# Ecological niche segregation within a community of sympatric dolphins around a tropical island

J Kiszka, B Simon-Bouhet, Ludivine Martinez, C Pusineri, P Richard, V Ridoux

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## To cite this version:

J Kiszka, B Simon-Bouhet, Ludivine Martinez, C Pusineri, P Richard, et al.. Ecological niche segregation within a community of sympatric dolphins around a tropical island. Marine Ecology Progress Series, 2011, 433, pp.273-288. 10.3354/meps09165. hal-05073052

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Submitted on 20 May 2025

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# Ecological niche segregation within a community of sympatric dolphins around a tropical island

Jeremy Kiszka<fnref n="1" />,<fnref n="2" />*, Benoit Simon-Bouhet<fnref n="1" />, Ludivine Martinez<fnref n="1" />, Claire Pusineri<fnref n="3" />, Pierre Richard<fnref n="1" />, Vincent Ridoux<fnref n="1" />

**ABSTRACT:** Investigating ecological segregation among organisms of a given community is challenging, especially when these organisms share similar patterns of distribution, and similar size and morphology. Around the island of Mayotte, a diversified community of at least 4 sympatric delphinids is present year round within a very restricted range: the Indo-Pacific bottlenose dolphin *Tursiops aduncus*, the spinner dolphin *Stenella longirostris*, the pantropical spotted dolphin *S. attenuata*, and the melon-headed whale *Peponocephala electra*. In addition, the Fraser's dolphin *Lagenodelphis hosei* makes temporary incursions into peri-insular waters as well. This study aims to assess niche segregation among this tropical dolphin community. We hypothesized that each species occupies its own distinct niche defined by the following axes: habitat, resources and time. We analysed habitat in relation to physiography, behavioural budgets and C and N stable isotope values from skin and blubber samples for each species. The results highlighted that habitat and behavioural budgets were relatively distinct among species, with few exceptions. However, in those species living on the outer reef slope where habitat and behaviour were not well discriminated, stable isotope analyses confirmed that species have different trophic levels (mostly reflected through δ¹⁵N values) or foraging habitat (mostly reflected through δ¹³C values). This study confirms that the use of multiple methodologies (habitat, behaviour and feeding ecology studies) help in discerning ecological niche segregation, especially when examining closely related species within a common restricted range.

**KEY WORDS:** Tropical dolphins · Ecological niche · Habitats · Stable isotopes · Carbon · Nitrogen · South-west Indian Ocean · Mayotte

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## INTRODUCTION

Understanding niche segregation processes is critical in ecology, particularly when investigating the ecology of species communities. A community can be defined as a collection of species that occurs together in a common environment or habitat, the organisms making up the community being somehow integrated or interacting as a society (Chapman & Reiss 1999). Each species has its own unique niche (Grinnell 1924). The ecological niche is a complex set of variables

structured along 3 main axes: habitat (influence of environmental variables), diet (diet composition, trophic level and prey quality) and time (use of habitat and resources according to time, such as seasons and time of day). Sympatric species with similar ecological requirements would compete for resources and their coexistence requires some degree of habitat and resource segregation (Pianka 1974). Similar species that co-occur are thought to compete for resources unless they occupy different physical locations or feed on different prey. A shared resource in limited supply

<footnote n="1">¹Littoral Environnement et Sociétés (LIENSs), UMR 6250 CNRS-Université de la Rochelle, 2 rue Olympe de Gouges, 17000 La Rochelle, France</footnote>

<footnote n="2">²Direction de l'Environnement et du Développement Durable, Collectivité Départementale de Mayotte, BP 101, 97600 Mamoudzou, Mayotte, France</footnote>

<footnote n="3">³Office National de la Chasse et de la Faune Sauvage, Cellule Technique Océan Indien, BP 27, Coconi, Mayotte, France</footnote>
will bring about competition between members of the same species (intra-specific competition) or between individuals of different species (inter-specific competition) (Roughgarden 1976). Intra-specific competition may be expressed by sex or age related difference in habitat and resource use and has consequences on social structures. Inter-species competition can take various forms, including direct interference (aggressive behaviour) and exploitation-competition, in which individuals indirectly compete for resources (Begon et al. 1986).

Investigating segregation processes within communities of organisms that have similar size and morphology has been particularly challenging. In such communities, niche partitioning is difficult to assess as it can occur over small spatial and temporal scales. For example, in species with similar morphology (e.g. body size, jaw or beak shape, etc.), feeding niches are distinct even when feeding occurs in both species within the same area (MacArthur 1958). Niche segregation has been investigated in a number of top marine predator communities, including large teleost fish (Potier et al. 2004, Ménard et al. 2007), sharks (Estrada et al. 2003, Domi et al. 2005, Papastamatiou et al. 2006), seabirds (Ridoux 1994, Cherel et al. 2008, Jaeger 2009), and marine mammals (Das et al. 2003, Whitehead et al. 2003, Praca & Gannier 2008) including delphinids (Pusineri et al. 2008, Gross et al. 2009, Kiszka et al. 2010). Methods used to discriminate niches were variable, including stomach content, stable isotope and heavy metal analyses and habitat assessment (including habitat modelling). For example, niche partitioning has been assessed in polar communities using stable isotope analyses of C and N, such as in Antarctic pinnipeds, showing clear ecological segregation between species (Zhao et al. 2004). Conversely, in tropical sympatric seabirds, important overlap of feeding niches has been found, which may be interpreted by the low productivity of tropical oligotrophic waters, leading these predators to share same feeding resources that are not quantitatively limited (Cherel et al. 2008). In the tropical cetacean community of the Bahamas, it has been shown using a habitat analysis that the ecological niches of 4 cetacean species (Atlantic spotted dolphin *Stenella frontalis*, Blainville's beaked whale *Mesoplodon densirostris*, Cuvier's beaked whale *Ziphius cavirostris* and dwarf sperm whale *Kogia simus*) do not overlap. Other cetacean species are observed in the area only during the season when prey abundance is sufficiently high to support their presence, while they are competitively excluded for the rest of the year (MacLeod et al. 2004).

Around the tropical island of Mayotte (Comoros, SW Indian Ocean), a great diversity of cetaceans has been found within a limited geographical range, i.e. at least

19 species within an area of 2500 km² (Kiszka et al. 2007). In this area, high cetacean diversity may be associated by the presence of a wide range of marine habitats within close proximity to one another: turbid mangrove fronts, fringing reef systems, clear lagoon areas, barrier and double barrier reef-associated habitats, a steep insular slope and deep oceanic waters. In some locations <3 km away from the barrier reef around the Mayotte lagoon, water depth extends beyond 1,000 m. The permanent presence of odontocetes within a restricted range suggests that fine-scale mechanisms allow for the partitioning of habitats and/or resources. The 4 most common dolphin species there range in size from the 1.8 m spinner dolphin *Stenella longirostris* (the smallest) to the 2.8 m melon-headed whale *Peponocephala electra* (the largest). Other species include Indo-Pacific bottlenose dolphin *Tursiops aduncus*, pantropical spotted dolphin *S. attenauata* and Fraser's dolphin *Lagenodelphis hosei* (Kiszka et al. 2007). The Indo-Pacific bottlenose dolphin is typically a coastal species, feeding on inshore prey (Amir et al. 2005), and lives inside the lagoon around Mayotte (Gross et al. 2009). Conversely, the other species of the community are oceanic and primarily occur outside the lagoon and feed on epipelagic to mesopelagic oceanic prey (Dolar et al. 2003, Brownell et al. 2009). A preliminary study of the tropical delphinid community around the island of Mayotte indicated that their ecological niches at least partially, overlapped (Gross et al. 2009). Using sighting data related to environmental variables and stable isotope analyses from biopsy samples, it was shown that the Indo-Pacific bottlenose dolphin had a coastal/lagoonal distribution, while the spinner dolphin, melon-headed whale and pantropical spotted dolphin had similar habitat characteristics along the outer reef slope. Stable isotope analyses from a small amount of biopsy samples allowed species of the community to be discriminated isotopically, except the 2 congeneric and 'sibling' dolphins of the genus *Stenella*, having similar morphological characteristics and frequently forming inter-species aggregations. Methodological constraints and limited sample size are likely explanations for the absence of measurable differences between species. Therefore, the present work aims to characterize habitat and resource partitioning among delphinids living in sympatry around the island of Mayotte from multiple lines of evidence along the following axes: habitat, diet (more particularly trophic level and foraging habitat) and time (seasons and time of day, Table 1). In this study, we hypothesized that each delphinid species occupies its own ecological niche, defined by at least 1 of the indicator used. Indeed, for any given pair of species, statistical difference should be found for at least 1 of the variables tested (habitat, stable isotope
<table><caption>Table 1. Methodology used to explore the 3 main dimensions of the ecological niche. All explore seasonal variation</caption><thead><tr><th rowspan="2">Variables tested</th><th colspan="3">Niche dimensions</th></tr><tr><th>Habitats</th><th>Resources</th><th>Time</th></tr></thead><tbody><tr><td>Distribution and associated habitat characteristics</td><td>Habitat defined on physiographic aspects</td><td></td><td></td></tr><tr><td>Activity budget</td><td></td><td></td><td>Daily activity rhythm</td></tr><tr><td>N isotopic signature</td><td></td><td>Trophic level</td><td></td></tr><tr><td>C isotopic signature</td><td>Habitat along a coastal-oceanic gradient</td><td></td><td></td></tr></tbody></table>

values and temporal variations). We investigated habitat of delphinids in relation to physiographical variables, activity budgets and their variability among species and according to time, and stable isotope analyses (δ¹³C and δ¹⁵N) from biopsy samples. δ¹³C and δ¹⁵N isotopes help elucidate habitat use (e.g. δ¹³C values typically vary from ¹³C depleted in offshore, or pelagic-derived, to ¹³C enriched from inshore or benthic-derived C) and the position of the consumer in the food chain, respectively (Hobson 1999). They can also reflect local baseline differences in coastal waters (Mallela & Harrod 2008). The use of these isotopes provided alternative information from which to better understand top predator ecology, including marine mammals (Das et al. 2003). Activity budgets were investigated for the 3 most common species (spinner, spotted and Indo-Pacific bottlenose dolphins) in order to compare daily variation in behaviour and habitat utilization. It allowed us to investigate 1 of the temporal dimension of the niche at a short time scale (time of day). We also assessed seasonal variations of habitat preferences, behavioural budgets and stable isotope signatures, as seasonality may be a major factor segregating species among them.

## MATERIALS AND METHODS

**Study area.** Mayotte (12° 50' S, 45° 10' E) is located in the north-eastern Mozambique Channel and is part of the Comoros archipelago (Fig. 1). The island is surrounded by a 197 km long barrier reef, with a second double-barrier in the southwest and the submerged reef complex of Iris in the northwest. The lagoon and surrounding reef complexes are 1500 km² with an average depth of 20 m and a maximum depth of 80 m found in the western, older region of the lagoon (Quod et al. 2000). The insular slope on the exterior of the barrier reef is very steep and contains many submarine canyons and volcanoes (Audru et al. 2006). The island

of Mayotte is characterized by the presence of high cetacean diversity (19 species including 12 delphinids; Kiszka et al. 2007). The most common species are the spinner dolphin *Stenella longirostris*, the pantropical spotted dolphin *S. attenuata*, the Indo-Pacific bottlenose dolphin *Tursiops aduncus* and the melon-headed whale *Pepo-nocephala electra*; these occur year-round (Kiszka et al. 2007).

**Data and sample collection.** From July 2004 to April 2009, small boat based surveys were undertaken around Mayotte. Several types of boats were

used to collect data. Surveys were conducted throughout the study period during the day between 07:00 and 18:00 h in sea conditions not exceeding Beaufort 3. Survey vessels did not follow pre-defined transects, but every attempt was made to sample the whole daylight period as well as each habitat type within the surrounding waters of Mayotte, i.e. coastal areas, lagoonal waters, barrier reef associated areas (inner and outer slopes) and oceanic or slope waters (>500 m). When delphinids were encountered, standard sighting data were recorded: species, group size (maximum,

<figure><img src="image_3.png" /><figcaption>Fig. 1. The study area: Mayotte Island (12° 50' S, 45° 10' E), Comoros archipelago</figcaption></figure>
minimum, best estimate), geographic position and be-
havioural activity. The predominant activity was de-
fined as the behavioural state in which most animals
(>50%) of the group were involved at each instanta-
neous sampling. Typically, >90% of the animals in a
group were engaged in the same activity.

In order to measure behaviour of the focal dolphin
species and determine their behavioural budgets, focal
group follows were used (Mann 1999). While one of
the preferred options in behaviour sampling is to fol-
low a focal individual (Mann 1999), this method was
not suitable for large aggregations of oceanic dolphins.
In addition, following groups, rather than individuals,
is more suitable for behavioural studies as appropriate
conditions for individual sampling are rare in diving
cetaceans (Whitehead 2004). Individual follows were
generally possible in the easily identifiable Indo-
Pacific bottlenose dolphins, but not on every occasion,
as some individuals were not identifiable; for compara-
tive purposes, we used a focal group protocol that has
been used in other studies on similar models (Neu-
mann & Orams 2006). The encountered group was
approached slowly (typically at 2 to 3 knots) from the
side and rear, with the vessel moving in the same
direction as the animals. Groups were scanned, includ-
ing all individuals, to negate attention being drawn to
only specific individuals or behaviours (Mann 1999).
During focal follows, dolphin behaviour was recorded
every 5 min. Five categories of behavioural states were
defined: milling, resting, travelling, feeding/foraging
(hereafter foraging), and socializing as defined in pre-
vious studies (e.g. Norris & Dohl 1979, Bearzi 2005,
Neumann & Orams 2006, Degrati et al. 2008). Feeding
was characterised by loose to disperse group forma-
tions, and dolphins were observed swimming in circles
and pursuing fishes (prey observed at the surface).
Preys were frequently seen at the surface during
foraging activity. Bottlenose dolphins frequently
exhibited large preys at the surface. Travelling con-
sisted of persistent and directional movements of all
the individuals of a group. Milling was characterised
by non-directional movements of the dolphin, with
frequent changes in heading. Socialising consisted in
frequent interactions between individuals in the form
of body contacts, with high-speed movements, fre-
quent changes in direction and aerial displays. Resting
was characterised by low level of activity, with
groups in tight formations and little evidence of for-
ward propulsion. Surfacings are slow and relatively
predictable.

For stable isotope analyses, biopsy attempts were
made when groups and individuals were easily ap-
proachable and when conditions were optimal (Beau-
fort < 2, dolphins closely approaching the boat). Opti-
mal weather conditions allowed stability of the

research boat and better chances to sample the ani-
mals successfully and safely. Biopsies were collected
by using a crossbow (Barnett Veloci-Speed Class,
68-kg draw weight) with Finn Larsen (Ceta-Dart) bolts
and tips ( dart: 25 mm long, 5 mm diameter). A conical
plastic stopper caused the bolt to rebound after the
impact with the dolphin. The dolphins were hit below
the dorsal fin when sufficiently close (3 to 10 m) to the
research boat. Approaches of focal groups/individuals
were made under power at speeds of 1 to 4 knots.
Blubber and skin biopsy samples were preserved indi-
vidually in 90% ethanol before shipping and sub-
sequent analysis. Ethanol was the most suitable
preservative that could be used due to logistical con-
straints. The increase in δ¹³C values is generally con-
sidered to be due to the extraction of some lipids, but
because lipids are depleted in ¹³C, they are typically
extracted (or corrected arithmetically, e.g. Kiljunen et
al. 2006) to avoid a bias in estimates of δ¹³C values (De
Niro & Epstein 1978, Tieszen et al. 1983) that likely
cancels any potential effect of storage in ethanol
(Kiszka et al. 2010). Biopsy sampling was conducted
under French scientific permits no. 78/DAF/2004 (Sep-
tember 10, 2004) and no. 032/DAF/SEF/2008 (May 16,
2008) after examination of the project by the Conseil
National de Protection de la Nature.

Muscle samples from several fish species were also
collected for stable isotope analyses, especially to
investigate trophic interactions between delphinids
and potential dolphin preys as well as fish species with
clear ecological profiles (see below). Fish specimens
were collected in a local fish market. Fish muscle sam-
ples were sampled in April 2009 and preserved in
ethanol before subsequent analyses. The fish species
selected were pelagic, demersal and benthic species
from reef associated habitats, i.e. from various environ-
ments in the lagoon and surrounding waters, and dif-
ferent trophic levels (herbi-, plankti- and piscivorous):
*Hemiramphus far*, epipelagic, inhabiting waters near
reef systems and feeding on the pelagic zooplankton;
*Mulloidichthys vanicolensis*, demersal on seaward
reefs, feeding on small worms and crustaceans;
*Siganus argenteus*, demersal, inhabiting coastal and
inner reef slopes and feeding on algae; *Scarus russelii*,
demersal, inhabiting shallow coastal reef and feeding
on algae by grazing on coral bubble; and *Caranx
melampygus*, demersal and pelagic predator feeding
on small schooling fishes (Froese & Pauly 2010). *H. far*
and *C. melampygus* were sampled because they re-
gularly enter the diet of the Indo-Pacific bottlenose
dolphin (J. Kiszka & C. Pusineri pers. obs.).

**Habitat analyses.** We constituted a database in which every dolphin group observation was associated with the physiographic characteristics (distance from the coast and from the nearest reefs, depth and slope of
seafloor) corresponding to the GPS fixes of the observation. Bathymetric data were obtained from Service Hydrographique et Océanographique de la Marine (SHOM). Interpolation of bathymetry data, needed to generate depth and slope data for each sighting, was undertaken with the extension Spatial Analyst by kriging transformation of the raster file into an interpolated data file. The distance data were obtained using GIS software ArcView (ArcGIS 8.3) by ESRI (Environmental Systems Research Institute). We represented the distribution of the 4 dolphin species investigated in relation to the environmental predictors using kernel density plots to view the distribution of species. In order to differentiate species niches, we performed multidimensional scaling (MDS) using Euclidian distances between individual habitat characteristics. Metric multidimensional scaling (MDS) takes a set of dissimilarities and returns a set of points such that the distances between the points are approximately equal to the dissimilarities. It displays the structure of distance-like data as a geometrical picture (Gower 1966). In other words, the purpose of MDS is to provide a visual representation of the pattern of proximities (i.e. similarities or distances) among a set of objects. This multivariate analysis was used in order to discriminate species in their habitat preferences. Presence-absence models were not used due to heterogeneous sampling of the study area (for further details see Clarke & Warwick 2001).

In order to complement this multivariate approach, univariate non-parametric pairwise Wilcoxon tests were used to compare species distribution for each environmental variable. Seasonal differences of habitat preferences were investigated using Mann-Whitney U-tests for each species in relation to the 4 environmental co-variates that were used. We considered 2 seasons: summer (rainy; November to April) and winter (dry; May to October). Analyses were performed using Rv2.10.0 (R Development Core Team 2009).

**Behavioural budget analyses.** To analyse diel patterns of behaviour, we defined 3 time-blocks: morning (before 10:00 h), noon (between 10:01 h and 14:00 h) and evening (after 14:01 h). The seasons considered were identical to those used for the habitat analyses (dry and rainy season). Diurnal and seasonal patterns were investigated by assigning a behavioural sequence to a time block or a season. Contingency table analyses were used in order to compare behavioural budgets among species. Nonparametric tests were selected because assumptions regarding normality and homogeneity of variance were not met.

**Stable isotope analyses.** Blubber and skin were separated for each dolphin biopsy sample. Fish muscle tissues were used for stable isotope analyses. The ethanol was evaporated at 45°C over 48 h, and the samples

were ground and freeze-dried (Hobson et al. 1997). Lipids were removed from both blubber and skin samples by 2 successive extractions (1 h shaking in cyclohexane at room temperature and subsequent centrifugation) prior to analysis. After drying, small subsamples (0.35 to 0.45 ± 0.001 mg) were prepared for analysis. Stable isotope measurements were performed with a continuous-flow isotope-ratio mass spectrometer (Delta V Advantage, Thermo Scientific, Germany) coupled to an elemental analyser (Flash EA1112 Thermo Scientific, Italy). Reference gas were calibrated against International Reference Materials (IAEA-N1, IAEA-N2 and IAEA-N3 for nitrogen; NBS-21, USGS-24 and IAEA-C6 for carbon). Results are expressed in the δ notation relative to PeeDee Belemite and atmospheric N₂ for δ¹³C and δ¹⁵N, respectively, according to the equation:

$$ \delta X = \left[ \frac{R_{\text{sample}}}{R_{\text{standard}}} - 1 \right] \times 1000 \quad (1) $$

where X is ¹³C or ¹⁵N and R is the isotope ratio ¹³C/¹²C or ¹⁵N/¹⁴N, respectively. Replicate measurements of a laboratory standard (acetanilide) indicated that analytical errors were <0.1‰ for δ¹³C and δ¹⁵N. Percent C and N elemental composition of tissues were obtained using the elemental analyzer and used to calculate the sample C:N ratio, indicating good lipid removal efficiency when C:N < 4. Differences of stable isotopes values of δ¹⁵N and δ¹³C among species were tested using non-parametric Kruskal-Wallis and Mann-Whitney U-tests. Seasonal variations were investigated using Mann-Whitney U-tests. Like for seasonal variations of habitat preferences, dry summer and rainy winter season were considered.

# RESULTS

## Field effort and data collected

From July 2004 to April 2009, during 224 boat-based surveys, a total of 355 sightings of the targeted species was collected (92% of cetacean encounters around Mayotte): 195 for *Stenella longirostris*, 95 for *Tursiops aduncus*, 53 for *S. attenuata* and 12 for *Peponocephala electra*. The spatial distribution of observation effort and initial encounters is presented in Fig. 2A,B. Overall, spatial distribution of effort was heterogeneous but covered all available habitats around the island, both inside and outside the lagoon.

We collected biopsy samples from the 4 focal delphinids from December 2004 to April 2009 (*Stenella longirostris*, n = 28; *S. attenuata*, n = 22; *Tursiops aduncus*, n = 28 and *Peponocephala electra*, n = 20) and
from another species, the Fraser's dolphin *Lagenodelphis hosei* (n = 7), during a single and unique encounter (in association with a group of melon-headed whales) in January 2005. Seasonal distribution of sighting data and biopsy samples was balanced, allowing for analyses of seasonal patterns of variation of habitat and stable isotope signatures (Table 2). For fish and stable isotope analyses in muscle samples, sample size was distributed as follows: *Hemiramphus far*, n = 5; *Mulloidichthys vanicolensis*, n = 5; *Siganus argenteus*, n = 5; *Scarus russelii*, n = 5; and *Caranx melampygus*, n = 2.

Focal follows were performed on 33 groups of spinner dolphins (total time spent = 37.1 h; n = 466 behavioural sequences), 28 groups of Indo-Pacific bottlenose dolphins (25.5 h; n = 413) and 12 groups of pantropical spotted dolphins (16.3 h; n = 193). The melon-headed whale was not included in the behavioural budget analysis as sample size was too small (4 focal follows). Focal follows were undertaken all around the island.

## Habitat differentiation

Table 3 presents distribution of the 4 species investigated in relation to environmental predictors. Table 4

<table><caption>Table 2. Seasonal distribution (winter: dry, May–Oct; summer: rainy, Nov–Apr) of sightings and biopsy samples collected Dec 2004–Apr 2009</caption><thead><tr><th rowspan="2">Species</th><th colspan="2">Sightings</th><th colspan="2">Biopsies</th></tr><tr><th>Winter</th><th>Summer</th><th>Winter</th><th>Summer</th></tr></thead><tbody><tr><td>Tursiops aduncus</td><td>48</td><td>43</td><td>12</td><td>16</td></tr><tr><td>Stenella longirostris</td><td>101</td><td>67</td><td>12</td><td>13</td></tr><tr><td>Stenella attenuata</td><td>13</td><td>23</td><td>12</td><td>10</td></tr><tr><td>Pepuocephala electra</td><td>5</td><td>6</td><td>10</td><td>10</td></tr><tr><td>Lagenodelphis hosei</td><td>0</td><td>1</td><td>0</td><td>7</td></tr></tbody></table>

presents correlations between variables. Only 2 variables were significantly correlated: distance from the coast and depth (p = 0.001). Density plots show that habitat of the 4 species were not well differentiated, excluding 2 habitat axes: depth and distance from the coast (Fig. 3). For these variables, the Indo-Pacific bottlenose dolphin occurs significantly closer to the shore and in shallower waters, whereas the 3 other species are not well discriminated. For the MDS, Axes 1 and 2 explained 78.4 and 21.2% of the variance, respectively (Fig. 4). The plot slightly discriminated the Indo-Pacific bottlenose dolphin, but segregation among the other 3 species appeared relatively weak. The pairwise comparison (Wilcoxon tests) of species distribution for each

<figure><img src="image_4.png" /><figcaption>Fig. 2. Spatial distribution of (a) observation effort per 1 km² cell and (b) dolphin sightings around Mayotte, Jul 2004–Apr 2009</figcaption></figure>
<table><caption>Table 3. Distribution of delphinids in relation to physiographic variables. Q1 and 3: 1st and 3rd quartiles</caption><thead><tr><th></th><th>Mean</th><th>Median</th><th>SD</th><th>Q1</th><th>Q3</th></tr></thead><tbody><tr><td><strong>Depth (m)</strong></td><td></td><td></td><td></td><td></td><td></td></tr><tr><td>Tursiops aduncus</td><td>48</td><td>32</td><td>70</td><td>20</td><td>45</td></tr><tr><td>Stenella longirostris</td><td>221</td><td>231</td><td>176</td><td>72</td><td>286</td></tr><tr><td>Stenella attenuata</td><td>301</td><td>276</td><td>277</td><td>45</td><td>370</td></tr><tr><td>Peponocephala electra</td><td>487</td><td>462</td><td>244</td><td>275</td><td>666</td></tr><tr><td><strong>Slope (°)</strong></td><td></td><td></td><td></td><td></td><td></td></tr><tr><td>T. aduncus</td><td>2.1</td><td>0</td><td>6.7</td><td>0</td><td>0.8</td></tr><tr><td>S. longirostris</td><td>9.5</td><td>0</td><td>17.9</td><td>0</td><td>7.9</td></tr><tr><td>S. attenuata</td><td>9.7</td><td>0</td><td>19.7</td><td>0</td><td>2.9</td></tr><tr><td>P. electra</td><td>13.6</td><td>0</td><td>20.4</td><td>0</td><td>39.8</td></tr><tr><td><strong>Distance coast (m)</strong></td><td></td><td></td><td></td><td></td><td></td></tr><tr><td>T. aduncus</td><td>2002</td><td>996</td><td>2170</td><td>488</td><td>2779</td></tr><tr><td>S. longirostris</td><td>5259</td><td>5068</td><td>2764</td><td>3217</td><td>7192</td></tr><tr><td>S. attenuata</td><td>6295</td><td>5772</td><td>3331</td><td>3922</td><td>8603</td></tr><tr><td>P. electra</td><td>6666</td><td>7086</td><td>2131</td><td>5370</td><td>8520</td></tr><tr><td><strong>Distance reef (m)</strong></td><td></td><td></td><td></td><td></td><td></td></tr><tr><td>T. aduncus</td><td>1363</td><td>509</td><td>2072</td><td>269</td><td>1474</td></tr><tr><td>S. longirostris</td><td>1060</td><td>700</td><td>1145</td><td>478</td><td>1321</td></tr><tr><td>S. attenuata</td><td>2012</td><td>1210</td><td>2000</td><td>722</td><td>2702</td></tr><tr><td>P. electra</td><td>2452</td><td>1363</td><td>3015</td><td>928</td><td>2564</td></tr></tbody></table>

<table><caption>Table 4. Correlation between variables. Above diagonal: Pearson's correlation values. Below diagonal: associated p values</caption><thead><tr><th></th><th>Distance coast</th><th>Distance reef</th><th>Slope</th><th>Depth</th></tr></thead><tbody><tr><td>Distance coast</td><td>-</td><td>0.27</td><td>-0.13</td><td>0.01</td></tr><tr><td>Distance reef</td><td>&lt;0.001</td><td>-</td><td>0.13</td><td>0.34</td></tr><tr><td>Slope</td><td>0.020</td><td>0.028</td><td>-</td><td>0.24</td></tr><tr><td>Depth</td><td>&lt;0.001</td><td>0.731</td><td>&lt;0.001</td><td>-</td></tr></tbody></table>

variable provided more significant results. For depth, the 3 species occurring essentially outside the lagoon (*Stenella longirostris*, *S. attenuata* and *Peponocephala electra*) could not be discriminated (p > 0.05), while the *Tursiops aduncus* significantly differed from the 3 others (all p < 0.001). Slope did not segregate any species. The variable 'distance from the coast' significantly segregated *T. aduncus* from the 3 other species (all p < 0.0001). The variable 'distance from the nearest reef' was significantly discriminant among the oceanic species: *S. longirostris* with *S. attenuata* (p = 0.002), *S. longirostris* with *P. electra* (p = 0.03). For all variables, *P. electra* and *S. attenuata* were never discriminated (p > 0.05). In all delphinid species, no seasonal variation of habitat preferences was observed for any variable (all p > 0.05).

## Behavioural budgets

As we used 4 types of vessel for collecting behavioural data, we tested for a potential boat effect on the data but failed to find a significant difference ($\chi^2 = 3.238$; df = 4; p = 0.569); therefore, subsequent analyses reflect a pooled data set. In Indo-Pacific bottlenose dolphins, the most frequent activities recorded were milling (32%), travelling (22%) and foraging (16%) (Fig. 5). A quite similar pattern was also observed in the pantropical spotted dolphin, with travelling being the prevalent activity (32%), followed by milling (22%) and foraging (18%). In the spinner dolphin, socialising was the most commonly recorded behaviour (28%), followed by travelling (26%) and milling (22%) (Fig. 5), while foraging behaviour was not observed. Among the 3 species, significant differences in activity budgets were found ($\chi^2 = 177.33$; df = 12; p < 0.0001). These differences were confirmed when performing pairwise comparisons: *Tursiops aduncus* versus *Stenella longirostris* ($\chi^2 = 137.50$; df = 6; p < 0.0001), *T. aduncus* versus *S. attenuata* ($\chi^2 = 53.42$; df = 6; p < 0.001) and *S. longirostris* versus *S. attenuata* ($\chi^2 = 109.18$; df = 6; p < 0.0001).

## Temporal variation of activity budgets

For all species, no significant variations of activity patterns were observed among seasons ($H = 3.816$; df = 3; p = 0.439). Contrasting, behaviour patterns varied significantly according to time of day for Indo-Pacific bottlenose dolphin ($\chi^2 = 48$; df = 5; p < 0.001), spinner dolphin ($\chi^2 = 13$; df = 5; p = 0.002) and pantropical spotted dolphin ($\chi^2 = 11$; df = 5; p = 0.009) (Fig. 6A–C). In Indo-Pacific bottlenose dolphins, foraging activities were prevalent during the morning and decreased throughout the day, whereas socializing was more frequent in the afternoon. In spinner dolphins, travelling activities increased along the day and social activities were more observed in the morning and the afternoon, whereas resting behaviour was more predominant around noon time. Finally, in pantropical spotted dolphins, feeding behaviour prevailed during the afternoon, along with travelling.

Activity budgets did not vary with water depth in Indo-Pacific bottlenose dolphin ($H = 2.060$; df = 4; p = 0.725), spinner dolphin ($H = 5.621$; df = 4; p = 0.229) and pantropical spotted dolphin ($H = 8.049$; df = 4; p = 0.09). However, activity budget varied with distance from the coast for Indo-Pacific bottlenose dolphin ($H = 9.542$; df = 4; p = 0.04; especially increasing foraging activity closer to shore), although not for either spinner ($H = 3.251$; df = 4; p = 0.517) or pantropical spotted dolphins ($H = 4.201$; df = 4; p = 0.379). Feeding activities of
<figure><img src="image_5.png" /><figcaption>Fig. 3. Density plots of dolphin sightings around Mayotte in relation to physiographical variables: distance from (a) the nearest reefs (m) and (b) the coast (m); (c) slope (°); and (d) depth (m). Pe: *Peponocephala electra*; Ta: *Tursiops aduncus*; Sl: *Stenella longirostris*; Sa: *S. attenuata*</figcaption></figure>

the Indo-Pacific bottlenose dolphin increased with decreasing distance from coast.

Stable isotope analyses

Stable isotope values of delphinids and fish were sig-
nificantly different, as shown in Fig. 7. The most appar-
ent pattern was the higher trophic level of delphinids,
reflected by higher δ¹⁵N values. In addition, δ¹³C val-
ues in delphinids were lower than in fish.

In delphinids, stable isotope values were lower in
blubber than in skin. However, the pattern of differ-
ences observed between species was similar in both tis-
sues (Figs. 8 & 9). The Fraser's dolphin shows a high
marginality in comparison to the other species, with sig-
nificantly higher δ¹⁵N values in the blubber (Fig. 8).
However, for skin values, an overlap was observed with
the melon-headed whale (Table 5). Overall, among
species, significant differences in the skin existed for
δ¹⁵N (*H* = 33.6; df = 2; p < 0.0001) and δ¹³C (*H* = 53.6; df =
1; p < 0.0001). For blubber, significant differences were

also found for δ¹⁵N (*H* = 49.7; df = 1; p < 0.0001) and δ¹³C
(*H* = 63; df = 1; p < 0.0001). A similar statistical differ-
ence among species for blubber tissue was found, even
when excluding the Fraser's dolphin, very different to
the 4 other species (*H* = 34; df = 2; p < 0.0001 for δ¹⁵N
and *H* = 60; df = 2; p < 0.0001 for δ¹³C). The Indo-Pacific
bottlenose dolphin had the greatest δ¹³C values, while
the lowest values were observed in the Fraser's dolphin
and in the 2 species of the genus *Stenella*. The melon-
headed whale had intermediate values of δ¹³C, both for
skin and blubber (Figs. 8 & 9). When looking at pair-
wise comparisons of δ¹⁵N and δ¹³C values in blubber
and skin tissues, however, some degrees of overlap can
be observed (Table 5). From skin samples, δ¹⁵N values
were significantly different between species pairs, ex-
cept between *S. attenuata* and *Tursiops aduncus* and
between *Lagenodelphis hosei* and *Peponocephala*
*electra* (U-tests, p > 0.05). For δ¹³C values, overlap was
evident between *L. hosei* and the 2 species of the genus
*Stenella*. Finally, for blubber tissue, δ¹⁵N values were
significantly different between species pairs, except
between *S. attenuata* and *P. electra* and between *S. at-*
<figure><img src="image_6.png" /><figcaption>Fig. 4. Metric MDS plot of delphinid habitat in relation to physiographical variables. Pe: *Peponocephala electra*; Ta: *Tursiops aduncus*; Sl: *Stenella longirostris*; Sa: *Stenella attenuata*</figcaption></figure>

values in delphinids. Among fish, significant differences were observed for $\delta^{13}$C ($H$ = 11.2; df = 4; p = 0.02) and $\delta^{15}$N ($H$ = 11.6; df = 4; p = 0.01). *Siganus argenteus* and *Scarus russelii* (herbivores) had the lowest trophic position ($\delta^{15}$N), while *Caranx melampygus*, the most predatory species, had the highest trophic level ($\delta^{13}$N). Their foraging habitats were also well discriminated, with *Mulloidichthys vanicolensis* having the highest $\delta^{13}$C values and *C. melampygus* with *Hemiramphus far* the lowest (Fig. 7). These latter were about 0.5 to 1.5‰ $\delta^{13}$C and 3 to 4‰ $\delta^{15}$N lower than *T. aduncus*.

Seasonal variations of stable isotope signatures were observed in all species for skin and blubber tissues (Table 6). In the 2 species of the genus *Stenella* and the melon-headed whale, $\delta^{13}$C values were more negative during the rain season. A reverse situation was observed in *Tursiops aduncus* during the rainy season; $\delta^{15}$N values were decreasing for *Stenella* dolphins and *Peponocephala electra*, while they increased in *T. aduncus*.

However, while (sometimes) statistically significant in some cases, seasonal variations appear to be limited.

<figure><img src="image_7.png" /><figcaption>Fig. 5. Overall activity budgets for Indo-Pacific bottlenose dolphins, pantropical spotted dolphins and spinner dolphins around Mayotte, 2004–2009</figcaption></figure>

*Stenella attenuata* and *T. aduncus*. $\delta^{13}$C values showed the highest degrees of overlap, particularly between *S. longirostris* and *S. attenuata*, between *S. attenuata* and *L. hosei*, and between *L. hosei* and *P. electra* (U-tests; p > 0.05; Table 5). Stable isotope values from fish samples were useful in order to provide a context to interpret

# DISCUSSION

## General

This work represents a detailed study on habitat and resource segregation among tropical dolphins around Mayotte, in the southwest Indian Ocean. It integrates several methods implemented over 4 yr, with varying temporal resolutions: from instantaneous sighting data and behavioural observations collected during daylight hours, to stable isotope analyses on skin, which represent the foraging niche over days, or on the blubber, which integrates stable isotope signatures over months (Abend & Smith 1995). The indicators were selected for their ability to document the main dimensions of the ecological niche along which segregation might occur: physiographic characteristics describe the spatial dimension of the ecological niche, C isotopic signature focuses on the coastal-offshore gradient of the foraging niche, N isotopic signature expresses the resource dimension of the niche, and the daily activity budget deals with the temporal dimension.

Overall, the main finding of this work is that none of the indicators of trophic niche dimensions on their own
<figure><img src="image_8.png" /><figcaption>Fig. 6. Within day variations of behavioural budget in (a) spinner dolphin, (b) Indo-Pacific bottlenose dolphin and (c) pantropical spotted dolphin around Mayotte, 2004–2009</figcaption></figure>

reveal complete ecological segregation amongst the 4 species studied, but the combination of all indicators do (Table 7). Hence, physiographic characteristics of habitats used by the dolphins during daylight, when visual observations were possible, only allow the Indo-pacific bottlenose dolphin to be differentiated from the others. Carbon isotope signatures allow the melon-headed whale to be separated from the *Stenella* dolphins. Finally N isotopic signature and activity budget identify differences between spinner and pantropical spotted dolphins.

Identifying the limitations of the study is necessary for delineating its validity range. Most daily field trips were undertaken from Mayotte's main harbour located on the east coast of the island and were limited to daylight hours. Hence, effort was concentrated in the lagoon and the vicinity of the barrier reef's outer slope, within the 1000 m isobath, and nocturnal distribution and activity could not be documented. The resource dimension of the niche was documented in a very integrated way, as C and N isotopic contents of a predator express foraging habitat and trophic level but not diet *per se*, which is only documented by sporadic direct observations when no biological material is available. Also, in stable isotopes analyses, as in most studies relying on the use of ecological tracers transmitted via food (e.g. fatty acids, contaminants, heavy metals), only differences in stable isotope contents are really informative, whereas similarities may result from a variety of prey combinations. Finally, behavioural budget data is limited by our capacity to infer dolphin underwater activity from surface events. In particular, foraging, which is the key activity to consider when investigating segregation mechanisms, can either be associated to no or barely visible surface events or to explicit and often highly dynamic ones. Nonetheless, in a multifaceted approach as the one followed here,

the limitations of each indicator tend to be compensated by the others. For instance, stable isotope analyses reveal foraging habitat and trophic level of prey eaten day and night over the past few days or months, which is extremely useful to disentangle the inherent ambiguities of observations limited to daylight hours. Conversely, behavioural data can help identify differences in foraging strategies that cannot be found in stable isotope analyses.

The ecological significance of these indicators will now be interpreted sequentially from those related to the spatial, the resource and finally the temporal dimensions of the ecological niche.

## Spatial segregation inferred from direct observations and $\delta^{13}$C signatures

This study confirms that *Tursiops aduncus* is associated with coastal, shallow water and reef habitats. Its ecological niche clearly differs spatially from the other species of the community. Coastal foraging habitats are confirmed by high $\delta^{13}$C value indicating a benthic carbon source that is primarily available in coastal environments (France 1995, Hobson 1999). Preference for coastal habitat is reported throughout species range, a preference shared with the Indo-pacific humpback dolphin *Sousa chinensis*, which is present in very low numbers around Mayotte, but could not be considered in this work.

*Stenella longirostris* and *S. attenuata* co-occur in waters along the outer slope of the barrier reef around Mayotte. They overlap extensively, but the latter tends to occur in deeper waters, located further offshore. Low $\delta^{13}$C values found in both species, with extensive overlap, are in line with foraging habitats located outside the lagoon at epipelagic depths; this interpretation
<figure><img src="image_9.png" /><figcaption>Fig. 7. Stable isotope values (in ‰) in (a) dolphin skin and fish muscle, (b) lipid-treated dolphin blubber, and (c) lipid-treated dolphin skin. Means ± SE and SD. Bold line: SE, thin line: SD</figcaption></figure>

is reinforced by the overlap also found between the 2 *Stenella* species and the Fraser's dolphin, a typically oceanic dolphin. The pattern observed around Mayotte has also been reported from other insular populations, such as off La Réunion where spotted dolphins occur in deeper, more offshore waters than spinners do (Dulau-Drouot et al. 2008). These 2 species are not restricted to peri-insular waters; instead, populations of the 2 species also dwell in the open ocean (Wade & Gerrodette 1992, Ballance & Pitman 1998). In this situation, extensive overlap in preferred habitat is also observed, as reported from the western South Atlantic and the eastern tropical Pacific (Polacheck 1987, Moreno et al. 2005).

For melon-headed whale, a fairly limited number of sightings were collected, allowing only a partial description of its habitat preferences. Nevertheless, habitat physiographic characteristics of *Peponocephala electra* as documented in this work were significantly different from *Stenella longirostris*, but could not be differentiated from *S. attenuata*. The melon-headed whale has a more oceanic distribution than the other species (Brownell et al. 2009) and it is unknown whether the groups seen around Mayotte are mostly oceanic dwellers that occasionally visit peri-insular waters or if they display some group-specific preference for the peri-insular slope, a habitat that they could exploit around all islands, reefs and seamounts from off the northern end of Madagascar to Grande Comore (western Comoros Archipelago). Quite interestingly, δ¹³C values measured in the melon-headed whale are intermediate between the epi- to mesopelagic *Stenella* and Fraser's dolphins and the coastal dwelling Indo-pacific bottlenose dolphin, rather than being identical to the *Stenella* carbon isotopic content as could be expected from the similarity found in physiographic characteristics. This would suggest spatial segregation along a vertical axis, with melon-headed whales foraging deeper and hence closer to detritic carbon sources than *Stenella* spp. do.

## Resource partitioning inferred from δ¹⁵N signatures

Nitrogen isotopic signatures are the main source of information on resource utilization by dolphins in Mayotte. Direct evidences of resource use are limited to some anecdotal observations of prey hunting or capture by *Tursiops aduncus* and *Stenella attenuata* (J. Kiszka & C. Pusineri, unpubl. obs.). Carbon isotopic signatures of fish collected in the lagoon also convey some contextual information on plausible prey for the more coastal dolphins. Finally, when comparing trophic levels inferred from δ¹⁵N signatures, one should only consider in the comparison dolphin species with
<table><caption>Table 5. Pairwise Mann-Whitney *U*-test *p* values for each pairs of delphinid species in carbon (C) and nitrogen (N) in skin and blubber</caption><thead><tr><th></th><th>Lagenodelphis hosei</th><th>Pepono-cephala electra</th><th>Stenella attenuata</th><th>Stenella longirostris</th></tr></thead><tbody><tr><td><strong>Skin</strong></td><td></td><td></td><td></td><td></td></tr><tr><td><strong>N</strong></td><td></td><td></td><td></td><td></td></tr><tr><td>Tursiops aduncus</td><td>0.01</td><td>0.001</td><td>0.125</td><td>&lt;0.001</td></tr><tr><td>Stenella longirostris</td><td>&lt;0.001</td><td>&lt;0.001</td><td>&lt;0.001</td><td></td></tr><tr><td>Stenella attenuata</td><td>0.01</td><td>0.009</td><td></td><td></td></tr><tr><td>Peponocephala electra</td><td>0.232</td><td></td><td></td><td></td></tr><tr><td><strong>C</strong></td><td></td><td></td><td></td><td></td></tr><tr><td>T. aduncus</td><td>&lt;0.001</td><td>&lt;0.001</td><td>&lt;0.001</td><td>&lt;0.001</td></tr><tr><td>S. longirostris</td><td>0.339</td><td>&lt;0.001</td><td>0.02</td><td></td></tr><tr><td>S. attenuata</td><td>0.157</td><td>0.008</td><td></td><td></td></tr><tr><td>P. electra</td><td>0.008</td><td></td><td></td><td></td></tr><tr><td><strong>Blubber</strong></td><td></td><td></td><td></td><td></td></tr><tr><td><strong>N</strong></td><td></td><td></td><td></td><td></td></tr><tr><td>T. aduncus</td><td>&lt;0.001</td><td>0.022</td><td>0.08</td><td>&lt;0.001</td></tr><tr><td>S. longirostris</td><td>&lt;0.001</td><td>&lt;0.001</td><td>&lt;0.001</td><td></td></tr><tr><td>S. attenuata</td><td>&lt;0.001</td><td>0.485</td><td></td><td></td></tr><tr><td>P. electra</td><td>&lt;0.001</td><td></td><td></td><td></td></tr><tr><td><strong>C</strong></td><td></td><td></td><td></td><td></td></tr><tr><td>T. aduncus</td><td>&lt;0.001</td><td>&lt;0.001</td><td>0.001</td><td>0.001</td></tr><tr><td>S. longirostris</td><td>0.02</td><td>&lt;0.001</td><td>0.182</td><td></td></tr><tr><td>S. attenuata</td><td>0.242</td><td>&lt;0.001</td><td></td><td></td></tr><tr><td>P. electra</td><td>0.112</td><td></td><td></td><td></td></tr></tbody></table>

<table><caption>Table 6. Pairwise Mann-Whitney *U*-test *p* values for seasonal differences of stable isotope signatures for each species and type of tissue. *p* values: ***<0.001, **<0.01, *<0.05</caption><thead><tr><th>Species/Season</th><th>Blubber</th><th>Skin</th></tr></thead><tbody><tr><td><em>Tursiops aduncus</em></td><td></td><td></td></tr><tr><td>Winter</td><td>...</td><td>...</td></tr><tr><td>Summer</td><td>&gt;0.05</td><td>&gt;0.05</td></tr><tr><td><em>Peponocephala electra</em></td><td></td><td></td></tr><tr><td>Winter</td><td>&gt;0.05</td><td>&gt;0.05</td></tr><tr><td>Summer</td><td>&gt;0.05</td><td>**</td></tr><tr><td><em>Stenella attenuata</em></td><td></td><td></td></tr><tr><td>Winter</td><td>&gt;0.05</td><td>&gt;0.05</td></tr><tr><td>Summer</td><td>*</td><td>...</td></tr><tr><td><em>Stenella longirostris</em></td><td></td><td></td></tr><tr><td>Winter</td><td>&gt;0.05</td><td>*</td></tr><tr><td>Summer</td><td>&gt;0.05</td><td>&gt;0.05</td></tr></tbody></table>

<table><caption>Table 7. Ecological niche dimensions among the Mayotte delphinid community. Letters: grouping of species that segregate for the indicator being considered; ni = not investigated</caption><thead><tr><th>Indicator of<br>niche dimensions</th><th>Tursiops<br>aduncus</th><th>Stenella<br>attenuata</th><th>Stenella<br>longirostris</th><th>Peponocephala<br>electra</th></tr></thead><tbody><tr><td>Physiographic characteristics</td><td>A</td><td></td><td>B</td><td></td></tr><tr><td>Carbon isotopic values</td><td>A</td><td></td><td>B</td><td>C</td></tr><tr><td>Nitrogen isotopic values</td><td></td><td>A</td><td></td><td>B</td></tr><tr><td>Daily activity rhythm</td><td>A</td><td>B</td><td>C</td><td>ni</td></tr></tbody></table>

overlapping δ¹³C signatures, i.e. living in the same habitat, because reference levels of δ¹⁵N in oceanic versus lagoon habitats are unknown.

Indo-pacific bottlenose dolphin's isotopic content can be compared to the isotopic values of putative prey fish collected in the lagoon. The herbivorous fish *Siganus argenteus* and *Scarus russelii* have δ¹³C values 2 to 4‰ higher than *Tursiops aduncus*, and would therefore unlikely be important components of its diet. In contrast, blue trevally *Caranx melampygus* and blackbarred halfbeak *Hemiramphus far* display C and N signatures ~0.5–1.5 and 3–4‰ lower respectively than *T. aduncus*; such differences fit well with an enrichment of 1 trophic level. Therefore, these 2 predatory fish would be plausible major prey for *T. aduncus*. Anecdotal direct observations in Mayotte are in line with this interpretation even if other fishes, like the mullet *Mulloidichthys vanicolensis*, were also observed being preyed upon (J. Kiszka & C. Pusineri unpubl.

obs.). Our result is also consistent with existing information on the diet of the Indo-Pacific bottlenose dolphin in the region (Zanzibar, Tanzania), suggesting this species forages on a large number of prey species, especially reef fish (Amir et al. 2005). Elsewhere, *T. aduncus* is known to feed on fish species that do not aggregate in large schools (Mann et al. 2000).

The 2 *Stenella* species have largely overlapping ranges of both physiographic habitats and C isotopic contents, even if *S. attenuata* is seen slightly further offshore and is nonetheless slightly carbon-enriched (higher δ¹³C ratios). According to δ¹⁵N values, pantropical *S. attenuata* are on average 1.5‰ higher than spinner dolphins, i.e. half a trophic level, which would express some degree of niche segregation between the 2 species. In addition to this, *S. attenuata* seems to have a wider niche breadth than *S. longirostris*. Pantropical spotted dolphins have been frequently observed feeding close to the barrier reef where their prey aggregate (fishes of the genus Exocoetidae; J. Kiszka & C. Pusineri unpubl. obs.), in agreement with their slightly higher δ¹³C signature. Fine-scale processes allowing niche differentiation between the 2 *Stenella* species have also been found in other regions, such as in the eastern tropical
Pacific (Perrin et al. 1973). Spinner dolphins there are reported to feed at night upon scattering-layer organisms, i.e. on vertically migrating mesopelagic fishes, cephalopods and crustaceans caught in the upper 200 m and occasionally as deep as 400 m (Perrin et al. 1973, Norris et al. 1994, Dolar et al. 2003). Conversely, pantropical spotted dolphins would feed day and night on epipelagic fishes and cephalopods (Perrin et al. 1973).

Melon-headed whales were observed in much the same habitats as pantropical spotted dolphins, but comparatively higher δ¹³C values suggested vertical segregation could occur. Nitrogen isotopic content further suggests a slightly higher trophic level (about 1/3 trophic level). Earlier works report mesopelagic fishes and cephalopods, supposedly preyed upon in the upper 700 m, as the main component of its diet (Young 1978, Brownell et al. 2009). An element of comparison is provided by Fraser's dolphin, which was added to the study in an attempt to provide isotopic reference for a true oceanic predator; in addition to this, the species is frequently observed forming a mixed group with melon-headed whale (Jefferson & Barros 1997, Kiszka et al. 2007, Dulau-Drouot et al. 2008). Not surprisingly, Fraser's dolphins displayed the second lowest δ¹³C values, in agreement with their oceanic lifestyle, and the highest δ¹⁵N values, that fit well with the higher trophic level, likely associated with its preference for larger prey already reported elsewhere (Dolar et al. 2003). Studies of stomach contents from the Pacific suggest this species feeds on relatively large mesopelagic fish and cephalopods from near the surface to probably as deep as 600 m (Robison & Craddock 1983, Dolar et al. 2003). In Mayotte, Fraser's dolphins and melon-headed whales, although generally seen associated, do not overlap in their isotopic niches, the latter being more δ¹³C enriched than the former, which could be interpreted as feeding a deeper food source, possibly associated to peri-insular slopes, whereas the Fraser's dolphin would rely on large epito-mesopelagic truly oceanic prey. These 2 species might associate for other reasons than foraging, such as social advantage or vigilance against predators.

## Temporal segregation inferred from seasonal patterns and activity budgets

Our study did not reveal seasonal variations of occurrence or habitat preferences as based on the analyses of visual observations; this could be linked to the absence of seasonal variability in tropical environments. On the other hand, stable isotope values displayed significant differences between dry and rainy seasons in all species. Oceanic species, i.e. spinner,

pantropical spotted dolphins and melon-headed whales, showed similar levels of variation. Conversely, the Indo-Pacific bottlenose dolphin differed. This species only foraged in the lagoon and, during the rainy season, its δ¹³C values were enriched, which could be linked to increasing hydrodynamic activity and remobilisation of benthic sources of C in the lagoon. It is therefore suggested that all species have the same habitat use year-round, but isotopic content can vary seasonally as a result of hydro-climatic processes.

At a finer time scale, segregation mechanisms could rely on differential daily activity budgets between species; this aspect was investigated in the bottlenose and the 2 *Stenella* dolphins, but not in the melon-headed whale. Foraging activities of *Tursiops aduncus* were observed throughout the day, but more frequently in the morning, closer to shore. A similar pattern was observed in common bottlenose dolphins (*T. truncatus*) in Florida (Shane 1990). Pantropical spotted dolphins feed during daylight, with an increase in feeding activity along the day. Nocturnal feeding is not excluded for these 2 species but could not be accessed directly. Spinner dolphins would only feed at night as foraging was never observed during daylight hours. Behavioural ecology of spinner and pantropical spotted dolphins around Mayotte is more similar than in other areas, including around Hawaii and in the oceanic eastern tropical Pacific (Perrin et al. 1973, Norris et al. 1994). Our results underline a clear pattern of niche segregation along the time dimension, at least during the day.

## CONCLUSION

Three main dimensions define the ecological niche of a species: habitat, diet and time. Our study integrated these 3 axes to investigate ecological niche segregation among the delphinid community found around Mayotte. Habitat has been assessed through the investigation of the relationships between delphinid distribution and environmental variables (particularly physiography). Trophic level and foraging habitat have been assessed indirectly, through the use of stable isotopes of N and C respectively (De Niro & Epstein 1978, Kelly 2000). Finally, the temporal component of the ecological niche has been integrated through the study of behavioural budgets, especially their diurnal variations that may potentially segregate species' ecological niche. The use of multiple approaches (habitat, behaviour and feeding ecology studies) was most useful to investigate ecological niche segregation, especially when looking at closely related species within a common restricted range. We propose a conceptual scheme of resource partitioning inferred
from these measurements: (1) The Indo-pacific bottle-nose dolphin is mostly confined to the inner lagoon or at least to shallow reef-associated habitats. They feed diurnally (possibly nocturnally as well, although this could not be documented), with daily routines that follow variation in prey catchability during the day, e.g. mullet being often caught close to the coast in the morning, and *Caranx melampygus* and *Hemiramphus far* the rest of the day across the lagoon; (2) The spinner dolphin lives in outer reef habitats and forage only nocturnally on small mesopelagic prey; (3) The pantropical spotted dolphin also lives in outer reef habitats that largely overlap with the spinner dolphins but feed at least partly diurnally and at dawn on epipelagic prey, which include flying fish caught closer to the barrier reef; (4) The melon-headed whale is seen in the same habitat as pantropical spotted dolphins, but forages deeper over the peri-insular slope.

This ecological segregation is more significant than in other communities, such as in some epipelagic seabirds (Ridoux 1994, Cherel et al. 2008). Conversely, in diving predators such as large pelagic fish and dolphins, ecological niche segregation is clearly distinguishable (Potier et al. 2004, Ménard et al. 2007, Praca & Gannier 2008). This could be related to the low spatial structure of marine ecosystems in tropical and oligotrophic areas. Conversely, clear isotopic and resource-related gradients can be found in subpolar and polar environments over large spatial scales (Jaeger 2009) as well as vertically (including in the tropics), at a small spatial scale in the water column (this study). This vertical gradient is accessible to fish and dolphins, and not in epipelagic seabirds.

Improvement in our understanding of resource partitioning mechanisms among Mayotte delphinids may be obtained in several directions: (1) acoustically investigating dolphins' nocturnal distribution and activity; (2) documenting the regional isoscape by analyzing C and N isotopic composition in phytoplankton collected along a coastal-offshore gradient and along a vertical gradient as well; (3) investigating residency patterns of dolphin groups living around Mayotte by using photo-identification or individual telemetry approaches, in order to establish whether they are genuinely associated to these peri-insular structures or have a more oceanic lifestyle, occasionally approaching islands.

*Acknowledgements.* The data from July 2004 to June 2006 were collected during a dolphin research project conducted by the Office National de la Chasse et de la Faune Sauvage (ONCFS, Game and Wildlife Service) and the Direction de l'Agriculture et de la Forêt (DAF, Agriculture and Forestry Office). From May 2007 to April 2009, data were collected during a joined program of the University of La Rochelle, the ONCFS and the Collectivité Départementale de Mayotte.

Funding was provided by the Conseil Général de Mayotte (CDM), the Ministère de l'Energie, l'Ecologie, le Développement Durable et de la Mer (MEEDDM), the University of La Rochelle and the ONCFS. We thank R. Rolland, A. Jamon, I. Ousseni, J. Wickel (DAF), S. Caceres, F. Charlier, D. Girou (ONCFS), D. Fray (CDM) and the personnel of Brigade Nature (CDM and ONCFS) for assistance in the field in Mayotte. Thanks are also addressed to K. Layssac (Service des Affaires Maritimes de Mayotte) for his contribution in the collection of fish samples. We are also grateful to G. Guillou (University of La Rochelle) for running the mass spectrometer analyses. The authors also thank G. Bearzi (Tethys Research Institute, Italy), M. Degrati (Marine Mammal Laboratory, Argentina), K. Stockin (Marine Coastal Group, Massey University, New Zealand) and F. Caurant (University of La Rochelle) for their constructive comments on the manuscript. The authors thank the 4 anonymous reviewers who provided constructive comments that greatly improved our manuscript.

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