Revista de Biología Marina y Oceanografía ISSN: 0717-3326 [email protected] Universidad de Valparaíso Chile
Pérez-Alvarez, M. José; Carrasco, Pablo; Sepúlveda, Maritza; Quiñones, Renato A. Comparison of behavioral patterns of South American sea lions between breeding and non-breeding seasons Revista de Biología Marina y Oceanografía, vol. 48, núm. 1, abril, 2013, pp. 155-163 Universidad de Valparaíso Viña del Mar, Chile
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M. José Pérez-Alvarez1,2,3, Pablo Carrasco4, Maritza Sepúlveda2,3 and Renato A. Quiñones4
1Instituto de Ecología y Biodiversidad (IEB), Facultad de Ciencias, Universidad de Chile, Las Palmeras 3425, Ñuñoa, Santiago, Chile. [email protected] 2Centro de Investigación Eutropia, Ahumada 131 Oficina 912, Santiago, Chile 3Centro de Investigación y Gestión en Recursos Naturales (CIGREN), Facultad de Ciencias, Universidad de Valparaíso, Av. Gran Bretaña 1111, Playa Ancha, Valparaíso, Chile 4Programa de Investigación Marina de Excelencia (PIMEX), Facultad de Ciencias Naturales y Oceanográficas, Universidad de Concepción, Casilla 160-C, Concepción, Chile
Resumen.- Se han descrito tácticas reproductivas para machos y hembras en sistemas reproductivos poligínicos, dentro de las cuales, una respuesta conductual sexo-específico sería esperable para maximizar el éxito reproductivo. El presente estudio da cuenta de un seguimiento conductual del lobo marino común Otaria flavescens durante la época reproductiva (ER) y no reproductiva (ENR) en el Santuario de la Naturaleza Lobería Cobquecura, Chile central. Se registraron patrones conductuales de machos, hembras, juveniles y crías entre mayo de 2008 y diciembre de 2009. Los machos presentaron más registros de conductas asociadas a agresión, desplazamiento y reconocimiento durante ER, mientras que la conducta descanso fue mayor durante ENR. Hembras y juveniles presentaron mayores registros de reconocimiento durante ENR mientras que las otras categorías conductuales no presentaron diferencias entre ER y ENR. Las conductas agresivas por parte de los machos así como las relacionadas al cuidado parental por parte de las hembras podrían ser estrategias conductuales desarrolladas por ambos sexos para asegurar la viabilidad poblacional. Este estudio contribuye al conocimiento de los patrones conductuales reproductivos de la especie y forma parte de uno de los seguimientos conductuales reproductivos más continuos desarrollados en la actualidad en el lobo marino común. Dado que el estudio se realiza en un área protegida dentro del marco legal de Santuario de la Naturaleza, los resultados expuestos serán de utilidad para futuras comparaciones con loberas reproductivas afectadas por actividad antrópica.
Palabras clave: Sistema reproductivo poligínico, comportamiento reproductivo, otáridos, Otaria flavescens, Chile
Abstract.- In a polygynous mating system males and females have different reproductive strategies; so it is expectable that both sexes have evolved different reproductive behavioral responses to maximize their reproductive success. We analyze the behavior of different sex/age classes of Otaria flavescens during breeding (BS) and non-breeding seasons (NBS) at a Nature Sanctuary breeding colony, central Chilean coast. From May 2008 to December 2009 data of males, females, juveniles and pups were recorded. Males performed more aggression, locomotion and recognizing behaviors during the BS, while they mostly rested during the NBS. Females and juveniles performed more recognizing behavior in the NBS, while the other behavior categories did not show differences between the NBS and the BS. As reproductive behavioral strategies, male aggression and maternal care may increase the overall population viability. This study contributed to a better understanding of the reproductive behavior patterns of this species based on what is to our knowledge the most continuous monitoring of a South American sea lion breeding colony. Since the study has been undertaken in a Nature Sanctuary, the results may be used as a baseline to compare with behavioral data from colonies perturbed by human activities.
Key words: Polygynous mating system, reproductive behavior, otariids, Otaria flavescens, Chile
INTRODUCTION In a polygynous mating system, males and females number of offspring. In contrast, females can produce maximize their reproductive success in different ways. In only a limited number of young and must maximize their general, males tend to maximize reproductive success by reproductive success by producing and successfully mating with as many females as possible to increase the rearing high quality offspring (Cézilly & Danchin 2008).
Vol. 48, Nº 1, 2013 155 Revista de Biología Marina y Oceanografía In most otariid species (sea lions and fur seals), as in (Arctocephalus forsteri) during the non-breeding season other mammals, the predictable spatial and temporal differs markedly from the activities performed during the clustering of breeding females has favored the evolution breeding season. of a polygynous mating system (Coltman et al. 1998). In The South American sea lion Otaria flavescens (Shaw, otariids, maternal gestation and lactation provide the 1800) represents an interesting study species with a nutrient requirements for developing young and polygynous social mating system (Campagna 1985, consequently females provide most of the parental care Fernandez-Juricic et al. 2003, Cassini 2003). The breeding (Boness & Bowen 1996). Thus males are free to devote period extends from about the third week of December to the bulk of their time and energy to competing for access March (austral summer) (Aguayo & Maturana 1973, Vaz- to receptive females (Mesnick & Ralls 2002, Tyack 2002). Ferreira 1982, Acevedo et al. 2003). During this period Hence, since males and females have different males defend territories (breeding sites) and/or females reproductive goals, it is expectable that the sexes have (Campagna & Le Boeuf 1988a, b, Cappozzo 2002). Females evolved different behavioral adaptations to maximize their copulate and give birth within the territories established reproductive success (Tyack 2002). by the males (Campagna & LeBoeuf 1988a, Sielfeld 1999, During the breeding season, males perform territoriality Acevedo et al. 2003). At the end of the breeding season, displays and defense tactics to attempt to monopolize reproductive activity ceases and the abundance of males females directly (Boness et al. 2006). In this period fighting gradually decrease (Sepúlveda et al. 2001, Acevedo et al. among males is frequent, especially during the first few 2003). Since pups are not able to swim long distances, days of the breeding season when territorial boundaries females remain with their pups in the colony until May, are being established (Riedman 1990). Once boundaries and leave the breeding colony once pups are more are established, fighting and agonistic displays between proficient swimmers (Sepúlveda et al. 2009). neighboring males become less frequent, although they Behavioral studies of O. flavescens have been mostly may advertise their ownerships by constant vocalizing undertaken along the Atlantic coast of South America and aggressive displays (Cassini 2003). Males of several (Argentina) (Fernandez-Juricic et al. 2003, Cassini & species of otariids are also able to herd females, Fernandez-Juricic 2003, Fernandez-Juricic & Cassini 2007, preventing them from leaving their territories (Campagna Cappozzo et al. 2008), and have been mainly focused on & LeBoeuf 1988a). Females, in contrast, perform different a specific age class category. In Chile there have been agonistic behaviors during this period mainly related to few studies on the reproductive behavior of this species the care of their pups. First, females choose the territory (Rivera 1990, Acevedo 2000). All of the mentioned studies to haul-out and when the pup is born, it has to display were performed in a short time period and only during the recognition behaviors. Mutual vocal and olfactory breeding season, so fluctuations in behavior, whether recognition are common in otariids, due to the fact that seasonally or per age and sex classes were not the focus mothers and pups often separate during the mother’s of the past studies. Here we report detailed observations foraging trips and the reunion depends on mutual of South American sea lion behavior during almost 2 years recognition (Mann 2002, Trimble & Insley 2010, Trimble in a breeding colony of the central coast of Chile. In order & Charrier 2011). to investigate whether the breeding period has an effect During the non-breeding season, otariid males do not on the behavior of the species, behavioral activities of need to defend a female and/or a territory; females different age and sex classes of O. flavescens were distribute their time between taking care of their offspring analyzed, covering both the breeding and non-breeding on land and foraging in the ocean (Bonner 1984, seasons. Campagna & Le Boeuf 1988a). Thus it is expected that the dissimilarities between breeding and non-breeding MATERIALS AND METHODS seasons will be reflected in different behavioral patterns displayed by males and females, and in general in the STUDY AREA activity budget of otariids. Unfortunately, the partitioning of behavioral activities for different otariids outside the The study was conducted at the Cobquecura breeding breeding season has received much less attention. A colony, Lobera Cobquecura, situated in the central coast study done by Johnstone & Davis (1987) found that the of Chile (36°07’S; 72°48’W) (Fig. 1). The Cobquecura activity budget of males of the New Zealand fur seal colony is a chain of three rock formations, distant
156 Pérez-Alvarez et al. Behavioral pattern of South American sea lion in breeding and non-breeding season Figure 1. Geographic location of the South American sea lion (Otaria flavescens) breeding colony, Lobera Cobquecura, central coast of Chile / Ubicación geográfica de la lobera reproductiva del lobo marino común (Otaria flavescens), Lobera Cobquecura, Chile central
approximately 80-100 m from the coast. Cobquecura is sessions per day, from 09:00 to 17:00 hrs. The data was the most important sea lion colony of the central Chilean recorded alternately by the observers. Each session lasted coast, with nearly 2,500 individuals (Sepúlveda et al. 2011). 45 min and behavior was recorded at 5-min sample The Cobquecura colony is part of an area officially intervals for a randomly selected individual. Individuals declared as a Nature Sanctuary by the Chilean Government were observed using 10 x 15 binoculars and a konuspot- in 1992 (Quiñones et al. 2011)1 65 15-45x65 zoom spotting scope.
ETHOGRAMS DESIGN BEHAVIOR CATEGORIES From mid May 2008 to late December 2009 a total of 1,305 Five behavior categories and one ‘out of sight’ category individuals were observed. The study period was divided were previously identified in the colony, and their into ‘breeding season’ (BS) (from December 19th to March occurrence was recorded during the complete study 18th) and ‘non-breeding season’ (NBS) (from March 19th period (Table 1). Similar behavioral categories have been to December 18th). These dates were selected according used in other studies of terrestrial and aquatic mammals to the reproductive events described by Acevedo et al. (Schusterman 1981, Mallapur et al. 2005, Klinka & (2003). Behavioral patterns were assessed by focal time Reimchen 2009, Gerber et al. 2010, Smith & Litchfield 2010). sampling following Altmann (1974) and Martin & Bateson Individuals were classified into 4 classes according to (1993). Observations were conducted 2-3 days/week by 2 sex and age: adult males (M), adult females (F), juveniles experimented observers, completing a total of 7-8 (J) (both sexes, including yearlings born during the
1Quiñones RA, M Sepúlveda, P Carrasco, MJ Pérez, R Moraga, L Hückstädt & E Pedreros. 2011. Ecología y biología del lobo marino común, Otaria flavescens, en el Santuario Islote Lobería de Cobquecura. Informe de Avance Período Mayo 2008-Diciembre 2010. Programa de Investigación Marina de Excelencia (PIMEX), Facultad de Ciencias Naturales y Oceanográficas, Universidad de Concepción, Concepción, 148 pp.
Vol. 48, Nº 1, 2013 157 Revista de Biología Marina y Oceanografía Table 1. Description of the behavioral categories recorded in the study of the South American sea lion (Otaria flavescens) in Cobquecura breeding colony, central Chile / Descripción de las categorías conductuales registradas en el estudio del lobo marino común (Otaria flavescens) en la Lobera Cobquecura, Chile central
previous season), and pups (P). Age and sex were then females (30.13%), juveniles (24.11%) and finally pups determined from differences in size, body shape and/or (5.05%). During the BS, resting behavior was more coloration (Hamilton 1934, King 1983). The pup category commonly observed in males and females in comparison (born during the current breeding season) was considered to juveniles (M-J: χ2 = 18.07, d.f = 1, P < 0.0001; F-J: between January to mid March (BS) due their diagnostic χ2 = 28.89, d.f = 1, P < 0.0001) and pups (M-P: χ2= 58.68, characteristics and easy identification. After their first d.f = 1, P < 0.0001; F-P: χ2 =75, d.f = 1, P < 0.0001). molt, they are easily confused with the juvenile category, Recognition was more frequently recorded for pups than so during NBS pups were included in the juvenile males (P-M: χ2= 9.5, d.f. = 1, P < 0.01) and females (P-F: category in order to minimize misclassification. χ2 = 11.92, d.f. = 1, P < 0.001). Males performed more aggressive activities than females (M-F: χ2 = 3.7, d.f. = 1, P < 0.05) and pups, but not more than juveniles (M-P: χ2= DATA ANALYSES 3.7, d.f. = 1, P < 0.05; M-J: χ2= 1.05, d.f. = 1, P = 0.306). No To test whether the behavioral categories varied between significant differences were obtained for locomotion and the BS and the NBS for each sex/age class, and if the retreat behaviors among the different age and sex classes behavioral categories differ among them within each (excluding pups). season 2x2 contingency tables were carried out (Zar 1999). During the NBS the pup category was not considered, as Similar to the BS, during the NBS resting behavior was mentioned above. All the analyses were performed in more frequently observed in males and females compared Statistica 7.0 (StatSoft, Inc. 2004) and the significance to juveniles (M-J: χ2 = 34.03, F-J: χ2 = 20.49, d.f. = 1, level was set at α = 0.05. P < 0.0001) (Fig. 3). On the contrary, juveniles showed more recognition behavior than males (J-M: χ2= 10.35, d.f. = 1, P < 0.01). Locomotion activity was significantly RESULTS less in males than in juveniles (M-J: χ2 = 6.44, d.f. = 1, P < All the behavioral categories established were observed 0.05: M-F: χ2 = 2.45, d.f. = 1, P = 0.11). No significant for the South American sea lion during the study period. differences were found by sex/age class for aggression Overall, the most common activity for O. flavescens was and retreat behaviors. resting (R), both in the BS and NBS (Fig. 2). Also, in both periods recognition was the second most frequent When behavioral categories were compared between category observed followed by locomotion, aggression the BS and the NBS, differences according to sex/age and retreat (Fig. 2). classes were identified. For males, resting behavior increased significantly during the NBS (χ2 = 86.33, d.f. = Behavior categories were analyzed for each sex/age 1, P < 0.0001). However, they performed more locomotion, class during the BS and the NBS (Fig. 3). The most recognizing, and aggression during the BS (Locomotion: common sex/age category recorded was males (40.68%),
158 Pérez-Alvarez et al. Behavioral pattern of South American sea lion in breeding and non-breeding season Figure 2. Behavior categories recorded for the South American sea lion (Otaria flavescens), during the (A) Breeding and (B) Non-breeding season, in Cobquecura breeding colony, central Chile. Different letters indicate statistically significant differences between behavioral categories (α = 0.05) / Categorías conductuales registradas para el lobo marino común (Otaria flavescens), durante la época (A) Reproductiva y (B) No reproductiva en Lobera Cobquecura, Chile central. Letras diferentes indican diferencias estadísticas significativas (α = 0,05) entre categorías conductuales
Figure 3. Behavior categories recorded for the South American sea lion (Otaria flavescens) by age and sex classes (A: Males, B: Females, C: Juveniles, D: Pups) during the breeding (gray columns) and non-breeding (black columns) seasons, in Cobquecura breeding colony, central Chile / Categorías conductuales registradas para el lobo marino común (Otaria flavescens) según sexo y categoría etaria (A: Machos, B: Hembras, C: Juveniles, D: Crías) durante la época reproductiva (gris) y No reproductiva (negro) en Lobera Cobquecura, Chile central
Vol. 48, Nº 1, 2013 159 Revista de Biología Marina y Oceanografía χ2= 32.95, d.f. = 1, P < 0.00001; Recognizing: χ2 = 5.40, d.f. Le Boeuf 1988a, Campagna et al. 1988, 1992, Fernández- = 1, P < 0.05; Aggression: χ2= 31.1, d.f. = 1, P < 0.0001). Juricic et al. 2001, 2003), in which males exhibit a complex Females and juveniles showed a higher frequency of repertoire of threat calls that are associated with formalized recognizing behavior in the NBS (χ2 = 20.04, d.f. = 1, P < visual display behavior and tend to be individualistic 0.0001; χ2 = 26.6, d.f. = 1, P < 0.0001, respectively). The (Insley et al. 2003). other behavior categories did not present significant Differences in behavior categories were found for each differences between the NBS and the BS. age and sex class during the BS and the NBS. The results show that for males, resting behavior increased during DISCUSSION the NBS, while locomotion, aggression and recognizing This study is a contribution to the understanding of the behavior rose in the BS. Additionally, males performed reproductive behavior of polygynous species of otariids more aggressive activities than females and pups. These specifically in O. flavescens. Our results are based on, to results are in accordance with the expected for a resource- our knowledge, the most continuous monitoring of a defense polygynous breeding system. During the BS, South American sea lion breeding colony, and suggest a reproductively active males defend territories. Aggressive significant effect of the breeding season on the behavior encounters between males are frequent and males who of this species expressed by changes in behavioral initiate interactions are usually the ones who hold patterns of each sex/age class. territories (Gerber et al. 2010). Males chase and bite other individuals as a strategy to monopolize females Overall, the most common activity for O. flavescens (Campagna 2002), raising the number of offspring via was resting in both breeding and non-breeding seasons. defense of mates (Campagna 1985, Fernández-Juricic & Similar results were found in female Steller sea lions Cassini 2007). Harassment of females by males may also (Eumetopias jubatus) by Milette (1999). This author contribute to the increment of aggressive behavior during reports that resting behavior is the main component of the BS. Males, including satellite males, try to obtain mates the land activity of females, suggesting that they must by retaining females arriving to the colony from the sea, spend a substantial amount of time resting ashore due to and initiating group raids into the breeding area to seize the energetic costs of lactation. Likewise, Boness (1984) females (Campagna et al. 1988). Aggressive behavior mentioned that the high level of inactivity recorded begins to decline at the end of the BS mainly due at the during the BS in male Grey seals (Halichoerus grypus) is end of the breeding season, reproductive activity ceases due to the fact that males fast and do not devote energy (Sepúlveda et al. 2001, Acevedo et al. 2003). These may to searching for food. Fasting during the BS should have explain the increment of resting behavior performed by led to the evolution of a restricted energy regime males in this study during the NBS. Gerber et al. (2010) (Sandregen 1976). Bester & Rossouw (1994) suggested mentioned that both male and female behavior influence that inactivity in otariids serves a dual purpose; it is population viability in the sea lions. Male aggression may required to supplement physiological thermoregulation, separate mother-pup pairs, affecting nursing (Ono & being a behavioral response to restrict endogenous heat Boness 1996) or may cause direct mortality of pups due loading, and it is probably the most efficient way to reduce to an increasing in the risk of trampling (Gerber et al. energy expenditure. 2010). On contrary, female aggression has been observed Recognition activity was, after resting, the most as a protection behavior of their pups (Le Boeuf & frequent behavioral category observed in this colony all Campagna 1994, Campagna 2002), giving protection year round and in all sex/age classes. Recognition behavior directly or by securing higher quality resting and breeding seems to be an adaptation to gregarious living, and is areas (Gerber et al. 2010). probably a response to the selection pressures imposed Recognizing behavior was more frequently recorded (Picher et al. 2010). This behavior is a critical process for by females and juveniles in the NBS. These results may the social structure of the colony and its population be associated with the mutual mother-pup recognition dynamics since mother-pup recognition is a critical factor demonstrated in otariids (Insley et al. 2003) and with the in offspring survival (Fernández-Juricic et al. 1999, Trimble reproductive behavioral pattern of this species & Insley 2010, Trimble & Charrier 2011). Additionally, it is (Campagna 1985, Campagna & Le Boeuf 1988a, also crucial for identification of the female estrus period Fernández-Juricic & Cassini 2007). Females alternate (Riedman 1990) and for territorial defense (Campagna & foraging trips at sea with suckling periods ashore, and
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The evolution of maternal care the contrary, during the BS months, the category of in pinnipeds. Bioscience 46: 645-654. juveniles corresponds to individuals of approximately one Boness D, W Bowen, B Buhleier & G Marshall. 2006. year of age that were almost or fully weaned. Mating tactics and mating system of an aquatic-mating pinniped: the harbor seal, Phoca vitulina. Behavioral Our data are consistent with a behavioral reproductive Ecology Sociobiology 61: 119-130. strategy in a polygynous mating system. Since female Bonner W. 1984. Lactation strategies in pinnipeds: problems and male behavior influence female fecundity and for a marine mammalian group. In: Peaker M, RG Vernon & consequently population viability, the understanding of CH Knight (eds). Physiological strategies in lactation. behavioral and ecological factors that influence Symposia of the Zoological Society of London 51: 253- population dynamics may support proactive management 372. 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Received 26 September 2012 and accepted 6 March 2013 Associated Editor: Mauricio Landaeta D.
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