Aspects of behavioral ecology of Sotalia guianensis in Sepetiba Bay, southeast Brazil

MARINE MAMMAL SCIENCE, 24(3): 503–515 (July 2008)

C 2008 by the Society for Marine Mammalogy DOI: 10.1111/j.1748-7692.2008.00198.x

Aspects of behavioral ecology of Sotalia guianensis in Sepetiba Bay, southeast Brazil LEONARDO FLACH Projeto Boto Cinza, Rua Sta Terezinha, 531, Muriqui, 23870-000 Mangaratiba, Rio de Janeiro, Brazil and Whale Unit, Mammal Research Institute, University of Pretoria, c/o P.O. Box 61, Cape Town 8000, South Africa E-mail: flachleo@hotmail.com

PATRICIA A. FLACH Projeto Boto Cinza, Rua Sta Terezinha, 531, Muriqui, 23870-000 Mangaratiba, Rio de Janeiro, Brazil

ADRIANO G. CHIARELLO Programa de P´os-graduac¸a˜ o em Zoologia de Vertebrados, PUC-Minas, Avenida Dom Jos´e Gaspar 500, Pr´edio 41, Belo Horizonte, Brazil, 30.535-610

ABSTRACT Boat-based surveys were conducted from August 2002 to July 2003 to study the activity patterns, spatial pattern of area use, and group characteristics of Sotalia guianensis in Sepetiba Bay, southeast Brazil. Predetermined routes covered the entrance and interior of the bay, resulting in 210 dolphin sightings during 3,300 km total effort. Data on activity were collected using scan group sampling with instantaneous recording after 5 min of observation. Dolphins were sighted more frequently in the entrance of the bay, where water is deeper, and salinity and transparency are higher, than in the interior of the bay, where the environment is more influenced by freshwater inputs. Foraging and feeding were the most frequent activities, and occurred predominantly between 0600 and 1000. Foraging and feeding peaked during ebbing, low, and flooding tides, while socializing predominated at high tide. Mean group size was larger in the interior of the bay and when seabirds were present. Large aggregations containing >100 individuals of Sotalia guianensis seen year-round indicate that Sepetiba Bay is an important area for this species in coastal Brazil.

Key words: activity pattern, Sotalia guianensis, habitat use, group size, Rio de Janeiro.

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Dolphin activity patterns can be influenced by time of day, season, water depth, bottom topography, tide flow, and human activities (Shane 1990). In addition, the dolphins’ responses to these ecological variables are somewhat unpredictable and can differ depending on the habitat in which the animals are studied (Shane 1990).

The study of activity patterns is important as this parameter is one of the prime factors directly influencing the group size and, indirectly, the social organization of dolphins (Shane et al. 1986). Also, activity rhythms of animals reflect adaptation to seasonal and diurnal variations of environmental factors and are a result of a complex compromise between optimal foraging/feeding time, social activities, and environmental constraints (Nielsen 1983).

Based on differing morphometry and genetics, the genus Sotalia has been divided into two species, the riverine species S. fluviatilis and the marine species S. guianensis (Monteiro-Filho et al. 2002, Cunha et al. 2005, Cabalero et al. 2007). S. guianensis is perhaps one of the most commonly observed and best studied coastal dolphins in the southwest Atlantic Ocean. The broad pattern of distribution of S. guianensis along the coasts of Central and South America is well known. Although many aspects of its natural history, behavior, reproduction, geographic fidelity, and home range have been studied, few studies have been published (da Silva and Best 1996, Ramos et al.

2000, Santos et al. 2001, Rosas and Monteiro-Filho 2002, Flores and Bazzalo 2004).

Therefore, details of fine-scale spatial and temporal distribution, patterns of area use, and group characteristics are scarce in the literature.

Threats to S. guianensis from bycatch, chemical pollutants, and loss of important habitat (e.g., mangroves), are significant (Reeves et al. 2003). Thus, factors affecting habitat use, activity, and social dynamics are critical for assessing their conservation and management status. The goals of this study were to: (1) investigate the spatial and temporal distribution pattern of S. guianensis population in southeast Brazil, (2) verify how activities and spatial area usage relate to environmental parameters, and (3) describe group characteristics of S. guianensis in the Sepetiba Bay region.

MATERIAL AND METHODS Study Area Sepetiba Bay is located in the southern part of Rio de Janeiro State (22◦ 54 –23◦ 04 , 43◦ 36 –44◦ 02 W) spanning 526 km2 with an average depth of 8.0 m and dredged channels 20–30 m deep. In this study the bay was sectioned into two regions (entrance and interior) due to its environmental differences (Fig. 1). The northern portion is bordered by mountain chains and sand beaches separated by rocky shores. At the western part lies the entrance, with a number of islands, rocks, and the main connection to the Atlantic Ocean. This area, influenced by open waters, has a sand and gravel substrate, high salinity, and high transparency. The eastern part (interior) has extensive mangrove areas with river drainage systems that contribute most of the mud and ´ silt substrate, as well as low salinity, transparency, and depths (Pessanha and Araujo 2003) (Fig. 1). Despite its high number of habitats and species diversity, the bay suffers from increasing industrial outflows, port activities, losses of mangrove areas, ´ and Azevedo 2001, Pessanha and Araujo ´ and industrial fishing activities (Araujo 2003).

Field Methods Three months of pilot surveys were carried out to investigate the best sampling protocols and to construct an ethogram (Table 1). Moreover, 64 h of total effort

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Figure 1. Distribution of sightings of Sotalia guianensis in Sepetiba Bay during winter ( ) and summer (◦). The vertical line shows where the bay was divided into interior and entrance for analysis purposes (see Methods). Map and GIS processing by Andr´e Hirsch.

(24 h searching for the animals and 40 h of direct observation) were used to train the observers. After that, data were collected from 12 mo from August 2002 to July 2003.

During this period, 78 survey days traversed 3,300 km (entrance: 1,873 km; interior: 1,427 km) covering an area of 455 km2 (entrance: 205 km2 ; interior: 250 km2 ) and produced 210 dolphin sightings during “good” sea state (Beaufort 0–3). Thus, we sampled on average 1 group/day (interior) to 4.3 groups/day (entrance). For these 210 sightings, a total of 317 h of effort was spent, with 224 h searching for the dolphins and 93 h in direct observation.

Two observers in a 7.5-m boat equipped with a 225-hp outboard engine conducted the surveys. Line transects were established in order to cover the entire area of the bay and thus to assess different habitat characteristics used by the dolphins. These transects were covered at an average speed of 12–15 km/h. Starting positions and time of day were alternated randomly for each survey, and starting time of each survey was recorded to register the number of hours spent searching for the dolphins Table 1. Ethogram of S. guianensis in Sepetiba Bay. Activity Forage-feed Social Travel Rest Unknown

Definition Surface behavior characterized by repeated, fast and arched dives, changing directions suddenly and concentrating in one location.

Some individuals of the group in physical contact, spending most of the time at the surface with one another, rubbing, rolling, chasing, and also displaying leaps, tail slaps, belly up, and other surface behavior.

Moving steadily in one direction and showing body not arched, often in constant speed and sometimes presenting porpoise and leaps.

Slow movement at the surface, dorsal fin exposed, body little arched.

Moving in various directions in one location, showing no surface behavior.

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and in direct observation effort. When a group of dolphins was sighted the boat was stopped and search effort suspended. Then a quick approach to the group was taken to collect data on time, position, group size, group composition, and behavior activity. The behavior activities were recorded using the scan group sampling with instantaneous recording after 5 min of observation (Altmann 1974, Mann 1999).

Associations between dolphins and marine birds such as frigates, Fregata magnificens, boobies, Sula leucogaster, and terns, Sterna sp., were recorded. After data collection was complete, the time was registered and the route was resumed from the point where it was interrupted.

Definitions and Analysis Each time a group of dolphins was detected, it was recorded as a sighting (after Karczmarski 1999). Five categories of activity were distinguished (adapted from Shane 1990 and Karczmarski and Cockcroft 1999) (Table 1). Age categories were classified as neonate, calf, juvenile, and adult (see Shane 1990). The term “group” refers to dolphins that were detected visually by the observers forming one or several subgroups next to another and in an apparent association and engaged in similar activities. The term “large aggregations” in this study refers to groups containing >100 dolphins usually engaged in predominantly foraging/feeding or socializing activities (see Norris and Dohl 1980, Norris and Schilt 1988). Environmental parameters, including surface water temperature, turbidity, salinity, and depth were measured for each sighting position using a thermometer, secchi disc, refractometer, and fish finder, respectively. Tidal state (high, ebbing, low, flooding) was categorized using a tidal chart, and spring and neap tides were considered for the analysis. The high and low tides lasted 1 h each and the rest of the time was assigned to flooding and ebbing tides. In order to estimate water depth availability, a nautical chart of Sepetiba Bay was divided into squares of 30 of latitude and longitude, with water depth from each vertex (n = 442) used as a proxy of depth availability.

Two seasons (winter and summer) were distinguished using the annual mean sea surface temperature (25.6◦ C), an approach adopted from Karczmarski et al. (1999).

In general sea surface temperatures were below the annual mean (25.6◦ C) in winter (May–October) and above this value in summer (November–April) (see Results). The Mann-Whitney test was used to check for seasonal differences (winter vs. summer) in water parameters (depth, temperature, salinity, and turbidity) and in group size.

The chi-square test was used to check if depth of dolphin sightings varied according to depth availability in the bay, as measured above, and also to contrast activity frequency between seasons and time of day. All expected frequencies were calculated proportional to sample effort. A statistical table (Rohlf and Sokal 1981) was used to find the significance (P) for the chi-square test. The Kruskal-Wallis test was used to check if water parameters differed among categories of activity (one test for each water parameter), and if group size differed among categories of activity.

RESULTS Spatial Distribution and Environmental Parameters of Sightings Sightings were more frequent (80.5%, n = 169) in the entrance of the bay than in the interior (19.5%, n = 41) (chi-square with Yates correction: 2 = 48.055, df = 1,

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Table 2. Seasonal variation in water parameters collected during sightings of S. guianensis in Sepetiba Bay. Season

Depth (m)

Temperature (◦ C)

Salinity (‰)

Turbidity (m)

Winter Summer Mann-Whitney U P

11.37 11.4 5348 0.938

23.89 26.71 938.5 0

31.29 30.82 4235 0.01

3.38 3.06 2412.5 0.098

P < 0.001) (Fig. 1). This sighting frequency did not vary by seasons ( 2 = 0.469, df = 1, P = 0.493).

Sightings recorded in winter showed lower water temperature and higher water salinity than summer sightings (Table 2). Sightings that occurred in the entrance of the bay, closer to the open ocean, were in deeper water of higher salinity and less turbidity (higher Secchi values) than sightings in the interior of the bay (Table 3).

The dolphins were recorded less frequently than expected at depths <6 m and more than expected at depths >11 m (Fig. 2) ( 2 = 120.806, df = 3, P < 0.001).

Activity Patterns The behavior observed most frequently was foraging/feeding (62.9% of sightings), followed by unknown (13.3%) and traveling (11.0%), while socializing (7.6%) and resting (5.2%) were the least frequently observed behaviors. This pattern of activity was similar between areas ( 2 = 3.036, df = 4, P > 0.100) and between seasons ( 2 = 4.445, df = 4, P > 0.100). Frequency of activities varied significantly according to time of the day ( 2 = 19.752, df = 8, P < 0.001): foraging/feeding peaked in early morning (0600–1000) while resting and social activities were more frequently seen in the afternoon (1400–1800) (Fig. 3).

Activity did not differ based on temperature [Kruskal-Wallis test: temperature (H = 1.734, df = 3, P = 0.629); salinity (H = 1.724, df = 3, P = 0.623); turbidity (H = 5.858, df = 3, P = 0.119), and water depth (H = 1.421, df = 3, P = 0.701)].

However, significant differences were detected in relation to (spring) tides ( 2 = 21.438, df = 3, P < 0.040), with higher frequency of foraging/feeding during low, flooding and ebbing tides, and higher frequency of socializing during high tides (Fig. 4).

Table 3. Differences between entrance and interior of the bay in water parameters collected during sightings of S. guianensis in Sepetiba Bay. Area 2

Entrance (205 km ) Interior (250 km2 ) Mann-Whitney U P

Depth (m)

Temperature (◦ C)

Salinity (‰)

Turbidity (m)

12.14 8.29 1877 0

25.48 25.59 3122 0.728

31.35 29.68 1769 0

3.29 2.8 1609 0.029

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Frequency

100 80 60 40

20 0

<6

6 to < 11

11 to <16

â&#x2030;Ľ 16

Depth category (m) Figure 2. Observed ( ) and expected ( ) frequency of sighting of S. guianensis by water depth at Sepetiva Bay. Expected frequencies were calculated proportionate to the bathymetry (see Methods).

Group Characteristics Group size ranged from one to approximately 280 dolphins (mean = 30.2, SE = 3.43, median = 12) and was significantly larger in the interior (70.9, SE = 13.2 dolphins/group) than at the entrance of the bay (20.5, SE = 2.29 dolphins/group) (MannWhitney, U = 2,250, P < 0.0001). Group sizes were highly variable. Most groups (68%) contained between two and 20 dolphins (n = 142), while large aggregations

Figure 3. Percentage occurrence of main group activities of S. guianensis at Sepetiba Bay during three time periods.

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Figure 4. Group activity frequency of S. guianensis according to different spring tide type in Sepetiba Bay.

accounted for 7% of the sightings (n = 14) and were present year-round (Fig. 5).

Group size did not vary significantly between seasons (Mann-Whitney, U = 5,358, P = 0.850) and changed little with behavior (Kruskal-Wallis, H = 7.587, df = 3, P = 0.056). Solitary dolphins were observed on only two occasions. Sea birds were observed in association with dolphins on 32 occasions. In the majority of these observed associations with seabirds (n = 31) dolphins were feeding (in the remaining case they were socializing). Dolphin groups with seabirds present were larger (mean = 58.9, SE = 13.0, n = 32) than groups without birds (mean = 25.0, SE = 3.1, n = 178) (Mann-Whitney, U = 1,570, P < 0.0001). Among seabirds, the most common association was between dolphins and boobies (Sula leucogaster, 50.0%), followed by terns (Sterna sp., 15.6%) frigates (Fregata magnificens, 9.4%), or mixed birds association (terns/boobies, 15.6%) and (boobies/frigates, 9.4%).

40 30 20

Figure 5. Frequency distribution of S. guianensis group size in Sepetiba Bay.

> 100

66- 70

61- 65

56- 60

51- 55

71- 100

Group Size

46- 50

41- 45

36- 40

31- 35

26- 30

21- 25

16- 20

11- 15

0

6-10

10

1-5

Frequency

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DISCUSSION Spatial Distribution and Environmental Parameters of Sightings This study shows that S. guianensis uses the entrance of the bay most often, where water is deeper, with higher salinity and transparency, clearly a result of stronger ´ et al. (2002), these environmental influence of open water. According to Araujo characteristics, together with a sea bottom relief of rocks and channels, allow higher fish diversity with little variability throughout the year in the entrance of Sepetiba Bay. This stable fish assemblage is perhaps the main reason for preference of S. guianensis for this part of the bay. The dolphins were observed more often than expected in areas with depths over 11 m, showing an intense utilization of deep areas with steep bottom, within channels, and near rocks. A similar pattern of sightings concentrated in deeper waters is known for Guanabara Bay, Rio de Janeiro State (Azevedo et al.

2007), although most other studies indicate that S. guianensis uses areas with depths <6 m (Lodi 2003, Flores and Bazzalo 2004, Daura-Jorge et al. 2005). Studies of other species, such as bottlenose and humpback dolphins, also showed preferences for deep areas and channels, which might host a greater concentration of prey (Maze ¨ and Wursig 1999, Jefferson 2000, Hastie et al. 2004). However, humpback dolphins of South Africa and bottlenose dolphins of Argentine are confined to shallow waters ¨ ¨ and rock shores (Wursig and Wursig 1979, Karczmarski et al. 2000), indicating that dolphins adapt to local conditions and thus depth preference is, perhaps, locationspecific.

Activity Patterns The high frequency of foraging/feeding activity observed in this study was also ¨ observed by others authors working with other species and S. guianensis (Wursig and ¨ Wursig 1980, Br¨ager 1993, Karczmarski and Cockcroft 1999, Daura-Jorge et al.

2005, Azevedo et al. 2007). Possible reasons include the mobility and size of small cetaceans, such as S. guianensis and other small odontocete species, which must feed often to fuel their high field metabolic rate (Costa and Williams 1999). Neither the entrance nor the interior was used preferentially by S. guianensis to engage in specific activities, similar to what has been observed with this species at Guanabara Bay (Azevedo et al. 2007) and humpback dolphins in Hong Kong waters ( Jefferson 2000). Nonetheless, S. guianensis used specific areas for given activities in southern Brazil (Daura-Jorge et al. 2005). The relatively small variation of sea surface water temperature throughout the year (when compared to higher latitudes) and the small ´ et al. 2002, Pessanha and Araujo ´ 2003), might fluctuation of prey abundance (Araujo explain the lack of seasonal differences in activity patterns in Sepetiba Bay, which is also observed in Guanabara Bay (Azevedo et al. 2007). On the other hand, at Norte Bay (Santa Catarina State, Brazil), the southernmost limit of distribution of the species, higher fluctuations in sea surface temperature and food resources influenced activity patterns of S. guianensis, which changed seasonally (Daura-Jorge et al. 2005). It is important to note, however, that in this study relatively large areas were compared and microhabitats were not discriminated between the entrance and interior. Also, the groups of dolphins were not followed all day long, raising the possibility that the results could be different if such approaches were chosen. Therefore, the apparent absence of seasonal and spatial variation in activity patterns at Sepetiba Bay should be interpreted cautiously.

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The early morning foraging/feeding activity peaks are similar to those reported for other S. guianensis and bottlenose dolphins (Hanson and Defran 1993, Bearzi et al. 1999, Daura-Jorge et al. 2005, Azevedo et al. 2007). This probably relates to the higher necessity of energy intake in early morning or to diel variation in prey activity/availability because food resource can be more active, concentrated, or accessible during certain times of the day or at certain points of the tidal cycle (Stevick et al. 2002). The decrease in light intensity at dusk and its increase at dawn serves as signals of change in biotic environmental conditions, which is reflected in the behavior of fish (Hobson 1972, McFarland 1991). In this regard, it is possible that the prey of S. guianensis is more accessible and susceptible to being captured during the crepuscular transition, as observed for bottlenose dolphins in coastal California (Hanson and Defran 1993). On the other hand, the socializing and resting activity were more frequent in the afternoon, indicating either that food resource is less available or more difficult to capture during this time of day, as observed for S. guianensis and bottlenose and humpback dolphins (Shane 1990, Br¨ager 1993, Karczmarski and Cockcroft 1999, Azevedo et al. 2007).

In Sepetiba Bay water parameters such as depth, surface temperature, turbidity, and salinity did not affect the activity patterns of the dolphins. These variables are known to influence the distribution and abundance of those fish species that are most ´ 2002, Araujo ´ et al. 2002, Pessanha common in Sepetiba Bay (da Costa and Araujo ´ 2003, Pessanha et al. 2003). Because distribution of cetaceans is often and Araujo linked with the distribution and abundance of their prey (Barros and Wells 1998) such variables may play a more important role in the spatial distribution of the dolphins than to their behavioral activities. Of all the environmental parameters tested, only the spring tides significantly influenced behavioral activities. The peaks of foraging/feeding activities were observed during low, flooding and ebbing tides, which according to local fisherman, correspond with movements of schooling fish in and out of the bay. Socializing activity was more frequent during high tides following flood tides, indicating that dolphins may prefer to socialize during high slack water, and after feeding in more prey-rich tides. A similar sequence of behavior associated with the tidal cycle was also reported for bottlenose dolphins in the Adriatic Sea (Bearzi et al. 1999). In Guanabara Bay, however, the tidal cycle and depth did not affect the behavioral activities of the dolphins (Azevedo et al. 2007).

Group Characteristics The mean group size of S. guianensis in this study (30.2 individuals) is one of the largest observed for the species, comparable only with group sizes in Paraty Bay (Rio de Janeiro State, Brazil) (32.4 individuals) and Norte Bay (Santa Catarina State, Brazil) (29 individuals) (Lodi 2003, Daura-Jorge et al. 2005, Flores and Fontoura 2006). Most studies of S. guianensis report mean group sizes ranging from 3 to 13 dolphins (Di Beneditto et al. 2001, Edwards and Schnell 2001, Azevedo et al. 2005, Spinelli et al. ´ and Azevedo (2001), Sepetiba and Paraty bays share the 2006). According to Araujo same fish assemblages that form large schools and are distinct from other estuaries and bays of south and southeast Brazil. Apart from Sepetiba, large aggregations of S. guianensis such as reported here, have been observed only in Paraty (Lodi 2003), perhaps reflecting similarities in the food base mentioned above. The dolphin group sizes were larger during the interactions with seabirds (mostly boobies), which is probably linked to large schools of fish that attracts both large groups of dolphins

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and seabirds. The foraging/feeding behavior was the predominant activity observed during such interactions. Similar results have been reported for dusky dolphins in New Zealand (Markowitz et al. 2004).

The largest group sizes occurred during socializing and smallest during traveling activities, although the difference was marginally significant. Similarly, as seen in bottlenose dolphins along the coast of the southern United States (Maze-Foley and ¨ Wursig 2002, Shane 2004), the S. guianensis at Guanabara Bay also showed largest groups during socializing activities (Azevedo et al. 2005). In contrast, in other areas (Lodi 2003, Daura-Jorge et al. 2005) the larger groups of S. guianensis were observed during foraging/feeding. Clearly, activity pattern is one of the factors influencing the group size of different species of dolphins, including S. guianensis. The lack of significant seasonal changes in group size of dolphins corresponds with findings in other studies (Azevedo et al. 2005) and has also been observed for bottlenose dolphins and humpback dolphins in Florida and Hong Kong, respectively (Irvine et al. 1981, Jefferson 2000). Findings from other sources are varied, however. In Paraty Bay and Norte Bay, for example, S. guianensis showed larger group size during the summer (Lodi 2003, Daura-Jorge et al. 2005) whereas, the largest group sizes elsewhere ¨ occur during other seasons (Wursig 1978, Karczmarski et al. 1999). These varied results suggest that seasonal variation of group size may be related to idiosyncrasies of environmental constraints among habitats. The main findings reported here on group size and frequency of large aggregations set the Sepetiba population apart from the other populations already studied in Brazil. Another distinctive factor is the size of this population, which is estimated to be between 739 and 2,196 individuals (Flach et al., in press), the largest population of the species thus far estimated for the Brazilian coast. These characteristics should stimulate further studies to understand better this population and help plan a conservation strategy for it.

ACKNOWLEDGMENTS This work would not have been possible without the full financial support of the company VALE, which is gratefully acknowledged. We wish to express our thanks to Leandro Quadros, Francisco Lafet´a, Rubens Vianna, Felisbello Dalseco, Paulo Horta, and Tadeu Guerra for their help during all aspects of this work. And our gratitude to the helpful research background ¨ acquired from our colleagues Leszek Karczmarski, Paula Moreno, and Bernd Wursig at the MMRP-Texas A&M. This article was greatly improved by generous critiques and comments from Dr. Leszek Karczmarski, Dr. Janet Mann, and anonymous reviewer. One of the authors (AGC) has a research grant (# PQ-301100/2005-5) from The Brazilian Science Council (CNPq).

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Received: 3 October 2006 Accepted: 5 November 2007