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South American Sea Lions Otaria flavescens, a good indicator of relative spatial and temporal changes in the distribution and abundance of marine resources?

Lobos marinos de un pelo sudamericanos Otaria flavescens ¿buenos indicadores de cambios espaciales y temporales relativos en la distribución y abundancia de los recursos marinos?

ABSTRACT.

Oceanographic fluctuations and changes in ocean productivity directly affect the abundance and distribution of prey species, which in turn, affect the population status of their predators. In order to have a better understanding of this predator-prey relationship, the aim of the present study was to analyze the diet of the South American Sea Lion Otaria flavescens (Shaw, 1800) in two rookeries of the San Matias Gulf, in northern Patagonia (Argentina). A total of 52 scat samples of O. flavescens were collected in the Promontorio Belén colony and 35 in Caleta de los Loros during the late spring of 2011. The analysis of the samples indicated that at both localities fish occurred in 100% of scats with prey remains, followed by cephalopods (32.3%) and crustaceans (21.4%). The fish Raneya brasiliensis (Kaup, 1856) constituted the main prey taxon, both in terms of occurrence and numerical abundance. The octopod Octopus tehuelchus (d’ Orbigny, 1834) and squids of the genus Doryteuthis constituted the dominant cephalopod prey. It is concluded that sea lions focused their foraging activity on those species of demersal and benthic habits, associated with coastal and shelf waters. Furthermore, this study reports for the first time the feeding habits of the South American Sea Lion colony of Promontorio Belén, second in population size of Río Negro province.

KEYWORDS.
Pinnipeds; trophic ecology; San Matias Gulf

RESUMEN.

Lobos marinos de un pelo sudamericanos Otaria flavescens ¿buenos indicadores de cambios espaciales y temporales relativos en la distribución y abundancia de los recursos marinos? Las fluctuaciones oceanográficas y los cambios en la productividad del océano afectan directamente a la abundancia y distribución de las especies presa, que a su vez afectan al estado de la población de sus predadores. Con el fin de tener una mejor comprensión de esta relación predador-presa, el objetivo del presente trabajo fue analizar la dieta del lobo marino de un pelo sudamericano Otaria flavescens (Shaw, 1800) en dos apostaderos del Golfo San Matias, en Patagonia norte (Argentina). Se colectaron un total de 52 muestras de fecas de O. flavescens en el apostadero de Promontorio Belén y 35 en Caleta de los Loros durante la primavera tardía de 2011. El análisis de las muestras indicó que en ambas localidades los peces ocurrieron en el 100% de las muestras con remanentes alimentarios, seguidos por cefalópodos (32.3%) y crustáceos (21.4%). El pez Raneya brasiliensis (Kaup, 1856) constituyó el principal taxón presa, tanto en términos de ocurrencia como de abundancia numérica. El octópodo Octopus tehuelchus (d’ Orbigny, 1834) y los calamares del género Doryteuthis constituyeron los cefalópodos presa dominantes. Se concluye que los lobos marinos centraron su actividad forrajera en aquellas especies de hábitos demersales y bentónicos, asociado a aguas costeras y de plataforma. Además, este estudio analiza por primera vez los hábitos alimenticios de la colonia de lobos marinos de un pelo sudamericanos en el apostadero de Promontorio Belén, segunda en tamaño poblacional de la provincia de Río Negro.

PALABRAS CLAVE.
Pinnipedos; ecología trófica; Golfo San Matias

Oceanographic fluctuations and changes in ocean productivity directly affect the abundance and distribution of prey species, which in turn affects the population status of their predators (Guinet et al., 2001Guinet, C.; Dubroca, L.; Lea, M. A.; Goldsworthy, S.; Cherel, Y.; Duhamel, G.; Bonadonna, F. & Donnay, J. P. 2001. Spatial distribution of foraging in female Antarctic fur seals Arctocephalus gazella in relation to oceanographic variables: a scale-dependent approach using geographic information systems. Marine Ecology Progress Series 219:251-264.; Mc Mahon et al., 2005Mc Mahon, C. R.; Van Den Hoff, J. & Burton, H. R. 2005. Handling intensity and the short-and long-term survival of Elephant Seals: addressing and quantifying research effects on wild animals. Ambio: A Journal of the Human Environment 34(6):426-429.; Melin et al., 2012Melin, S.; Orr, A.; Harris, J.; Laake, J. & Delong, R. 2012. California sea lions: an indicator for integrated ecosystem assessment of the California Current System. California Cooperative Ocean and Fisheries Investigations Reports 53:140-152.; Loeb & Santora, 2015Loeb, V. & Santora, J. 2015.Climate variability and spatio temporal dynamics of five Southern Ocean krill species. Progress in Oceanography 134:91-122.; Abreu et al., 2019Abreu, J.; Staniland, I.; Rodrigues, C. F.; Queirós, J. P.; Pereira, J. M. & Xavier, J. C. 2019. Squid in the diet of Antarctic fur seals: potential links to oceanographic conditions and Antarctic krill abundance. Marine Ecology Progress Series 628:211-221.). A better understanding of this predator-prey relationship would allow predators to be used as indicators of changes in the marine environment. Sea lions, as top predators, could be good indicators of relative spatial and temporal changes in the distribution and abundance of marine resources. A comprehensive analysis of biological and oceanographic information has the potential to provide a better understanding of the dynamics of the marine ecosystem and its influence on shaping the life history of predators (Soto et al., 2006Soto, H. K.; Trites, A.W. & Arias Schreiber, M. 2006. Changes in diet and maternal attendance of South American sea lions indicate changes in the marine environment and prey abundance. Marine Ecology Progress Series 312:277-290.; Constable et al., 2014Constable, A.; Melbourne-Thomas, J.; Corney, S.; Arrigo, K.; Barnes, D.; Bindoff, N.; Boyd, P.; Brandt, A.; Costa, D.; Davidson, A.; Ducklow, H.; Emmerson, L.; Fukuchi, M.; Gutt, J.; Hindell, M.; Hofmann, E.; Hosie, G.; Iida, T. & Ziegler, P. 2014. Climate change and Southern Ocean ecosystems I: How changes in physical habitats directly affect marine biota. Global Change Biology. 20(10):3004-3025. 10.1111/gcb.12623.
https://doi.org/10.1111/gcb.12623...
).

In reference to the feeding ecology of the South American sea lions, Otaria flavescens (Shaw, 1800), its study is of utmost importance if we consider that one of the factors affecting the population fluctuations of marine mammals is the availability of food in the ocean (Crespo & Pedraza, 1991Crespo, E. A. & Pedraza, S. N. 1991. Estado actual y tendencia de la población de lobos marinos de un pelo (Otaria flavescens) en el litoral norpatagonico. Ecología Austral 1:87-95.; Soto et al., 2006Soto, H. K.; Trites, A.W. & Arias Schreiber, M. 2006. Changes in diet and maternal attendance of South American sea lions indicate changes in the marine environment and prey abundance. Marine Ecology Progress Series 312:277-290.). The information available on the diet of O. flavescens has increased in the last two decades in different areas of its distributional range (Soto et al., 2006Soto, H. K.; Trites, A.W. & Arias Schreiber, M. 2006. Changes in diet and maternal attendance of South American sea lions indicate changes in the marine environment and prey abundance. Marine Ecology Progress Series 312:277-290.; Hückstädt et al., 2007Huckstadt, L. A.; Rojas, C. P. & Antezana, T. 2007. Stable isotope analysis reveals pelagic foraging by the Southern Sea lion in central Chile. Journal of Experimental Marine Biology and Ecology 347:123-133. doi:10.1016/j.jembe.2007.03.014
https://doi.org/10.1016/j.jembe.2007.03....
; Bustos et al., 2014Bustos, R. L.; Daneri, G. A.; Volpedo, A. V.; Harrington, A. & Varela, E. A. 2014. Diet of the South American sea lion Otaria flavescens during the summer season at Río Negro, Patagonia, Argentina. Aquatic Biology 20:235-243., 2019Bustos, R. L.; Daneri, G. A.; Varela, E. A.; Harrington, A.; Volpedo, A. V.; Ceia, F. R. & Xavier, J. C. 2019. South American sea lions Otaria byronia as biological samplers of local cephalopod fauna in the Patagonian shelf marine ecosystem. Journal of the Marine Biological Association of the United Kingdom 99(6):1459-1463. https://doi.org/10.1017/S0025315419000432
https://doi.org/10.1017/S002531541900043...
; Cárdenas-Alayza et al., 2022Cárdenas-Alayza, S.; Adkesson, M. J.; Edwards, M. R.; Hirons, A. C.; Gutiérrez, D.; Tremblay, Y. & Franco Trecu, V. 2022. Sympatric otariids increase trophic segregation in response to warming ocean conditions in Peruvian Humboldt Current System. PLoSONE 17(8):e0272348. https://doi.org/10.1371/journal.pone.0272348
https://doi.org/10.1371/journal.pone.027...
). These studies suggest that O. flavescens has a generalistic and opportunistic trophic behaviour, with differences in the diet between males and females, probably associated with different feeding areas (Koen Alonso et al., 2000Koen Alonso, M.; Crespo, E. A. & Pedraza, S. N. 2000. Food habits of the South American sea lion, Otaria flavescens, off Patagonia, Argentina. Fishery Bulletin 98:250-263.; Naya et al., 2000Naya, D. E.; Vargas, R. & Arim, M. 2000. Análisis preliminar de la dieta del león marino del sur (Otaria flavescens) en Isla de Lobos, Uruguay. Boletín de la Sociedad Zoológica de Uruguay 12:14-21.; Drago et al., 2009Drago, M.; Cardona, L.; Crespo, E. A. & Aguilar, A. 2009. Ontogenic dietary changes in South American sea lions. Journal of Zoology 279:251-261.; Crespo et al., 2012Crespo, E. A.; Oliva, D.; Dans, S. & Sepúlveda, M. 2012. Estado de situación del lobo marino común en su área de distribución. Valparaiso, Sello Editorial Universidad de Valparaiso. 200p.; Zenteno et al., 2015Zenteno, L.; Crespo, E. A.; Vales, D.; Silva, L.; Saporiti, F; Oliveira, L. R.; Secchi, E. R.; Drago, M.; Aguilar, A. & Cardona, L. 2015. Dietary consistency of male South American sea lions (Otaria flavescens) in southern Brazil during three decades inferred from stable isotope analysis. Marine Biology 162:275-289.). Up to date, dietary studies in the maritime coast of Río Negro province (North Patagonia) have been focused on the colonies of Punta Bermeja and Caleta de los Loros (Bustos et al., 2012Bustos, R. L.; Daneri, G. A.; Volpedo, A. V.; Harrington, A. & Varela, E. A. 2012. The diet of the South American sea lion (Otaria flavescens) at Río Negro, Patagonia, Argentina, during the winter-spring period. Iheringia, Série Zoologia 102:394-400., 2014Bustos, R. L.; Daneri, G. A.; Volpedo, A. V.; Harrington, A. & Varela, E. A. 2014. Diet of the South American sea lion Otaria flavescens during the summer season at Río Negro, Patagonia, Argentina. Aquatic Biology 20:235-243., 2019Bustos, R. L.; Daneri, G. A.; Varela, E. A.; Harrington, A.; Volpedo, A. V.; Ceia, F. R. & Xavier, J. C. 2019. South American sea lions Otaria byronia as biological samplers of local cephalopod fauna in the Patagonian shelf marine ecosystem. Journal of the Marine Biological Association of the United Kingdom 99(6):1459-1463. https://doi.org/10.1017/S0025315419000432
https://doi.org/10.1017/S002531541900043...
). These have indicated differences in the relative proportions of the dominant prey taxa between both rookeries.

In this regard, it is important to highlight that this study is the first to analyze the feeding habits of the sea lions’ colony of Promontorio Belén, second in importance in terms of population size of Río Negro province. On the other hand, the colony of Caleta de los Loros, unlike that of Promontorio Belén, is smaller in size and located within the bounds of a Protected Natural Area which is administered by the Secretaría de Ambiente y Cambio Climático of Río Negro Province. Both colonies are permanent, with seasonal variation in number of individuals throughout the year and catalogued as “mixed colonies”, i.e. important reservoirs of juveniles with small breeding areas in constant growth (Dans et al., 2004Dans, S. L.; Crespo, E. A.; Pedraza, S. N. & Koen Alonso, M. 2004. Recovery of the South American sea lion population (Otaria flavescens) in northern Patagonia. Canadian Journal Fisheries and Aquatic Science 61:1681-1690.). It is worth mentioning that the study season, late spring, constitutes a stage immediately prior to the beginning of the reproductive period of this otariid species. Therefore, it provides important information on the type and availability of prey in a key stage of the annual cycle of the species.

On the other hand, another factor that may influence the population status of pinnipeds is their interaction with fisheries. This overlap could exist in those areas where this group of marine mammals feed and fisheries activities occur (Wickens et al., 1992Wickens, P. A.; Japp, D. W.; Shelton, P. A.; Kriel, F.; Goosen, P. C.; Rose, B.; Augustyn, C. J.; Bross, C. A. R.; Penney, A. J. & Krohn, R. G. 1992. Seals and fisheries in South Africa - competition and conflict. South African Journal of Marine Science 12(1):773-789.). The aims of the present study were to: a) examine for the first time the diet of O. flavescens from the Promontorio Belén rookery, b) assess whether or not there was geographical variation in the feeding habits of O. flavescens between the two rookeries analysed, c) evaluate the potential/actual overlap between sea lions and fishery activities in the use of marine resources within the study area.

MATERIALS AND METHODS

Field data collection.

During the first half of December 2011, a total of 87 fresh scats of O. flavescens were collected at the sea lion rookeries of Promontorio Belén (PB: 41°09’S, 63°48’W) (n=52) and Caleta de los Loros (CL: 41°02’S, 64°10’W) (n=35) (Fig. 1). The faecal samples were preserved in 70% ethanol and brought to the laboratory for further analysis.

Fig. 1.
Study area showing the location of the rookeries analysed at Río Negro Province, Argentina.

Additionally, in order to obtain a general picture of the population size and structure of each colony sampled, the total number of individuals were counted and catalogued in the following sex-age classes according to Dans et al. (2004Dans, S. L.; Crespo, E. A.; Pedraza, S. N. & Koen Alonso, M. 2004. Recovery of the South American sea lion population (Otaria flavescens) in northern Patagonia. Canadian Journal Fisheries and Aquatic Science 61:1681-1690.).

1. Adult + subadult males (~>3 years old).

2. Adult females + unknown sex juveniles (including under yearlings).

Laboratory analysis.

Hard prey remains were recovered using sieves of different mesh size (2.5-0.5 mm) and rinsing water and, whenever possible, the different prey taxa were identified to the lowest possible taxonomical level. Fish were recognized from otoliths, bones, eye lenses and scales (teleost), teeth and dorsal plates (elasmobranchs); cephalopods from beaks, eye lenses and pens and crustaceans from exoskeleton remains. Fish otoliths and cephalopod beaks were identified by comparison with available catalogues (Torno, 1976Torno, A. E. 1976. Descripción y Comparación de los otolitos de algunas familias de peces de la plataforma Argentina. Revista del Museo Argentino de Ciencias Naturales “Bernardino Rivadavia”, Zoología 12:27-43.; Clarke, 1986Clarke, M. R.1986. A handbook for the identification of cephalopod beaks. Clarendon, Oxford Press, 220p.; Volpedo & Echeverría, 2000Volpedo, A.V. & Echeverría, D. D. 2000. Catálogo y claves de otolitos para la identificación de peces del Mar Argentino. Peces de importancia comercial. Buenos Aires, Editorial Dunken. 90p.; Volpedo et al., 2017Volpedo, A. V.; Thompson, G. & Avigliano, E. 2017. Atlas de otolitos de peces de Argentina; Buenos Aires, CAFP-BA CAPES. 320p.; Xavier & Cherel, 2021Xavier, J. C. & Cherel, Y. 2021. Cephalopod beak guide for the Southern Ocean: an update on taxonomy. British Antarctic Survey, Cambridge, UK, 129p. 978-0-85665-227-1.) and reference collections housed in the Laboratorio de Sistemática, Anatomía y Bioecología de Mamíferos Marinos, División Mastozoología of the Museo de Ciencias Naturales “Bernardino Rivadavia” (MACN-CONICET) and COLV in the Instituto de Investigaciones en Producción Animal (INPA/UBA-CONICET). The size and weight of the fish identified in the scats were estimated using regression equations (Torno, 1976Torno, A. E. 1976. Descripción y Comparación de los otolitos de algunas familias de peces de la plataforma Argentina. Revista del Museo Argentino de Ciencias Naturales “Bernardino Rivadavia”, Zoología 12:27-43.; Hecht, 1987Hecht, T. 1987. A guide to the otoliths of Southern Ocean Fishes. South African Journal of Antarctic Research 17(1):1-187.; Baldás et al., 1997Baldás, M. I.; Pérez Macri, G.; Volpedo, A. V. & Echeverría, D. D. 1997. Morfología de la sagita de peces marinos de la costa bonaerense de la Argentina I: Carangidae, Scianidae Mullidae. Atlântica 19:99-112.; Koen Alonso et al., 2000Koen Alonso, M.; Crespo, E. A. & Pedraza, S. N. 2000. Food habits of the South American sea lion, Otaria flavescens, off Patagonia, Argentina. Fishery Bulletin 98:250-263.; Volpedo & Echeverría, 2000Volpedo, A.V. & Echeverría, D. D. 2000. Catálogo y claves de otolitos para la identificación de peces del Mar Argentino. Peces de importancia comercial. Buenos Aires, Editorial Dunken. 90p. and Volpedo et al., 2017Volpedo, A. V.; Thompson, G. & Avigliano, E. 2017. Atlas de otolitos de peces de Argentina; Buenos Aires, CAFP-BA CAPES. 320p.). In the case of otoliths, a correction factor was applied according to the degree of erosion following Reid (1995Reid, K. 1995. The diet of Antarctic fur seals, Arctocephalus gazella, during winter at South Georgia. Antarctic Science 7:241-249.). Those specimens highly eroded were not taken into account and excluded from further analysis following Daneri et al. (2008Daneri, G. A.; Carlini, A. R.; Harrington, A.; Balboni, L. & Hernández, C. M. 2008. Interannual variation in the diet of non-breeding male Antarctic fur seals, Arctocephalus gazella, at Isla 25 de Mayo/King George Island. Polar Biology 31:1365-1372.). In regard to cephalopods, allometric equations were used to determine dorsal mantle length (ML in mm) and wet mass (W in g) from their beak sizes (Clarke, 1986Clarke, M. R.1986. A handbook for the identification of cephalopod beaks. Clarendon, Oxford Press, 220p.; Pineda et al., 1996Pineda, S. E.; Aubone, A. & Brunetti, N. 1996. Identificación y morfometría comparada de las mandíbulas de Loligo gahi y Loligo sanpaulensis (Cephalopoda, Loliginidae) del Atlántico Sudoccidental. Revista de Investigación y Desarrollo Pesquero 10:85-99.; Koen Alonso et al., 2000Koen Alonso, M.; Crespo, E. A. & Pedraza, S. N. 2000. Food habits of the South American sea lion, Otaria flavescens, off Patagonia, Argentina. Fishery Bulletin 98:250-263.; Xavier & Cherel, 2021Xavier, J. C. & Cherel, Y. 2021. Cephalopod beak guide for the Southern Ocean: an update on taxonomy. British Antarctic Survey, Cambridge, UK, 129p. 978-0-85665-227-1.). For the main prey taxa identified, the percentage frequency of occurrence (%FO), numerical abundance (%N), biomass (%W), prey importance index (IIMP) and a modified version of the Index of Relative Importance (IRI) were calculated (Reid, 1995Reid, K. 1995. The diet of Antarctic fur seals, Arctocephalus gazella, during winter at South Georgia. Antarctic Science 7:241-249.; García-Rodríguez & De La Cruz-Agüero, 2011García-Rodríguez, F. J. & De La Cruz-Agüero, J. 2011. A comparison of indexes for prey importance inferred from otoliths and cephalopod beaks recovered from pinniped scats. Journal of Fisheries and Aquatic Science 6(2):186-193.; Bustos et al., 2014Bustos, R. L.; Daneri, G. A.; Volpedo, A. V.; Harrington, A. & Varela, E. A. 2014. Diet of the South American sea lion Otaria flavescens during the summer season at Río Negro, Patagonia, Argentina. Aquatic Biology 20:235-243.). In order to make the interpretation of both indices easier, these were expressed on a percent basis (%IRI, %IIMP) following Cortes (1997Cortes, E.1997. A critical review of methods of studying fish feeding based on analysis of stomach contents: application to elasmobranch fishes. Canadian Journal of Fisheries and Aquatic Sciences 54:726-738.).

Statistical analysis.

A nested ANOVA test was performed to detect geographical differences in the sizes of the dominant prey species consumed in common by sea lions from both colonies. This analysis allowed testing of the null hypothesis of no differences between localities. In addition, a chi-squared test was performed to assess geographical variation in the occurrence of the main prey taxa of O. flavescens as well as in the population composition (sex-age classes) of each sea lions colony.

RESULTS

Sea lion population composition.

During the sampling period the females-juveniles category made up the largest portion of the population at both rookeries, being the occurrence of males negligible (Tab. I).

Tab. I.
Sea lion population composition during the spring of 2011 at the rookeries of Promontorio Belén and Caleta de los Loros, Río Negro province, Argentina.

Notwithstanding, there were significant differences between colonies in the relative proportions of the sex-age classes assigned (X2 yates: 17.4 P< 0.0001). In proportion, the contribution of males was much lower in Promontorio Belén than in Caleta de los Loros.

Overall diet.

The analysis of faecal samples containing prey remains (n=75) indicated that, for both rookeries, 100% of scats contained fish, followed by cephalopods and crustaceans with a frequency of occurrence of 32.3% and 21.4% respectively. There were significant differences between rookeries in the frequencies of occurrence of these three prey taxa (X2 = 8.02; p <0.05) with crustaceans being more frequent in Caleta de los Loros (PB 15.2% vs. CL 27.6%) and cephalopods more representative in Promontorio Belén (PB 54.3% vs. CL 10.3%) (Fig. 2).

Fig. 2.
Frequency of occurrence of the main prey taxa in the diet of Otaria flavescens (Shaw, 1800) from the San Matías Gulf, Argentina.

Regarding both colonies combined, fish were represented by a total of 335 otoliths. Their identification indicated that the most frequent and dominant fish species was Raneya brasiliensis (Kaup,1856), with a mean frequency of occurrence of 82.4% and contributing 95.6% to the IRI and 60.8% to the IIMP. Of lesser importance were Porichthys porosissimus (Cuvier, 1829) (%IRI = 1.3, %IIMP = 12.3) and Acanthistius brasilianus (Cuvier, 1828) (%IRI = 1.2, %IIMP = 7.6). The diversity of fish prey species identified differed between both sites (PB: 11 vs. CL: 4) (Tab. II). There were no significant differences between rookeries in the sizes (standard length) of R. brasiliensis preyed upon by O. flavescens (Nested ANOVA F = 2.29, p = 0.15), with greater mean lengths in Caleta de los Loros (18.5 ± 3.2 mm) than in Promontorio Belén (16.3 ± 3.4 mm). Regarding cephalopods, beaks belonging to different teuthoid species (mainly Doryteuthis spp.) were found only at Promontorio Belén, while the octopod Octopus tehuelchus (d’ Orbigny, 1834) was the only species found in common at both sampling areas.

Tab. II.
Taxonomic composition of teleost fish prey remains recovered from scats of Otaria flavescens (Shaw, 1800) during the spring of 2011 at Río Negro province, Argentina, expressed as percentage of frequency of occurrence (FO%), total number (N%), wet weight (W%), prey importance index (IIMP%) and index of relative importance (IRI%).

Promontorio Belén.

A total of 52 scats were collected at this colony. The analysis of the samples with hard remnants (n= 46) indicated that 100% of them contained fish remains. The identification of the sagittal otoliths (n = 275) indicated that the most frequent (%FO = 81.5) and dominant fish species was R. brasiliensis, which, alone, constituted 75.6% in numbers and 71.3% in biomass of the total fish preyed on by sea lions. Acanthistius brasilianus was second in terms of frequency of occurrence (%FO = 22.2) and biomass (%M= 7.9), while Merluccius hubbsi (Marini, 1933) did so in numbers (%N = 4.4) (Tab. II). In regard to cephalopods, these were found in 54.3% of the samples and were mainly represented in numbers by O. tehuelchus (%N=56), followed by the teuthoid Doryteuthis gahi (d’ Orbigny, 1835) which represented 28% of cephalopods consumed. Measurement of lower hood/rostral length (LHL/LRL) of beaks represented specimens of a range of 23.7 - 67.9 mm ML and 4.5 - 81 g wet mass for O. tehuelchus and 112.3 -209.8 mm ML and 28.2 - 140.7 g wet mass for D. gahi. Crustaceans were of minor relevance, occurring in 15.2 % of samples.

Caleta de los Loros.

A total of 35 samples were collected, of which 29 contained prey remains. Of these, 100% present teleost species and 17.2% elasmobranchs. A total of 60 otoliths from four different species were retrieved from samples containing fish remains, with a dominance of R. brasiliensis in terms of frequency, number and biomass (85.7%, 83.3% and 72% respectively). Of lesser importance was P. porosissimus, with a frequency of occurrence of 28.6% and Macruronus magellanicus (Lönnberg, 1907) in terms of number and biomass (5% and 14.5% respectively) (Tab. II). Cephalopods were represented uniquely by three beaks (upper n =1 and lower n = 2) and one eye lens of the octopod O. tehuelchus.

Measurement of lower hood length (LHL) of both lower beaks represented specimens of 36.6 - 82.6 mm ML and 14.8 - 139.1 g wet mass. In regard to crustaceans, these were mainly represented by decapods and occurred in 27.6% of scats.

DISCUSSION

The diet of pinnipeds can be analyzed throughout different methods, i.e. scats, stomach contents, stable isotopes, among others (Croxall, 1993Croxall, J. P. 1993. Diet. In: Laws, R. M. ed. Antarctic seals: Research methods and techniques. Cambridge, Cambridge University Press, p. 268-290.). In Otariids, particularly, scat analysis has been used for several decades around the world, due to the high fidelity of its results (Reid & Arnould, 1996Reid, K. & Arnould, J. P. Y. 1996. The diet of Antartic fur seals Arctocephalus gazella during the breeding season at South Georgia. Polar Biology 16:105-114.; Daneri et al., 2008Daneri, G. A.; Carlini, A. R.; Harrington, A.; Balboni, L. & Hernández, C. M. 2008. Interannual variation in the diet of non-breeding male Antarctic fur seals, Arctocephalus gazella, at Isla 25 de Mayo/King George Island. Polar Biology 31:1365-1372.; Páez-Rosas & Aurioles-Gamboa, 2010Páez-Rosas, D. & Aurioles-Gamboa, D. 2010. Alimentary niche partitioning in the Galapagos sea lion Zalophus wollebaeki. Marine Biology 157:2769-2781.; Harrington et al., 2017Harrington, A.; Daneri, G. A.; Carlini, A. R.; Reygert, D. S. & Corbalán, A. 2017. Seasonal variation in the diet of Antarctic fur seals, Arctocephalus gazella, at 25 de Mayo/King George Island, South Shetland Islands, Antarctica. Polar Biology 40:471-475.). One of the main advantages of this method is that large numbers of scats can be easily collected, without the need to manipulate the animals or alter the colonies. However, this methodology presents some biases, such as the underestimation of those prey taxa that lack hard remains (crustaceans, elasmobranches), due to their total or partial digestion (Tollit et al., 1997Tollit, D. J.; Steward, M. J.; Thompson, P. M.; Pierce, G. J.; Santos, M. B. & Hughes, S. 1997. Species and size differences in the digestion of otoliths and beaks: implications for estimates of pinniped diet composition. Canadian Journal of Fisheries and Aquatic Sciences 54(1):105-119.; Bowen, 2000Bowen, W. D. 2000. Reconstruction of pinniped diets: accounting for complete digestion of otoliths and cephalopod beaks. Canadian Journal of Fisheries and Aquatic Sciences 57:898-905.). Notwithstanding, Dellinger & Trillmich, 1988Dellinger, T. & Trillmich, F. 1988. Estimating diet composition from scat analysis in otariid seals (Otariidae): Is it reliable? Canadian Journal Zoology 66:1865-1870. stated that the numerical proportion of the different prey species can be correctly estimated from large samples of scats.

The results of the present study showed that, although sea lions consumed a wide variety of prey, a few species predominate in their diet. Fish were the most frequent and abundant prey at both sampling locations. This is in line with previous dietary studies of O. flavescens at other localities of the Southwest Atlantic which have reported the dominance of this prey taxon in its diet (Thompson et al., 1998Thompson, D. C.; Duck, D.; Mc Connell, B. J. & Garrett, J. 1998. Foraging behavior and diet of lactating female southern sea lions (Otaria flavescens) in the Falkland Islands. Journal of Zoology 246:135-146.; Koen Alonso et al., 2000Koen Alonso, M.; Crespo, E. A. & Pedraza, S. N. 2000. Food habits of the South American sea lion, Otaria flavescens, off Patagonia, Argentina. Fishery Bulletin 98:250-263.; Suárez et al., 2005Suárez, A. A.; Sanfelice, D.; Cassini, M. H. & Cappozzo, H. L. 2005. Composition and seasonal variation in the diet of the South American sea lion (Otaria flavescens) from Quequén Argentina. The Latin American Journal of Aquatic Mammals 4(2):163-174.; Romero et al., 2011Romero, M. A.; Dans, S. L.; González, R.; Svendsen, G. M.; García, N. & Crespo, E. A. 2011. Solapamiento trófico entre el lobo marino de un pelo Otaria flavescens y la pesquería de arrastre demersal del Golfo San Matías, Patagonia, Argentina. Latin American Journal of Aquatic Science 39(2):344-358.; Bustos et al., 2012Bustos, R. L.; Daneri, G. A.; Volpedo, A. V.; Harrington, A. & Varela, E. A. 2012. The diet of the South American sea lion (Otaria flavescens) at Río Negro, Patagonia, Argentina, during the winter-spring period. Iheringia, Série Zoologia 102:394-400., 2014Bustos, R. L.; Daneri, G. A.; Volpedo, A. V.; Harrington, A. & Varela, E. A. 2014. Diet of the South American sea lion Otaria flavescens during the summer season at Río Negro, Patagonia, Argentina. Aquatic Biology 20:235-243.; Jarma et al., 2019Jarma, D.; Romero, M. A.; García, N. A.; Svendsen, G.; González, R.; Dans, S. L. & Crespo, E. A. 2019. Small-scale variation in the diet of the South American Sea lion (Otaria flavescens) in northern Patagonia (Argentina). Regional Studies in Marine Science 28:100592.). Furthermore, R. brasiliensis was the most important fish prey species at both rookeries, both in terms of %IRI (more than 95%) and IIMP (0.61%). It is remarkable that this demersal fish has also been reported to be an important prey item in the diet of O. flavescens in other seasons and localities from northern Patagonia and Buenos Aires province (Koen Alonso et al., 2000Koen Alonso, M.; Crespo, E. A. & Pedraza, S. N. 2000. Food habits of the South American sea lion, Otaria flavescens, off Patagonia, Argentina. Fishery Bulletin 98:250-263.; Suárez et al., 2005Suárez, A. A.; Sanfelice, D.; Cassini, M. H. & Cappozzo, H. L. 2005. Composition and seasonal variation in the diet of the South American sea lion (Otaria flavescens) from Quequén Argentina. The Latin American Journal of Aquatic Mammals 4(2):163-174.; Romero et al., 2011Romero, M. A.; Dans, S. L.; González, R.; Svendsen, G. M.; García, N. & Crespo, E. A. 2011. Solapamiento trófico entre el lobo marino de un pelo Otaria flavescens y la pesquería de arrastre demersal del Golfo San Matías, Patagonia, Argentina. Latin American Journal of Aquatic Science 39(2):344-358.; Bustos et al., 2012Bustos, R. L.; Daneri, G. A.; Volpedo, A. V.; Harrington, A. & Varela, E. A. 2012. The diet of the South American sea lion (Otaria flavescens) at Río Negro, Patagonia, Argentina, during the winter-spring period. Iheringia, Série Zoologia 102:394-400., 2014Bustos, R. L.; Daneri, G. A.; Volpedo, A. V.; Harrington, A. & Varela, E. A. 2014. Diet of the South American sea lion Otaria flavescens during the summer season at Río Negro, Patagonia, Argentina. Aquatic Biology 20:235-243.). Moreover, for the sea lions colony of Punta Bermeja, the biggest of Río Negro province and the closest to the sampling areas in this study, Bustos et al. (2012Bustos, R. L.; Daneri, G. A.; Volpedo, A. V.; Harrington, A. & Varela, E. A. 2012. The diet of the South American sea lion (Otaria flavescens) at Río Negro, Patagonia, Argentina, during the winter-spring period. Iheringia, Série Zoologia 102:394-400., 2014Bustos, R. L.; Daneri, G. A.; Volpedo, A. V.; Harrington, A. & Varela, E. A. 2014. Diet of the South American sea lion Otaria flavescens during the summer season at Río Negro, Patagonia, Argentina. Aquatic Biology 20:235-243.) reported that R. brasiliensis was the predominant fish prey species consumed by sea lions in terms of frequency of occurrence and numerical abundance.

According to Gosztonyi et al. (2007Gosztonyi, A. E.; Kuba, L. & Mansur, L. E. 2007. Estimation of body size using morphometric relationships of head bones, pectoral fin bones and bony precaudal distance in Raneya brasiliensis (Kaup, 1856) (Pisces, Ophidifformes, Ophidiidae) in Patagonian waters. Revista de Biología Marina y Oceanografía 42(1):1-5.), this ophidiid constitutes a key species in the food web of the South Atlantic marine ecosystem, being an important prey item in the diet of marine mammals, marine birds and fishes. The fact that there were no significant differences in the estimated sizes of R. brasiliensis between rookeries, might indicate that sea lions preyed upon similar components (i.e. age classes) of this fish population during spring. It is interesting to mention that the less relevant fish species found in the present study, such as A. brasilianus, P. porosissimus, Paralichthys sp. and M. hubbsi, among others, also present demersal-benthic habits and a general distribution in the southwest Atlantic Ocean, from southern Brazil to northern Patagonia in Argentina (Cousseau & Perrotta, 2004Cousseau, M. B. & Perrotta, R. G. 2004. Peces marinos de Argentina. Biología, distribución, pesca. 3ed. Mar del Plata, INIDEP. 167p.).

Octopods dominated the cephalopod portion of the diet of O. flavescens at Promontorio Belén, while teuthoids were of lesser importance. Moreover, at Caleta de los Loros, only octopods occurred as cephalopod prey of sea lions, and in low numbers.

Different dietary studies carried out at northern Patagonia have shown that, in relation to the cephalopod prey of sea lions, there seems to be an alternation in the dominance of either octopods or teuthoids which varies according to the season, year and location of sampling. This, in turn, should reflect the opportunistic behavior of O. flavescens, whose pattern of predation probably depends on the prey availability at a given time and place (Tab. III).

Tab. III.
Dominant cephalopod prey taxon (at the order level) in the diet of Otaria flavescens (Shaw, 1800) according to season, year, locality, area and methodology.

In the present study, we found different contribution of crustaceans to the diet of sea lions between localities; while in Promontorio Belén they occurred in low proportions (15.2%), in Caleta de los Loros they represented the second most important prey item (27.6%). In this sense, some authors have mentioned that this taxon constitutes an important food item of sea lions (Hamilton, 1934Hamilton, I. E. 1934. The southern sea lion Otaria byronia (de Blainville) Discovery Reports 8:269-318.; Thompson et al., 1998Thompson, D. C.; Duck, D.; Mc Connell, B. J. & Garrett, J. 1998. Foraging behavior and diet of lactating female southern sea lions (Otaria flavescens) in the Falkland Islands. Journal of Zoology 246:135-146.; Soto et al., 2006Soto, H. K.; Trites, A.W. & Arias Schreiber, M. 2006. Changes in diet and maternal attendance of South American sea lions indicate changes in the marine environment and prey abundance. Marine Ecology Progress Series 312:277-290.), while others have suggested that crustaceans might not be as important as previously considered but could represent prey of prey (secondary items), regarding that fish and cephalopods are partially carcinophagous (Bustos et al., 2014Bustos, R. L.; Daneri, G. A.; Volpedo, A. V.; Harrington, A. & Varela, E. A. 2014. Diet of the South American sea lion Otaria flavescens during the summer season at Río Negro, Patagonia, Argentina. Aquatic Biology 20:235-243.).

Nevertheless, and considering the opportunistic feeding behaviour of this otariid species, it is interesting to mention a particular situation observed with the argentine red shrimp Pleoticus muelleri (Bate, 1888), at the San Matías Gulf. This crustacean species experienced an exceptional increase in population numbers in the mid 2010’s, generating an intense commercial fishing activity on this resource (De Carli et al., 2012De Carli, P.; Braccalenti, J. C.; García-De-León, F. J. & Acuña Gómez, E. P. 2012. La pesquería del langostino argentino Pleoticus muelleri (Crustacea: Penaeidae) en patagonia, ¿un único stock? Anales Instituto de la Patagonia (Chile), 40(2):103-112.; Boschi et al., 2016Boschi, E. E. 2016. Los crustáceos de interés pesquero y otras especies relevantes en los ecosistemas marinos. Mar del Plata, Instituto Nacional de Investigación y Desarrollo Pesquero INIDEP. 271p. (Boschi, E. E. 1ed., El Mar Argentino y sus Recursos Pesqueros).).

Coincidentally, during this period, P. muelleri unusually contributed in high proportions to the diet of O. flavescens from Caleta de los Loros during the summer of 2015 (A. Harrington and G. A. Daneri, unpubl. data).

The knowledge on the degree of interaction between pinnipeds and fisheries is an important tool for the management of this otariid species. In the San Matías Gulf, the Argentine Hake M. hubbsi constitutes the main target of fisheries (Irusta et al., 2003Irusta, G.; Pérez, M. & Renzi, C. R. 2003. Pesca comercial de Merluza al sur de 41°S y estimación de índices de abundancia derivados de la flota fresquera. Informe Técnico Int. INIDEP, No. 51/03, Mar del Plata, INIDEP .). Despite that some dietary studies, based on the analysis of stomach contents, have reported that M. hubbsi is an important prey item of O. flavescens (Koen Alonso et al., 2000Koen Alonso, M.; Crespo, E. A. & Pedraza, S. N. 2000. Food habits of the South American sea lion, Otaria flavescens, off Patagonia, Argentina. Fishery Bulletin 98:250-263.; Romero et al., 2011Romero, M. A.; Dans, S. L.; González, R.; Svendsen, G. M.; García, N. & Crespo, E. A. 2011. Solapamiento trófico entre el lobo marino de un pelo Otaria flavescens y la pesquería de arrastre demersal del Golfo San Matías, Patagonia, Argentina. Latin American Journal of Aquatic Science 39(2):344-358.), other approaches based on scat analysis indicated that this fish was absent or poorly represented. In the present study, this fish species was absent in the sea lion scats from Caleta de los Loros, while in those from Promontorio Belén its presence was of minor relevance both in terms of %FO =11.1 and %IIMP = 6.46. In regard to R. brasiliensis, this is not targeted by fisheries, hence overlapping with O. flavescens is negligible. Regarding O. tehuelchus, although not commercially important, it is an important target of the artisanal fisheries of the San Matías Gulf during spring and summer. Two fishing arts are used by fishermen: pot-longline in the subtidal zone and hand gathering in the intertidal areas (Storero et al., 2010Storero, L. P.; Ocampo-Reinaldo, M.; González, R. A. & Narvarte, M. A. 2010. Growth and life span of the small octopus Octopus tehuelchus in San Matías Gulf (Patagonia): three decades of study. Marine Biology 157:555-564.). Therefore, the use of this resource can generate some degree of overlap between sea lions and artisanal fisheries.

Regionally, the species of Doryteuthis support local fisheries; both D. sanpaulensis (Brakoniecki, 1984) and D. gahi are target species of the argentine fishing fleet. The former is caught from southern Brazil to the San Jorge Gulf with trawls, as by catch in the shrimp and prawn fishery. On the other hand, D. gahi is captured in the southeast of the Malvinas Islands in two annual seasons, one from February to May and the other between August and October. In addition, it is caught incidentally by the freezer fishing fleet and factory ships (Brunetti et al., 1999Brunetti, M. E.; Ivanovic, M. L. & Sakai, M. 1999. Calamares de importancia comercial en Argentina. Biología, distribución, pesquerías, muestreo biológico. Mar del Plata, Japan International Cooperation Agency, Contribución, INIDEP. 45p. (Contribución INIDEP N° 1121).). From this information, one should expect a low degree of overlap between O. flavescens and fisheries in the consumption of these species.

In brief, the results obtained in the present study corroborate the opportunistic and generalist nature of O. flavescens as top predator of the San Matías Gulf. The diversity of prey species found in its diet, especially in Promontorio Belén, reflects the high availability of prey resources for the sea lion colonies in the study area. An interseasonal/interannual long term monitoring program of the diet of O. flavescens is strongly recommended in order to better understand the feeding ecology of this species. This, in turn, will aid to detect possible changes in local prey availability and thus in the food chains of the North Patagonian marine ecosystem.

Acknowledgements.

This work was supported by UBACYT 20020150100052 BA, PICT 2015-1823, UBACYT 20020190100069 BA, PICT -2019-03888, Argentina. We thank the Secretaría de Ambiente y Cambio Climático of Río Negro Province, Argentina, for the permission to sample in the area. We also thank to Lucas Bustos, Mauricio Failla, Roberto Lini and Ramón Conde for logistic support and the group of rangers from Río Negro province, for field support. We are also grateful to Mr. Daniel Oks for facilitating the access to the colony.

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Publication Dates

  • Publication in this collection
    04 Nov 2022
  • Date of issue
    2022

History

  • Received
    10 Sept 2021
  • Accepted
    05 Sept 2022
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