J. Mar. Biol. Ass. U.K.

(2007), 87, 13271335 Printed in the United Kingdom

doi: 10.1017/S0025315407056366

Dolphin sympatric ecology in a tropical fjord: habitat partitioning by bathymetry and topography as a strategy to coexist
Lenin Oviedo*
*Maestra de Ciencias Marinas y Costeras, Universidad Nacional (UNA), Costa Rica. Proyecto Delphinus, Isla de Margarita, Nueva Esparta,Venezuela 6010. Biotrpica: Centro de Investigacin y Conservacin de la Biodiversidad Tropical, Caracas, Venezuela 1001. Fundacin Vida Marina, Drake Bay, Osa Pennsula, Costa Rica. E-mail: biotropica2@yahoo.com

Sympatric species need to avoid pervasive competition to counter its suppressor effects. Dietary divergence and habitat partitioning are strategies for coexistence. Golfo Dulce is a tropical fjord located in the southern Pacific waters of Costa Rica. This embayment is characterized by the mixture of neritic and oceanic-like features. Sympatric populations of spotted and bottlenose dolphins share this particular marine ecosystem. To analyse the means of coexistence among both dolphin populations, an approach using the marginality and specialization indices of ecological niche factor analysis was used to establish separation between realized niches of both species. Habitat partitioning is sustained by difference in habitat use; bathymetry and topography separated both species ecological niches. Dietary divergence could not be concluded because of lack of accurate dietary information. Nevertheless, it is likely to be separated by consumption of demersal prey by Tursiops truncatus, and pelagic prey by Stenella attenuata, accordingly with the differences in habitat use. Golfo Dulce could be perceived as an area of conservation importance: a geographical unit considered to contain special conservation values for both dolphin species.

INTRODUCTION
Interspecific competition has a mutual suppressor effect on the populations of different species; each species contributes to the regulation of the other as well as itself. Since under certain conditions competition can mean the potential elimination of one of the populations, interspecific competition is considered a crucial factor in the determination of which species can coexist within a habitat (Ojasti, 2000; Ricklefs, 2001). Bearzi (2005a) has made a detailed description of sympatric populations of the family Delphinidae worldwide and analysed the nature of habitat and resource partitioning, highlighting the relevance of dietary divergence and different habitat use as coexistence strategies. Golfo Dulce (Peninsula de Osa, Costa Rica) is a particular ecosystem, usually termed as a tropical fjord, where both neritic and offshore features converge. Productivity is limited; however, it is compensated by riparian discharges. Nevertheless, it sustains sympatric populations of more than 80 bottlenose dolphins, Tursiops truncatus (Acevedo & Matthews, 2005), and more than 300 pantropical spotted dolphins, Stenella attenuata (Oviedo, unpublished data). Pantropical spotted dolphins are probably the most widespread and representative odontocete in Costa Rican waters. Records on the species are abundant through a period of more than 20 years of surveys (May-Collado et al., 2005). In northern Costa Rica, the majority of the records come from Golfo Papagayo, particularly from Culebra Bay
Journal of the Marine Biological Association of the United Kingdom (2007)

and Islas Murcielagos (525 sighting events accounting for 12,311 individuals). In the southern zone, first records were reported by Acevedo (1996) and Acevedo & Buckhart (1998) in Golfo Dulce basin (200 sightings). Tursiops truncatus have been widely reported in territorial waters of Costa Rica. In Cocos Island, detailed studies on feeding ecology and behaviour (Acevedo 1999, 2002; Acevedo & Parker, 2000) and bio-acoustics (Acevedo & Stienessen, 2004) have been carried out. Records of bottlenose dolphins in Golfo Dulce, 529 sightings (Acevedo, 1996; Acevedo & Burkhart, 1998), also included data on association patterns and abundance (Acevedo & Matthews, 2005). Certainly T. truncatus resides within the gulf and key survival activities such as feeding and reproduction have been documented. Spotted dolphin habitat use still remains unclear; it is suspected that the species transits between the gulf and the open ocean on a regular basis (Acevedo & Burkhart, 1998; Cubero Pardo, 1998a). This contribution seeks to compare records from recent surveys with previously documented data on both species (bottlenose and spotted dolphins) in Golfo Dulce inner basin, and elucidate the significance of habitat partitioning as an ecological strategy of avoiding direct interspecific competition among sympatric dolphin species. An approach similar to the basics of the ecological niche factor analysis (Hirzel et al., 2002) is used; marginality, specialization and tolerance are employed as indicators of affiliation to determinant eco-geographical variables (bathymetry and topography) and habitat use, in order to determine different ecological niches.

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Sympatric dolphins in a tropical fjord, Costa Rica Table 1. Number of surveys, summary of research effort, and sighting frequencies (sightings/hour) of cetacean species in Golfo Dulce inner basin between March 2005February 2006.

MATERIALS AND METHODS Study area Golfo Dulce (830'N 8316'W) is an embayment of tectonic origin. It is 50 km long and 1015 km wide approximately; the total surface area is about 750 km2. Golfo Dulce comprises two important areas: a deep inner basin steeply sloped with a flat bottom of a maximum depth of 217 m, and a shallow outer basin with a sill depth of 70 m (Wolff et al., 1996). The dominant coastline on the north coast is steep forested rocky shore. There is about 2000 hectares of mangrove ecosystem associated with rivers flowing into the gulf. Water circulation is restricted similar to high latitude fjord, with slow deep water renewal by occasional intrusion of dense subsurface waters. There is a considerable tidal range: 24 m, with significant influence on the shoreline and freshwater courses. Productivity is relatively low, with poor nutrient levels near the surface, typical of non-upwelling shelf-waters. According to Wolff et al. (1996), Golfo Dulce remains an undisturbed estuary that acts differently from most tropical coastal ecosystems, as it is dominated by biomass and energy flow within the pelagic domain more closely resembling an open ocean system rather than an estuarine one.
Cetacean surveys Cetacean surveys in this contribution were accomplished through a platform of opportunity (Evans & Hammond, 2004). Two important aspects framed the research effort: (1) based on the two most important cetacean studies in the gulf (Acevedo & Burkhart, 1998; Cubero Pardo, 1998a), boat trips were directed to hot spot areas of occurrence within the inner basin: the entire rocky shoreline of the north coast, including the areas of influence of the Rincon River in the north-west, and the Esquinas River in the north-east; plus the central part of the inner basin; (2) observations were performed on boats used on a small local dolphin watching operation, during tours in morning hours from 0800 to 1200 h. Field trips temporal distribution ranges from late dry season (mid March 2005) to mid dry season (mid February 2006). Data gathering and cetacean identification were done by a trained observer (L.O.). Geographical coordinates of sightings were recorded using a hand held Garmin GPS Etrex. Photographic records were collected using a Sony DSC-H1 digital camera with 12 optical zoom. Behavioural observations were collected by ad libitum sampling (Altmann, 1974), but employing a modified behaviour key based on Schneider (1999) and used in dolphins surveys close to the study area (for a detailed description of the key see Garca & Dawson, 2003). For the purpose of determining habitat partitioning based on foraging evidence, only feeding behaviour descriptions are included in the analysis. Only sightings done by the author were considered. Data analysis Habitat characterization was accomplished by correlating spatial distribution of dolphin sightings with two ecogeographical variables (Gregr & Trites, 2001; Hirzel et al., 2001, 2002; Compton; 2004): (a) a continuous variable represented by the bathymetry; and (b) a categorical variable
Journal of the Marine Biological Association of the United Kingdom (2007)

Field efforts Boat trips Total number of boat trips Boat trips with cetacean observations Research efforts (in hours) Hours spent in the field Hours with cetacean sightings Average observation time Average effective observation time (AvEOT) Sightings (in events per unit of efforts) Stenella attenuata Number of sightings Sighting frequency (no. sightings/AvEOT) Tursiops truncatus Number of sightings Sighting frequency (no. sightings/AvEOT) Other cetaceans Number of sightings Sighting frequency (no. sightings/AvEOT)

20052006

30 24 120 96 4 3.2

12 3.43 13 3.71 4 1.14

(topography); expressed in relief/depth-classes through a slope index. Using a GIS (Map Info v. 4.0), a grid of 1 minute latitude by 1 minute longitude quadrants was established in the study area. The slope index (SI) related to sightings of both species (Oviedo et al., 2005; Mignucci, 1998) was calculated through the following formula: SI=ZmaxZmin/ZmaxRA100 Zmax is the maximum depth of a specific quadrant; Zmin is the minimum depth, considered 1 m for coastal areas; and ZmaxRA is the maximum depth of the research area. The slope indices and maximum depths were grouped into relief and bathymetry classes by an Euclidean distance cluster analysis (Statgraphic Plus v. 3.1). The basic indices of the ecological niche factor analysis (ENFA) developed by Hirzel et al. (2002), were calculated for both Stenella attenuata and Tursiops truncatus, with the variant of being calculated individually for each eco-geographical variable considered. To assess the bathymetry, Zmax was considered per each quadrant, while the SI (as a proportion to one) was the input data for topography: Marginality; Specialization; Tolerance; M=GDSa/1.96GD Esp=GD/Sa Tol=Sa/GD.

where GD is the regional mean of the study area, per each eco-geographical variable in each 1 min1 min quadrant, Sa is the mean of the distribution of S. attenuata and T. truncatus,

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Figure 1. Map of sightings distribution in Golfo Dulce inner basin, circles correspond with spotted dolphins, triangles with bottlenose dolphins.

per factor in each 1 min1 min quadrant. GD is the regional dispersion of the data, given by the standard deviation, and Sa is the dispersion in the spotted and bottlenose dolphins specific distributions in each environmental factor. These indices evaluate if the average environmental conditions associated with a particular distribution pattern, differ from the average environmental conditions of the total study area. Hence an M (marginality) value closer to one expresses a distribution of values associated with particular environmental factors and separated from the regional conditions. If the value of specialization (Esp) is high, then there is a trend of being particularly specialized on one or more factors. Following the suggestion of Hirzel et al. (2004), to ease the interpretation of specialization, the tolerance (Tol) coefficient; which is the inverse of the specialization, is given as it is an indicator of the species niche breadth. Before calculating the indices, data were tested for normality using the ShapiroWilk test. Significant differences in subsamples were estimated by the MannWhitney U-test and KruskalWallis one way ANOVA (Analyze it v. 1.71) since the statistical distributions of most of the datasets were not normal (Zar, 1996).

out of sight or sampling ended). Sightings frequencies of spotted and bottlenose dolphins were extremely similar throughout the study period. All sightings recorded during the field sampling were single species groups. Distribution of cetaceans in Golfo Dulces inner basin Topography and bathymetry: cluster analysis of 1 min1 min quadrants (N=253) with slope index and maximum depth, grouped the sampled area into eight subdivisions of topography features (Figure 2) and four classes of bathymetry (Figure 3) using 0.4 as a cut off distance value to distinguish the groups: very low slope (0.14.1%), low slope (4.222%), medium low slope (22.130%), medium

RESULTS Cetacean sightings in Golfo Dulces inner basin Cetacean records were collected on 29 occasions on 24 field trips with positive cetacean sightings (Table 1), all along the inner basin of the gulf (Figure 1). The successful sessions accounted for 96 continuous hours of observation out of 120 total hours spent in the field. Hours spent in the field were the sum of all the time invested in field sessions (4 hours each), while hours of cetacean sightings equal the effective observation time: the time of the initial encounter with a group of dolphins until the sighting was terminated (dolphins
Journal of the Marine Biological Association of the United Kingdom (2007)

Figure 2. Grouping of topography (slope) classes through a cluster analysis of Golfo Dulce (N=253 quadrants), arrow shows the cut off distance to distinguish eight groups: very low slope (0.14.1%), low slope (4.222%), medium low slope (22.130%), medium slope (30.137.4%), medium high slope (37.547.9%), high slope (4880.1%), steep slope (80.199.4%) and very steep slope (>99.5%).

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Sympatric dolphins in a tropical fjord, Costa Rica Table 3. Marginality, specialization and tolerance indices considering bathymetry and topography as eco-geographical variables.
Marginality Specialization Tolerance (M) (Esp) (Tol)

Species Bathimetry (Zmax) Stenella. attenuata Tursiops. truncatus Topography (SI) Stenella. attenuata Tursiops. truncatus

0.554 0.062 0.430 0.706

1.958 1.530 0.682 1.017

0.511 0.654 1.465 0.983

Figure 3. Grouping of bathymetry (Zmax) classes through a cluster analysis of Golfo Dulce (N=253 quadrants), arrow shows the cut off distance to distinguish four groups: shallow waters (0.139.9 m), medium waters (4098 m), deep waters (98.1168 m) and very deep waters (168217 m).

slope (30.137.4), medium high slope (37.547.9%), high slope (4880.1%), steep slope (80.199.4%), very steep slope (>99.5%), shallow waters (0.139.9 m), medium waters (4098 m), deep waters (98.1168 m) and very deep waters (168217 m), respectively. During the sampling period both species, spotted and bottlenose dolphins, seemed to have a non-random

distribution limited by the 100-m isobath. The marginality index for pantropical spotted dolphins (Table 3) in relation to depth showed a particular separation of the mean depth of Stenella attenuata sightings, with the regional mean for bathymetry in Golfo Dulce (Table 2), evidencing a notable preference towards deeper water. The specialization index (Table 3), also demonstrated a considerable degree of limitation to deep waters and lack of tolerance to shallow areas in the species range. This trend is supported by

Table 2. Means and standard deviations of Golfo Dulce, spotted dolphins sighting distribution and bottlenose dolphins sighting distribution and differences between samples in association with bathymetry (Zmax) and topography (slope index:SI).

Slope index and bathymetry analysis Golfo Dulce Total number of quadrants GD topography Slope index mean (SIGD) Slope index standard deviation (SIGD) GD bathymetry Maximum depth mean (ZmaxGD) Maximum depth standard deviation (ZmaxGD) Stenella attenuata Slope index mean (SISa) Slope index standard deviation (SISa) Maximum depth mean (ZmaxSa) Maximum depth standard deviation (ZmaxSa) Tursiops truncatus Slope index mean (SITt) Slope index standard deviation (SITt) Maximum depth mean (ZmaxTt) Maximum depth standard deviation (ZmaxTt) Statistical differences (MannWhitney U-test) ZmaxGD ZmaxSa ZmaxGD ZmaxTt SIGD SISa SIGD SITt ZmaxTt ZmaxSa SITt SISa
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253 0.168 (ShapiroWilk test: P<0.1) 0.217 93.74 (ShapiroWilk test: P<0.1) 70.72 0.350 (ShapiroWilk test: P=0.13) 0.317 170.54 (ShapiroWilk test: P<0.1) 36.12 0.467 (ShapiroWilk test: P=0.78) 0.213 102.40 (ShapiroWilk test: P=0.78) 46.23 P<0.025 (U=2217) P>0.025 (U=1389) P<0.025 (U=1968) P<0.025 (U=2175) P<0.025 (U=14) P>0.025 (U=70)

Sympatric dolphins in a tropical fjord, Costa Rica Table 4. Distribution and differences of spotted and bottlenose dolphins sightings per bathymetry and topography classes.
Slope index and bathymetry S. attenuata 0 0 1 2 9 H= 6.39, P<0.05 2 3 0 1 3 1 2 0 H=10.69, P>0.05

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Bathymetry Classes Shallow waters (0.139.9 m) Medium waters (4098 m) Deep waters (98.1168 m) Very Deep waters (168.1217 m) Differences between classes per sightings (KruskalWallis one way ANOVA) Topography Classes (Slope) Very low slope (0.14.1 %) Low slope (4.222%) Medium low slope (22.130%) Medium slope (30.137.4%) Medium high slope (37.547.9%) High slope (4880.1%) Steep slope (80.199.4%) Very steep slope (>99.5%) Differences between classes per sightings (KruskalWallis one way ANOVA)

T. truncatus 0 0 9 3 1 H=8.02, P<0.05 0 2 0 2 5 3 1 0 H=11.30, P<0.05

significant differences (MannWhitney U-test: U=2217, P<0.025) shown in Table 3 between the maximum depths associated with spotted dolphin sightings and the regional distribution of bathymetry in Golfo Dulce, and with the differentiation of sightings between depth-classes (Kruskal Wallis test: H=6.39, P<0.05) in Table 4. Influence of sea floor relief as a determinant factor in habitat use by spotted dolphins showed a weaker influence than bathymetry. There was not a clear pattern of slopeclasses associated with spotted dolphin observations as seen in Table 4 (KruskalWallis test: H=10.69, P>0.05) and the global mean of the whole basin, as expressed by the marginality in Table 3. At the same time, there is a high tolerance toward slopes greater than 30%. Bottlenose dolphins, on the other hand, did not demonstrate a particular preference in terms of depths when compared

Figure 4. Feeding events per tide cycle and species (Sa, Stenella attenuata; Tt, Tursiops truncatus) in Golfo Dulce inner basin during the sampling period.
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with the regional distribution of maximum bathymetry in the whole basin, due to similarities between means (Mann Whitney U-test: U=1389, P>0.025) of maximum depth distribution in Golfo Dulce (93.74 m) and that related with Tursiops truncatus sightings (102.40 m). Nevertheless, results in Table 4 suggest significant differences between sightings against deep water classes, in addition to a high degree of specialization toward shallower waters (Table 3). Marginality indicates that sea floor relief precludes a specific habitat for bottlenose dolphins, but with low specialization towards a particular slope-class. Differences between bottlenose dolphin sightings and slope-classes in Table 4 were supported statistically (KruskalWallis test: H=11.30, P<0.05). Depth-classes associated with bottlenose sightings on the northern coast of the inner basin showed a prevalence of medium depths over deeper waters beyond the 100 m. When comparing the factor distribution associated with the sightings pattern of both dolphins species as an indicator of preferences in bathymetry and topography in Table 2, significant differences in samples favoured depths (MannWhitney U-test: U=14, P<0.025) over underwater topography (MannWhitney U-test: U=70, P>0.025). Feeding activity within the inner basin: from 25 events of dolphin observation, 40% of the sightings (N=10, four events for S. attenuata and six for T. truncatus) evidenced feeding activities within the inner basin of Golfo Dulce. Both dolphin species were equally involved; however, all bottlenose dolphin feeding events were located within the area of influence of the Esquinas River on the north-east coast and the Rincn River on the north-west. Spotted dolphins engaged in feeding activity in very deep water in the centre of the basin, and in shallow areas of the Esquinas River as well as in the south-western part of the basin. All the feeding events of T. truncatus took place during ebb tide, as well as the majority of the feeding of S. attenuata (Figure 4).

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DISCUSSION
Dolphin sightings in Golfo Dulces inner basin The fact that observations were directed to hot spot areas of occurrence is an artefact of the type of platform of opportunity used: dolphin watching boats. This may represent a potential source of bias. However, the research effort had a relatively homogeneous spatial and temporal distribution, since equal effort was directed towards surveying both strata: shallow near shore waters and deep areas in the inner basin. Surveying localized areas within the inner basin enhanced considerably the effectiveness of the sampling. Cubero Pardo (1998a) reported 23.31% (N=114 h) of effective observation time in 91 field trips. The field survey of this investigation in 20052006 comprises 80% of effective observation time (Table 1). The similar sighting frequency of both spotted and bottlenose dolphins seemed to avoid concentration of recording and survey efforts towards a particular species. The trend of similar frequencies prevailed throughout the three seasons sampled. Acevedo & Burkhart (1998) as well as Cubero Pardo (1998a) recorded considerably more sightings of Tursiops truncatus than Stenella attenuata. In fact the small proportion of spotted dolphin sightings in contrast with more observations of bottlenose dolphins, plus the location of spotted dolphin groups outside the gulf, were taken as indicative of movements in and out of the gulf by S. attenuata. The equal proportion of observation of T. truncatus and S. attenuata did not rule out the potential movement of spotted dolphins outside the gulf basin. A major amount of Stenella observations, in comparison with previous studies, could be associated once again to localized survey efforts in hot spot areas of occurrence. The absence of mixed species aggregation recording throughout the field sampling is strong evidence of habitat partitioning in Golfo Dulce. Elsewhere in Costa Rica and worldwide, bottlenose dolphins are known to occur in interspecies groupings such as T. truncatus-Sotalia fluviatilis on the Caribbean coast of Costa Rica (Acevedo et al., 2005). There are tropical areas where dolphins of the genus Tursiops and Stenella co-exist, as in oceanic waters close to shore on the central coast of Venezuela. Over there, the majority of the sightings are mixed species associations of bottlenose and Atlantic spotted dolphins (Gonzles, 2000). On the other hand, in other locations around the Pacific coast of Central and South America, sympatric dolphin populations evidence competitive exclusion (Garca & Dawson 2003). In such cases spotted dolphins expand their ranges over depths and habitat where the potential competitor is absent or rare. Garca & Dawson (2003) also considered the influence of habitat suitability in areas where bottlenose and spotted dolphins could co-occur, but one of the species is not present. Divergence in foraging in spotted and bottlenose dolphins Cubero-Pardo (1998b) gave a specific account on feeding behaviour for both dolphin species in the study area. However, she reported just a 6% of time devoted to feeding by S. attenuata, vs 10 % for T. truncatus. The low amount of foraging observation was attributed to potential nocturnal
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feeding events, especially for spotted dolphins. Montero (2005) recorded a higher proportion of feeding behaviour for S. attenuata in Drake Bay (62%). Garca & Dawson (2003) in Baha Honda (Panama) also documented a higher proportion of feeding events (38%), as did May Collado & Morales (2005) on the north pacific coast of Costa Rica (55%). All these studies collected behaviour data through scan sampling, and everything indicates that records were taken during daylight hours. Diurnal observations made in this study included an important quantity of foraging events, although since they were registered through ad libitum sampling, these cannot be compared with previous records. Initially, the low number of feeding events within the inner basin of the gulf and the low productivity of this ecosystem encouraged the hypothetical assumption of Golfo Dulce being used as a shelter/nursery area rather than a feeding ground, at least for pantropical spotted dolphins. Even though such an assumption should not be ruled out at this research stage, prey capture and feeding might be more relevant for S. attenuata than previously documented. Bottlenose dolphin feeding was expected to be important, since all evidence points out that their spatial distribution is associated with a localized, predictable food source. Ebb tides seemed to provide an advantage for prey capture, it was observed with T. truncatus, which commonly aggregates near river mouths. But it was also seen during S. attenuata feeding events, with sightings of spotted dolphins near the Esquinas River and other areas close to shallow portions of the habitat on the eastern and western coasts of the inner basin. Habitat partitioning by diet preference for bottlenose and spotted dolphins in Golfo Dulce could be consequent on the trend of different prey preferences over diet overlap, based on the lack of observation of foraging mixed species aggregation. Acevedo & Burkhart (1998) report a mixed aggregation just once, but no details about whether it was a foraging event are given. Cubero Pardo (1998a) reported that both dolphins might take advantage of needle fish (Belonidae) as prey, but not simultaneously. The same author found seasonal similarities in specific activity as foraging for both dolphins, but not related to temporal and spatial overlap. Diet description and estimation of prey preference for spotted and bottlenose dolphins in Golfo Dulce are scarce. There is a description of the bottlenose dolphins diet in the trophic model developed by Wolff et al. (1996), but this account is not representative of the study area and the species, since it is based on dietary information of three different species of odontocetes (Lagenorhynchus obscurus, Stenella coeruleoalba and Phocenoides dalli) in mostly temperate ecosystems (central Peru, the Ligurian Sea and north Pacific respectively). There are other diet accounts for both dolphin species in Costa Rican waters, but they reflect entirely the occurrence in totally different habitat when compared with Golfo Dulce: the Nicoya Gulf (Tabash, 2005) and the north Pacific coast (Hernndez et al., 2006). May Collado & Morales (2005) did not detail the spotted dolphins diet in Golfo de Papagayo, but they considered the affiliation of seasonal productivity with what could be the common prey of S. attenuata graffmani;

Sympatric dolphins in a tropical fjord, Costa Rica squid and flying fish (Exocoetidae). Moreover these authors provide a behavioural description of foraging that concurs with the intake of such pelagic prey species. A general diet composition given by Pauly et al. (1998) on both species shows opposite preferences: pelagic prey constitute 60% of the diet of spotted dolphins (30% small squid, 20% large squid and 10% small pelagics), while the same kind of prey represents 40% of bottlenose dolphin dietary preference (20% small squid, 5% large squid and 15% small pelagics). Dietary preferences in highly overlapping diets of sympatric dolphins seemed to promote coexistence (Hoezel, 1998; Bearzi, 2005a,b). This would be supported by the information provided by Pauly et al. (1998); however, the latter is still a very general account and does not include other documented pelagic prey items of relevance such as Myctophid lanterfish (Robertson & Chivers, 1997; Wang et al., 2003), and poorly reflect important local particularities. The gap of information of spotted and bottlenose dolphin diet in Golfo Dulce precludes any conclusive remark related with habitat partitioning by dietary divergence. Nevertheless, feeding observations of both dolphin species suggest a potential diversification in prey preference, with T truncatus taking advantage of demersal prey aggregated near river mouths, while spotted dolphins might concentrate on pelagic schooling fish. There would be an overlap in certain prey species such as needle fish, especially when spawning concentrations occur and the resource is abundant. In such instance, the abundance of prey allows the two species to co-occur in the same area, as in the case with common and bottlenose dolphins in up-welling areas of the California Bight (Bearzi, 2005b), but with little or no overlap in a spatial microscale. Ecological separation by habitat use of dolphins in Golfo Dulces inner basin Topography and bathymetry: distribution related to depth and physiographic features for S. attenuata and T. truncatus were previously considered by both Acevedo & Burkhart (1998) and Cubero Pardo (1998a). They related spotted dolphin distribution to deep waters and the corresponding increased distance from shore, while bottlenose dolphin distribution was related with shallow bathymetry and low salinity (a by-product of being primarily sighted near river mouths). However details of the influence of a particular isobath or physiographic feature on habitat use are not given. Bearzi (2005a) considered depth and topography as indicators of ecological separation in sympatric odontocetes, and particularly when there is a clear definition of inshore and offshore habitats. When examining the spatial arrangement of S. attenuata in the inner gulf basin, two considerations arise: (1) spotted dolphins might show a separation of their realized ecological niche in association with bathymetry, that would be sustained by the divergence of the sub-sample mean of maximum depths associated with spotted dolphin sightings and the regional study area mean of bathymetry distribution (both estimators produced a relatively high marginality index and a considerable degree of specialization to such deep water); and (2) affiliation to the deepest part of the gulf might conceal the relevance of sea floor relief, the low
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and medium slope classes associated to the sightings could be a consequence of remaining in the deepest central part of the basin and avoiding the borders where the slope is steeper, especially on the east side where the eastern Golfo Dulce fault and some smaller parallel faults are located very close to shore (Hebbeln et al., 1996). The relatively high tolerance to elevated slopes precludes the determination of these escarpments as limits, but rather as physiographical references in their habitat. Bottlenose dolphin spatial distribution along the north coast of the inner basin could also be conditioned by a limiting bathymetry beyond 100 m, as indicated by a high specialization to shallow water near the coast and a low tolerance to high depths. Even though association between shallow waters could appear as absent, this is obscured by the fact that the analysis considered maximum depth per each quadrant. The latter could define a strictly neritic niche as opposed to the oceanic-like habitat of spotted dolphins in the basin. Coastal populations of T. truncatus use geographical features such as abrupt changes in depths as references and limits in their range (Hansen, 1990; Oviedo et al., 2005). Furthermore, differences between sightings samples of both dolphins were significant in terms of depths and possibly veiled when slope is considered, since both species evade steep slopes. As with spotted dolphins, such topography could represent references that characterize the T. truncatus physical habitat. Affiliation to particular bathymetric features and, to a lesser degree, to a specific underwater relief seemed to be relevant in the separation of the realized ecological niche of spotted and bottlenose dolphins. This trend represents strong evidence of habitat partitioning of Golfo Dulces inner basin. Dietary divergence can only be hypothesized due to the lack of dietary information in the Gulf, but the results presented here provide a robust illustration of differences in habitat use as a strategy to coexist and prevent pervasive direct competition between these two sympatric species. There should be a strong correlation between trophic dynamic and habitat use. It is clear that T. truncatus exploit resources associated with the habitat features defined by the favoured physical habitat; sightings and foraging in estuaries all along the study area appear to support that. Conversely, the foraging dynamic of pantropical spotted dolphins, even though potentially more relevant than previously thought, might be still conditioned by productivity in Golfo Dulce, which itself is still not clear, since there are indicators of upwelling processes outside the sills basin as far as Panama, based on zooplankton community structure and the intrusion of cold oxygen rich subsurface water to the inner basin (Quesada & Morales, 2004). Therefore a low abundance of potential prey, or an extremely seasonal availability of trophic resources, might drive the suspected movements of S. attenuata in and out of Golfo Dulce. The confluence of neritic and off-shore features within the same basin, among other environmental attributes, are strong arguments to support Golfo Dulce as an area of conservation importance (ACI): a geographical unit considered to contain special conservation values (Bearzi et al., 2004) for both pantropical spotted and bottlenose dolphins.

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The study of marine food webs and cetacean-fisheries interactions may help to identify areas of conflict and thus serve as a useful management tool. The available information does not allow for immediate model implementation. Research actions should aim to collect information in Golfo Dulce ACI on feeding ecology and prey species that may be used in more accurate and up-dated ecosystem models in the near future, with the ultimate goal of increased understanding of ecosystem function. Indeed, an ecosystem approach, involving a thorough assessment of the nature and scale of trophic interactions is needed for rigorous conservation planning (Hooker et al., 2002).
The author would like to acknowledge the valuable involvement of Villas Corcovado Hotel in OSA Peninsula, and the captains Taboga, Rony and Charlie. The author is also indebted to PROCMAR (Programa de Maestra en Ciencias Marinas y Costeras, Universidad Nacional); especially to Professors Dora Ingrid Rivera, Hilda Viquez, Luis Villalobos and Miguel Iiguez for their encouragement and support in the development of this research. Thanks to the Marine Science Station (ECMAR) of Universidad Nacional (UNA). Dr Alexandre Hirzel gave valuables insights to the final manuscript and Jim Hart Tzephyr kindly reviewed the final version. Finally many thanks to the whales and dolphins ladies: Romina Acevedo, Mara Alejandra Esteves and Noemi Silva; their support from outside Costa Rica has been crucial for the development of this contribution. This investigation was supported by a grant provided by the Society for Marine Mammalogy.

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Submitted 4 November 2006. Accepted 11 August 2007.

Journal of the Marine Biological Association of the United Kingdom (2007)