Flávia Bonfietti IZIDORO and Yvonnick LE PENDU*

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1 NORTH-WESTERN JOURNAL OF ZOOLOGY 8 (2): NwjZ, Oradea, Romania, 2012 Article No.: Estuarine dolphins (Sotalia guianensis) (Van Bénéden, 1864) (Cetacea: Delphinidae) in Porto de Ilhéus, Brazil: group characterisation and response to ships Flávia Bonfietti IZIDORO and Yvonnick LE PENDU* Universidade Estadual de Santa Cruz, Departamento de Ciências Biológicas, Grupo de Pesquisa em Mamíferos Aquáticos de Ilhéus, Ilhéus, Bahia, Brazil, * Corresponding author s yvonnickuesc@gmail.com Received: 25. May 2011 / Accepted: 11. April 2012 / Available online: 27. May 2012 / Printed: December 2012 Abstract. Living in group provides protection to small cetaceans and enhance prey capture. Boat traffic can impact group formation and activities of coastal dolphins. This study aims to characterise the occurrence, group characteristics and activity of estuarine dolphins (Sotalia guianensis) and their response to boat traffic in Porto de Ilhéus (BA), Brazil. Scan samplings were conducted from a unique fixed point during a total of hours of observation from September 2007 to August Estuarine dolphins were present in 89% of the 137 sampling days. A total of 481 groups were recorded entering the monitored area with a mean group size of 3.08 ± All age classes were recorded in the area throughout the year, but adults were more numerous. Three phases were delimited according to the presence of the dolphins in the area and water visibility. The dolphins rarely show noticeable behavioural response to the passage of small boats in their vicinity. Porto de Ilhéus may represent an attractive area for estuarine dolphins due to the presence of fishing boats that regularly discard fish that have no economic value but are consumed by dolphins. Moreover, the harbour is an area of socialisation for these individuals. Our results confirm the biological significance of Porto de Ilhéus and its surroundings, in agreement with the recent designation of a marine conservation unit in the area, Parque Municipal Marinho do Ilhéus. Key words: Sotalia guianensis, group structure, Brazil, Bahia, behaviour, boats. Introduction Sotalia guianensis is a small estuarine dolphin endemic to the coastal waters of the Western Atlantic Ocean (Borobia et al. 1991). The species mostly frequents estuaries, bays and other coastal waters (Flores & Da Silva 2009). Its known distribution occurs from Santa Catarina state, Brazil, in the south (Simões-Lopes 1988), to Nicaragua (Edwards & Schnell 2001), in the north, and in a continuous strip across Brazil (Da Silva & Best 1996). Nonetheless, genetic analyses identified three evolutionary significant units along the Brazilian coast (Cunha et al. 2005). Despite growing research efforts, information regarding the biology and conservation status of S. guianensis remains insufficient (Reeves et al. 2003, Secchi 2010), especially in the northern and north-eastern regions of Brazil (Monteiro-Filho & Monteiro 2008). The International Union for Nature Conservation (Secchi 2010) considers that information is scarce in order to make an assessment regarding the risk of extinction of S. guianensis (DD), but a careful evaluation of its conservation status was recently suggested, given the intense human pressure experienced by this coastal species throughout its distribution (Rosas 2010). The species has an estimated longevity of about 30 years (Rosas et al. 2003) and a multimale mating system with sperm competition has been suggested by Rosas & Monteiro Filho (2002). This species is usually found in groups of two to six individuals (Flores & Da Silva 2009). However aggregations of more than 200 animals have been registered in the Baía de Sepetiba bay (Rio de Janeiro state, Brazil) and of approximately 400 individuals in Baía de Ilha Grande bay (Lodi & Hetzel 1998). Such large aggregations are usually engaged in cooperative fishing activities (Flores & Da Silva 2009). Most cetacean group formations are related to the acquisition of resources and protection from predators (Connor 2000). There are also some latent costs in the life of a group, such as parasite transmission, competition for resources and enhanced chances of being detected by predators. Nonetheless the formation of groups is favoured when the benefits of being with other individuals surpasses those costs (Connor 2000). Estuarine dolphins are frequently observed in Ilhéus, Bahia, Brazil, mainly in two specific areas located at a distance of 4 km from each other: Baía do Pontal bay and the Ilhéus harbour, referred as Porto de Ilhéus in this study. The occurrence of S. guianensis at Baía do Pontal bay was already ana-

2 Groups of estuarine dolphins in Ilhéus lysed by Santos U.A. et al. (2010): in 2006, dolphins were more frequently observed in September and October than in other months, sightings were more frequent before 08:00 h and after 15:00 h and group size did not vary significantly throughout the year. Based on these findings, we were expecting variations in the frequency of group sighting during the day and season in Porto de Ilhéus. Information about the occurrence, behaviour and group dynamics of S. guianensis in Porto de Ilhéus is needed to hasten actions for the conservation of a population potentially vulnerable to increasing anthropogenic disturbances. Cargos and tugs are visiting the harbour throughout the year and can stay docked for several days. From December to March, cruise ships also dock at Porto de Ilhéus, usually for a day. Small fishing and recreation boats pass freely through the area, sometimes very close to the dolphins. Injuries caused to S. guianensis by boat collisions were reported in other areas (Van Bressem et al. 2007). A small marine conservation unit, the Parque Municipal Marinho dos Ilhéus, was delimited in 2011 to protect a reproduction area of the critically endangered fish Epinephelus itajara (Craig 2011). The border of the 773 ha conservation unit is delineated by the breakwater of Porto de Ilhéus (Parque Municipal Marinho de Ilhéus 2011a), location of the present study. This paper aims to analyse the presence, size and composition of the groups of estuarine dolphins in Porto de Ilhéus during a year and to verify if their behaviour is affected by the transit of ships and boats in the area. Materials and methods Study site Porto de Ilhéus (14 47 S, W) is located at the Enseada das Trincheiras cove, Malhado district, city of Ilhéus, on the south-eastern coast of Bahia state (Fig. 1). The climate is Af (tropical rain forest) according to the Köppen classification scheme (Mori et al. 1983, Thomas et al. 1998), hot and permanently humid, without a dry season (Romero et al. 2008). Rainless periods of one to three months occasionally occur, usually from December to March (Mori et al. 1983, Thomas et al. 1998). Predominant winds arise from the northeast and last from October to March, and from the southeast and east from April to September (Bittencourt et al. 2000). We chose Porto de Ilhéus to conduct this research due to a previous study that indicated an almost daily presence of estuarine dolphins during long periods in this area (Reis 2004). The facilitated recording of their behaviour was determinant in our choice of this fixed observation 233 point. The water depth around the fixed point varies from 5 to 12 m (Parque Municipal Marinho de Ilhéus 2011b). According to Santos M.S. (pers. comm. 2010), the animals remain at a median distance of 0.16 ± 0.18 km from the edge of a 2262 m breakwater and concentrate around the 5 m isobath. This is a site with great anthropic influence due to the intense flow of cargo ships, tourist and fishing boats and scuba divers who practice sport fishing (Parque Municipal Marinho de Ilhéus 2011b). Data collection Data was collected between September 2007 and August The monitored area was a circle with a radius of 320 m, the maximum distance that allowed age determination of each dolphin without doubt, using binoculars. Distance was measured using a digital LEICA T 110 theodolite and a buoy as a reference mark. We conducted 48 hours of sampling per month in four-hour sessions, alternating mornings and afternoons. Scan sampling (Altmann 1974) were conducted every 15 minutes using binoculars to verify the entrance or exit of groups from the monitored area. Data were registered on a standardised check sheet, including date, beginning and ending times of each session, Beaufort sea state (see below for details), sea swell, water visibility, and characteristics of each group of dolphins present in the monitored area (the term group includes singletons): number of individuals, age class of the animals, time of arrival and departure from the monitored area and time of scan samplings. Environmental variables (sea conditions, sea swell, and water visibility) were visually estimated at the beginning of each session and when any environmental change was detected. Classification of sea conditions (calm, slight, moderate and rough) was based on the Beaufort scale (Met Office 2010). Corresponding sea swell (based on the Douglas sea and swell scale, Met Office 2010) was classified as low (less than 1.25 m), moderate ( m) and rough (exceeding 4 m). Water visibility was estimated visually by the observer since the characteristics of the pier did not allow the use of a Secchi disk at the observation point. Water visibility was classified as high (clear, transparent water with blue tones and white foam), medium (water with brown or grey tones, brownish foam), and low (muddy and murky water, generally with sediments on the surface). A group was defined as a set of animals observed in apparent association, moving in the same direction and often, but not always, engaged in the same activity (Shane 1990). The groups were recorded as soon as they entered the monitored area. We considered that the animals had left the monitored area when they were not visualised for two successive scans (at an interval of 15 minutes). Individuals were identified as infants, juveniles and adults, according to colour pattern and body size, which were visually estimated. Infants were about half the size of an adult (Ramos et al. 2000) with a grey-pinkish colour (Randi et al. 2008). We estimated that juveniles were smaller than 2/3 of an adult s size. They displayed a grey back, including part of the chest and tail fins, with a characteristic stain in the centre of the dorsal fin (Randi et al. 2008). Adults sizes varied from 170 to 220 cm (Monteiro-

3 234 F.B. Izidoro & Y. Le Pendu Figure 1. Location of the harbour in the city of Ilhéus (modified from Reuss-Strenzel and Assunção 2008). The dashed circle (radius = 320 m) indicates the monitored area in Porto de Ilhéus. Filho & Monteiro 2008), they were predominantly grey bodied, with a lighter grey on the belly from the neck up to the genital region (Randi et al. 2008). The estimation of the body size is dependent of the observer s proximity to the dolphins, the conditions of observation and the observer s experience. Every fishing and recreation boat (i.e. sport fishing, diving and tourist boat) that passed through the monitored area was annotated on the check sheet. We analysed the activity of the dolphins whenever a boat reached a distance of approximately 50 m from the dolphins until the boat left the monitored area, to detect a potential behavioural response to the passage of the boat. We classified the responses as negative, neutral and positive, based on Pereira et al (2007). A negative response was registered when the dolphins escaped the boat usually with successive jumps out of the water (porpoising behaviour); a neutral response was recorded when they did not change their behaviour in the presence of the boat; a positive response was recorded if they showed interest (e.g. approaching or following) for the boat. We annotated every cargo ship, cruise ship and tug boat docked in the harbour s wharf (approximately 1000 m from the end of the haven) to verify if their presence influenced the occurrence of dolphins in the monitored area. Data analysis We used the chi-square test for the following purposes: (1) to check the influence of time on the arrival of groups in the monitored area via a comparison of the observed frequency distribution of group arrivals per hour in the monitored area with an expected frequency distribution based on the sampling effort; and (2) to verify whether the number of individuals of each age class sighted by the time unit varied according to the month. We investigated whether the occurrence of estuarine dolphins in the area varied with environmental conditions (season, sea conditions, sea swell and water visibility). We used the chisquare test to investigate the influence of the sea conditions and sea swell on the frequency of sightings of estuarine dolphins. We calculated the coefficient of variation of monthly averages of sightings per hour to identify homogeneous periods (phases). A Kruskal-Wallis one-way analysis of variance was conducted to determine if the number of dolphins observed during these phases was significantly different, followed by Dunn's multiple comparison tests. A G-test of adherence was used to test whether the groups of estuarine dolphins were sighted regardless of water visibility. A G-test of independence was conducted to observe whether the reactions of the animals were similar during the passing of fishing or recreation boats. A chi-square test was used to verify whether the type of ships docked at the harbour influenced the sightings of estuarine dolphins in the monitored area. All statistical analyses were performed using BioEstat 5.0. Results Data collection was conducted over a period of 137 days, corresponding to 548 hours and 22

4 Groups of estuarine dolphins in Ilhéus 235 Figure 2. Number of groups of estuarine dolphins arriving (n=481) and leaving (n=281) the monitored area in Porto de Ilhéus according to group size between September 2007 and August Figure 3. Relative frequencies of observed and expected arrivals of groups of estuarine dolphins in Porto de Ilhéus (n=481) according to time between September 2007 and August minutes of sampling effort ( x =45.7 ± 5.53 hours/ month). The animals were present in the monitored area 89% of the 137 sampling days and 52.4% of the duration of the sampling effort (287 hours and 24 minutes). The size of the groups arriving to the monitored area ranged from 1 to 18 individuals ( x =2.93; SD=1.69; mode=2; n=481 groups). 12% (n=56) of the group arrivals were singletons. The groups arriving or leaving the monitored area generally consisted of two to five animals (Fig. 2). The frequency of arrival of the groups varied significantly depending on the time of day (X 2 =32.98; p<0.001) and was higher between 7:00 h and 9:00 h and between 11:00 h and 13:00 h (Fig. 3). It was possible to define the age class of 63.61% (n=895) of the 1407 registered individuals. Animals of all age classes were observed during all the months of the data collection period, and adults were the most frequently observed class during all months (Fig. 4). The number of individuals of each age class varied significantly between the months: infants (X 2 =53.74; p<0.001), juveniles (X 2 =82.46; p<0.001) and adults (X 2 =86.72; p<0.001). The number of estuarine dolphins observed per hour of sampling in Porto de Ilhéus changed significantly throughout the year and three phases were defined by the coefficient of variation analysis (Fig. 5). There were significant differences in the number of sightings of estuarine dolphins between the three phases (H=25.525, p <0.0001): the first (September to December) and the second (January to April) phases differed significantly (Dunn, p<0.05), as well as the second and third (May to August) phases (Dunn, p<0.05).

5 236 F.B. Izidoro & Y. Le Pendu Figure 4. Number of infants, juveniles and adults of estuarine dolphins (n=895) observed in Porto de Ilhéus between September 2007 and August Figure 5. Box-plots (medians and quartiles) of the number of estuarine dolphins observed per hour of sampling in Porto de Ilhéus between September 2007 and August The dotted vertical lines delineate the three identified phases (see text). (n) = number of observation days during the month. The column graphs represent the observed and expected frequencies of groups of estuarine dolphins according to water visibility in September-December 2007 (n=165 groups), January-April 2008 (n=80 groups) and May-August 2008 (n=236 groups). Groups were sighted in similar proportions to what was expected in each condition of water visibility during the first and third phases (Fig. 5). The frequency of sightings differed significantly from the expected proportions during the second phase (G-test with Williams adjustment=19.09; p<0.001), when days with high water visibility were more frequent than during the other phases. Fewer dolphins were sighted when the visibility was high, and more were sighted when it was medium or low (Fig. 5). The lower number of individuals sighted during the second phase could be related to the high frequency of days with high water visibility during that period. Significantly more individuals were sighted when the sea surface was calm (X 2 =14.59; p=0.0022) and when the swell was low (X 2 =8.28; p=0.016). The dolphins were mostly indifferent (93.7%; n=224) to the passage of a boat in the monitored area and never manifested a positive response. Their response to the passage of fishing (n=187) and recreational boats (n=52) through the moni-

6 Groups of estuarine dolphins in Ilhéus 237 Figure 6. Observed and expected relative frequencies of estuarine dolphins in the absence or presence of several types of boats moored in Porto de Ilhéus between September 2007 and August tored area was similar (G-test with Williams adjustment=2.58; p=0.17): the animals escaped in 5% of the passages of fishing boats (n=9) and in 12% of recreation boats (n=6). Cargo ships, cruise and tug boats were present in 100 and absent in 37 of the sampling days. Cargo ships were docked and operative at the wharf 70% of the time of observation. In 26% of the sampling time, tug boats were docked. Cruise boats were in the harbour during only 3% of the sampling effort. The number of estuarine dolphins sighted was greater in the absence of ships and less than expected in the presence of tug and cruise boats. In the presence of cargo ships, the sighting of estuarine dolphins was similar to what was expected (Fig. 6). Discussion Group size The mean group size was similar to that found in other areas by Araújo et al. (2003), Havukainen et al. (2011) and Spinelli et al. (2002), with values of 2.7, 2.2 and 4.2 individuals per group, respectively. The groups in the Cananéia estuary (São Paulo state, Brazil) were composed of 2 to 5 individuals (Geise et al. 1999), and 80% of all observed groups by Monteiro-Filho (2000) were composed of 2 or 3 individuals. These studies presented information gathered from both land-based and boat-based platforms. When only considering the studies based on boat-based survey in Brazilian populations of S. guianensis, the mean group size is highly variable: 6.6 at Banco de Abrolhos (Rossi-Santos et al. 2006), 11.5 in Paranaguá Estuarine Complex (Santos M.C.O. et al. 2010), 12.4 in the Cananeia estuary (Santos & Rosso 2007, 2008) and 13 at Baía de Guanabara bay (Azevedo et al. 2005). Apparently, larger groups are more common in the south and south-eastern Brazilian coastal waters (Flores & Da Silva 2009). Singletons accounted for 12% of the groups entering the monitored area. This value is higher than that found by Azevedo et al. (2005) in Baía de Guanabara bay (0.9 %), Santos M.C.O. et al. (2010) in the Paranaguá Estuarine Complex (1.7%) and Santos & Rosso (2007) in the Cananéia estuary (1.9%). Batista et al. (2008) and Santos & Rosso (2008) suggested a lack of consistency in group membership in S. guianensis. According to Santos & Rosso (2008), abundant food resources, the lack of potential predators and monomorphism in S. guianensis favour fluid associations. The relative frequency of groups with more than five animals leaving the monitored area was higher than that of arriving large groups. Conversely, small groups were more frequently arriving than leaving the monitored area. We also observed more group fusions than fissions in this area (personal observation). Based on these observations, we formulate the hypothesis that frequent fusions of groups in Porto de Ilhéus may occur as a result of the attractiveness of the place due to a probable abundance of food resources. This attractiveness was confirmed by the larger presence of animals in this small monitored area in relation to other coastal areas of Ilhéus (personal observation). The fusion of groups occurs more frequently when the individual ability to perceive a congener is enhanced (Dubois et al. 2001). The high density of estuarine dolphins in Porto de Ilhéus increases the likelihood of fusion of groups. Consequently, the mean size of the groups leaving the monitored area is greater than the mean size of the arriving groups. The arrival of groups in the monitored area

7 238 was more frequent between 7:00 h and 9:00 h and between 11:00 h and 13:00 h. In other places, such as the Cananéia estuary, Baía de Guanabara bay (Geise 1991), Baía Norte bay (Santa Catarina state, Brazil, Daura-Jorge et al. 2005), Baía dos Golfinhos bay (Rio Grande do Norte state, Brazil, Araújo et al. 2003) and Praia de Iracema beach (Ceará state, Brazil, Oliveira et al. 1995), a higher number of groups was observed in the mornings. Santos U.A. et al. (2010) registered more estuarine dolphins entering Baía do Pontal bay (Ilhéus) in the early morning hours and after 14:00 h. A photoidentification study at Baía do Pontal bay and Porto de Ilhéus that is currently in progress has already confirmed that some individuals frequent both areas. Age classes The presence of infants every month was already registered in Ilhéus by Santos U.A. et al. (2010) along with other populations (Araújo et al. 2003, Azevedo et al. 2005, Di Beneditto et al. 2001, Lodi 2003). However, we detected a significant monthly variation in the frequency of observations of infants, unlike what was observed on the coast of Paraná state by Rosas and Monteiro-Filho (2002) and Santos M.C.O. et al. (2010). According to Lodi (2003), the presence of infants in all seasons indicates a poliestric pan-seasonal species. Seasonality The number of individuals observed per hour of sampling was higher from September to December 2007 and from May to August 2008, being lower in summer (January-April 2008). The highest frequency of sightings at Baía do Pontal bay occurred in September and October (Santos U.A. et al. 2010). In Ilhéus, the two predominant seasons differ according to water visibility. In summer, water is crystal clear in shades of blue, whereas in winter, the water is turbid due to the rains that carry sediments from the rivers to the sea, similar to what occurs in the Paranaguá Estuarine Complex in the rainy summer season (Santos M.C.O. et al. 2010). The sighting of groups was higher in the months when the visibility was predominantly intermediate. According to Ballance (1992), the occurrence of cetaceans may be due to local concentrations of prey that influence their foraging behaviour. Among the most abundant fish species in the study area (Moraes et al. 2009), 42.85% are prey of estuarine dolphins. According to the identifications of several authors (Di Beneditto & Siciliano 2007, Di Beneditto et al. 2001, F.B. Izidoro & Y. Le Pendu Gurjão et al. 2003, Oliveira et al. 2008, Santos et al. 2002, Santos M.C.O. et al. 2010), these species are Isopisthus parvipinnis, Larimus breviceps, Macrodon ancylodon, Paralonchurus brasiliensis, Stellifer brasiliensis and Stellifer stellifer. From December to April, Moraes (pers. comm. 2011) registered a reduction not only of the abundance of ichthyofauna but also of the abundance of each prey species of the estuarine dolphins. Such reduction may explain the lowest observation frequency of estuarine dolphins during those months, with the animals being forced, perhaps, to look for food in other areas. Behavioural response to boats A neutral response to the passage of small fishing and recreation boats was the most frequently observed response, as reported by Araujo et al. (2008) for seven types of vessels, even large ships, in a study for which data was partly collected in port areas. The dolphins may have become used to such disturbances provoked by ships, due to the intense daily boat traffic, as observed by Pereira et al. (2007), in Baía Norte Bay, Santa Catarina, which recorded an increase of neutral and a decrease in negative responses to tourist boats. Nonetheless, some authors pointed out that boat traffic can modify acoustic communication (Rezende 2008). The sightings of estuarine dolphins increased when cargo ships were moored in the harbour and decreased in the presence of cruises. During the transfer of cargo, some of it ends up falling into the sea. Many loads are alimentary products (soybeans, cocoa, maize and others), and when they fall into the sea, they attract fish to the area, which represents a greater amount of food for the estuarine dolphins in the harbour. Dolphin-watching boats are more stressful and can reduce the foraging activity (Carrera et al. 2008), increase the travelling frequency (Santos-Jr et al. 2006) and sometimes result in S. guianensis leaving the area (Carrera et al. 2008). The control of such activity can minimize the impact on S. guianensis (Tosi & Ferreira 2009). Fishing boats remain anchored near the area of the Porto de Ilhéus, and some bring their trawl nets full of fish still immersed in the sea as they return to the anchorage. Many boats perform disposal of fish near the harbour, even before they reach the harbour. On several occasions, some animals were sighted close to these boats and ate the discarded fishes (personal observation). This practice contributes to the abundance of food resources and can influence the preference for that

8 Groups of estuarine dolphins in Ilhéus area, the benefits outweighing the risks and disturbances caused by boat traffic. Conclusion Porto de Ilhéus represents an attractive area for estuarine dolphins because the fishing boats discard their load that is consumed by these animals and because cargo operations attract fishes that are also part of the dolphins diet. The daily presence of the species in the Porto de Ilhéus and the fact that more than 80 individuals have been photoidentified in the monitored area over the last three years (unpublished data) emphasises the ecological importance of this place for the local population of estuarine dolphins. Therefore, our results reinforce the biological importance of the Parque Municipal Marinho dos Ilhéus to maintain the balance between the ecological requirements of the marine wildlife and the economic activities developed in Porto de Ilhéus. Acknowledgements. We thank the Universidade Estadual de Santa Cruz (UESC) for logistic support; we are grateful to the directors and staff of the Companhia das Docas do Estado da Bahia, Codeba-Ilhéus for permission to access the study area and support for the development of the research; and we thank Mariana Soares Santos, who supplied the theodolite data. We are grateful to anonymous reviewers for their constructive comments and Joyce Greck for English corrections. Financial Support: This study was financed by Fundação de Amparo a Pesquisa do Estado da Bahia (FAPESB) by means of the grant of a master s degree scholarship (Term 15/2007) and thesis financial aid (Term APR0018/2009). References Altmann, J. (1974): Observational study of behavior - sampling methods. Behavior 49: Araújo, J.P., Passavante, J.Z.O., Souto, A.S. (2003): Behavior of the estuarine dolphin Sotalia guianensis at Dolphin Bay, Pipa, Rio Grande do Norte, Brazil. 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