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Daily and seasonal variation in the haul-out behavior of the South American sea lion
Mammalian Biology 77 (2012) 288–292
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Mammalian Biology journal homepage: www.elsevier.de/mambio
Original Investigation
Daily and seasonal variation in the haul-out behavior of the South American sea lion b,c ˜ Maritza Sepúlveda a,∗ , Renato A. Quinones , Pablo Carrasco b , M. José Pérez-Álvarez a a
Centro de Investigación y Gestión en Recursos Naturales (CIGREN), Facultad de Ciencias, Universidad de Valparaíso, Av. Gran Breta˜ na 1111, Playa Ancha, Valparaíso, Chile Programa de Investigación Marina de Excelencia (PIMEX), Facultad de Ciencias Naturales y Oceanográficas, Casilla 160-C, Universidad de Concepción, Chile c Centro de Investigación Oceanográfica en el Pacífico Sur Oriental (COPAS), Departamento de Oceanografía, Facultad de Ciencias Naturales y Oceanográficas, Casilla 160-C, Universidad de Concepción, Chile b
a r t i c l e
i n f o
Article history: Received 5 September 2011 Accepted 9 March 2012 Keywords: Southern sea lion Otaria flavescens Haul-out activity Census time
a b s t r a c t In the South American sea lion (Otaria flavescens), daily fluctuations in abundance have been analyzed based on sequential counts of the number of animals hauled-out. However, no studies have analyzed haul-out activity in relation to an annual cycle or according to different age/sex classes. The objective of this study was to determine the daily and seasonal haul-out patterns of each age/sex class of South American sea lions as a function of the time of the day. A total of 222 days were analyzed in a breeding colony of Chile, from May 2008 to December 2010. During the non-breeding season (March to December) males, females, and juveniles showed a unimodal pattern, in which few sea lions are hauled-out in the morning and maximum numbers are found in the rookery during the early afternoon (1330–1630). In contrast, during the breeding season (austral summer) the proportion of individuals hauled-out shifted from a unimodal to a bimodal pattern, especially in the case of juveniles. Our results indicate that there are fine scale differences in haul-out behavior among age/sex classes, as well as larger scale seasonal differences in the proportion of sea lions ashore. These differences appear to be related to reproductive activities, food availability and thermoregulatory requirements. These patterns of seasonal variability of South American sea lion haul-out should be taken into consideration when planning surveys to estimate population abundance. © 2012 Deutsche Gesellschaft für Säugetierkunde. Published by Elsevier GmbH. All rights reserved.
Introduction Most seals and sea lions spend part of their lives in terrestrial habitats on land or ice to raise young, mate, molt, and rest (Riedman, 1990; Reder et al., 2003). However, the time these animals spend on land is highly variable, because it depends upon several factors that have been demonstrated to affect strongly their daily and seasonal terrestrial abundance and haul-out behavior, including prey availability, predator avoidance, thermoregulation, social activity, and environmental effects such as tides, weather, time of day and seasons (Reder et al., 2003). In particular, time of day has typically been examined to determine daily trends in haul-out patterns, relating the observed patterns to the ambient temperature, intensity of solar radiation and prey availability in the water column (Calkins et al., 1999). Understanding how the time of day influences daily and seasonal haul-out patterns is useful for gaining insight into how animals respond to environmental conditions in relation to their physiology (Lake et al., 1997), energy requirements (Thompson et al., 1998; Andrews-Goff et al., 2010), behavior
∗ Corresponding author. Tel.: +56 32 2508346; fax: +56 32 2508072. E-mail address: [email protected] (M. Sepúlveda).
(Thompson and Harwood, 1990) and life history (Sepúlveda et al., 2001). Daily fluctuations in the abundance of seals and sea lions have been mostly studied based on sequential counts of the number of animals hauled-out (e.g. Ainley et al., 1982; Thompson and Harwood, 1990; Lake et al., 1997; Reder et al., 2003). For the South American sea lion (Otaria flavescens), Sepúlveda et al. (2001), working with non-breeding colonies in central Chile, reported that few sea lions are hauled-out in the morning and maximum numbers of individuals are hauled-out in the afternoon. A similar result was found by Rosas et al. (1994) for a non-breeding colony in the Atlantic coast; they described a similar behavioral pattern in which groups go out from the colony at sunset and come back at sunrise, reaching the greatest number of animals on land at noon. Thompson et al. (1998), using satellite-linked data loggers on four females in the Falkland/Malvinas Islands, reported that the vast majority of the foraging trips were nocturnal; females spent more time ashore during the day. All of these studies suggest a strong diurnal component to South American sea lion haul-out behavior, with most individuals on land between mid morning and late afternoon. However, none of these studies analyzed the haul-out activity among different age/sex classes or during an entire annual cycle, therefore they collected only a narrow range of information.
1616-5047/$ – see front matter © 2012 Deutsche Gesellschaft für Säugetierkunde. Published by Elsevier GmbH. All rights reserved. http://dx.doi.org/10.1016/j.mambio.2012.03.008
M. Sepúlveda et al. / Mammalian Biology 77 (2012) 288–292
Fig. 1. Map of the study area.
The South American sea lion exhibits a marked breeding period, which extends from about mid-December to mid-March (austral summer) (Acevedo et al., 2003). During this period males defend territories (breeding sites) and/or females (Campagna and LeBoeuf, 1988a,b; Capozzo, 2002), and stay in the colony during practically all of this period, fighting, mating and fasting (King 1983). Once arrived, a female gives birth to her pup and after 7–10 days copulates with the male (Campagna and LeBoeuf, 1988a; Sielfeld, 1999; Acevedo et al., 2003). At the end of the breeding season, most of the males disperse for feeding and rest (Sepúlveda et al., 2001; Acevedo et al., 2003). Since pups are not able to swim long distances, females must remain with them in the colony, alternating their time between pup attendances on land and foraging trips in ˜ et al., 2012). Durthe ocean (Campagna and LeBoeuf, 1988a; Munoz ing the rest of the year (mid-March to mid-December), sea lions of all age and sex classes can be seen in the rookeries, although the number of sea lions hauled-out varies considerably in different months (Sepúlveda et al., 2001). Thus the breeding season constitutes a strong component that influences the haul-out patterns of this species. The main objective of this study was to determine the daily and seasonal haul-out patterns of different age/sex classes of a South American sea lion rookery during a period of 30 months. To our knowledge, this is the first study that analyzes the haul-out activity of South American sea lions in a breeding colony during almost three annual cycles considering age and sex categories differences as well. Material and methods This study was conducted at the Cobquecura breeding colony, situated in the central coast of Chile (36◦ 07 S, 72◦ 48 W) (Fig. 1). The Cobquecura colony is a chain of three rock formations, distant approximately 80–100 m from the coast. Cobquecura is the most important sea lion colony of the central Chilean coast, with nearly 2500 individuals (Sepúlveda et al., 2011).
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Field work took place from May 2008 to December 2010. The haul-out site was monitored 3–4 days/week by two observers simultaneously. For the final abundance estimate the average of the counts from both observers was used. A total of 222 days were analyzed during the study period. Observations were made from land at a distance of about 80 m from the colony. Aggregations of sea lions were counted using 10 × 15 binoculars and hand tally counters. Counts were conducted at 60-min intervals between 0830 and 1730. During the first year (May 2008 to May 2009), only the total number of sea lions was recorded. During the second part of the study (June 2009 to December 2010), individuals were classified according to age/sex categories as males, females, and juveniles (both sexes), including yearlings born during the previous season. Age and sex were determined from differences in size, body shape and/or coloration (Hamilton, 1934; King, 1983). Additionally a category called “unknown” was included for those animals which due to their location in the colony could not be assigned to any of the previous categories. For each month, sea lion counts were averaged for each time of the day, and then expressed as a proportion of the maximum number of sea lions. Thus the proportion of sea lions at the time of maximum haul-out abundance was one. This eliminated differences between months in the number of sea lions in the colony (Lake et al., 1997). To test whether the proportion of sea lions hauled-out varied significantly with time of day and if this changed among different months and years, a repeated measures analysis of variance (ANOVA) was used, with time of day (10 levels), month (12 levels), and time of day nested in years (2008–2010) as factors, and proportion of sea lions as the dependent variable. If a factor was significant, a Tukey HSD post hoc test was computed to test differences among factor levels. The data set utilized is the monthly average proportion of sea lions hauled-out at each time of day, considering samples from May 2008 to December 2010. Repeated measures analysis was computed because the same population was sequentially measured (Underwood, 1997). Proportion data was logit-transformed log /(1 − ) in order to satisfy the normality assumptions (Warton and Hui, 2011). The relation between the proportion of animals and the time of day and month was also analyzed separately for each age/sex category. Only males, females, and juveniles were considered, because pups were not differentiated from juveniles during the non-breeding months (March to December). As before, a repeated measures ANOVA was used for each category, with proportion (logit transformed) of sea lions as the dependent variable. Also, the Tukey HSD post hoc test was used to test differences among factor levels. The data set utilized was the monthly average proportion of sea lions hauled-out at each time of day, considering samples from June 2009 to December 2010. Repeated measures ANOVA is a statistical methodology highly recommended for analyzing ecological data in which only one unit is sampled over time, as is in our case. This avoids problems of pseudoreplication, taking into account the correlation over time of the successive sampling (Underwood, 1997; Von Ende, 2001). Additionally, in order to test differences in haul-out average daily proportions among males, females and juveniles, during breeding (December to March) and non-breeding seasons, a Kolmorogov–Smirnov two sample test was performed. All analyses were performed with the Statgraphics 15 GLM Module software package. Results For males, females and juveniles, significant differences in average haul-out proportion distributions were found for time of day, months, and also the interaction between these factors (Table 1).
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Table 1 ANOVA results showing the differences among age/sex classes. Statistically significant differences are marked in bold. d.f.
Hour of day (between years) Hour of day (within years) Month Hour × Month
10,60 9,10 11,60 99,60
Males
Females
Juveniles
F
P
F
P
F
P
1.44 6.31 2.88 2.24
0.1863 0.0040 0.0042 0.0005
0.53 15.83 3.53 2.58
0.8608 0.0001 0.0007 0.0001
0.99 11.48 3.07 3.58
0.4643 0.0004 0.0025 0.0000
Because time of day between years did not show differences for any of the categories considered, analyses considered pooled data for 2008–2010. In general, there was a marked diurnal trend in the number of sea lions present at the colony. Haul-out numbers rapidly increased towards the afternoon, with a peak in the frequency at approximately 13:30–16:30 (Fig. 2). This bell-shape trend showed significant differences between the peak hours and both extremes of the bell (earlier and later hours; Tukey HSD test, P < 0.05). The monthly average proportion also showed variability throughout the year (Fig. 3), especially during March, when male and juvenile proportions were noticeably lower than in the rest of
Fig. 2. Average proportion of total sea lions hauled-out during the day for (a) males; (b) females; and (c) juveniles in breeding (circles) and non-breeding (triangles) seasons.
the year (Fig. 3a and c; Tukey HSD test, P < 0.05). It must be noted, however, that the average value for this month included counts carried out during March 2010, just a couple of weeks after the 8.8 earthquake and posterior tsunami whose epicenter occurred off Cobquecura, where our study site is located. Table 2 shows the comparison of average daily haul-out proportion distributions among age/sex classes during the breeding (B) and non-breeding (NB) seasons. Throughout the NB period, males,
Fig. 3. Monthly average proportion of total sea lions hauled-out during the year for (a) males; (b) females; and (c) juveniles. Bars correspond to the HSD Tukey interval of 95% confidence. Non-overlapping intervals denote significant differences between mean values.
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Table 2 Kolmogorov–Smirnov test comparing hourly average haul-out proportion distribution among the three age/sex classes of sea lions (males, females, and juveniles) by breeding (B) and non-breeding (NB) seasons. Statistically significant differences are marked in bold.
NB Males B Males NB Females B Females NB Juveniles
B Males
NB Females
B Females
NB Juveniles
B Juveniles
D = 0.5P = 0.164
D = 0.1P = 0.999 D = 0.4P = 0.894
D = 0.4P = 0.405 D = 0.3P = 0.759 D = 0.4P = 0.405
D = 0.2P = 0.988 D = 0.4P = 0.405 D = 0.2P = 0.988 D = 0.4P = 0.405
D = 0.7P = 0.015 D = 0.7P = 0.014 D = 0.7P = 0.014 D = 0.6P = 0.055 D = 0.6P = 0.055
females, and juveniles exhibited similar daily timing of haul-out patterns (Fig. 2). In the B season, no differences in the daily timing of haul-out patterns were found between male and female sea lions. The proportion of both sexes remained relatively invariable in the colony during the day. However, there were significant differences between juveniles during the B season (B Juveniles) and males both during the B and NB seasons, and also between B Juveniles and NB females. There were also nearly significant differences between B Juveniles and B females (P = 0.055) and between B Juveniles and NB Juveniles (P = 0.055) (Table 2). Furthermore, the haul-out pattern of juveniles during the B season showed two peaks, one around 10:00 and the other at 15:30 (Fig. 2). Discussion This study shows that the number of animals in the Cobquecura breeding colony presented a periodicity associated with the time of day. Males, females and juveniles showed a clear and similar haul-out activity along the day. In general, fewer animals are on land during the morning and in the evening. The abundance in the rookery rapidly increases towards the afternoon, reaching a maximum from 13:30 to 16:30. After this period animals begin to leave the colony again. This indicates that the South American sea lion presents a clear daily haul-out pattern in the Cobquecura colony. These results are consistent with data reported by Sepúlveda et al. (2001) in two non-breeding colonies of O. flavescens in central Chile. Using a similar methodology, these authors found that during daylight hours the population increases, reaching a maximum peak during the early afternoon. A similar unimodal pattern with peak haul-out after midday has been documented in other species of pinnipeds, such as crabeater seals Lobodon carcinophaga (Bengston and Cameron, 2004; Southwell, 2005), harbor seals Phoca vitulina (Jemison et al., 2006), Weddell seals Leptonychotes weddellii (Lake et al., 1997), and New Zealand fur seals Arctocephalus forsteri (Stirling, 1968). At least two non-exclusive hypotheses can be formulated to explain the presence of this pattern. One of the hypotheses explaining similar daily patterns in different species of seals and sea lions is that the timing of haul-out may be in response to air temperature, with sea lions more likely to haul-out under conditions of low wind and high temperature (Carlens et al., 2006; Andrews-Goff et al., 2010). Studies of Weddell seals suggested that they haul-out in greater proportion when air temperatures are warmer (i.e. at midday) (Lake et al., 1997). In this study, the effects of air temperature could be especially important during the NB season (March to December), when air temperature is noticeably lower than in summer months. Therefore, it is likely that the timing of haul-outs is partly governed by thermoregulatory requirements. The other hypothesis to explain the timing of haul-out involves the behavior of both predator and prey. The daily curve, characterized by a maximum proportion of sea lions in the rockery during the day and a minimum during the night, seems to be determined by the feeding habits of their prey, which concentrate mainly on the surface during the night (Fraser et al., 1995). Thus the smaller number of sea lions during the morning and in the evening is likely to be due to individuals going to and returning from the sea to feed
at night when food is more accessible (Thompson et al., 1989; Soto et al., 2006). Several of the prey species that compose the diet of O. flavescens in the study area move to the surface at night, such as the jack mackerel Trachurus murphyi (Bertrand et al., 2004), common sardine Strangomera bentincki (Castillo et al., 2002) and anchovy Engraulis ringens (Castillo et al., 2002). Thus the nocturnal feeding of the South American sea lion may be favored by energy saving in terms of easier access to prey (Thompson et al., 1998; Sepúlveda et al., 2001). We found that sea lions shift their daily activity pattern over the year in response to changes in reproductive activities and thermoregulatory constraints. During the non-breeding period (fall, winter and spring seasons) all the age/sex classes showed a similar unimodal pattern, in which few sea lions are hauled-out in the morning and maximum numbers are found in the rookery during the early afternoon. In contrast, during the breeding season (austral summer), the proportion of individuals hauled-out shifted from a unimodal to a bimodal pattern, especially in the case of juveniles (Fig. 2). During the breeding season, juveniles showed two peaks of high abundance. Numbers were highest early in the morning, went down around midday and rose again during the afternoon. A similar bimodal pattern has been previously reported in sea lion species that inhabit tropical and subtropical coasts during the breeding season (e.g. Campagna and LeBoeuf, 1988b). These shifts of unimodal to bimodal patterns in response to an increase in the environmental heat load have been widely documented in the literature, both for ectotherms and endotherms (e.g. Porter et al., 1973; Kenagy et al., 2002; Díaz and Cabezas-Díaz, 2004), in which around midday animals avoid the high temperatures by returning to their burrows. Thus for juvenile sea lions leaving to the sea before the sun is at its peak and returning afterwards is probably a good behavioral strategy to reduce the stressful heat load during the hot summer midday hours (Soto et al., 2006). Although adult males and females may certainly be affected by thermal stress. They tended to remain relatively stable during the day, showing only a slightly bimodal pattern during the breeding season (Fig. 2). The explanation for this finding is that adults are heavily influenced by their breeding status during the breeding season (Reder et al., 2003). Males in particular cannot compromise their reproductive success and mating strategy for thermal stress, so they have no choice to avoid overheating and must remain in the colony during the entire day to defend their positions from other males (Campagna and LeBoeuf, 1988a,b). Females are also restricted to leave the colony in hot hours during the breeding season, both because their movements are retained by the territorial bulls and because after a foraging trip they remain on land to suckle ˜ et al., 2012). The requirement of both males and their pups (Munoz females to stay in the colony during the day favors a territorial system in which best territories contain water or are close to the water, thus reducing thermal stress (Capozzo, 2002). The patterns of seasonal variability in the South American sea lion haul-outs have important implications for planning surveys to estimate population abundance. Visual surveys should be best carried out when the maximum proportion of sea lions are hauledout, and when variability between age/sex classes in haul-out
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behavior is low (Southwell, 2005). However, the wide daily variation in haul-out patterns found in this study shows that counts need to be carefully timed to coincide with periods when this variation is minimal. Also, the variation in activity patterns by age/sex classes found in this study suggests that estimates of population parameters based on the composition of haul-out groups are unlikely to reflect the population structure (Thompson et al., 1989). This study indicated that months with a summer haul-out pattern are better for survey work with respect to availability, because in these months a relatively high proportion of sea lions from the different age and sex classes are hauled-out on land and the proportion is relatively invariant during the day, and consequently less adjustment needs to be made using haul-out correction factors (Bengston and Cameron, 2004). Fortunately, most of the surveys conducted on O. flavescens in Chile have been performed during summer, because high numbers of animals are recorded on land and because population estimates based on newborn pups could be made (Sepúlveda et al., 2011). If it is necessary to carry out censuses in other seasons of the year, it is recommended that the surveys be done after midday, when the hauled-out proportion of sea lions is highest, and when visibility and survey conditions are also better. In conclusion, South American sea lions from the Cobquecura colony show a predictable daily haul-out pattern during nonbreeding months, with a preference for after midday haul-out. However, this study found fine-scale differences in haul-out behavior between different age/sex classes of South American sea lions, as well as larger scale seasonal differences in haul-out site use. These differences appear to be greatly influenced by reproductive activities (e.g. pupping), food availability, and/or thermoregulatory requirements (Thompson and Harwood, 1990; Andrews-Goff et al., 2010), each of which requires specific behavioral adjustments. Acknowledgements This research is part of the Programa de Investigación Marina de Excelencia (PIMEX-Nueva Aldea) of the Faculty of Natural and Oceanographic Sciences of the University of Concepción, funded by Celulosa Arauco and Constitución S.A. We acknowledge Danilo ˜ Alegría, Omar Munoz and Eduardo Pedreros for their help in the field, and to Lafayette Eaton for language corrections. We also thank Rodrigo Veas for his help with the statistical analyses. References Acevedo, J., Aguayo-Lobo, A., Sielfeld, W., 2003. Eventos reproductivos del león marino común, Otaria flavescens (Shaw 1800), en el norte de Chile (Pacífico suroriental). Rev. Biol. Mar. Oceanogr. 38, 69–75. Ainley, D.G., Huber, H.R., Bailey, K.M., 1982. Population fluctuations of California sea lions and the Pacific whiting fishery off Central California. Fish. Bull. 80, 253–258. Andrews-Goff, V., Hindell, M.A., Field, I.C., Wheatley, K.E., Charrassin, J.B., 2010. Factors influencing the winter haulout behaviour of Weddell seals: consequences for satellite telemetry. Endang. Species Res. 10, 83–92. Bengston, J.L., Cameron, M.F., 2004. Seasonal haulout patterns of crabeater seals (Lobodon carcinophaga). Polar Biol. 27, 344–349. Bertrand, A., Barbieri, M.A., Córdova, J., Hernández, C., Gómez, F., Leiva, F., 2004. Diel vertical behaviour, predator–prey relationships, and occupation of space by jack mackerel (Trachurus murphyi) off Chile. ICES J. Mar. Sci. 61, 1105–1112. Calkins, D.G., Mallister, D.C., Pitcher, K.W., Pendleton, G.W., 1999. Steller sea lion status and trend in Southeast Alaska: 1979–1997. Mar. Mammal Sci. 15, 462–477. Capozzo, H.L., 2002. South American sea lion Otaria flavescens. In: Perrin, W.F., Würsig, B., Thewissen, J.G.M. (Eds.), Encyclopedia of Marine Mammals. Academic Press, San Diego, pp. 1143–1146.
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Mammalian Biology journal homepage: www.elsevier.de/mambio
Original Investigation
Daily and seasonal variation in the haul-out behavior of the South American sea lion b,c ˜ Maritza Sepúlveda a,∗ , Renato A. Quinones , Pablo Carrasco b , M. José Pérez-Álvarez a a
Centro de Investigación y Gestión en Recursos Naturales (CIGREN), Facultad de Ciencias, Universidad de Valparaíso, Av. Gran Breta˜ na 1111, Playa Ancha, Valparaíso, Chile Programa de Investigación Marina de Excelencia (PIMEX), Facultad de Ciencias Naturales y Oceanográficas, Casilla 160-C, Universidad de Concepción, Chile c Centro de Investigación Oceanográfica en el Pacífico Sur Oriental (COPAS), Departamento de Oceanografía, Facultad de Ciencias Naturales y Oceanográficas, Casilla 160-C, Universidad de Concepción, Chile b
a r t i c l e
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Article history: Received 5 September 2011 Accepted 9 March 2012 Keywords: Southern sea lion Otaria flavescens Haul-out activity Census time
a b s t r a c t In the South American sea lion (Otaria flavescens), daily fluctuations in abundance have been analyzed based on sequential counts of the number of animals hauled-out. However, no studies have analyzed haul-out activity in relation to an annual cycle or according to different age/sex classes. The objective of this study was to determine the daily and seasonal haul-out patterns of each age/sex class of South American sea lions as a function of the time of the day. A total of 222 days were analyzed in a breeding colony of Chile, from May 2008 to December 2010. During the non-breeding season (March to December) males, females, and juveniles showed a unimodal pattern, in which few sea lions are hauled-out in the morning and maximum numbers are found in the rookery during the early afternoon (1330–1630). In contrast, during the breeding season (austral summer) the proportion of individuals hauled-out shifted from a unimodal to a bimodal pattern, especially in the case of juveniles. Our results indicate that there are fine scale differences in haul-out behavior among age/sex classes, as well as larger scale seasonal differences in the proportion of sea lions ashore. These differences appear to be related to reproductive activities, food availability and thermoregulatory requirements. These patterns of seasonal variability of South American sea lion haul-out should be taken into consideration when planning surveys to estimate population abundance. © 2012 Deutsche Gesellschaft für Säugetierkunde. Published by Elsevier GmbH. All rights reserved.
Introduction Most seals and sea lions spend part of their lives in terrestrial habitats on land or ice to raise young, mate, molt, and rest (Riedman, 1990; Reder et al., 2003). However, the time these animals spend on land is highly variable, because it depends upon several factors that have been demonstrated to affect strongly their daily and seasonal terrestrial abundance and haul-out behavior, including prey availability, predator avoidance, thermoregulation, social activity, and environmental effects such as tides, weather, time of day and seasons (Reder et al., 2003). In particular, time of day has typically been examined to determine daily trends in haul-out patterns, relating the observed patterns to the ambient temperature, intensity of solar radiation and prey availability in the water column (Calkins et al., 1999). Understanding how the time of day influences daily and seasonal haul-out patterns is useful for gaining insight into how animals respond to environmental conditions in relation to their physiology (Lake et al., 1997), energy requirements (Thompson et al., 1998; Andrews-Goff et al., 2010), behavior
∗ Corresponding author. Tel.: +56 32 2508346; fax: +56 32 2508072. E-mail address: [email protected] (M. Sepúlveda).
(Thompson and Harwood, 1990) and life history (Sepúlveda et al., 2001). Daily fluctuations in the abundance of seals and sea lions have been mostly studied based on sequential counts of the number of animals hauled-out (e.g. Ainley et al., 1982; Thompson and Harwood, 1990; Lake et al., 1997; Reder et al., 2003). For the South American sea lion (Otaria flavescens), Sepúlveda et al. (2001), working with non-breeding colonies in central Chile, reported that few sea lions are hauled-out in the morning and maximum numbers of individuals are hauled-out in the afternoon. A similar result was found by Rosas et al. (1994) for a non-breeding colony in the Atlantic coast; they described a similar behavioral pattern in which groups go out from the colony at sunset and come back at sunrise, reaching the greatest number of animals on land at noon. Thompson et al. (1998), using satellite-linked data loggers on four females in the Falkland/Malvinas Islands, reported that the vast majority of the foraging trips were nocturnal; females spent more time ashore during the day. All of these studies suggest a strong diurnal component to South American sea lion haul-out behavior, with most individuals on land between mid morning and late afternoon. However, none of these studies analyzed the haul-out activity among different age/sex classes or during an entire annual cycle, therefore they collected only a narrow range of information.
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M. Sepúlveda et al. / Mammalian Biology 77 (2012) 288–292
Fig. 1. Map of the study area.
The South American sea lion exhibits a marked breeding period, which extends from about mid-December to mid-March (austral summer) (Acevedo et al., 2003). During this period males defend territories (breeding sites) and/or females (Campagna and LeBoeuf, 1988a,b; Capozzo, 2002), and stay in the colony during practically all of this period, fighting, mating and fasting (King 1983). Once arrived, a female gives birth to her pup and after 7–10 days copulates with the male (Campagna and LeBoeuf, 1988a; Sielfeld, 1999; Acevedo et al., 2003). At the end of the breeding season, most of the males disperse for feeding and rest (Sepúlveda et al., 2001; Acevedo et al., 2003). Since pups are not able to swim long distances, females must remain with them in the colony, alternating their time between pup attendances on land and foraging trips in ˜ et al., 2012). Durthe ocean (Campagna and LeBoeuf, 1988a; Munoz ing the rest of the year (mid-March to mid-December), sea lions of all age and sex classes can be seen in the rookeries, although the number of sea lions hauled-out varies considerably in different months (Sepúlveda et al., 2001). Thus the breeding season constitutes a strong component that influences the haul-out patterns of this species. The main objective of this study was to determine the daily and seasonal haul-out patterns of different age/sex classes of a South American sea lion rookery during a period of 30 months. To our knowledge, this is the first study that analyzes the haul-out activity of South American sea lions in a breeding colony during almost three annual cycles considering age and sex categories differences as well. Material and methods This study was conducted at the Cobquecura breeding colony, situated in the central coast of Chile (36◦ 07 S, 72◦ 48 W) (Fig. 1). The Cobquecura colony is a chain of three rock formations, distant approximately 80–100 m from the coast. Cobquecura is the most important sea lion colony of the central Chilean coast, with nearly 2500 individuals (Sepúlveda et al., 2011).
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Field work took place from May 2008 to December 2010. The haul-out site was monitored 3–4 days/week by two observers simultaneously. For the final abundance estimate the average of the counts from both observers was used. A total of 222 days were analyzed during the study period. Observations were made from land at a distance of about 80 m from the colony. Aggregations of sea lions were counted using 10 × 15 binoculars and hand tally counters. Counts were conducted at 60-min intervals between 0830 and 1730. During the first year (May 2008 to May 2009), only the total number of sea lions was recorded. During the second part of the study (June 2009 to December 2010), individuals were classified according to age/sex categories as males, females, and juveniles (both sexes), including yearlings born during the previous season. Age and sex were determined from differences in size, body shape and/or coloration (Hamilton, 1934; King, 1983). Additionally a category called “unknown” was included for those animals which due to their location in the colony could not be assigned to any of the previous categories. For each month, sea lion counts were averaged for each time of the day, and then expressed as a proportion of the maximum number of sea lions. Thus the proportion of sea lions at the time of maximum haul-out abundance was one. This eliminated differences between months in the number of sea lions in the colony (Lake et al., 1997). To test whether the proportion of sea lions hauled-out varied significantly with time of day and if this changed among different months and years, a repeated measures analysis of variance (ANOVA) was used, with time of day (10 levels), month (12 levels), and time of day nested in years (2008–2010) as factors, and proportion of sea lions as the dependent variable. If a factor was significant, a Tukey HSD post hoc test was computed to test differences among factor levels. The data set utilized is the monthly average proportion of sea lions hauled-out at each time of day, considering samples from May 2008 to December 2010. Repeated measures analysis was computed because the same population was sequentially measured (Underwood, 1997). Proportion data was logit-transformed log /(1 − ) in order to satisfy the normality assumptions (Warton and Hui, 2011). The relation between the proportion of animals and the time of day and month was also analyzed separately for each age/sex category. Only males, females, and juveniles were considered, because pups were not differentiated from juveniles during the non-breeding months (March to December). As before, a repeated measures ANOVA was used for each category, with proportion (logit transformed) of sea lions as the dependent variable. Also, the Tukey HSD post hoc test was used to test differences among factor levels. The data set utilized was the monthly average proportion of sea lions hauled-out at each time of day, considering samples from June 2009 to December 2010. Repeated measures ANOVA is a statistical methodology highly recommended for analyzing ecological data in which only one unit is sampled over time, as is in our case. This avoids problems of pseudoreplication, taking into account the correlation over time of the successive sampling (Underwood, 1997; Von Ende, 2001). Additionally, in order to test differences in haul-out average daily proportions among males, females and juveniles, during breeding (December to March) and non-breeding seasons, a Kolmorogov–Smirnov two sample test was performed. All analyses were performed with the Statgraphics 15 GLM Module software package. Results For males, females and juveniles, significant differences in average haul-out proportion distributions were found for time of day, months, and also the interaction between these factors (Table 1).
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Table 1 ANOVA results showing the differences among age/sex classes. Statistically significant differences are marked in bold. d.f.
Hour of day (between years) Hour of day (within years) Month Hour × Month
10,60 9,10 11,60 99,60
Males
Females
Juveniles
F
P
F
P
F
P
1.44 6.31 2.88 2.24
0.1863 0.0040 0.0042 0.0005
0.53 15.83 3.53 2.58
0.8608 0.0001 0.0007 0.0001
0.99 11.48 3.07 3.58
0.4643 0.0004 0.0025 0.0000
Because time of day between years did not show differences for any of the categories considered, analyses considered pooled data for 2008–2010. In general, there was a marked diurnal trend in the number of sea lions present at the colony. Haul-out numbers rapidly increased towards the afternoon, with a peak in the frequency at approximately 13:30–16:30 (Fig. 2). This bell-shape trend showed significant differences between the peak hours and both extremes of the bell (earlier and later hours; Tukey HSD test, P < 0.05). The monthly average proportion also showed variability throughout the year (Fig. 3), especially during March, when male and juvenile proportions were noticeably lower than in the rest of
Fig. 2. Average proportion of total sea lions hauled-out during the day for (a) males; (b) females; and (c) juveniles in breeding (circles) and non-breeding (triangles) seasons.
the year (Fig. 3a and c; Tukey HSD test, P < 0.05). It must be noted, however, that the average value for this month included counts carried out during March 2010, just a couple of weeks after the 8.8 earthquake and posterior tsunami whose epicenter occurred off Cobquecura, where our study site is located. Table 2 shows the comparison of average daily haul-out proportion distributions among age/sex classes during the breeding (B) and non-breeding (NB) seasons. Throughout the NB period, males,
Fig. 3. Monthly average proportion of total sea lions hauled-out during the year for (a) males; (b) females; and (c) juveniles. Bars correspond to the HSD Tukey interval of 95% confidence. Non-overlapping intervals denote significant differences between mean values.
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Table 2 Kolmogorov–Smirnov test comparing hourly average haul-out proportion distribution among the three age/sex classes of sea lions (males, females, and juveniles) by breeding (B) and non-breeding (NB) seasons. Statistically significant differences are marked in bold.
NB Males B Males NB Females B Females NB Juveniles
B Males
NB Females
B Females
NB Juveniles
B Juveniles
D = 0.5P = 0.164
D = 0.1P = 0.999 D = 0.4P = 0.894
D = 0.4P = 0.405 D = 0.3P = 0.759 D = 0.4P = 0.405
D = 0.2P = 0.988 D = 0.4P = 0.405 D = 0.2P = 0.988 D = 0.4P = 0.405
D = 0.7P = 0.015 D = 0.7P = 0.014 D = 0.7P = 0.014 D = 0.6P = 0.055 D = 0.6P = 0.055
females, and juveniles exhibited similar daily timing of haul-out patterns (Fig. 2). In the B season, no differences in the daily timing of haul-out patterns were found between male and female sea lions. The proportion of both sexes remained relatively invariable in the colony during the day. However, there were significant differences between juveniles during the B season (B Juveniles) and males both during the B and NB seasons, and also between B Juveniles and NB females. There were also nearly significant differences between B Juveniles and B females (P = 0.055) and between B Juveniles and NB Juveniles (P = 0.055) (Table 2). Furthermore, the haul-out pattern of juveniles during the B season showed two peaks, one around 10:00 and the other at 15:30 (Fig. 2). Discussion This study shows that the number of animals in the Cobquecura breeding colony presented a periodicity associated with the time of day. Males, females and juveniles showed a clear and similar haul-out activity along the day. In general, fewer animals are on land during the morning and in the evening. The abundance in the rookery rapidly increases towards the afternoon, reaching a maximum from 13:30 to 16:30. After this period animals begin to leave the colony again. This indicates that the South American sea lion presents a clear daily haul-out pattern in the Cobquecura colony. These results are consistent with data reported by Sepúlveda et al. (2001) in two non-breeding colonies of O. flavescens in central Chile. Using a similar methodology, these authors found that during daylight hours the population increases, reaching a maximum peak during the early afternoon. A similar unimodal pattern with peak haul-out after midday has been documented in other species of pinnipeds, such as crabeater seals Lobodon carcinophaga (Bengston and Cameron, 2004; Southwell, 2005), harbor seals Phoca vitulina (Jemison et al., 2006), Weddell seals Leptonychotes weddellii (Lake et al., 1997), and New Zealand fur seals Arctocephalus forsteri (Stirling, 1968). At least two non-exclusive hypotheses can be formulated to explain the presence of this pattern. One of the hypotheses explaining similar daily patterns in different species of seals and sea lions is that the timing of haul-out may be in response to air temperature, with sea lions more likely to haul-out under conditions of low wind and high temperature (Carlens et al., 2006; Andrews-Goff et al., 2010). Studies of Weddell seals suggested that they haul-out in greater proportion when air temperatures are warmer (i.e. at midday) (Lake et al., 1997). In this study, the effects of air temperature could be especially important during the NB season (March to December), when air temperature is noticeably lower than in summer months. Therefore, it is likely that the timing of haul-outs is partly governed by thermoregulatory requirements. The other hypothesis to explain the timing of haul-out involves the behavior of both predator and prey. The daily curve, characterized by a maximum proportion of sea lions in the rockery during the day and a minimum during the night, seems to be determined by the feeding habits of their prey, which concentrate mainly on the surface during the night (Fraser et al., 1995). Thus the smaller number of sea lions during the morning and in the evening is likely to be due to individuals going to and returning from the sea to feed
at night when food is more accessible (Thompson et al., 1989; Soto et al., 2006). Several of the prey species that compose the diet of O. flavescens in the study area move to the surface at night, such as the jack mackerel Trachurus murphyi (Bertrand et al., 2004), common sardine Strangomera bentincki (Castillo et al., 2002) and anchovy Engraulis ringens (Castillo et al., 2002). Thus the nocturnal feeding of the South American sea lion may be favored by energy saving in terms of easier access to prey (Thompson et al., 1998; Sepúlveda et al., 2001). We found that sea lions shift their daily activity pattern over the year in response to changes in reproductive activities and thermoregulatory constraints. During the non-breeding period (fall, winter and spring seasons) all the age/sex classes showed a similar unimodal pattern, in which few sea lions are hauled-out in the morning and maximum numbers are found in the rookery during the early afternoon. In contrast, during the breeding season (austral summer), the proportion of individuals hauled-out shifted from a unimodal to a bimodal pattern, especially in the case of juveniles (Fig. 2). During the breeding season, juveniles showed two peaks of high abundance. Numbers were highest early in the morning, went down around midday and rose again during the afternoon. A similar bimodal pattern has been previously reported in sea lion species that inhabit tropical and subtropical coasts during the breeding season (e.g. Campagna and LeBoeuf, 1988b). These shifts of unimodal to bimodal patterns in response to an increase in the environmental heat load have been widely documented in the literature, both for ectotherms and endotherms (e.g. Porter et al., 1973; Kenagy et al., 2002; Díaz and Cabezas-Díaz, 2004), in which around midday animals avoid the high temperatures by returning to their burrows. Thus for juvenile sea lions leaving to the sea before the sun is at its peak and returning afterwards is probably a good behavioral strategy to reduce the stressful heat load during the hot summer midday hours (Soto et al., 2006). Although adult males and females may certainly be affected by thermal stress. They tended to remain relatively stable during the day, showing only a slightly bimodal pattern during the breeding season (Fig. 2). The explanation for this finding is that adults are heavily influenced by their breeding status during the breeding season (Reder et al., 2003). Males in particular cannot compromise their reproductive success and mating strategy for thermal stress, so they have no choice to avoid overheating and must remain in the colony during the entire day to defend their positions from other males (Campagna and LeBoeuf, 1988a,b). Females are also restricted to leave the colony in hot hours during the breeding season, both because their movements are retained by the territorial bulls and because after a foraging trip they remain on land to suckle ˜ et al., 2012). The requirement of both males and their pups (Munoz females to stay in the colony during the day favors a territorial system in which best territories contain water or are close to the water, thus reducing thermal stress (Capozzo, 2002). The patterns of seasonal variability in the South American sea lion haul-outs have important implications for planning surveys to estimate population abundance. Visual surveys should be best carried out when the maximum proportion of sea lions are hauledout, and when variability between age/sex classes in haul-out
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behavior is low (Southwell, 2005). However, the wide daily variation in haul-out patterns found in this study shows that counts need to be carefully timed to coincide with periods when this variation is minimal. Also, the variation in activity patterns by age/sex classes found in this study suggests that estimates of population parameters based on the composition of haul-out groups are unlikely to reflect the population structure (Thompson et al., 1989). This study indicated that months with a summer haul-out pattern are better for survey work with respect to availability, because in these months a relatively high proportion of sea lions from the different age and sex classes are hauled-out on land and the proportion is relatively invariant during the day, and consequently less adjustment needs to be made using haul-out correction factors (Bengston and Cameron, 2004). Fortunately, most of the surveys conducted on O. flavescens in Chile have been performed during summer, because high numbers of animals are recorded on land and because population estimates based on newborn pups could be made (Sepúlveda et al., 2011). If it is necessary to carry out censuses in other seasons of the year, it is recommended that the surveys be done after midday, when the hauled-out proportion of sea lions is highest, and when visibility and survey conditions are also better. In conclusion, South American sea lions from the Cobquecura colony show a predictable daily haul-out pattern during nonbreeding months, with a preference for after midday haul-out. However, this study found fine-scale differences in haul-out behavior between different age/sex classes of South American sea lions, as well as larger scale seasonal differences in haul-out site use. These differences appear to be greatly influenced by reproductive activities (e.g. pupping), food availability, and/or thermoregulatory requirements (Thompson and Harwood, 1990; Andrews-Goff et al., 2010), each of which requires specific behavioral adjustments. Acknowledgements This research is part of the Programa de Investigación Marina de Excelencia (PIMEX-Nueva Aldea) of the Faculty of Natural and Oceanographic Sciences of the University of Concepción, funded by Celulosa Arauco and Constitución S.A. We acknowledge Danilo ˜ Alegría, Omar Munoz and Eduardo Pedreros for their help in the field, and to Lafayette Eaton for language corrections. We also thank Rodrigo Veas for his help with the statistical analyses. References Acevedo, J., Aguayo-Lobo, A., Sielfeld, W., 2003. Eventos reproductivos del león marino común, Otaria flavescens (Shaw 1800), en el norte de Chile (Pacífico suroriental). Rev. Biol. Mar. Oceanogr. 38, 69–75. Ainley, D.G., Huber, H.R., Bailey, K.M., 1982. Population fluctuations of California sea lions and the Pacific whiting fishery off Central California. Fish. Bull. 80, 253–258. Andrews-Goff, V., Hindell, M.A., Field, I.C., Wheatley, K.E., Charrassin, J.B., 2010. Factors influencing the winter haulout behaviour of Weddell seals: consequences for satellite telemetry. Endang. Species Res. 10, 83–92. Bengston, J.L., Cameron, M.F., 2004. Seasonal haulout patterns of crabeater seals (Lobodon carcinophaga). Polar Biol. 27, 344–349. Bertrand, A., Barbieri, M.A., Córdova, J., Hernández, C., Gómez, F., Leiva, F., 2004. Diel vertical behaviour, predator–prey relationships, and occupation of space by jack mackerel (Trachurus murphyi) off Chile. ICES J. Mar. Sci. 61, 1105–1112. Calkins, D.G., Mallister, D.C., Pitcher, K.W., Pendleton, G.W., 1999. Steller sea lion status and trend in Southeast Alaska: 1979–1997. Mar. Mammal Sci. 15, 462–477. Capozzo, H.L., 2002. South American sea lion Otaria flavescens. In: Perrin, W.F., Würsig, B., Thewissen, J.G.M. (Eds.), Encyclopedia of Marine Mammals. Academic Press, San Diego, pp. 1143–1146.
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