mm3) 4200 3500 900

Basophils (%) 0 0 0

Eosinophils (%) 2 3 0

Mielocytes (%) 0 0 0

Metamielocytes (%) 0 0 0

Band shaped (%) 1 2 1

Segmented (%) 60 60 68

Lymphocytes (%) 35 30 28

Monocytes (%) 2 5 3

Platelets (mil/mm3) 189 155 120

Table 2. CBC results for the Franciscana dolphin during rehabilitation.

VETERINARY TREATMENT OF AN INJURED WILD FRANCISCANA DOLPHIN CALF 187

LAJAM 6(2): 185-187, December 2007

Acknowledgements

The authors express their gratitude to Leonardo Teixeirafrom IBAMA - Caraguatatuba, Shirley Pacheco de Souzafrom Instituto Terra & Mar, Fernando Alvarenga andtrainees from Ubatuba Aquarium and Projeto Tamar –IBAMA Base Ubatuba. We also thank Dr. CharlesManire and Dr. Marie-Françoise van Bressem for theirhelpful comments to the manuscript.

References

BOSSART, G.D. AND DIERAUF, L.A. (1990) Marine mammalClinical Laboratory medicine. Pages 1-52 in DIERAUF, L.A. (Ed.) Handbook of Marine Mammal Medicine, Health,Disease and Rehabilitation. Volume 2. CRC Press. BocaRaton, FL, USA.

CETACEAN SPECIALIST GROUP. (1996) Pontoporia blainvillei.In: IUCN 2006 Red List of Threatened Species.<www.iucnredlist.org>. Downloaded on 05 June 2007.

KINAS, P.G. (2002) The impact of incidental kills by gill

nets on the Franciscana dolphin (Pontoporia blainvillei) insouthern Brazil. Bulletin of Marine Science 70(2): 409-421.

REEVES, R.R., SMITH, B.D., CRESPO, E.A. AND DI SCIARA, N.G.(2003) Dolphins, Whales and Porpoises: 2002-2010Conservation Action Plan for the World’s Cetaceans. IUCN/SSC Cetacean Specialist Group. IUCN, Gland,Switzerland and Cambridge, United Kingdom.

SANTOS, M.C.O., VICENTE, A.F.C., ZAMPIROLLI, E.,ALVARENGA, F.S. AND SOUZA, S.P. (2002) Records ofFranciscana (Pontoporia blainvillei) from the coastalwaters of São Paulo State, southeastern Brazil. The LatinAmerican Journal of Aquatic Mammals 1(1): 169-174.

STOSKOPF, M.K. (1990) Marine Mammal Pharmacology.Pages 139-162 in DIERAUF, L.A. (Ed.) Handbook of MarineMammal Medicine, Health, Disease and Rehabilitation.Volume 2. CRC Press, Boca Raton, FL, USA.

SWEENEY, J.C. (1990) Marine mammal behavioraldiagnostics. Pages 53-72 in DIERAUF, L.A. (Ed.) Handbookof Marine Mammal Medicine, Health, Disease andRehabilitation. Volume 2. CRC Press, Boca Raton, FL, USA.

Received 2 July 2007. Accepted 30 November 2007.


1 Everest Tecnologia em Serviços Ltda. Av. João Batista Parra 633, 9th floor, Vitória, ES, 29052-123 Brazil.* Corresponding author, e-mail: [email protected] Santos, M. C. O. (1998) Hand-feeding wild Sotalia: A new matter of concern in Brazil? In abstract, 8º Reunião de Trabalhos de

Especialistas em Mamíferos Aquáticos da América do Sul, Recife, Brasil.

AN INTERACTION BETWEEN A JUVENILE CLYMENE DOLPHIN (STENELLA CLYMENE) ANDSEISMIC SURVEY VESSEL M/V RAMFORM CHALLENGER -PGS, BACIA DE SANTOS, BRAZIL

MICHELE F. FERNANDES1, *, ANDREA S. CORDEIRO1,

DEMETRIO M. R. CARVALHO1, WILSON R. SANTOS1 AND RENATA RAMOS1

KEYWORDS: Stenella clymene, behavior, seismic survey, human impact, cetaceans.

Interactions between cetaceans and vessels have beenwidely reported. Various studies have reported theimpacts of these interactions, in which researchers havebeen monitoring the effects of anthropogenic disturbanceon these animals, such as collision, changes to behaviorand on the social groups (Van Parijs and Corkeron, 2001;Lemon et al., 2005), separation between adults and young,abandonment of mating areas and even growingaccustomed to living alongside humans, as in the case ofone young Sotalia fluviatilis in Brazil (Santos, 19982). Withrespect to seismic surveys, aversion behavior by marinemammals in response to a seismic survey vessel has beenspecifically mentioned in several studies (e.g. Gould andFish, 1998; Madsen et al., 2002; Stone and Tasker, 2006;

Gailey et al., 2007; Yazvenko et al., 2007, a;b).

Many vessels, at one time or another, have had dolphinsaround bowride the vessel, and it is quite common for theseanimals to associate with boats. Extreme cases have alreadybeen cited, such as a Risso’s dolphin Grampus griseus(‘Pelorus Jack’), who for 24 years, from 1888 to 1912, wouldoften move in the bow-waves of steamers coming into NewZealand (Szabo, 1992 cited in Constantine and Baker, 1997).

On 22 July 2006, beginning at 08:07 hs, during seismicsurvey activity in the Santos Basin, Block BM-S-04 (24°04’Sto 24°42’S / 43°21’W to 43°12’W) (Figure 1), on board theship M/V Ramform Challenger/PGS, a young clymenedolphin (Stenella clymene) was sighted (Figure 2). This

Figure 1. Map indicating the location of Block BM-S-04 in the Santos Basin, southeastern Brazil.

190 M.F.FERNANDES, A.S.CORDEIRO, D.M.R.CARVALHO, W.R.SANTOS AND R.RAMOS

LAJAM 6(2): 189-192, December 2007

animal continued to accompany the vessel until 24 July2006, totalizing some 56 hours.

The animal was alone and, throughout the periodthat the ship was in the area (27 days prior to theappearance of the dolphin, 51 days in total), noadditional clymene dolphins were sighted. Theanimal was seen for the first time heading from sternto bow, to starboard, inside the seismic survey ‘safetyarea’. The safety area is a 500m radius zone aroundthe seismic survey sound source (air guns) if inwhich, according to the ‘Guide for MonitoringMarine Fauna in the Activity of Acquiring SeismicData’ (IBAMA, 2005), marine mammals or cheloniansare sighted, seismic surveys must cease. Seismicsurvey activity should only resume, according to theguidelines, when these animals have left the safetyzone and a 30 minute-period has elapsed without asighting within a radius of 1000m from the soundsource (the ‘Warning Area’).

Seismic activity was curtailed immediately afterobserving the dolphin inside the safety area. Theanimal continued to accompany the ship until 24 July2006, and seismic survey activity was not conductedthroughout this period. Between the 23 and 24 July the

dolphin strayed away from the ship (more than 1000m)and seismic survey activity was resumed on themorning of the 24 July. However, the animal came backto the safety area and the sound production wasstopped again, with the airgun array staying silent forthe entire day on 24 July. Joint action was set in motion,involving consultation between the onboard MarineMammal Observer (MMO), the seismic party chief, theship’s Master, the coordinators of the Everest Programfor Biota Monitoring and the PGS (Petroleum Geo-Service) Brazil Coordinator of EnvironmentalPrograms. The first step was to make contact withresearchers specializing in marine mammals, to checkwhat procedure could be applied in an unusualsituation such as this, since the Brazilian legislationforbids any attempt to chase or remove animals nearthe seismic survey vessel (IBAMA, 2005).

One idea was to put the ‘workboat’ (support boat)into the water to attract and lead the dolphin awayfrom the survey area. At 12:27h on 24 July 2006, thefirst attempt to attract the animal with the workboatwas made, with consent from CGPEG/IBAMA (theentity responsible for the Brazilian EnvironmentalLegislation), and with one MMO on board. A rope

Figure 2. Juvenile clymene dolphin (S. clymene)sighted on 22 July 2006, while interacting with theseismic survey ship M/V Ramform Challenger -PGS (Photo by Joanna Miladowska).

a

b

AN INTERACTION BETWEEN A JUVENILE CLYMENE DOLPHIN AND A SEISMIC SURVEY VESSEL, BACIA DE CAMPOS, BRAZIL 191

LAJAM 6(2): 189-192, December 2007

wrapped in aluminum foil was hung in the water toact as a lure for the animal. This first attempt wasmet with no success, as the animal was evasive,always seeking to get on the opposite side of theworkboat. Occasionally the juvenile dolphin didshow interest in the lure from the workboat, but assoon as this was removed the animal lost interestand once again moved to the opposite side of theship. At no time did the boat accelerate towards theanimal to frighten it, but even when the workboatapproached, the dolphin tended to swim in theopposite direction.

The animal remained within sight of the observers(workboat crew and the MMOs) the entire day, butwith less aerial activity (fewer leaps) than previouslyobserved and with periods of ‘disappearance’ (around20 minutes). These increased when the workboat wasin the water. Visual search for the animal wasconducted from the starboard and port wings of thebridge, and also from the stern and the bow of theship, to ensure that the dolphin had moved somedistance away from the vessel. The three MMOsonboard took turns, with two MMOs searching on theport and starboard wings of the bridge, respectively,and a third one searching at the bow and stern,simultaneously.

After a long period of disappearance, now in the lateafternoon (16:20h), the two support boats (theworkboat and the FRC – Fast Rescue Craft) wereplaced in the water, one to port and the other tostarboard, with an MMO always on board, in case theanimal should re-appear. On board the seismic shipwere the third MMO and the onboard oceanographer(responsible for the company’s other environmentalprojects), positioned on the wings of the bridge, tocontinue monitoring. In addition to these on-boardobservers, the seismic party chief, the ship’s masterand radio operator were also present. The boatsremained at a distance of some 300m from the ship,both of them with a lure.

The animal was once again sighted at over 500m fromthe seismic ship M/V Ramform Challenger. At thispoint, one of the support boats slowly approached theanimal, and the dolphin followed the boat, probably

as a result of the lure, and it was led towards the‘assistant vessel’ Big John I (a vessel that remains atsome 1-2 miles from the seismic vessel throughoutthe entire activity, assisting fishing boats, which wasaround one mile to starboard). The lure was handedover to a crew member of the assistant vessel, whichheaded to the distant area of Block BM-S-4, and wasfollowed by the dolphin, which was not resighted bythe survey vessel. Monitoring continued until it gotdark, with searches astern and ahead of the ship, plusthose to port/starboard, so that seismic surveyingcould continue.

During the three days of observation, the dolphinshowed no obvious outward signs of illness, starvationor injury, and was highly active throughout (performingtotal and partial leaps and ‘porpoising’ behavior at thebow and stern of the ship). The animal did appear to beforaging as on more than one occasion it was seen toattack small shoals of fish.

The reasons for such an extended dolphin-seismicvessel association are unclear. On one occasion, whenthe juvenile dolphin was some distance from vessel, itperformed several leaps and moved irregularly, thenapproached very closely to the vessel, practically upalongside the hull, as though it were, perhaps, fleeingfrom something and seeking protection from thevessels. Alternatively, the animal could also haveapproached the vessel to get into the ‘acoustic shadow’of the ship thereby evading higher sound levels aroundthe airgun array.

Stone and Tasker (2006) suggested that differenttaxonomic groups of cetaceans may adopt differentstrategies for responding to acoustic disturbance fromseismic surveys; the slower moving mysticetes orientaway from the vessel and increase their distance fromthe source but move away from the area completelywhile some small odontocetes move out of theimmediate area, however such behavior was notobserved in this study.

Over six years of monitoring marine biota during theseismic activities for PGS (between 2001-2006) in Brazil,some 20 species of cetaceans have been observed inthe seismic survey area (Silva, 2003; Moreira et al.,20043; Ramos et al., 20044; Dafferner et al., 20055;

3 Moreira, S., Fernandes, T., Erber, C., Alencastro, P., Silva, E.D., Rinaldi, G., Aragão, R., Figna, V. and Ramos, R. (2004) Ocorrência decachalotes (Physeter macrocephalus) na costa do Brasil. Pages 160-161 in Abstract, 11ª Reunión de Trabajo de Especialistas en MamíferosAcuáticos de América del Sur y 4º Congreso de la Sociedad Latinoamericana de Especialistas en Mamíferos Acuáticos. 11-17 deSeptiembre, Quito, Ecuador.

4 Ramos, R., Ribeiro, R., Moreira, S.C., Erber, C., Alencastro, P.M.R., Poletto, F.R., Silva, E.D., Fernandes, F., Bertoncini, A., Moraes, E.,Venturotti, A, Figueiredo, L.D., Fortes, R.C., Grando, A.P., Figna, V.N.D., Rinaldi, G.C. and Aragão, R.X. (2004) Monitoramento dabiota marinha em atividades petrolíferas: uma contribuição para o conhecimento da distribuição e ocorrência da fauna marinha.Page 414 in Abstract, Congresso Brasileiro de Oceanografia e XVI Semana Nacional de Oceanografia, 10 e 15 de outubro, UNIVALI,Itajaí, Santa Catarina.

5 Dafferner, G., Barbosa, M.B., Freitas, R.H.A., Penteado, J.P.C., Alencastro, P.M.R., Fortes, R.C., Laitano, K.S., Figna, V.N., Grando,A.P., Santos Jr., W.R., Silva Ribeiro, C.C., Gerhardinger. L.C. and Ramos, R.M.A. (2005) Resultados do esforço de observação decetáceos a bordo do navio sísmico Falcon Explorer durante as atividades nas Bacias de Campos e Santos (dez/04 a jun/05): umaabordagem descritiva. In Abstract, II Congresso Brasileiro de Oceanografia, 9 a 12 de outubro de 2005, Vitória, Espírito Santo.

192 M.F.FERNANDES, A.S.CORDEIRO, D.M.R.CARVALHO, W.R.SANTOS AND R.RAMOS

LAJAM 6(2): 189-192, December 2007

Erber et al., 2005, a6;b7). This was the first instance of aprolonged interaction (~56h) between a dolphin and aseismic ship.

Acknowledgments

We thank biologist Cristiano Vilardo Nunes (CGPEC/IBAMA), Professor Dr. Sheila Marino Simão (UFRJ),for use of the lure, biologists Dr. José Martins da Silva(Instituto Golfinho Rotador), and Dr. Salvatore Siciliano(Fundação Oswaldo Cruz), for identification of thedolphin to species level. We also thank veterinarianMilton Marcondes and biologist Marcos Rossi ofInstituto Baleia Jubarte. PGS (Petroleum Geo-Service)gave us permission to disclose the data. We are indebtedto the Coordinator of Environmental Procedures at PGS,Alexandre Bacellar Netto, plus the entire crew of theship M/V Ramform Challenger, especially the seismicparty chief, Esben Jettestad, Master Halvor Schia, radiooperator Tony Ferreira dos Santos and crew membersOld Drablos, Nigel Pardoe, Alex Townley, Dan Barrat,James de Long and Paul Jackson, who assisted our teamon board the support boats (workboat and FRC). JoanaMiladowska kindly allowed us to use the photographsshe took during the sighting. This manuscript wasgreatly improved by the comments of Dr. Chris Parsonsand an anonymous reviewer.

References

CONSTANTINE, R. AND BAKER, C.S. (1997) Monitoring the commercialswim-with-dolphin operations in the Bay of Islands, New Zealand.Science & Research Series No. 104. Department of Conservation,Wellington, New Zealand. 54 pp.

GAILEY, G., WÜRSIG, B. AND MCDONALD, T.L. (2007) Abundance,behaviour and movement patterns of western gray whales in relationsto a 3-D seismic survey, Northeast Sakhalin Island, Russian.

Environmental Monitoring and Assessment 134(1-3): 75-91.

GOULD, J.C. AND FISH, P.J. (1998) Broadband spectra of seismicsurvey air-gun emissions, with reference to dolphin auditorythresholds. Journal of the Acoustical Society of America 103:2177-2184.

LEMON, M., LYNCH, T.P., CATO, D.H. AND HARCOURT, R.G. (2005)Response of traveling bottlenose dolphins (Tursiops truncatus)to experimental approaches by a powerboat in Jervis Bay, NewSouth Wales, Australia. Biological Conservation 127: 363-372.

MADSEN, P.T., MOHL, B., NIELSEN, B.K. AND WAHLBERG, M. (2002)Male sperm whale behaviour during exposures to distant seismicsurvey pulses. Aquatic Mammals 28(3): 231-240.

VAN PARIJS, S.M AND CORKERON, P.J. (2001) Boat traffic affects theacoustic behaviour of Pacific humpback dolphins, Sousa chinensis.Journal of the Marine Biological Association of the UnitedKingdom 81: 533-538.

SAMUELS, A., BEJDER, L. AND HEINRICH, S. (2000) A review of theliterature pertaining to swimming with wild dolphins. Reportprepared for the Marine Mammal Commission, Washington, D.C.Contract Number T74463123. 57 pp.

SILVA, E.D. (2003) Ocorrência e distribuição de Mysticeti eOdontoceti (Cetacea) em bacias sedimentares da região sudestedo Brasil. MSc Thesis. Universidade Estadual Paulista Jaboticabal,SP, Brazil. 105 pp.

Stone, C.J. and Tasker, M.L. (2006) The effects of seismic surveyairguns on cetaceans in UK waters. Journal of Cetacean Researchand Management 8: 255-263.

YAZVENKO, S.B., MCDONALD, T.L., BLOKHIN, S.A., JOHNSON, S.R.,MELTON, H.R., NEWCOMER, M.W., NIELSON, R AND WAINWRIGHT, P.W.(2007a) Feeding of western gray whales during a seismic surveynear Sakhalin Island, Russian. Environmental Monitoring andAssessment 134(1-3): 93-106.

YAZVENKO, S.B., MCDONALD, T.L., BLOKHIN, S.A., JOHNSON, S.R.,MEIER , S.K., MELTON, H.R, NEWCOMER, M.W., N IELSON, R.,VLADIMIROV, V.L. AND WAINWRIGHT, P.W. (2007b). Distribution andabundance of western gray whales during a seismic survey nearSakhalin Island, Russia. Environmental Monitoring andAssessment 134(1-3): 45-73.

6 Erber, C., Moreira, S. C., Fernandes, T., Poletto, F.R., Alencastro, P.M.R., Grando, A.P., Figna, V.N.D., Dafferner, G., Freitas, R.H.A.,Carneiro, A.V., Miranda, C.M., Barbosa, M.B., Eliseire Jr., D., Almeida, A.N.F. and Ramos, R.M.A. (2005a). Avistagens de baleia-piloto, orca-pigméia, falsa-orca, orca e golfinho-de-Risso: dados inéditos para ampliar o conhecimento de espécies pouco conhecidas.Page 85 in Abstract, III Congresso Brasileiro de Mastozoologia, 12 a 16 de outubro, Vitória, Espírito Santo.

7 Erber, C., Moreira, S., Fernandes,T., Carneiro, A., Alencastro, P.; Poletto, F., Figueiredo,L., Fortes, R., Bertoncini, Á., Grando, A.,Rinaldi, G., Figna, V., Silva, E., Moraes, E. and Ramos, R. (2005b) The monitoring of marine mammals onboard seismic vessels as toolfor the knowledge of the distribution of the genus Stenella in the Brazilian coast. Page 68 in Abstract, 19th Annual Meeting of theSociety for Conservation Biology, 15 a 19 de Julho, Brasília, DF.



1 Fundación Ecuatoriana para el Estudio de Mamíferos Marinos (FEMM). PO Box 09-01-11905. Guayaquil, Ecuador.2 Pontificia Universidad Católica del Ecuador (PUCE). Av. 12 de Octubre and Patria, Quito, Ecuador.3 Universidad de Antioquia. Calle 67 Nº 53·108, Medellín, Colombia.4 Universidad Estatal Península de Santa Elena (UPSE). Vía La Libertad-Santa Elena, La Libertad, Ecuador.* Corresponding author, e-mail: [email protected] Gendron, D. and Sears, R. (1993) Blue whale and Nyctiphanes simplex surface swarms: a close relationship in the southwest Gulf of California,Mexico. Page 52 in Abstracts, X Biennial Conference on the Biology of Marine Mammals, 11-15 November, Galveston, TX, USA.

OBSERVATION OF A BLUE WHALE (BALAENOPTERA MUSCULUS)FEEDING IN COASTAL WATERS OF ECUADOR

FERNANDO FÉLIX1,2,*, NATALIA BOTERO1,3 AND JÉSSICA FALCONÍ1,4

ABSTRACT: The presence of the blue whale (Balaenoptera musculus) in continental waters of Ecuador is known from only a fewreports. Here we present photographic evidence of a blue whale feeding in costal waters of this country. The event occurred on17 July 2007, 2nm west of Salinas, Santa Elena Peninsula (2°12’08"’S, 81°02’31"W). The whale was followed during 31 minutesaboard a whalewatching boat. At one point, the whale was observed moving fast at the surface and rolling over its right sidewith its mouth open. Although the type of food being consumed was not evident, the behavior is similar to that described assurface feeding on euphausiid swarms. Despite the intense whale research effort conducted over the past 15 years in coastalwaters of Ecuador, this is the first time a blue whale is recorded in nearshore waters.

RESUMEN: La presencia de ballenas azules Balaenoptera musculus en aguas continentales de Ecuador es solamente conocida porunos pocos registros. En este artículo presentamos evidencia fotográfica del avistamiento de una ballena azul alimentándoseen aguas costeras de Ecuador. El suceso ocurrió el 17 de julio de 2007, apenas a 2mn al oeste de Salinas, península de SantaElena (2°12’08"S, 81°02’31"W). La ballena fue seguida por 31 minutos a bordo de un yate de turismo utilizado regularmentecomo plataforma de investigación. En un momento dado, la ballena fue observada nadando rápido en la superficie y girandosobre su lado derecho con la boca abierta. Aunque no se observó que tipo de alimento ingería, este comportamiento ha sidodescrito como una forma de alimentación de las ballenas azules sobre enjambres de eufáusidos que se concentran en la superficie.Pese al intenso esfuerzo de investigación de ballenas desarrollado en los últimos 15 años en aguas costeras de Ecuador, ballenasazules no habían sido registradas hasta ahora.

KEYWORDS: Blue whale, Balaenoptera musculus, feeding, distribution, Ecuador

Introduction

The blue whale (Balaenoptera musculus) is acosmopolitan species that is distributed mainly alongshelf margins and to a lesser extent in oceanic watersand coastal zones (Leatherwood and Reeves, 1983).In contrast to most balaenopterids that undergo longannual migrations between the feeding grounds inpolar zones and the breeding areas in tropical waters,the movements and migration patterns of blue whalesare less well known and seem to be more complexthan in species such as humpback (Megapteranovaeangliae) or fin whales (Balaenoptera physalus)(Perry et al., 1999; Branch et al., 2007).

In the eastern tropical Pacific, blue whales occurmainly in upwelling areas characterized by waters ofcool temperature and high primary productivity suchas Baja California, the Costa Rica Dome, theGalápagos Islands, and off southern Ecuador andnorthern Peru (Reilly and Thayer, 1990). Highconcentrations of euphausiids or “krill” is a commoncharacteristic to these areas, and is why it has beensuggested that the presence of blue whales in theseareas could be related to feeding activities (Reilly andThayer, 1990; Gendron and Sears, 19935; Fiedler et al.,1998; Palacios, 1999; Ballance et al., 2006; Branch etal., 2007).

Blue whales occur regularly along most of the SouthAmerican Pacific coast, as indicated by catches reportedfrom Peru and Chile during the 20th century (see Clarke,1980). The occurrence of the species during all monthsof the year off Peru (Ramírez, 1983) suggests thepresence of whales from both hemispheres in theirrespective winter and spring months, although it hasalso been suggested that a discrete sub-stock couldinhabit this part of the Eastern Pacific year round(Donovan, 1984; Branch et al., 2007). In contrast to othercountries of the Southeast Pacific, records of blue whalein Ecuador are scarce; most of them have been made inthe Galápagos Islands (1,000km west of Ecuador),particularly along the west side where upwelling isstrong (e.g. Reilly and Thayer, 1990; Wade andGerrodette, 1993; Merlen, 1995; Palacios, 1999). Thenumber of records from Galápagos, however, indicatesthat the species is currently not abundant there. Sincerecords have been made almost exclusively during theaustral winter and spring months, these whales wouldcorrespond to a Southern Hemisphere population(Reilly and Thayer, 1990; Palacios, 1999). The presenceof blue whales in continental waters of Ecuador is evenless well known. Clarke (1962) reported on a whalingexpedition in coastal waters of Ecuador in 1926 whosecatches mainly included young blue and fin whales. Inaddition to the few sightings reported by Reilly andThayer (1990) off southern Ecuador and north of Peru

194 F.FÉLIX, N.BOTERO AND J.FALCONI

LAJAM 6(2): 193-197, December 2007

between 1974 and 1988 (in fact all of them wererecorded off Peru, south of 4ºS), there is only oneadditional sighting in southern Ecuador, made in 1999(3ºS, 83ºW) during a marine mammal survey carriedout by a ship from the National Oceanic andAtmospheric Administration (NOAA) of the UnitedStates (Kinzey et al., 2000).

In this article we report on the sighting of a blue whalein coastal waters of Ecuador. In addition to being oneof the few sightings of this species in Ecuadorianwaters, the most relevant aspect is that the animal wasengaged in behavior consistent with feeding activity.

The record

On 17 July 2007, aboard of a whalewatching yacht usedregularly by Fundación Ecuatoriana para el Estudiode Mamíferos Marinos researchers as platform to study

humpback whales off Salinas, Ecuador, a blue whalewas recorded 2nm west of the Santa Elena Peninsula(2°12’08"S, 81°02’31"W; Figure 1). The tip of thepeninsula is the westernmost part of Ecuador andextends 12km into the Pacific Ocean, further restrictingthe already narrow continental shelf along this part ofthe coast (de Miro et al., 1976). According to theNavigation Chart I.O.A. 1056 the depth of the sightinglocation was ~ 50m.

The individual was followed for 29 minutes from 11:41hto 12:10h. The track during the sighting period showsthat the whale moved 1.8km in a southerly direction atan average speed of 3.72km/h, assuming a straight linemovement. On several occasions the animal was closeenough to be photographed and positively identifiedto species. Dives lasted at least 5 minutes, after whichthe animal took three breaths at the surface. As it cameup to breathe, the whale exposed the anterior and midupper part of its grayish back, and on a few occasions

Figure 1. Sighting site off the Santa Elena Peninsula, Ecuador. The arrow in the circle (left) indicates the direction and the distance

traveled by the whale during the observation period.

6 The chart is produced by the Oceanographic Institute of the Ecuadorian Navy (INOCAR).

OBSERVATION OF A BLUE WHALE FEEDING IN COASTAL WATERS OF ECUADOR 195

LAJAM 6(2): 193-197, Dcember 2007

the dorsal fin, which was low and falcate, located wellbehind in the lower back (Figure 2). At one point, theanimal made sudden fast movements at the surfaceand rolled over its right side with its mouth open,partially exposing the ventral groves and part of the leftrow of black-colored baleen plates (Figure 3). The leftflipper and part of the flukes were also visible abovethe surface at this time.

Discussion

Despite the intense whale research effort in coastalwaters of Ecuador during the past 15 years, with threeresearch teams studying humpback whales in severalsites of the central and northern coast during the australwinter (June-September) (see Félix and Haase, 2001,2005; Castro and González, 2002; Félix et al., in press),no blue whales have been reported previously in thisarea. Therefore, while our report could be consideredextraordinary, blue whales are known to occur alongshelf margins, so it is not ruled out that they may bemore abundant offshore. Unfortunately, it is not possible

to say much about their offshore occurrence because, inaddition to the marine mammal surveys by NOAA inthe eastern tropical Pacific, only a few expeditions tostudy whales have been conducted in offshore waters(e.g. Clarke, 1962; Loech, 1966; Chiriboga, 1972; Clarkeet al., 2002), all of which have failed to find blue whales.

The whale’s behavior of rolling at the surface with itsmouth open is similar to that described previouslyelsewhere and referred to as a form of surface feedingon euphausiid swarms (e.g. Fiedler et al., 1998; Palacios,1999), but such swarms were not evident during thesighting period nor have they been reported in coastalwaters of Ecuador. The largest volumes of both micro-and macro-zooplankton off mainland Ecuador havebeen associated with the Equatorial Front (2-3ºS),where cold northbound waters from the HumboldtCurrent meet the warm southbound waters of thePanama Current, and where primary productivity canbe as high as 760mgC/m3/d (Jiménez and Pesantes,1978; Jiménez, 1996). At the regional level, however,the productivity along the coast of Ecuador is notcomparable to the levels found in the upwelling zones

Figure 3. Behavior shown by the whale at the surface in waters off Santa Elena Peninsula, Ecuador. Note the open mouth and the leftrow of baleen plates (arrow) to the left of the pectoral fin.

Figure 2. Rear upper dorsum and dorsal fin of the whale sighted off Santa Elena Peninsula, Ecuador.

196 F.FÉLIX, N.BOTERO AND J.FALCONI

LAJAM 6(2): 193-197, December 2007

along the coasts of Peru and Chile (see Brown et al.,2005), sites that traditionally are known for thepresence of blue whales in the Southeast Pacific(Aguayo, 1974; Clarke, 1980; Ramírez, 1983).

Since our record was made during the austral winter, itcould be inferred that this individual belonged to aSouthern Hemisphere population, likely to the samepopulation found in Peruvian waters. However, fromthe data of blue whale abundance off Peru provided byRamírez (1983), it is noticed that the whales peaked inaustral summer (between January and February), witha minimum during the winter months; that is, the timewhen we recorded the whale in Ecuador. Recently,Branch et al. (2007) have provided new evidence tosupport the hypothesis of a discrete subpopulationcarrying out seasonal migrations within the SoutheastPacific, with animals moving from the south of Chile tothe coast of Peru, Ecuador and the Galápagos Islandsduring the summer, although with some whalesremaining in both zones during the entire year. Thecurrent state of knowledge indicates that blue whalesfrom the Southeast Pacific would be a differentsubpopulation from both pygmy and Antarctic bluewhales, with their own genetic, acoustic andmorphologic characteristics (Branch et al., 2007).

Genetic studies and the use of photo-identificationwould help to establish the identity of blue whalesinhabiting Ecuadorian waters, their relationship to bluewhales recorded in other areas of the Southeast Pacificsuch as Galápagos (Palacios, 1999), Chile (e.g. Hucke-Gaete et al., 2004; Galletti et al., 2007), and Peru (Ramírez,1983), thus improving our knowledge of the dynamicsand structure of the stock.

Acknowledgements

The authors thank the tourism agency Pesca Tour,owners of the yacht “China Linda”, aboard of which wemade the sighting. A special thanks to the yacht’s crewfor their patience and for taking us aboard during thetime we have been working in Salinas. Daniel Palacios,Diane Gendron and an anonymous reviewer madevaluable comments to improve the manuscript.

References

AGUAYO, A. (1974) Baleen whales off continental Chile. Pages209-217 in SCHEVILL, W.E. (Ed.) The Whale Problem. HarvardUniversity Press, Cambridge, MA, USA. 419pp.

BALLANCE, L.T., P ITMAN , R.L. AND F IEDLER, P.C. (2006)Oceanographic influences on seabirds and cetaceans of theeastern tropical Pacific: a review. Progress in Oceanography69: 360-390.

BRANCH, T.A., STAFFORD, K.M., PALACIOS, D.M., ALLISON, C.,BANNISTER, J.L., BURTON, C.L.K., CABRERA, E., CARLSON, C.A.,GALLETTI VERNAZZANI, B., GILL, P.C., HUCKE-GAETE, R., JENNER,K.C.S., JENNER, M.-N.M., MATSUKA, K., MIKHALEV, Y.A.,

MIYASHITA, T., MORRICE, M.G., NISHIWAKI, S., STURROCK, V.J.,TORMOSOV, D., ANDERSON, R.C., BAKER, A.N., BEST, P.B., BORSA,P., BROWNELL JR, R.L., CHILDERHOUSE, S., FINDLAY, K.P.,GERRODETTE, T., ILANGKOON, A.D., JOERGENSEN, M., KAHN, B.,LJUNGBLAD, D.K., MAUGHAN, B., MCCAULEY, R.D., MCKAY, S.,NORRIS, T.F., OMAN WHALE AND DOLPHIN RESEARCH GROUP,RANKIN, S., SAMARAN, F., THIELE, D., VAN WAEREBEEK, K. ANDWARNEKE, R.M. (2007) Past and present distribution, densitiesand movements of blue whales Balaenoptera musculus in theSouthern Hemisphere and northern Indian Ocean. MammalReview 37(2): 116-175.

BROWN, M., ORTIZ, J., PINTO, E., DE LA CUADRA, T., ZAMBRANO, E.,FLORES, R., GRADOS, C., PIZARRO, L. AND MUNAYLLA, U. (2005)Séptimo crucero regional conjunto de investigaciónoceanográfica en el Pacífico Sudeste, realizado en septiembre-octubre de 2004. Comisión Permanente del Pacífico Sur.Guayaquil, Ecuador. 48 pp.

CASTRO C. AND GONZÁLEZ, J. (2002) Población de la BallenaJorobada Megaptera novaeangliae en el Parque NacionalMachalilla, Ecuador. Ph.D. Thesis. Universidad Central delEcuador. Quito, Ecuador. 130 pp.

CHIRIBOGA, H.A. (1972) Las Ballenas en el Pacífico Sur Oriental.Instituto Oceanográfico de la Armada del Ecuador, Salinas,Ecuador. 54 pp.

CLARKE, R. (1962) Whale observation and whale marking offthe coast of Chile in 1958 and from Ecuador and beyond theGalapagos Islands in 1959. Hvalfangst Tidente 7: 265-287.

CLARKE, R. (1980) Catches of sperm whales and whalebonewhales in the southeast Pacific between 1908 and 1975. Reportof the International Whaling Commission 30: 285-288.

CLARKE, R, FÉLIX, F., PALIZA, O. AND BRTNIK P. (2002) Ballenas ydelfines observados por la expedición Ballenas Libres duranteel crucero oceanográfico CO-II-01 entre Guayaquil y las IslasGalápagos del 17 de septiembre al 9 de octubre de 2001. ActaOceanográfica del Pacífico, Instituto Oceanográfico de la Armadadel Ecuador (INOCAR), Ecuador 11(1): 173-180.

DE MIRO, M., AYÓN, H. AND BENITES, S. (1976) Morfología yestructura del margen continental del Ecuador. InstitutoOceanográfico de la Armada del Ecuador (INOCAR).Guayaquil, Ecuador. 22 pp.

DONOVAN, G.P. (1984) Blue whales off Peru, December 1982,with special reference to pygmy blue whales. Report of theInternational Whaling Commission 34: 473-476.

FÉLIX, F. AND HAASE, B. (2001) The humpback whale off the coastof Ecuador, population parameters and behavior. Revista deBiología Marina y Oceanografía 36(1): 61-74.

FÉLIX, F. AND HAASE, B. (2005) Distribution of humpback whalesalong the coast of Ecuador and management implications.Journal of Cetacean Research and Management 7(1): 21-31.

FÉLIX, F., CASTRO, C., LAAKE, J., HAASE B. AND SCHEIDAT, M. (Inpress) Abundance and survival estimates of the SoutheasternPacific humpback whale stock from 1991-2006 photo-identification surveys in Ecuador. Journal of Cetacean Researchand Management (special issue).

FIEDLER, P.C., REILLY, S.B., HEWITT, R.P. DEMER, D., PHILBRICK,A., SMITH, S., ARMSTRONG, W., CROLL, D.A., TERSHY, B.R. ANDMATE, B.R. (1998) Blue whale habitat and prey in the CaliforniaChannel Islands. Deep-Sea Research II 45: 1781-1801.

OBSERVATION OF A BLUE WHALE FEEDING IN COASTAL WATERS OF ECUADOR 197

LAJAM 6(2): 193-197, Dcember 2007

GALLETTI, B., CARLSON, C.A., CABRERA, E. AND BROWNELL JR. R.L.(2007) Status of blue whales off isla de Chiloe, Chile, during2007 field season. Document SC/59/SH1. Presented to the 59th

Scientific Committee of the International WhalingCommission, Anchorage, USA, 7-18 May 2007.

HUCKE-GAETE, R., OSMAN L.P., MORENO, C.A., FINDLAY, K.P. ANDLJUNGBLAD, D.K. (2003) Discovery of a blue whale feeding andnursing ground in southern Chile. Proceedings of the RoyalSociety of London B (Supplement) 271: 170-173.

JIMÉNEZ, R. (1996) Segunda Parte: biología, ecología yacuacultura. Pages 117-223 in Comisión Asesora Ambientalde la Presidencia de la República (CAAM). Sistemas Biofísicosen el Golfo de Guayaquil. Guayaquil, Ecuador. 223 pp.

JIMÉNEZ, R. AND PESANTES, F. (1978) Fitoplancton, producciónprimaria y pigmentos en aguas costeras ecuatorianas.Publicación Instituto Oceanográfico de la Armada del Ecuador(INOCAR) 2(1): 1-30.

KINZEY, D., GERRODETTE, T., BARLOW, J., DIZON, A., PERRYMAN, W.AND OLSON, P. (2000) Marine mammal data collected during asurvey in the eastern tropical Pacific Ocean aboard the NOAAships “McArthur” and “David Starr Jordan”, July 28-December9, 1999. NOAA Technical Memorandum NOAA-TM-NMFS-SWFC 293: 1-89.

LEATHERWOOD, S. AND REEVES, R.R. (1983) The Sierra ClubHandbook of Whales and Dolphins. Sierra Club Books. San

Francisco, CA, USA. 302 pp.

LOESCH, H. (1966) Observación de ballenas en aguasecuatorianas. Informe de datos, mayo de 1963 y enero-febrerode 1964. Boletín Científico y Técnico 1: 1-18.

MERLEN, G. (1995) A Field Guide to the Marine Mammals ofGalapagos. Instituto Nacional de Pesca, Guayaquil, Ecuador.130 pp.

PALACIOS, D.M. (1999) Blue whale (Balaenoptera musculus)occurrence off the Galápagos Islands, 1978-1995. Journal ofCetacean Research and Management 1(1): 41-51.

PERRY, S.C., DE MASTER, D.P. AND SILBER, G.K. (1999) The greatwhales history and status of six species listed as endangeredunder the US Endangered Species Act of 1972. Marine FisheriesReview (special issue) 61(1): 1-74.

RAMÍREZ P. (1983) Capturas y observaciones de la ballena azulBalaenoptera musculus, L, en Paita-Perú 1961-1966 y 1975-1982IMARPE. Revista de la Comisión Permanente del. Pacífico Sur13: 97-102.

REILLY, S.B. AND THAYER, V.C. (1990) Blue whale (Balaenopteramusculus) distribution in the Eastern Tropical Pacific. MarineMammal Science 6(4): 265-277.

WADE P.R., AND GERRODETTE, T. (1993) Estimates of cetaceanabundance and distribution in the eastern tropical Pacific.Report of the International Whaling Commission 43: 477-493.



1 Eutropia. Centro de Investigación de Aves y Mamíferos Marinos de Chile. 1 Poniente 960, Depto. 1102, Viña del Mar, Chile.2 Centro de Investigación y Gestión en Recursos Naturales (CIGREN), Facultad de Ciencias, Universidad de Valparaíso. Gran Bretaña

1111, Playa Ancha, Valparaíso, Chile.* Corresponding author. Tel.: +56322508346; fax: +56322508072. E-mail address: [email protected].

PRESENCE AND RE-SIGHTING OF SOUTHERN ELEPHANT SEAL, MIROUNGA LEONINA (L. 1758),ON THE NORTH-CENTRAL COAST OF CHILE

MARITZA SEPÚLVEDA1,2,*, MARÍA JOSÉ PÉREZ-ALVAREZ1,2, PAULA LÓPEZ1 & RODRIGO MORAGA

1,2

KEYWORDS: Mirounga leonina, southern elephant seal, phocids, Chile, re-sightings, molt

The southern elephant seal (Mirounga leonina) is a largepredator in the higher levels of trophic webs, and oneof the principal consumers of squid and fish in thesouthern marine ecosystem (Bradshaw et al., 2003;Hindell et al., 2003). The annual cycle of this species ischaracterized by two terrestrial phases: one for breeding(September to November) and one for molting(December to March); and two pelagic foraging phases:post-breeding (for about 2-3 months), and post-molt(lasting 7 months) (Campagna et al., 1993; 2000).

This species has a circumpolar distribution throughoutthe Southern Ocean with a total world populationestimated of 664000 individuals (Laws, 1994), and majorbreeding areas close to the Antartic Polar Front (Laws,1994; Lewis et al., 1998). The world population is dividedinto four distinct groups, namely the Kerguélen stock inthe South Indian Ocean, the South Georgia stock in the

South Atlantic Ocean, the Macquarie stock in the southernPacific Ocean, and Península Valdés stock in Argentina(Lewis et al., 1998; 2006; McMahon et al., 2003; Bester andHofmeyr, 2005). Although there are no records ofbreeding colonies along the Chilean coast, opportunisticsightings of the species have been described for the north-central coast of Chile, Isla Diego Ramírez, MagellanicRegion and Isla de Pascua (Sielfeld, 1978; Aguayo et al.,1995; Torres et al., 2000; Lewis et al., 2006). Additionally,historical information indicates the presence of M. leoninaon Isla Juan Fernandez (Sielfeld, 1983). Nevertheless, sitefidelity has been not mentioned in these studies. This notereports the presence and re-sigthing of southern elephantseals within the Reserva Nacional Pingüino de Humboldt(RNPH), in central Chile.

Monthly boat-surveys have been performed sinceFebruary 2003 as part of the research project ‘Photo-

identification of bottlenosedolphin Tursiops truncatusaround the RNPH. The studyarea comprises three islandsthat belong to the MarineProtected Areas ‘ReservaMarina Isla Chañaral’ (29°02’S,71°36’W) and ‘Reserva MarinaIslas Choros-Damas’ (29°14’S,71°32’W) north central Chile(Figure 1). During some of thesurveys, the presence of M.leonina was recorded based ondiagnostic characteristicsobserved by 8 x 42 binoculars.Once the species was identified,its geographic position andphotographs were taken.Categorization of eachindividual was done followingLaws (1953).

During the summer monthsfrom 2004 to 2007, foursightings of southern elephantseals were recorded. The firsttwo sightings (28 December2004 and 27 November 2005)were recorded in Isla Chañaral.

Figure 1. Study area, Marine Protected Areas ‘Reserva Marina Isla Chañaral’ and ‘ReservaMarina Islas Choros-Damas’, on the north-central coast of Chile.

200 M.SEPÚLVEDA, M.J.PÉREZ-ALVAREZ, P.LÓPEZ AND R.MORAGA

LAJAM 6(2): 199-202, December 2007

These referred to the same individual, which wasclassified as an immature male. The identification wasbased on a notorious scar on its back (Figure 2). In 2005,the seal was observed larger and darker than the previousyear, and presented clear evidence of molting.Additionally, the scar was less visible than the previousrecord. The other two sightings (30 January 2006 and 30January 2007) were registered in Isla Choros. Bothindividuals were classified as immature males, but theyrepresented different individuals to the male found inIsla Chañaral.

Though Chile does not represent a regular breeding areafor southern elephant seals, their presence in this areais not an anomalous record. Recent foraging studiesdemonstrate that elephant seals show some of thegreatest horizontal movements of any mammal,traveling over 5000km from their breeding areas

(Hindell and McMahon, 2000; Hindell et al., 2003;Campagna et al., 2007). Similarly, a site preference andlong-term fidelity to breeding and molting regions havebeen demonstrated both in juvenile and adult elephantseals (Hindell and Burton, 1988; McMahon et al., 1999;Lewis et al., 2006). The re-sighted individual for twoconsecutive years corroborates the hypothesis thatelephant seals are able to select sites early in their life(Bradshaw et al., 2004).

However, why do elephant seals select the RNPHduring summer months? At least two explanations canbe hypothesized. First, the area is an isolated and calmsite that allows a seal to rest and molt, as was observedin the re-sighted individual in 2005. Second, the presenceof seals in the study area could be associated with anabundant food resource as characterized by upwellingevents during spring and summer (Marín et al., 2003).

Figure 2. Mirounga leonina re-sighted individual in the Reserva Marina Isla Chañaral; (a) December 2004, and (b) November 2005.

PRESENCE AND RE-SIGHTING OF SOUTHERN ELEPHANT SEAL, MIROUNGA LEONINA (L. 1758) ON THE NORTH-CENTRAL COAST OF CHILE 201

LAJAM 6(2): 199-202, December 2007

It is generally believed that top predators such asmarine mammals and birds use regions of higherproductivity to supply sufficient food for survival andreproductive output (Bradshaw et al., 2002). Theupwelling off Coquimbo, Chile (30°S) in the HumboldtCurrent ecosystem represents a highly dynamic coastalenvironment that supports one of the most productiveglobal fisheries (Montecino et al., 1996; Montecino andQuiroz, 2000), and it serves as nutritional sources fora great diversity of marine animals, including marinebirds such as Humboldt’s penguins (Spheniscushumboldtii), Peruvian diving petrels (Pelecanoidesgarnotti), marine otters (Lontra felina), South Americansea lions (Otaria flavescens), and cetaceans such asbottlenose dolphins (Tursiops truncatus), humpbackwhales (Megaptera novaeangliae) and fin whales(Balaenoptera physalus) (Capella et al., 1999; Pérez et al.,2006). Additionally, shallow depths located around thestudy area could be an advantage for seals, which couldreduce the energy expenditure while foraging(Campagna et al., 2007).

The presence and residence of elephant seals withinthe RNPH contributes to the marine ecosystembiodiversity and supports the importance of anintegrated conservation of the area. A marine reservehas been recently created around the area in order toconserve and protect the ecologically representativemarine environment, ensuring the sustainable use ofmarine resources (Subsecretaría de Pesca, Decrees no.150 and 151, 2005). However, an effective managementplan is urgently needed to minimize anthropogenicimpacts and threats on marine mammals and to protectunique habitats and resident marine communities,which are the ultimate goals of Marine Protected Areas(Boersma and Parrish, 1999). The occurrence and sitefidelity of M. leonina within this area allowed for theimplementation of systematic scientific researchfocused on the migratory patterns of the species, aswell as the development of a sustainable base for eco-tourism.

Acknowledgments

We thank Patricio Ortiz and Aurelio Aguirre for theirexperience and support on fieldwork. We also thankDoris Oliva who provided helpful comments on earlyversions of the manuscript, and to Mirtha Lewis and ananonymous reviewer for their insightful suggestions.

References

AGUAYO, A., IBAÑEZ, P., RAUCH, M. AND VALLEJOS, V. (1995)Primer registro del elefante marino del sur, Mirounga leonina,en la Isla de Pascua, Chile. Serie Científica Instituto AntárticoChileno (INACH) 45: 123-129.

BESTER, M.N. AND HOFMEYR, G.J.G. (2005) Numbers of elephantseals at Prince Edward Island, Southern Ocean. South AfricanJournal of Wildlife Research 35(1): 85-88.

BOERSMA, P. AND PARRISH, J. (1999) Limit abuse: marine protectedarea, a limited solution. Ecological Economics 31: 287-304.

BRADSHAW, C.J.A., HINDELL, M.A., MICHAEL, K.J. AND SUMNER, M.D.(2002) The optimal spatial scale for the analysis of elephant sealforaging as determined by geo-location in relation to sea surfacetemperatures. ICES Journal of Marine Science 59: 770-781.

BRADSHAW, C.J.A., HINDELL, M.A., BEST, N.J., PHILLIPS, K.L., WILSON,G. AND NICHOLS, P.D. (2003) You are what you eat: describingthe foraging ecology of southern elephant seals (Miroungaleonina) using blubber fatty acids. Proceedings of the Royal Societyof London Series B, Biological Sciences 270: 1283-1292.

BRADSHAW, C.J.A., HINDELL, M.A., SUMNER, M.D. AND MICHAEL,K.J. (2004) Loyalty pays: potential life history consequencesof fidelity to marine foraging regions by southern elephantseals. Animal Behaviour 68: 1349-1360.

CAMPAGNA, C., LEWIS, M. AND BALDI, R. (1993) Breeding biologyof southern elephant seals in Patagonia. Marine Mammal Science9: 34-47.

CAMPAGNA, C., RIVAS, A.L. AND MARIN, M.R. (2000) Temperatureand depth profiles recorded during dives of elephant sealsreflect distinct ocean environments. Journal of Marine Systems24: 299-312.

CAMPAGNA, C., P IOLA, A.R., MARIN, M.R., LEWIS, M.,ZAJACZKOVSKI, U. AND FERNÁNDEZ, T. (2007) Deep divers inshallow seas: Southern elephant seals on the Patagonian shelf.Deep Sea Research Part I: Oceanographic Research Papers 54(10):1792-1814.

CAPELLA, J., VILINA, Y. AND GIBBONS, J. (1999) Observación decetáceos en isla Chañaral y nuevos registros para el área de laReserva Nacional Pingüino de Humboldt, norte de Chile.Estudios Oceanológicos 18: 57-64.

HINDELL, M.A. AND BURTON, H.R. (1988) Seasonal haul-outpatterns of the southern elephant seal (Mirounga leonina. L.) atMacquarie Island. Journal of Mammalogy 69: 81-88.

HINDELL, M.A. AND MCMAHON, C.R. (2000) Long distancemovement of a southern elephant seal (Mirounga leonina)from Macquarie Island to Peter 1 Øy. Marine Mammal Science16: 504-507.

HINDELL, M.A., BRADSHAW, C.J.A., SUMNER, M.D., MICHAEL, K.J.AND BURTON, H.R. (2003) Dispersal of female southern elephantseals and their prey consumption during the austral summer:relevance to management and oceanographic zones. Journalof Applied Ecology 40: 703–715.

LAWS, R.M. (1953) The elephant seal (Mirounga leonina Linn.). I.Growth and age. Falkland Islands Dependencies Survey.Scientific Report No. 8, London. 66 pp.

LAWS, R.M. (1994) History and present status of southernelephant seal populations. Pages 49-65 in LE BOEUF, B.J. AND LAWS,R.M. (Eds) Elephant Seals: Population Ecology, Behavior andPhysiology. University of California Press, Berkeley, CA, USA.

LEWIS, M., CAMPAGNA, C., QUINTANA, F. AND FALABELLA, V. (1998)Estado actual y distribución de la población del elefantemarino del sur en la Península de Valdés, Argentina.Mastozoología Neotropical 5(1): 29-40.

LEWIS, M., CAMPAGNA, C., MARIN, M.R. AND FERNÁNDEZ, T. (2006)Southern elephant seals north of the Antarctic Polar Front.Antarctic Science 18(2): 213–221.

202 M.SEPÚLVEDA, M.J.PÉREZ-ALVAREZ, P.LÓPEZ AND R.MORAGA

LAJAM 6(2): 199-202, December 2007

MARÍN, V.H., DELGADO, L. AND LUNA-JORQUERA, G. (2003) S-chlorophyll squirts at 30° S off the Chilean coast (eastern SouthPacific): Feature-tracking analysis. Journal of GeophysicalResearch 108(12): 1-6.

MCMAHON, C.R., BURTON, H.R. AND BESTER, M.N. (1999) First-year survival of southern elephant seals, Mirounga leonina, atsub-Antarctic Macquarie Island. Polar Biology 21: 279-284.

MCMAHON, C.R., BURTON, H.R. AND BESTER, M.N. (2003) Ademographic comparison of two southern elephant sealpopulations. Journal of Animal Ecology 72: 61–74.

MONTECINO, V. AND QUIROZ, D. (2000) Specific primaryproduction and phytoplankton cell size structure in anupwelling area off the coast of Chile (30°S). Aquatic Science62: 364-380.

MONTECINO, V., PIZARRO, C. AND QUIROZ, D. (1996) Dinámica

fitoplanctónica en el sistema de surgencia frente a Coquimbo(30° S) a través de la relación funcional entre fotosíntesis eirradianza (P-I). Gayana Oceanologia 4(2): 139-151.

PÉREZ, M.J., THOMAS, F., URIBE, F., SEPÚLVEDA, M., FLORES, M. ANDMORAGA, R. (2006) Fin whale (Balaenoptera physalus) feedingon Euphausia mucronata in nearshore waters off North-CentralChile. Aquatic Mammals 32(1): 109-113.

SIELFELD, W. (1978) Algunas consideraciones sobre fócidos(Pinnipedia) asociados a las costas de Chile. Anales del Institutode la Patagonia 9: 153-156.

SIELFELD, W. (1983) Mamíferos Marinos de Chile. Ediciones de laUniversidad de Chile, Santiago, Chile. 199 pp.

TORRES, D., AGUAYO-LOBO, A. AND ACEVEDO, J. (2000) MamíferosMarinos de Chile. II. Carnivora. Serie Científica INACH50: 25-103.

Received 11 August 2007. Accepted 30 November 2007.


1 Columbia University Department of Ecology, Evolution and Environmental Biology, New York, NY, USA.2 Sackler Institute for Comparative Genomics at the American Museum of Natural History (AMNH).

Ocean Giants Program at Wildlife Conservation Society.Fundación Aquamarina, CECIM, Argentina.

+ Both authors contributed equally to this publication.* Corresponding author, e-mails: [email protected], [email protected]. Department of Environmental Ecology and

Evolutionary Biology, Columbia University, 1200 Amsterdam Avenue MC5557, New York, NY 10027 USA. Phone: (212) 854 - 9987;fax: (212) 854 - 8188; mobile: (917) 331 - 2408.

MARINE PROTECTED AREAS IN SOUTH AMERICA:

SPATIAL ASSESSMENT OF CETACEAN DISTRIBUTION COVERAGE

ANDRÉS GÓMEZ1,+,* AND MARTÍN MENDEZ

1, 2,+

KEYWORDS: Marine protected areas, cetaceans, South America.

Recent attention to the great biological diversity of theworld’s oceans and the serious threats it currently faces hasgarnered support for the establishment of marine protectedareas (MPAs) (Lovejoy, 2006), defined by the WorldConservation Union (IUCN) as “any area of intertidal orsubtidal terrain, together with its overlying water andassociated flora, fauna, historical and cultural features, whichhas been reserved by law or other effective means to protectpart or all of the enclosed environment” (Hoyt, 2005). Recentevidence suggests that MPAs can effectively contribute tothe conservation of biological resources and the economicactivities that depend on them (Behrens and Lafferty, 2004;Floeter et al., 2006; Guidetti, 2007). Consequently, althoughthe number of MPAs has increased dramatically in recentyears, the creation of new ones is still considered a priority(Mora et al., 2006; Remington et al., 2007).

In the context of the expansion of national protected areanetworks, spatially explicit analyses of current coverage helpidentify major gaps and therefore to guide the establishment,design and management of new reserves. However, to date,most such analyses have been done for the terrestrial realm(Rodrigues and Gaston, 2001; Scott et al., 2001; Sanderson etal., 2002; Rodrigues et al., 2004). Although MPAs worldwidehave largely proven successful in protecting marine taxaand habitats (Guenette et al., 1998; Halpern, 2003), theappropriateness of existing MPAs to adequately protectcetaceans may be limited (Reeves, 2000).

Typical MPAs are too small to offer adequate coveragefor cetaceans, as these are species characterized by highdispersal capabilities (Hoelzel, 1994). As a consequenceof their migratory behavior and complex habitatrequirements, cetaceans have been proposed as ‘umbrellaspecies’ that could be used to strategically create MPAscapable of offering coverage to both these marinemammals and a variety of other marine species with lessextensive dispersal requirements (Hooker and Gerber,2004). South America (SA) holds a significant fraction ofthe world’s marine biological diversity, which includesat least 48 cetacean species (Table 1). Protected areasystems in SA are extensive, but the degree to which theyrepresent species and major terrestrial ecological units isvaried and critical gaps still exist (Esty et al., 2006; Soutullo

and Gudynas, 2006). Here, we analyze the degree towhich MPAs in SA cover the ranges of cetacean species.

Since conservation policy is normally planned andexecuted at the national level, and because legislation andenforcement are problematic in international waters, welimited our analysis to the exclusive economic zones (EEZ;200 nautical miles from the shore, as defined by the UnitedNations Law of the Sea Convention) of all coastal countriesin SA, namely: Argentina, Brazil, Chile, Colombia,Ecuador, French Guiana, Guyana, Peru, Suriname,Uruguay and Venezuela. We collected distributioninformation for the 48 cetacean species present within thesenational waters. To minimize species distributioninaccuracies from particular sources, we integrated datafrom the Marine Mammals of the World section of theWorld Biodiversity Database (http://nlbif.eti.uva.nl/bis/index.php) and from three widely used marine mammalfield guides (Carwardine, 1999; Reeves et al., 2002; Reeveset al., 2003). When a species’ range differed among thedifferent sources, we considered the broadest distributionlimits as a conservative estimate. A potential caveat is thatspecies occurrence data recorded in these sources may beincomplete and therefore fine-scale observations must alsobe considered when using analyses such as this one todelineate conservation strategies.

We compiled a list of MPAs in SA using the MPAGlobal database (http://www.mpaglobal.org,accessed 15 March 2007) and included in this analysisall MPAs present in its database regardless of theirIUCN category and the completeness of the associatedinformation, except when spatial coordinates or totalarea information were unavailable. Our initial databasecontained 166 MPAs. We then collated this list withthe 2006 World Database on Protected Areas (UNEP-WCMC, 2006) and obtained boundary polygons whenavailable. For those areas in which only point data wereavailable, we drew a circular polygon on theappropriate area around the central coordinates. Wecalculated the area of each MPA situated over the water(i.e. beyond the continent coastline, including estuariesand deltas) and used this fraction to estimate the coverageprovided to each species (percent coverage, Table 1).

204 A.GÓMEZ AND M.MENDEZ

LAJAM 6(2): 203-207, December 2007

Table 1. Percent coverage provided to cetacean species in South America by the current marine protected area network. Fields markedby an asterisk (*) reflect pooled information for more than one species, subspecies or form, since exact distribution data are lacking.Minke whale’s data reflect coverage for both subspecies (B. bonaerensis and B. acutorostrata). Common dolphin’s coverage is pooled forboth long-beaked common dolphin (D. capensis) and short-beaked common dolphin (D. delphis) data. Both the tucuxi and Guianadolphin are pooled under Sotalia spp.

SCIENTIFIC NAME COMMON NAME CONSERVATION STATUSA % COVERAGE

Phocoena dioptrica Spectacled porpoise Data defficient 0.14

Balaenoptera bonaerensis (*) Minke whale Lower risk (LC) 1.93

Balaenoptera borealis Sei whale Endangered 1.93

Balaenoptera edeni Bryde's whale Data defficient 1.93

Balaenoptera musculus Blue whale Endangered 1.93

Balaenoptera physalus Fin whale Endangered 1.93

Berardius arnuxii Arnoux's beaked whale Lower risk (CD) 0.09

Caperea marginata Pygmy right whale Lower risk (LC) 0.09

Cephalorhynchus commersonii Commerson's dolphin Data defficient 0.10

Cephalorhynchus eutropia Chilean dolphin Data defficient 0.06

Delphinus spp. (*) Common dolphin Lower risk (LC) 1.93

Eubalaena australis Southern right whale Lower risk (CD) 0.25

Feresa attenuata Pygmy killer whale Data defficient 2.61

Globicephala macrorhynchus Short-finned pilot whale Lower risk (CD) 2.68

Globicephala melas Long-finned pilot whale Lower risk (LC) 0.09

Grampus griseus Risso's dolphin Data defficient 1.93

Hyperoodon planifrons Southern bottlenose whale Lower risk (CD) 0.08

Kogia breviceps Pygmy sperm whale Lower risk (LC) 2.48

Kogia sima Dwarf sperm whale Lower risk (LC) 3.05

Lagenodelphis hosei Fraser's dolphin Data defficient 3.79

Lagenorhynchus australis Peale's dolphin Data defficient 0.14

Lagenorhynchus cruciger Hourglass dolphin Lower risk (LC) 0.09

Lagenorhynchus obscurus Dusky dolphin Data defficient 0.11

Lissodelphis peronii Southern right whale dolphin Data defficient 0.10

Megaptera novaeangliae Humpback whale Vulnerable 1.93

Mesoplodon densirostris Blainville's beaked whale Data defficient 2.23

Mesoplodon europaeus Gervais' beaked whale Data defficient 0.98

Mesoplodon ginkgodens Ginkgo-toothed beaked whale Data defficient 9.85

Mesoplodon grayi Gray's beaked whale Data defficient 0.22

Mesoplodon hectori Hector's beaked whale Data defficient 0.15

Mesoplodon layardii Strap-toothed whale Data defficient 0.08

Mesoplodon peruvianus Lesser beaked whale Data defficient 3.73

Orcinus orca Killer whale Lower risk (CD) 1.93

Peponocephala electra Melon-headed whale Lower risk (LC) 3.89

Phocoena spinipinnis Burmeister’s porpoise Data defficient 0.16

Physeter macrocephalus Sperm whale Vulnerable 1.93

Pontoporia blainvillei Franciscana dolphin Data defficient 0.53

Pseudorca crassidens False killer whale Lower risk (LC) 2.45

Sotalia spp. (*) Tucuxi/Guiana dolphin Data defficient 1.73

Stenella attenuata Pantropical spotted dolphin Lower risk (CD) 2.96

Stenella clymene Clymene dolphin Data defficient 1.23

Stenella coeruleoalba Striped dolphin Lower risk (CD) 2.89

Stenella frontalis Atlantic spotted dolphin Data defficient 1.29

Stenella longirostris Spinner dolphin Lower risk (CD) 3.71

Steno bredanensis Rough-toothed dolphin Data defficient 3.10

Tasmacetus shepherdi Shepherd's beaked whale Data defficient 0.14

Tursiops truncatus Common bottlenose dolphin Data defficient 3.23

Ziphius cavirostris Cuvier's beaked whale Data defficient 1.93

a Data from www.redlist.org, accessed March 15 2007. LC: Least concern, CD: Conservation dependent.

MARINE PROTECTED AREAS IN SOUTH AMERICA 205

LAJAM 6(2): 203-207, December 2007

Our final database contained littoral and sublittoralcomponents of 143 MPAs. To reduce the magnitude ofspatial errors that might lead to overestimation, weremoved all resulting polygons of less than 1km2 (thesepolygons belonged to 24 MPAs or 16.7% of the MPAsin our final database). We then estimated the percentageof the range of each species that is included in aprotected area.

We found that a significant fraction of the areas listedin the MPA database we consulted had no jurisdictionbeyond the intertidal zone. MPAs in our databasegenerally included small areas that in total covered lessthan 3.5% of the EEZs in SA. Only three MPAs includedocean areas larger than 10000km2 whereas 40% hadareas of less than 10km2. Finally, although managementand enforcement in the open ocean are essential giventhe high connectivity in marine systems (Cawardine,2002; Hoyt, 2005; Norse, 2005), in this case exemplifiedby inshore and offshore cetacean stocks or populations(Palumbi, 2003; Norse, 2005), there were currently noestablished high-seas MPAs in the region (i.e. protectedareas that do not share a border with a terrestrialcomponent, whether continental or insular).

Not surprisingly, cetacean distribution ranges wereminimally covered by MPAs in SA. Across all species,the average percentage of the cetacean range includedin a MPA was 1.7% (range 0.06-9.8%). A total of 19species had less than 1% of their range covered in thecurrent MPA system, including nine species whoseranges have less than 0.1% coverage (Table 1). Further,we found that the average range coverage for endemicspecies (0.45%) was lower than the average for all speciesand was independent of conservation status (Table 1).It is important to note that the overall inclusion levels(e.g. the total percentage of the range that is included ina MPA) reported here do not explicitly account for thenumber of individual polygons that contribute to thetotal area under protection. Given the small size of mostoceanic polygons in MPAs in SA (as above, the protectedfractions that extend beyond the shore), the percentageof inclusion of a species’ range is overwhelminglyrepresented by the sum of several small areas. Thisfragmentation of protected areas can further limit theirconservation potential for cetaceans. Taken together,these results indicate that cetaceans are inadequatelyrepresented in MPA networks in SA. Those species thatare considered as endangered, vulnerable or datadeficient, as well as the endemic species (Table 1) couldserve as a starting point in identifying candidates forconservation priorities in the region.

Mapped boundaries were absent in a large fraction(48.5%) of the MPAs included in this analysis, as wasinformation about management, regulation and zoning.Zoning regimes delineate different conservation goalsand regulations within the boundaries of some protectedareas, resulting in different levels of protection affordedto cetacean species and their habitats within each of ourmapped polygons. Since we treated all polygons in this

analysis as a uniform conservation unit, strict protectionof cetacean ranges is overestimated in our results.Although we do not expect any significant effect on ourresults given the low coverage afforded to cetaceans,any bias introduced by such overestimation would besmall and would only reinforce our conclusions.However, species’ distributions are not uniformthroughout their ranges and MPAs in the region maycontain critical areas (e.g. feeding or mating grounds),which would increase their conservation value in spiteof a relatively small area protected. In the absence ofmore detailed spatially defined datasets, analyses suchas this one necessarily incorporate errors, both ofomission and commission; we hope that in the futurenational environmental authorities will refine andupdate their datasets, but suggest that qualitatively ourconclusions remain valid.

Given the multi-factorial nature of the current threatsfaced by cetaceans, MPAs represent only one approachto cetacean conservation. For instance, the most recentassessment of South American small cetacean species bythe International Whaling Commission (IWC) highlightedthe need for information on abundance, distribution,population structure, life history and habitat of these taxa(IWC, 2009). The theory underlying the design of MPAsis in its infancy and remains context dependent (Botsfordet al., 2003; Gerber et al., 2003; IWC, 2009); moreover, withfew exceptions, most MPAs are not typically designed toprotect cetaceans specifically (Hoyt, 2005). In any planto expand current levels of protection, it is necessary tocarefully balance the need for larger areas underprotection with actual capacity for enforcement, andconsideration to whether increasing the number of MPAsand the total area under protection provides addedbenefits to the protection granted by other means. At alocal scale, future MPAs aimed at conserving cetaceanswould benefit from cetacean habitat preferenceassessments and modeling efforts that identify potentialareas of higher occurrence and abundance (Reilly, 1990;Reilly and Fiedler, 1994; Baumgartner et al., 2001; Daviset al., 2002; Redfern et al., 2006). Important issues relatedto cetacean demography in the context of a complex anddynamic environment could be best approached byintegrating data across disciplines (Palumbi, 2003;Palumbi et al., 2003). For instance, in cetaceans, geneticapproaches offer high resolution to characterizepopulation structure, connectivity, and identifymanagement units (Hoelzel, 1998; DeSalle, 2004), whichcould be further enhanced by detailed oceanographicinformation to contextualize such assessments. Data onseafloor physiographic features, bathymetry, marineproductivity and sea surface temperature, among otheroceanographic features, have proven relevant to pinpointareas of potential population subdivision in cetaceans(Fullard et al., 2000; Wares et al., 2001; Elwen and Best,2004a, b; Norse, 2005; Rosa et al., 2005; Mendez et al., 2008).Although not yet legally established in the region, high-seas reserves may be particularly relevant, as these areas

206 A.GÓMEZ AND M.MENDEZ

LAJAM 6(2): 203-207, December 2007

play important roles in the origin and maintenance ofmarine biodiversity. Pelagic fisheries, migratory speciesand top predators currently impacted in the high seashave a profound impact on coastal ecosystems throughmassive species removal and trophic web alteration(Reeves, 2000; Dans et al., 2003; Amaral and Jablonski,2005; Fernandez and Castilla, 2005). Current efforts forhigh-seas conservation in the region include the Sea andSky project in the South Atlantic, which seeks to protectan outstandingly large area between the 30°S and 60°S,and extending from the east coast of South America to50°W (http://sea-sky.org). In addition, a recent proposalto the IWC by the Governments of Argentina, Brazil andSouth Africa seeks to establish a whale sanctuarydelimited by the Equator to the north, the coasts of SouthAmerica and Africa to the east and west, and a southernboundary varying between 40°S at its easternmost pointand 60°S at its western limit (Truda Palazzo et al., 2008).

Cetaceans in South America suffer from a variety ofthreats that seriously compromise their persistence,including intentional and incidental catch andentanglement, habitat alteration, prey removal, noise andchemical pollution, collisions with vessels and climatechange (Dans et al., 2003; Amaral and Jablonski, 2005;Fernandez and Castilla, 2005). Despite these conspicuousthreats, which vary in intensity and by species, there is alack of rigorous research and appropriate reporting ofthe status of a significant fraction of the species in theregion (Table 1) (IUCN, 2006). Due to its spatialdistribution and limited overall area, the current MPAnetwork in SA likely provides few real conservationbenefits to cetaceans in the region. To achieve fullrepresentation and adequate area coverage of cetaceanspecies, MPA site selection and design should respondto the conservation a series of hierarchical ecologicalprocesses in space, from demographic stability andconnectivity at the population level, to multispeciesinteractions, to oceanographic processes controllingspecies distribution and abundance in an appropriate eco-regional framework.

Acknowledgments

Both authors are supported by Columbia UniversityGraduate School of Arts and Sciences FacultyFellowships and the Whitley Fund for Nature. E. Nicholsimproved an earlier version of this manuscript. Ananonymous reviewer, Ms. Mônica Borobia and Mr.Daniel Palacios provided useful comments thatenhanced this article.

References

AMARAL, A.C.Z. AND JABLONSKI, S. (2005) Conservation of marine andcoastal biodiversity in Brazil. Conservation Biology 19(3): 625-631.

BAUMGARTNER, M.F., MULLIN, K.D., MAY, L.N. AND LEMING, T.D.(2001) Cetacean habitats in the northern Gulf of Mexico. FisheryBulletin 99(2): 219-239.

BEHRENS, M.D. AND LAFFERTY, K.D. (2004) Effects of marine reservesand urchin disease on southern Californian rocky reefcommunities. Marine Ecology Progress Series 279: 129-139.

BOTSFORD, L.W., MICHELI, F. AND HASTINGS, A. (2003) Principles forthe design of marine reserves. Ecological Applications 13(1): S25-S31.

CARWARDINE, M. (1999) Whales, dolphins, and porpoises. New York,NY, Checkmark Books.

CAWARDINE, M., (Ed). (2002) Whales, Dolphins, and Porpoises.Smithsonian Handbooks. New York, Dorling Kindersley Books.

DANS, S.L., ALONSO, M.K., PEDRAZA, S.N. AND CRESPO, E.A. (2003)Incidental catch of dolphins in trawling fisheries off Patagonia,Argentina: Can populations persist? Ecological Applications13(3): 754-762.

DAVIS, R.W., ORTEGA-ORTIZ, J.G., RIBIC, C.A., EVANS, W.E., BIGGS,D.C., RESSLER, P.H., CADY, R.B., LEBEN, R.R., MULLIN, K.D. ANDWURSIG, B. (2002) Cetacean habitat in the northern oceanic Gulf ofMexico. Deep-Sea Research 49(1): 121-142.

DESALLE, R. AND AMATO, G. (2004) The expansion of conservationgenetics. Nature Review Genetics 5: 702-713.

ELWEN, S.H. AND BEST, P.B. (2004a) Environmental factorsinfluencing the distribution of southern right whales (Eubalaenaaustralis) on the south coast of South Africa I: Broad scale patterns.Marine Mammal Science 20(3): 567-582.

ELWEN, S.H. AND BEST, P.B. (2004b) Environmental factorsinfluencing the distribution of southern right whales (Eubalaenaaustralis) on the south coast of South Africa II: Within baydistribution. Marine Mammal Science 20(3): 583-601.

ESTY, D.C., LEVY, M.A., SREBOTNJAK, T., SHERBININ, A. DE, KIM, C.H.AND ANDERSON, B. (2006) Pilot 2006 Environmental Performance Index.New Haven, CT, Yale Center for Environmental Law & Policy,New Haven, CT, USA.

FERNANDEZ, M. AND CASTILLA, J.C. (2005) Marine Conservation inChile: Historical Perspective, Lessons, and Challenges.Conservation Biology 19(6): 1752-1762.

FLOETER, S.R., HALPERN, B. S. AND FERREIRA, C.E.L. (2006) Effects offishing and protection on Brazilian reef fishes. BiologicalConservation 128(3): 391-402.

FULLARD, K., EARLY, G., HEIDE-JORGENSEN, M., BLOCH, D., ROSING-ASVID, A. AND AMOS, W. (2000) Population structure of long-finnedpilot whales in the North Atlantic: a correlation with sea surfacetemperature? Molecular Ecology 9(7): 949-958.

GERBER, L.R., BOTSFORD, L.W., HASTINGS, A., POSSINGHAM, H.P.,GAINES, S.D., PALUMBI, S.R. AND ANDELMAN, S. (2003) Populationmodels for marine reserve design: A retrospective and prospectivesynthesis. Ecological Applications 13(1): S47-S64.

GUENETTE, S., LAUCK, T. AND CLARK, C. (1998) Marine reserves: fromBeverton and Holt to the present. Reviews in Fish Biology andFisheries 8(3): 251-272.

GUIDETTI , P. (2007) Potential of marine reserves to causecommunity-wide changes beyond their boundaries. ConservationBiology 21(2): 540-545.

HALPERN, B.S. (2003) The impact of marine reserves: Do reserves workand does reserve size matter? Ecological Applications 13(1): S117-S137.

HOELZEL, A. (1994) Genetics and ecology of whales and dolphins.Annual Review of Ecology and Systematics 25: 377-399.

HOELZEL, A.R. (1998) Genetic structure of cetacean populations insympatry, parapatry, and mixed assemblages: Implications forconservation policy. Journal of Heredity 89(5): 451-458.

MARINE PROTECTED AREAS IN SOUTH AMERICA 207

LAJAM 6(2): 203-207, December 2007

HOOKER, S.K. AND GERBER, L.R. (2004) Marine reserves as a tool forecosystem-based management: The potential importance ofmegafauna. Bioscience 54(1): 27-39.

HOYT, E. (2005) Marine Protected Areas For Whales Dolphins andPorpoises: A World Handbook for Cetacean Habitat Conservation.London, Earthscan, London, UK.

IWC (2009) Report of the Scientific Committee. Annex L. Reportof the Sub-Committee on Small Cetaceans. Journal of CetaceanResearch and Management (Suppl.) 11: 311-333.

LOVEJOY, T.E. (2006) Protected areas: a prism for a changing world.Trends in Ecology & Evolution 21(6): 329-333.

MENDEZ, M., ROSENBAUM, H.C. AND BORDINO, P. (2008) Conservationgenetics of the franciscana dolphin in Northern Argentina:population structure, by-catch impacts, and managementimplications. Conservation Genetics 9(2): 419-435.

MORA, C., ANDREFOUET, S., COSTELLO, M.J., KRANENBURG, C., ROLLO, A.,VERON, J., GASTON, K.J. AND MYERS, R.A. (2006) Coral reefs and the globalnetwork of marine protected areas. Science 312(5781): 1750-1751.

NORSE, E.A. AND CROWDER, L.B. (2005) Marine Conservation Biology: TheScience of Maintaining the Sea’s Biodiversity. Washington, Island Press.

PALUMBI, S.R. (2003) Population genetics, demographicconnectivity, and the design of marine reserves. EcologicalApplications 13(1): S146-S158.

PALUMBI, S. ., GAINES, S.D., LESLIE, H. AND WARNER, R.R. (2003) Newwave: high-tech tools to help marine reserve research. Frontiers inEcology and the Environment 1(2): 73-79.

REDFERN, J.V., FERGUSON, M.C.,BECKER, E.A., HYRENBACH, K.D., GOOD,C., BARLOW, J., KASCHNER, K., BAUMGARTNER, M.F., FORNEY, K.A.,BALLANCE, L.T., FAUCHALD, P., HALPIN, P., HAMAZAKI, T., PERSHING,A.J., QIAN, S.S., READ, A., REILLY, S.B., TORRES, L. AND WERNER, F.(2006) Techniques for cetacean-habitat modeling. Marine EcologyProgress Series 310: 271-295.

REEVES, R.R. (2000) The value of sanctuaries, parks and reserves(Protected areas) as tools for conserving marine mammals. Final reportto the Marine Mammal Commission. Bethesda, Maryland, USA.

REEVES, R.R., FOLKENS, P.A., STEWART, B.S., CLAPHAM, P.J. AND POWEL,J.A. (2002) National Audubon Society Guide to Marine Mammals ofthe World. New York A.A. Knopf.

REEVES, R.R., SMITH, B.D., CRESPO, E.A. AND NOTARBARTOLO DI SCIARA,G. (2003) Dolphins, whales and porpoises: 2002-2010 ConservationAction Plan for the World’s Cetaceans. Gland, Switzerland andCambridge, UK, IUCN/SSC Cetacean Specialist Group: 139pp.

REILLY, S.B. (1990) Seasonal-Changes in Distribution and HabitatDifferences among Dolphins in the Eastern Tropical Pacific. Marine

Ecology Progress Series 66(1-2): 1-11.

REILLY, S.B. AND FIEDLER, P.C. (1994) Interannual Variability ofDolphin Habitats in the eastern tropical Pacific .1. Research vesselsurveys, 1986-1990. Fishery Bulletin 92(2): 434-450.

REMINGTON, N., STEVENS, R.D., WELLS, R.S., HOLN, A., DHUNGANA,S., TABOY, C.H., CRUMBLISS, A.L., HENKENS, R. AND BONAVENTURA,C. (2007) Genetic diversity of coastal bottlenose dolphinsrevealed by structurally and functionally diverse hemoglobins.Gene 398(1-2): 123-131.

RODRIGUES, A.S.L., ANDELMAN, S.J., BAKARR, M.I., BOITANI, L., BROOKS,T.M., COWLING, R.M., FISHPOOL, L.D.C., FONSECA, G.A.B. DA, GASTON,K.J., HOFFMANN, M., LONG, J.S., MARQUET, P.A., PILGRIM, J.D., PRESSEY,R.L., SCHIPPER, J., SECHREST, W., STUART, S.N., UNDERHILL, L.G.,WALLER, R.W., WATTS, M.E.J. AND YAN, X. (2004) Effectiveness ofthe global protected area network in representing species diversity.Nature 428(6983): 640-643.

RODRIGUES, A.S.L. AND GASTON, K.J. (2001) How large do reservenetworks need to be? Ecology Letters 4(6): 602-609.

ROSA, S., MILINKOVITCH, M.C., VAN WAEREBEEK, K., BERCK, J., OPORTO,J., ALFARO-SHIGUETO, J., VAN BRESSEM, M.F., GOODALL, N. AND CASSENS,I. (2005) Population structure of nuclear and mitochondrial DNAvariation among South American Burmeister’s porpoises(Phocoena spinipinnis). Conservation Genetics 6(3): 431-443.

SANDERSON, E.W., REDFORD, K.H., VEDDER, A., COPPOLILLO, P.B. ANDWARD, S.E. (2002) A conceptual model for conservation planningbased on landscape species requirements. Landscape and UrbanPlanning 58(1): 41-56.

SCOTT, J.M., MURRAY, M., WRIGHT, R.G., CSUTI, B., MORGAN, P. ANDPRESSEY, R.L. (2001) Representation of natural vegetation inprotected areas: capturing the geographic range. Biodiversity andConservation 10(8): 1297-1301.

SOUTULLO, A. AND GUDYNAS, E. (2006) How effective is theMERCOSUR’s network of protected areas in representing SouthAmerica’s ecoregions? Oryx 40(1): 112-116.

TRUDA-PALAZZO, J., AUGUSTOWSKI, M., BARRETO, A.S., ENGEL, M., GALES,N., GARCIA, R., GEDAMKE, P.J., GROCH, K.R., IÑIGUEZ, M., LIMA, R.P. DE,MARCONDES, M.C., OOSTHUIZEN, H., SIRONI, M. AND TOSSENBERGER, V.(2008) The South Atlantic: a sanctuary for whales. Paper SC60\57-4rev2 presented to the IWC Scientific Committee. Santiago, Chile,June 2008. [Available from IWC Secretariat, Cambridge, UK].

UNEP-WCMC (2006) World Database on Protected Areas.Available at sea.unep-wcmc.org/wdpa.

WARES, J.P., GAINES, S.D. AND CUNNINGHAM, C.W. (2001) Acomparative study of asymmetric migration events across amarine biogeographic boundary. Evolution 55(2): 295-306.

Received 27 May 2007. Accepted 30 November 2007.

CONTENTS

Incidental mortality of franciscana dolphin (Pontoporia blainvillei) in Argentina ................ 127Humberto L. Cappozzo, Maria F. Negri, Fabián H. Pérez, Diego Albareda, Florencia Monzón andJavier F. Corcuera

The ontogeny of shape disparity in three species of Otariids (Pinnipedia: Mammalia) ....... 139Daniela Sanfelice and Thales R. O. de Freitas

Age estimation in giant otters (Pteronura brasiliensis) (Carnivora: Mustelidae) using growthlayer groups in canine teeth ....................................................................................................... 155Gabriel da Cruz de Oliveira, José Fernando Marques Barcellos and Fernando César Weber Rosas

Activity budgets and distribution of bottlenose dolphins (Tursiops truncatus) in the PatosLagoon estuary, southern Brazil .................................................................................................. 161Paulo H. Mattos, Luciano Dalla Rosa and Pedro F. Fruet

Prey occurrence in the stomach contents of four small cetacean species in Peru ................... 171Ignacio García-Godos, Koen Van Waerebeek, Julio C. Reyes, Joanna Alfaro-Shigueto and MilenaArias-Schreiber

Veterinary treatment of an injured wild franciscana dolphin calf (Pontoporia blainvillei, Gervais& D‘Orbigny, 1844) ........................................................................................................................ 185Paula Baldassin, Max Rondon Werneck, Carla Beatriz Barbosa, Berenice Maria Gomes Gallo, HugoGallo and Michael Walsh

An interaction between a juvenile Clymene dolphin (Stenella clymene) and seismic surveyvessel M/V Ramform Challenger - GS, Bacia de Santos, Brazil ................................................. 189Michele F. Fernandes, Andrea S. Cordeiro, Demetrio M. R. Carvalho, Wilson R. Santos and Renata Ramos

Observation of a blue whale (Balaenoptera musculus) feeding in coastal waters of Ecuador .... 193Fernando Félix, Natalia Botero and Jéssica Falconí

Presence and re-sighting of southern elephant seal, Mirounga leonina (L. 1758), on the north-central coast of Chile ..................................................................................................................... 199Maritza Sepúlveda, María José Pérez-Alvarez, Paula López and Rodrigo Moraga

Marine protected areas in South America: spatial assessment of cetacean distributioncoverage ........................................................................................................................................... 203Andrés Gómez and Martín Mendez

Printed by

IMOS Gráfica e Editora Ltda.

the latin american journal of aquatic · pdf filethe latin american journal of aquatic mammals...

Documents