habitat and resource partitioning among indo-pacific bottlenose dolphins in moreton bay, australia

MARINE MAMMAL SCIENCE, **(*): ***–*** (*** 2014)© 2014 Society for Marine MammalogyDOI: 10.1111/mms.12153

Habitat and resource partitioning among Indo-Pacificbottlenose dolphins in Moreton Bay, Australia

INA C. ANSMANN1 and JANET M. LANYON, Marine Vertebrate Ecology Research Group,

School of Biological Sciences, The University of Queensland, St Lucia, Queensland 4072, Aus-

tralia; JENNIFER M. SEDDON, School of Veterinary Science, The University of Queensland,

Gatton, Queensland 4343, Australia; GUIDO J. PARRA, Cetacean Ecology, Behaviour

and Evolution Lab, School of Biological Sciences, Flinders University, Adelaide, South Austra-

lia 5001, Australia and South Australian Research and Development Institute (SARDI),

Aquatic Sciences, 2 Hamra Avenue, West Beach, South Australia 5024, Australia.

Abstract

Investigating resource partitioning among mobile marine predators such as ceta-ceans is challenging. Here we integrate multiple methodologies (analyses of habitatuse, stable isotopes and trace elements) to assess ecological niche partitioningamongst two genetically divergent sympatric subpopulations (North and South) ofIndo-Pacific bottlenose dolphins (Tursiops aduncus) in Moreton Bay, Australia. Com-parisons of the mean locations (latitude, longitude) and environmental variables (dis-tance from sandbanks, distance from shore and water depth) observed at sightings ofbiopsy-sampled individuals indicated that the North subpopulation occurred in thenorthwestern bay in significantly deeper water than the South subpopulation, whichwas found in southeastern nearshore waters and closer to sandbanks. Ratios of stablecarbon and nitrogen isotopes in skin samples suggested that North dolphins foragedon higher trophic level prey in relatively more pelagic, offshore habitats, while Southdolphins foraged on lower trophic prey in more nearshore, demersal and/or benthichabitats. Habitat partitioning was also reflected in higher blubber concentrationsof most of the 13 measured trace elements, in particular lead, in the coastal Southcompared to the more pelagic North dolphins. These findings indicate that geneticsubpopulations of bottlenose dolphins in Moreton Bay are adapted to differentniches.

Key words: habitat use, Indo-Pacific bottlenose dolphin, niche specialization,resource partitioning, stable isotope ratios, trace elements, Tursiops aduncus.

Gene flow and lack of population structure are expected consequences of the dis-persal ability of highly mobile wildlife (Bohonak 1999). However, recent studies onapex predators in marine systems have revealed genetic structuring of populationsover spatial scales that are often small relative to their dispersal abilities (Parsonset al. 2006, Bilgmann et al. 2007, Ansmann et al. 2012b, Lowther et al. 2012). Forexample, genetic analysis of white sharks (Carcharodon carcharias) revealed significant

1Corresponding author (e-mail: [email protected]).

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population subdivision between Queensland and New South Wales along the eastcoast of Australia, despite their high vagility (Blower et al. 2012). Similarly, com-mon bottlenose dolphins (Tursiops truncatus) in the northern Bahamas showed signifi-cant population structuring over relatively short (<250 km) geographical distancesdespite their potential for long-distance movements (Parsons et al. 2006). Geneticstudies of common bottlenose dolphins along the Atlantic coast of North Americaand within the Gulf of Mexico have revealed a complicated mosaic of populations.Strong divergence was found between offshore dolphins in waters beyond 34 kmfrom shore and coastal dolphins 7.5 km from shore, thought to represent differentecotypes (Torres et al. 2003). However, even within the coastal bottlenose dolphinscontinuously distributed along this coastline, genetically differentiated populationshave been found with overlapping distributions in some areas (Rosel et al. 2009).Similar patterns were observed within the Gulf of Mexico with distinct inshore pop-ulations in separate embayments as well as a divergent coastal population (Sellaset al. 2005). The mechanisms driving these fine scale patterns of intraspecific popula-tion subdivision in highly mobile marine species are poorly understood, but arethought to be related to ecological (Hoelzel 1998, Natoli et al. 2005, M€oller et al.2007), social (Hoelzel et al. 2007, Andrews et al. 2010), and anthropogenic factors(Mendez et al. 2008, Ansmann et al. 2012a).In the absence of obvious historical factors, isolation by distance or barriers to

dispersal, resource partitioning has been proposed as the main mechanism leadingto fine scale genetic differentiation in large carnivorous mammals with broad geo-graphical distributions (Rueness et al. 2003, Pilot et al. 2006, Sacks et al. 2008,Munoz-Fuentes et al. 2009). However, it is difficult to assess if resource partition-ing is the initial driver of genetic structure or if it develops secondarily to geneticisolation with consequent reinforcement. Many large marine predators such aswhales, dolphins, and sharks are distributed across a variety of habitats, and inter-and intra-specific adaptations to specific habitats and variation in resource use arecommon (Parra 2006, Kiszka et al. 2012). Such differential resource use (i.e.,resource polymorphism), facilitated by small-scale variation in habitat, can lead toor reinforce reproductive isolation, assortative mating or natal habitat–biased dis-persal resulting in discretely subdivided populations (Davis and Stamps 2004, Funket al. 2006). In top predators living in groups, resource specializations coupled withsocial cohesion and learning can also promote local philopatry, and lead to geneticdifferentiation (Hoelzel et al. 2007). Identifying the ecological and behavioral fac-tors associated with spatial patterns of genetic population structure is crucial forenhancing our understanding of the mechanisms that may influence populationstructure. Moreover, if particular environmental conditions drive genetic differenti-ation, identifying these conditions is important for conservation of genetic diversityand underlying evolutionary processes (Crandall et al. 2000, Moritz 2002).Moreton Bay (~1,400 km2; Fig. 1), Australia, is a highly diverse marine ecosystem

consisting of temperate as well as tropical habitats including seagrass, mangrove,coral, and salt marshes, with more than 3,000 species of macro-invertebrates and over700 species of fish (Davie and Hooper 1998). This wide variety of habitats and preysupports significant populations of marine mammals including Indo-Pacific bottle-nose dolphins (Tursiops aduncus) (Chilvers et al. 2005), hereafter referred to as bottle-nose dolphins. Bottlenose dolphins are found year-round and are continuouslydistributed across Moreton Bay. Analysis of mitochondrial and nuclear DNA hasrevealed significant levels of genetic population structure at the scale of only tens ofkilometers among bottlenose dolphins in Moreton Bay (Ansmann et al. 2012b). Two

2 MARINE MAMMAL SCIENCE, VOL. **, NO. **, 2014

subpopulations (“South” and “North”) have been identified: dolphins geneticallyassigned to a South subpopulation were more likely to be found in the nearshore shal-low areas of the southern bay and near the large areas of intertidal to subtidal sand-banks characterizing the southeastern bay. These sandbanks are mostly submergedbut shallow, ranging from ≤1 to 5 m depth. Members of a North subpopulation weremostly found in deeper open waters of the northern and central bay. A third group of

Figure 1. Map of Moreton Bay, Queensland (QLD), Australia (inset), showing water depth(m) contour lines and sightings of individually identified bottlenose dolphins geneticallyassigned to three groups, North, Mixed, and South. Black dashed lines delineate study area.Shaded areas indicate shallow sandbanks.

ANSMANN ET AL.: RESOURCE PARTITIONING IN DOLPHINS 3

genetically “Mixed” individuals could not be confidently assigned to either North orSouth subpopulations, indicating these two subpopulations were not completelyspatially segregated and genetic mixing did occur (Ansmann et al. 2012b).The genetic structuring amongst inshore bottlenose dolphins in a relatively

small geographic area, within an embayment lacking any obvious environmental bar-riers to dispersal, suggests that ecological factors may influence genetic structuring(Ansmann et al. 2012b). However, aside from the apparent differences in use of space,nothing is known about resource partitioning between these sympatric subpopula-tions. If ecological variation and niche specializations are important drivers of fine-scale population structure in cetaceans as previously suggested (Hoelzel 1998, Natoliet al. 2005, M€oller et al. 2007), then population genetic differentiation identifiedamong these two sympatric subpopulations of bottlenose dolphins should be reflectedin differential habitat and/or resource use.The aim of this study was to assess whether the two sympatric subpopulations of

bottlenose dolphins inhabiting Moreton Bay, Australia, show significantly differen-tial resource use related to their genetic divergence. This would form the basis for fur-ther examination on the mechanisms or pathways through which this structuringmay have developed. Investigating resource partitioning among delphinids is chal-lenging, especially for putative populations that occupy sympatric ranges and forageon a wide variety of prey (Kiszka et al. 2011, Qu�erouil et al. 2013). Therefore weused an integrative approach that combined analyses of habitat use, stable isotopesand trace element concentrations in skin and blubber biopsy samples, to discernresource and habitat partitioning between these sympatric dolphin subpopulations.

Materials and Methods

Data Collection

Regular systematic boat-based surveys of bottlenose dolphins were conducted inMoreton Bay (27�000–27�350S, 153�000–153�270E) throughout four field seasonsover two years (July–September 2008, January–March 2009, July–September 2009,January–March 2010), totaling 86 survey days. Surveys followed predetermined zig-zag line transects designed to optimize sampling coverage of all areas and habitattypes within Moreton Bay. For detailed survey methodology, see Ansmann (2011)and Ansmann et al. (2013). Upon encountering bottlenose dolphins, survey effort wassuspended to record location (using GPS), water depth (using depth sounder), andcollect a skin–blubber biopsy sample from adult dolphins. Dolphins were categorizedas adults (>2 m body length, Hale et al. 2000), juveniles (about two-thirds of adultsize and not closely associated with a particular adult), or dependent calves (less thantwo-thirds of adult size and closely associated with an adult, the presumed mother).Only adults were targeted for biopsy sampling.Biopsy samples were collected using the PAXARMS remote biopsy system specifi-

cally designed for small cetaceans (Kr€utzen et al. 2002). Tissue samples were chilledon ice, and then stored frozen at –20°C upon return from the field. During sampling,we photographically identified each individual based on the size, shape, location, andpattern of notches on the trailing and leading edges of the dorsal fin, and dorsal andlateral body markings (W€ursig and W€ursig 1977, W€ursig and Jefferson 1990). Onlybiopsy samples from unique individuals (based on photographic identification as wellas unique genotypes) were used in the following analyses.


A total of 97 different adult bottlenose dolphins were biopsy-sampled within Mor-eton Bay. These samples were also used for genetic analysis by Ansmann et al.(2012b), excepting one dolphin that was regularly provisioned at a local tourist resort.DNA extracted from tissue samples was used to sex individuals genetically usingamplification of the ZFX and SRY genes (Gilson et al. 1998) as described inAnsmann et al. (2012b).As described in detail in Ansmann et al. (2012b), dolphins were assigned to one of

three groups using the Bayesian model-based clustering method implemented inSTRUCTURE 2.3.3 (Pritchard et al. 2000) using genotypes at 19 polymorphicmicrosatellite loci (Shinohara et al. 1997, Hoelzel et al. 1998a, Kr€utzen et al. 2001,Nater et al. 2009). Clustering analysis identified two genetically distinct clusters orsubpopulations (North: n = 21, South: n = 32); a third group of individuals (Mixed:n = 44) showed a mixed genetic background and could not be confidently assigned toeither of the two subpopulations (Ansmann et al. 2012b). Here we analyze these twopreviously identified subpopulations and admixed individuals as three separategenetic groups in order to compare habitat and resource use patterns between the twoclearly distinguished subpopulations (North and South) and investigate whether theMixed individuals show intermediate patterns of habitat use between the twosubpopulations or similar patterns to either.

Habitat Use

Sighting locations of the 97 biopsy-sampled individuals were plotted onto a mapof Moreton Bay using ArcMap in ArcGIS 9.3 Geographic Information Software,ESRI (Environmental Systems Research Institute) (Fig. 1). We acknowledge that itis possible that dolphin groups sighted may have included individuals from morethan one subpopulation. However, as it was not feasible to obtain genetic samplesfrom all individuals within each group, this could not be tested. Hence the followinganalysis is restricted to sightings of biopsy-sampled individuals regardless of theirassociation with other individuals.When sightings of the two subpopulations were plotted on a map (Fig. 1), South

individuals appeared to be restricted to the southern half of Moreton Bay, with a fewsightings in the northern half but still very close to shore. South sightings also seemedto follow the outline of the large sandbanks in southeastern parts of the bay. Thus, toinvestigate the importance of these factors in relation to the distribution of the sub-populations, we compared the means of locations (latitude and longitude) and envi-ronmental variables (distance from shore, distance from sandbanks, and water depth)observed at sightings of biopsy sampled individuals from the three genetic groups.For each of the 97 individuals, distance from nearest shore and sandbanks were

measured at the starting position of each sighting of that individual using the mapcreated with ArcMap in ArcGIS 9.3. Water depth was directly measured at the start-ing position of each sighting using a depth finder. The mean of these distances andwater depths for each individual was used for comparisons between subpopulations.Similarly, the mean of the latitudes and longitudes of each sighting location of eachsampled individual was used in further analysis. Data variances of all five variables(mean latitude, longitude, distance from shore, distance from sandbanks, and waterdepth) were not equal (Levene’s test: all P < 0.01), so nonparametric Kruskal-Wallisand Mann-Whitney U tests were used to compare means between all three geneticgroups and each pair of groups, respectively. All statistical tests (including thosereferred to in the following sections) were performed in SPSS version 12.0 (IBM).


Stable Isotope Ratios

To investigate potential dietary partitioning, the skin layer of biopsy samples froma subset of 40 individuals, for which sufficient tissue was available (North: n = 15,Mixed: n = 13, and South: n = 12), were analyzed for d15N and d13C stable isotoperatios. A consumer’s tissue d15N values show a predictable enrichment of an average3&–5& with each trophic level in the food chain, so that d15N measures have beenused to assess an animal’s trophic position (Peterson and Fry 1987, Kelly 2000). Incontrast, d13C levels are only slightly (~1&) or not enriched in the tissues of verte-brate consumers, but instead allow for identification of different carbon sources at thebase of food chains, as these vary between different primary producers (Peterson andFry 1987, Kelly 2000). In the marine environment, d13C ratios tend to be higher inbenthic/demersal and near-shore sources relative to pelagic offshore sources of carbon(Rubenstein and Hobson 2004, Crawford et al. 2008). However, it should be notedthat trophic enrichment (or discrimination) factors are highly variable and influencedby the consumer’s taxonomic group, age, and type of tissue analyzed, as well as thediet’s isotopic ratio and lipid content (Caut et al. 2009, Browning et al. 2014). Incommon bottlenose dolphin skin, d15N enrichment factors were found to be lowerthan previously suggested, at around 2& (Browning et al. 2014).Skin samples (0.01–0.11 g wet weight) were oven-dried at 60°C overnight and

finely ground to a homogenous powder. Dried, ground samples were then oxidized athigh temperatures and combusted using a EuroEA 3000 (EuroVector, Italy) elemen-tal analyzer. The resulting N2 and CO2 gases were separated chromatographicallyand isotope ratios were determined using an IsoPrime (Micromass, U.K.) isotoperatio mass spectrometer. Primary standards used were ambient air, IAEA-305a fornitrogen and sucrose IAEA-CH-6 for carbon. Elemental compositions of standardswere cross referenced using acetanilide.Lipids were not extracted prior to analysis. Thus, we used the mathematical model

proposed by Post et al. (2007) to account for the effects of lipid content in the tissueon carbon isotopic ratios. This model derives normalized carbon isotope ratios(d13Cnormalized) from measured d13C as well as the ratio of carbon to nitrogen concen-trations (C:N) in the sample, as the latter has been found to be strongly related tolipid content in aquatic animals (Post et al. 2007):

d13Cnormalized ¼ d13Cmeasured � 3:32þ 0:99� C:N

As stable isotope data were approximately normally distributed and co-varianceswere equal (Box’s M = 12.33, P = 0.08), MANOVA was used to compare means ofstable isotope ratios in dolphin skin tissue between the three groups, followed byANOVAs for each isotope (Levene’s test for homogeneity of variance: d15N: F =1.09, P = 0.35; d13Cnormalized: F = 0.11, P = 0.90) and Tukey HSD post hoc multiplecomparisons of each pair.In this study, samples from the South group included more females (6 out of 12)

than samples from the North (3 out of 15) or Mixed (3 out of 13). To test for anysex-related differences, we used t-tests, after assessing homogeneity of variance usingLevene’s test, to compare isotopic ratios between skin samples from adult females(n = 6) and males (n = 6) from the South group (as this group had equal sample sizesfor both sexes). We acknowledge that sample size for this analysis of differencesbetween sexes was small, thus results should be treated with caution and regarded asan indication of possible trends only.


Stable isotope ratios capture information about diet at different temporal scalesdepending on the turnover rate of the tissue examined. Cetacean skin has a relativelylong turnover time with the estimated time required for cell migration from the basallamina to the outermost surface of the skin being at least two months: 70–75 d incommon bottlenose dolphins (Hicks et al. 1985). However, retention times of stableisotopes in common bottlenose dolphin skin have been found to be as short as 20–32d (Browning et al. 2014). Therefore, stable isotope ratios measured in skin biopsysamples reflect the dolphin’s recent diet during the month prior to sampling. Thiscould have influenced the comparative results of this study if samples from differentsubpopulations were collected at different times of the year and diet of the dolphinsvaried by season. The majority of biopsy samples used in this analysis was collectedduring austral winter field seasons (July–September) because generally calmerweather at this time of year resulted in improved survey conditions and greaterbiopsy sampling success. Only 4 out of 15 North samples, 2 out of 13 Mixed samplesand 2 out of 12 South samples were collected during summer field seasons (January–March). To assess whether sampling season may have biased the stable isotope analy-sis, we repeated the statistical analyses after removing the eight samples collected insummer.

Trace Elements

The partial blubber layer section of the same subset of 40 biopsy samples (as above)from adult dolphins from each of the three groups was analyzed for a suite of 13 traceelements including toxic heavy metals: arsenic (As), barium (Ba), cadmium (Cd),chromium (Cr), copper (Cu), iron (Fe), mercury (Hg), manganese (Mn), nickel (Ni),lead (Pb), selenium (Se), strontium (Sr), and zinc (Zn). Each blubber sample (0.03–0.14 g wet weight) was digested in Trace Select Ultra nitric acid (Fluka, Sigma-Aldrich Corp., St. Louis, MO), in accordance with EPA method 3051A using a CEMMDS2000 microwave digester and Teflon digestion vessels. Digests were analyzed byinductively coupled plasma mass spectrometry (ICPMS) using a Platform Life ICPMSinstrument (Micromass, U.K.). Results were reported on a wet weight basis.Mean concentrations of each trace element in dolphin blubber were compared

between the three groups using MANOVA followed by ANOVAs and Tukey HSDpost hoc tests or nonparametric Kruskal-Wallis and Mann Whitney U tests as appro-priate. Concentrations of some trace elements may vary with sex of adult animals(Bryan et al. 2007, Stavros et al. 2007). To test for any sex-related bias in trace ele-ment levels, we compared blubber concentrations of adult females (n = 6) and males(n = 6) from the South group using t-tests after assessing homogeneity of varianceusing Levene’s test.

Results

Habitat Use

Individuals genetically assigned to the South group were found further south andeast (Fig. 2), closer to shore and sandbanks (Fig. 3a), and in shallower waters(Fig. 3b) than those from North and Mixed. All environmental variables (mean lati-tude, longitude, distance from shore, distance from sandbanks and water depth) inwhich dolphins were encountered were significantly different between the three


genetically defined groups of dolphins (North, Mixed and South) (Kruskal-Wallis:v2 = 46.01, v2 = 24.81, v2 = 22.78, v2 = 46.95, and v2 = 28.01 respectively, all df =2, all P < 0.001). Specifically, all variables were significantly different between Southand North dolphins (Mann-Whitney U: Z = −5.71, Z = −4.29, Z = −4.67,Z = −5.64, and Z = −4.11, respectively; all P < 0.001) as well as between South andMixed (Z = −5.46, Z = −4.25, Z = −3.43, Z = −5.72, and Z = −4.88; all P < 0.001).Only latitude and distance from sandbanks were significantly different between

-27.5

-27.4

-27.3

-27.2

-27.1

153.2 153.3 153.4

Latit

ude

S

Longitude E

NorthMixedSouth

(n=21)(n=44)(n=32)

Figure 2. Means and 95% confidence intervals of sighting locations (latitude and longi-tude) of adult bottlenose dolphins from three genetically defined groups (North, Mixed, andSouth) in Moreton Bay.

BA

Figure 3. Range (whiskers), quartiles (shaded box), median (black horizontal line) and out-liers (asterisk) of (a) distance from shore and sandbanks (km), and (b) water depth (m) mea-sured at sightings of individual adult bottlenose dolphins from three genetically definedgroups (North, Mixed, and South) in Moreton Bay.


North and Mixed dolphins (Z = −2.75 and Z = −2.53, respectively; both P < 0.05)but not longitude, distance from shore, or water depth (Z = −0.83, Z = −1.53, and Z= −0.05, respectively; all P > 0.1).

Stable Isotope Ratios

The distribution of stable isotope ratios in skin samples of adult bottlenosedolphins from Moreton Bay showed relatively high individual variation (Fig. 4a).Nitrogen (d15N) ratios ranged from 10.9 to 18.8 indicating dietary variation acrosstwo to three trophic levels. Normalized Carbon (d13Cnormalized) ratios ranged from−18.4 to −13.7, suggesting that dolphins were utilizing a range of prey along thenearshore-offshore or benthic-pelagic gradient of habitats. Neither mean nitrogennor mean carbon isotopic ratios were significantly different between males (n = 6)and females (n = 6) within the South group (d15N: t = −1.63, df = 10, P = 0.13;d13Cnormalized: t = 1.05, df = 10, P = 0.32). Both isotopic d15N and d13Cnormalized

ratios were significantly different between groups (MANOVA: F = 14.38, df = 72,P < 0.001). Post hoc multiple comparisons showed significant differences in both iso-topes between the North and South groups as well as between Mixed and South, butnot between North and Mixed (Fig. 4b). Mean d15N was significantly higher in skinsamples from the North and Mixed groups (mean � SD: 14.45& � 1.24& and14.83& � 1.89&, respectively) than in South (12.63& � 1.31&) (ANOVA:F = 7.60, df = 39, P = 0.002; Tukey HSD: North-Mixed: P = 0.78, North-South:P = 0.01, Mixed-South: P = 0.002) suggesting that North and Mixed dolphins werefeeding at a slightly higher trophic level than South dolphins. Mean d13Cnormalized

was significantly higher in samples from South (mean � SD: −15.09& � 0.75&)than in the North or Mixed groups (−16.93& � 0.76& and −16.86& � 0.89&,respectively) (ANOVA: F = 21.39, df = 39, P < 0.001; Tukey HSD: North-Mixed:P = 0.98, North-South: P < 0.001, Mixed-South: P < 0.001) (Fig. 4b) indicating

A B

Figure 4. Isotopic ratios of nitrogen (d15N) and carbon (d13C) in skin samples of adult bot-tlenose dolphins from three genetically defined groups (North, Mixed, and South) in MoretonBay: (a) Scatter plot showing distribution of values for all sampled individuals, and (b) meansand 95% confidence intervals of ratios for each of the three groups.


that the South group was feeding in more demersal, nearshore habitats, whereas theNorth and Mixed groups appear to be foraging in relatively more pelagic, offshoreareas.Removing the eight samples collected in summer, in order to test for bias caused

by seasonal variation, resulted in only minor changes to mean values (mean d15N forNorth, Mixed, South = 14.68, 15.26, and 12.50, respectively; mean d13Cnormalized forNorth, Mixed, South = −16.90, −17.02, and −15.11, respectively). It did not changethe results of the comparative analyses presented above.

Trace Elements

All assayed trace elements were at detectable levels in blubber of all adult dolphins.Mean concentrations of most of the elements were below or around 1 lg/g wetweight. Exceptions were the essential elements iron (Fe) and zinc (Zn), with meanconcentrations of 13 � 6 (SD), 15 � 6 and 18 � 11 lg/g of Fe, and 21 � 13 (SD),41� 56, and 21� 7 lg/g of Zn in the North, Mixed, and South groups respectively.There was high individual variation for many of the elements, with some sample con-centrations varying by up to three orders of magnitude (Table 1). Mean levels of trace

Table 1. Mean concentrations (lg/g wet weight) of trace elements in blubber samples ofadult bottlenose dolphins from three genetically defined groups (North, Mixed, and South) inMoreton Bay, with standard deviation in parentheses and range below. Values in bold weresignificantly different (P < 0.01) between groups.

Northn = 15

Mixedn = 13

Southn = 12

As 0.71 (0.41)0.03–1.36

0.76 (0.26)0.38–1.15

0.85 (0.50)0.04–1.91

Ba 0.57 (0.35)0.18–1.36

0.49 (0.27)0.14–1.18

0.78 (0.46)0.30–1.53

Cd 0.07 (0.03)0.02–0.13

0.06 (0.03)0.01–0.12

0.08 (0.04)0.01–0.15

Cr 0.26 (0.12)0.05–0.48

0.38 (0.22)0.14–0.95

0.45 (0.38)0.09–1.30

Cu 0.45 (0.20)0.13–0.71

0.49 (0.28)0.11–1.03

0.57 (0.27)0.23–1.02

Fe 12.49 (6.08)4.94–26.95

14.76 (5.87)6.55–23.66

17.75 (11.19)7.08–39.71

Hg 0.07 (0.05)0.02–0.19

0.09 (0.05)0.02–0.17

0.07 (0.03)0.03–0.13

Mn 0.40 (0.26)0.04–0.89

0.59 (0.34)0.14–1.45

0.67 (0.37)0.16–1.42

Ni 0.90 (0.39)0.33–1.82

1.00 (0.55)0.24–2.25

1.11 (0.71)0.09–2.20

Pb 0.44 (0.29)0.06–1.00

0.46 (0.31)0.06–1.25

0.84 (0.43)0.35–1.62

Se 0.48 (0.17)0.09–0.85

0.79 (1.25)0.04–4.89

0.59 (0.21)0.17–0.98

Sr 0.66 (0.30)0.14–1.15

0.86 (0.36)0.25–1.54

0.87 (0.58)0.13–2.31

Zn 21.30 (13.40)4.98–61.73

41.10 (55.88)0.11–215.42

20.95 (7.23)9.35–36.79


elements were not significantly different between males (n = 6) and females (n = 6)within the South group (all P > 0.05).Mean levels of almost all trace elements (As, Ba, Cd, Cr, Cu, Fe, Mn, Ni, Pb,

and Sr) were highest in blubber samples of dolphins from the South group (Table 1).However, blubber concentrations of these trace elements were not significantlydifferent between the three groups (MANOVA: F = 1.12, df = 48, P = 0.36), exceptfor lead (Pb), which was significantly higher in South (mean � SD: 0.84 lg/g �0.43) than in North (0.44 lg/g � 0.29) and Mixed dolphins (0.46 lg/g � 0.31,Fig. 5) (Levene’s test for equal variances: F = 1.30, P = 0.29; ANOVA: F = 5.67,df = 39, P = 0.007; Tukey HSD: North-Mixed: P = 0.98, North-South: P = 0.01,Mixed-South: P = 0.02).

Discussion

Niche specializations have been suggested as important drivers of fine-scale popu-lation structure in cetaceans (Hoelzel 1998, Natoli et al. 2005, M€oller et al. 2007).Using an integrated approach combining environmental variables and chemicalsignatures of habitat and resource use (stable isotope and trace element concentra-tions), we found resource partitioning in spatial distribution, habitat, and diet amongbottlenose dolphins in Moreton Bay, Australia, concordant with the general patternof genetic subdivision into subpopulations.

Resource Partitioning among Bottlenose Dolphins in Moreton Bay

Comparisons of environmental variables at sighting locations indicated distinctspatial and habitat segregation between individuals genetically assigned to the twosubpopulations of bottlenose dolphins in Moreton Bay (North and South). Dolphins

Figure 5. Range (whiskers), quartiles (gray box), median (black horizontal line), and out-liers (asterisk) of lead (Pb) levels (lg/g) in blubber samples of adult bottlenose dolphins fromthree genetically defined groups (North, Mixed, and South) in Moreton Bay.


belonging to the North subpopulation were distributed in deeper (≤23 m deep)waters of northern and central Moreton Bay while dolphins from the South subpopu-lation occurred in nearshore shallow (<15 m deep) waters of southern and easternMoreton Bay and in close proximity to shallow sandbanks. Future surveys in thestudy area are recommended to assess the importance of other environmental variablessuch as sea surface temperature or chlorophyll a levels (as an indicator of primary pro-ductivity), or ecological variables such as prey availability or predation risk, all ofwhich may influence dolphin habitat use (e.g., Heithaus and Dill 2002, Garaffo et al.2011).Analysis of stable isotopes provided evidence of diet partitioning linked to differ-

ential use of space. Stable isotope ratios indicated that the two subpopulations of bot-tlenose dolphins were feeding at different relative trophic levels and in differentforaging habitats. Dolphins from the North subpopulation were feeding at a slightlyhigher trophic level in relatively more pelagic and/or offshore habitats than Southdolphins, which were feeding in more demersal and/or coastal habitats.A limitation of many dietary tracers including stable isotope ratios is that only dif-

ferences in results can be interpreted unambiguously, whereas similar results canreflect a variety of different prey combinations (Kiszka et al. 2011). Thus, in this case,the similar isotopic ratios observed in bottlenose dolphins from the North subpopula-tion and those with Mixed genetic background may indicate that these two groupsutilized similar prey items or alternatively that they fed on different prey items withsimilar isotopic values or that they used different combinations of a range of preyitems that resulted in similar overall isotopic make-up. The aim of this study was tocompare relative differences in diets between the subpopulations. Stable isotope com-positions of potential prey items or carbon sources in Moreton Bay were not investi-gated, thus it was not possible to identify particular food items in the diets. Thiswould be a valuable extension for future studies, which should consider incorporatingtraditional methods such as stomach content analysis of stranded dolphins as well assampling potential prey items and carbon sources for stable isotope analyses tocharacterize the isotopic composition of different habitats in Moreton Bay.The two subpopulations (North and South) also varied with regard to concentra-

tions of trace elements in blubber, where mean levels of almost all elements, in partic-ular lead (Pb), were higher in the South subpopulation. Lead (Pb) levels in bottlenosedolphins from Moreton Bay were within the range reported for common bottlenosedolphins elsewhere throughout Australia but higher than in all other species ofAustralian marine mammals reported by Kemper et al. (1994). Inhabiting coastalnearshore environments may expose the South bottlenose dolphins to higher levels ofPb from anthropogenic sources such as coastal developments, waste-water runoff ormining (Lavery et al. 2008). The northern parts of Moreton Bay are more regularlyflushed by oceanic water while the semienclosed southern bay retains higher concen-trations of river runoff carrying pollutants (Patterson and Witt 1992, Quinn 1992).This may explain the overall higher trace element levels found in the South subpopu-lation of bottlenose dolphins, reflecting their nearshore distribution in the semien-closed southern bay waters, and suggesting that they are resident within this area.In cetaceans, concentrations of some trace elements vary with age (e.g., Meador

et al. 1999, Parsons 1999) and/or sex (Bryan et al. 2007, Stavros et al. 2007). Inthis study, absolute age could not be determined, thus it was not possible to test sta-tistically for age-related bias. However, only adults were sampled, which shouldreduce the magnitude of any potential bias. Further, blubber contaminant levels aregenerally expected to be lower for adult female than male bottlenose dolphins,


because reproductively mature females offload some of their accumulated body burdenof contaminants through pregnancy and lactation (Cockcroft et al. 1989, Yordy et al.2010). However, while this seems to be the case for lipophilic organic pollutants likeorganochlorines or PCBs, studies examining trace elements have found either no sig-nificant difference between sexes (e.g., Lavery et al. 2008) or opposite trends for someelements with higher concentrations in females (e.g., Meador et al. 1999, Yang et al.2002, Bryan et al. 2007). We found no evidence of sex-related variation in trace ele-ment concentrations in dolphins sampled within the South subpopulation. Futurestudies of stranded specimens, measuring heavy metal levels in blubber and otherbody tissues would elucidate potential differential bioaccumulation pathways.

Resource Partitioning and Population Structure

Delphinids (family Delphinidae) are the most diverse and widespread family ofcetaceans (Perrin et al. 2002) with some species known to exhibit substantial intra-specific behavioral and ecological polymorphisms. Bottlenose dolphins (Tursiops spp.)show a high degree of ecological and behavioral plasticity. They are found in a varietyof environments worldwide, ranging from shallow coastal (e.g., Irvine et al. 1981) todeep offshore habitats (e.g., Klatsky et al. 2007) and from tropical (e.g., Bahamas, Par-sons et al. 2006) to temperate waters (e.g., Scotland, Wilson et al. 1997). Bottlenosedolphins (Tursiops spp.) forage alone as well as in groups, and employ a wide range offoraging behaviors that reflect their diverse prey (mostly fish and cephalopods) (Con-nor et al. 2000b). In some areas, bottlenose dolphins (Tursiops spp.) have developedhighly specialized foraging techniques, such as lifting up conch shells to shake outhidden prey (Allen et al. 2011), carrying marine sponges on their rostra presumablyto protect them from injuries while foraging on benthos (Smolker et al. 1997), scar-ing fish out of shallow water seagrass with a percussive tail slap on the water surface(Connor et al. 2000a) or even beaching themselves in pursuit of prey (Silber and Fertl1995, Sargeant et al. 2005). Such foraging behaviors have been correlated with theindividual dolphins’ home ranges and habitat use (Torres and Read 2009), physicalcharacteristics of their prey (Patterson and Mann 2011), as well as social behavior(Chilvers and Corkeron 2001, D�ıaz L�opez and Shirai 2008). The resource and habitatpartitioning among sympatric subpopulations of bottlenose dolphins within anembayment (Moreton Bay) described here, further demonstrates the behavioral andecological plasticity of bottlenose dolphins and their ability to utilize a large varietyof habitats and prey.Niche specializations, as indicated by differences in space use and diet, have been

suggested as the possible mechanisms by which coexistence of sympatric species ismediated and competition avoided (Pimm and Rosenzweig 1981; Rosenzweig 1981,1991; Schoener 1986). Such resource partitioning mechanisms have been observedamong sympatric species of delphinids (Gowans and Whitehead 1995, Parra 2006,Kiszka et al. 2011) and have been suggested at the intraspecific level for allopatric,parapatric and sympatric populations (Hoelzel et al. 1998b, Gannon and Waples2004, Natoli et al. 2005, M€oller et al. 2007). In turn, fine scale genetic differentia-tion of dolphin populations living in very close geographic proximity has appeared tobe related to resource polymorphisms in relation to prey and feeding (Hoelzel andDover 1991, Sellas et al. 2005).Niche specializations are considered important drivers of genetic differentiation

by adaptive divergence (Sk�ulason and Smith 1995, Hoelzel 1998, Beheregaray andSunnucks 2001, M€oller et al. 2007, Wiszniewski et al. 2010). However, disentan-


gling the causal relationships of resource partitioning, social isolation and genetic dif-ferentiation is complex, with studies identifying only concordant patterns. For exam-ple, segregated spatial distribution and significant genetic differentiation have beenfound within a population of Indo-Pacific bottlenose dolphins within the Port Ste-phens embayment in southeastern Australia, approximately 600 km further southalong the eastern Australian coastline (Wiszniewski et al. 2009, 2010). Other studiesof dolphins (Natoli et al. 2005; Sellas et al. 2005; Bilgmann et al. 2007; M€oller et al.2007, 2011; Wiszniewski et al. 2010), as well as marine fish (Beheregaray and Sun-nucks 2001), have also found cases of such resource- or habitat-related genetic differ-entiation over small distances. Lowther et al. (2012) proposed that individualforaging specializations limited the dispersive capacity of female Australian sea lions(Neophoca cinerea) to distinct preferred foraging areas and habitats, which in turnresulted in genetic differentiation within the population. Similarly genetic structur-ing in highly mobile terrestrial top predators including wolves (Canis lupus, Pilotet al. 2006), lynx (Lynx canadensis, Rueness et al. 2003), and coyotes (Canis latrans,Sacks et al. 2004) is related to habitat type and explained by individual specializationand preferential dispersal of individuals to their natal habitat (Sacks et al. 2004,2008; Pilot et al. 2006).It is unclear at this stage whether the two subpopulations of bottlenose dolphins in

Moreton Bay have diverged from a single original population, or whether they weretwo distinct populations that have more recently connected and interbred to somedegree. Thus, based on currently available data, it is impossible to discern whetherthe observed resource partitioning led to genetic divergence or whether the subpopu-lations were originally genetically distinct and originated from different habitats(e.g., within the bay vs. coastal waters outside the bay). However, our findings showthat resource specializations do exist among these subpopulations which may limittheir movements and thus may either be a principal driving factor of the observedgenetic structuring or may be reinforcing existing genetic segregation within thispopulation. Extension of our study area into surrounding coastal waters may shedlight onto the process(es) underlying the observed resource partitioning and geneticheterogeneity.

Genetically Mixed Individuals Suggest Directional Gene Flow

Most of the indicators of resource partitioning (longitude, distance from shore,water depth, stable isotopes, and trace elements) examined here were not significantlydifferent between dolphins assigned to the North subpopulation and those withMixed genetic background. In contrast, both North and Mixed differed significantlyfrom South dolphins in terms of the environmental characteristics at which they wereencountered, and in their tissue stable isotope ratios and lead concentrations. Thissuggests that the majority of animals of mixed heritage were using the same or simi-lar habitat as the North subpopulation, even though they had a larger distributionalrange across the whole of Moreton Bay. Analysis of differential nuclear vs. mitochon-drial genetic patterns, as well as genetically inferred sex-biased dispersal (Ansmannet al. 2012b), suggested that the Mixed group was likely predominantly generated byfemales from the North subpopulation breeding with males from the South. Calvesof bottlenose dolphins remain with their mothers for several years, during which timethey learn different behaviors including feeding strategies (Smolker et al. 1992,Mann and Sargeant 2003). Our observation that Mixed dolphins use similar habitatand resources as North individuals is consistent with the hypothesis that calves of


North mothers and South fathers remain in the North subpopulation with their moth-ers. It is likely also that at least some Mixed dolphins back-cross into the North sub-population, explaining the previous observation that the North subpopulation is moregenetically diverse than the South subpopulation (Ansmann et al. 2012b), resulting ina net gene flow in this scenario from the South into the North subpopulation.

Conclusions

The combined analyses of habitat characteristics and chemical tracers, such as sta-ble isotope ratios and trace element concentrations has provided valuable informationon the underlying ecological factors shaping habitat and resource partitioningbetween the subpopulations of bottlenose dolphins in Moreton Bay. This integratedapproach together with information on population genetic structure and demographyafforded more information on population structure than the different sources of infor-mation provided alone. Results show that different habitats, including both near-shore, as well as deeper or more pelagic parts of Moreton Bay, are important forbottlenose dolphins. Thus, management efforts should seek to maintain and/orimprove the health of both of these habitat types as well as habitat heterogeneitywithin the bay in order to preserve inshore bottlenose dolphin populations.

Acknowledgments

We thank the many volunteers who assisted with field work; Michael Noad, Anne Goldi-zen, Celine Frere, Simon Blomberg, and Brian Fry for comments and advice; Rene Diocares(Science, Environment, Engineering and Technology Group, Griffith University) and DavidAppleton (School of Agriculture and Food Sciences, University of Queensland) for lab support;and Chris Roelfsema (School of Geography, Planning and Environmental Management, Uni-versity of Queensland) for providing bathymetry contour data for Moreton Bay. This studywas supported by the Winifred V. Scott Foundation. ICA was supported during the course ofthis study by a University of Queensland Research Scholarship (UQRS) and University ofQueensland International Research Award (UQIRA). Samples were collected under permitsfrom the Queensland Government Environmental Protection Agency (WITK04729707), theQueensland Parks and Wildlife Service (QS2008/CVL1413) and under approval by the Uni-versity of Queensland Animal Ethics Committee (SVS/622/08/OPCF and SVS/350/10/WVSCOTT FOUNDATION).

Literature Cited

Allen, S. J., L. Bejder and M. Kr€utzen. 2011. Why do Indo-Pacific bottlenose dolphins(Tursiops sp.) carry conch shells (Turbinella sp.) in Shark Bay, Western Australia? MarineMammal Science 27:449–454.

Andrews, K. R., L. Karczmarski, W. W. L. Au, et al. 2010. Rolling stones and stable homes:Social structure, habitat diversity and population genetics of the Hawaiian spinnerdolphin (Stenella longirostris). Molecular Ecology 19:732–748.

Ansmann, I. C. 2011. Fine-scale population structure of Indo-Pacific bottlenose dolphins,Tursiops aduncus, in Moreton Bay, Queensland, Australia. Ph.D. dissertation, Universityof Queensland, St Lucia, Australia. 184 pp.

Ansmann, I. C., G. J. Parra, B. L. Chilvers and J. M. Lanyon. 2012a. Dolphins restructuresocial system after reduction of commercial fisheries. Animal Behaviour 84:575–581.


Ansmann, I. C., G. J. Parra, J. M. Lanyon and J. M. Seddon. 2012b. Fine-scale geneticpopulation structure in a mobile marine mammal: Inshore bottlenose dolphins inMoreton Bay, Australia. Molecular Ecology 21:4472–4485.

Ansmann, I. C., J. M. Lanyon, J. M. Seddon and G. J. Parra. 2013. Monitoring dolphins in anurban marine system: Total and effective population size estimates of Indo-Pacificbottlenose dolphins in Moreton Bay, Australia. PLOS ONE 8(6):e65239.

Beheregaray, L. B., and P. Sunnucks. 2001. Fine-scale genetic structure, estuarine colonizationand incipient speciation in the marine silverside fish Odontesthes argentinensis. MolecularEcology 10:2849–2866.

Bilgmann, K., L. M. M€oller, R. G. Harcourt, S. E. Gibbs and L. B. Beheregaray. 2007.Genetic differentiation in bottlenose dolphins from South Australia: Associationwith local oceanography and coastal geography. Marine Ecology Progress Series 341:265–276.

Blower, D., J. Pandolfi, B. Bruce, M. Gomez-Cabrera and J. Ovenden. 2012. Populationgenetics of Australian white sharks reveals fine-scale spatial structure, transoceanicdispersal events and low effective population sizes. Marine Ecology Progress Series455:229–244.

Bohonak, A. J. 1999. Dispersal, gene flow, and population structure. Quarterly Review ofBiology 74:21–45.

Browning, N. E., C. Dold, J. I-Fan and G. A. J. Worthy. 2014. Isotope turnover rates anddiet-tissue discrimination in skin of ex situ bottlenose dolphins (Tursiops truncatus). TheJournal of Experimental Biology 217:214–221.

Bryan, C. E., S. J. Christopher, B. C. Balmer and R. S. Wells. 2007. Establishing baselinelevels of trace elements in blood and skin of bottlenose dolphins in Sarasota Bay, Florida:Implications for non-invasive monitoring. Science of the Total Environment 388:325–342.

Caut, S., E. Angulo and F. Courchamp. 2009. Variation in discrimination factors (D15N andD13C): The effect of diet isotopic values and applications for diet reconstruction. Journalof Applied Ecology 46:443–453.

Chilvers, B. L., and P. J. Corkeron. 2001. Trawling and bottlenose dolphins’ social structure.Proceedings of the Royal Society of London, Series B 268:1901–1905.

Chilvers, B. L., I. R. Lawler, F. Macknight, H. Marsh, M. Noad and R. Paterson. 2005.Moreton Bay, Queensland, Australia: An example of the co-existence of significantmarine mammal populations and large-scale coastal development. BiologicalConservation 122:559–571.

Cockcroft, V. G., A. C. De Kock, D. A. Lord and G. J. B. Ross. 1989. Organochlorines inbottlenose dolphins Tursiops truncatus from the east coast of South Africa. South AfricanJournal of Marine Science 8:207–217.

Connor, R. C., M. R. Heithaus, P. Berggren and J. L. Miksis. 2000a. “Kerplunking”: Surfacefluke-splashes during shallow-water bottom foraging by bottlenose dolphins. MarineMammal Science 16:646–653.

Connor, R. C., R. S. Wells, J. Mann and A. J. Read. 2000b. The bottlenose dolphin: Socialrelationships in a fission-fusion society. Pages 91–126 in J. Mann, R. C. Connor, P. L.Tyack and H. Whitehead, eds. Cetacean societies: Field studies of dolphins and whales.The University of Chicago Press, Chicago, IL.

Crandall, K. A., O. R. P. Bininda-Emonds, G. M. Mace and R. K. Wayne. 2000. Consideringevolutionary processes in conservation biology. Trends in Ecology and Evolution15:290–295.

Crawford, K., R. A. McDonald and S. Bearhop. 2008. Applications of stable isotopetechniques to the ecology of mammals. Mammal Review 38:87–107.

Davie, P. J. F., and J. N. A. Hooper. 1998. Patterns of biodiversity in marine invertebrate andfish communities of Moreton Bay. Pages 331–346 in I. R. Tibbetts, N. J. Hall and W.C. Dennison, eds. Moreton Bay and catchment. School of Marine Science, University ofQueensland, Brisbane, Australia.


Davis, J. M., and J. A. Stamps. 2004. The effect of natal experience on habitat preferences.Trends in Ecology Evolution 19:411–416.

D�ıaz L�opez, B., and J. A. B. Shirai. 2008. Marine aquaculture and bottlenose dolphins’(Tursiops truncatus) social structure. Behavioral Ecology and Sociobiology 62:887–894.

Funk, D. J., P. Nosil and W. J. Etges. 2006. Ecological divergence exhibits consistentlypositive associations with reproductive isolation across disparate taxa. Proceedings of theNational Academy of Sciences 103:3209–3213.

Gannon, D. P., and D. M. Waples. 2004. Diets of coastal bottlenose dolphins from the U. S.mid-Atlantic coast differ by habitat. Marine Mammal Science 20:527–545.

Garaffo, G., S. Dans, S. Pedraza, M. Degrati, A. Schiavini, R. Gonz�alez and E. A. Crespo.2011. Modeling habitat use for dusky dolphin and Commerson’s dolphin in Patagonia.Marine Ecology Progress Series 421:217–227.

Gilson, A., M. Syvanen, K. Levine and J. D. Banks. 1998. Deer gender determination bypolymerase chain reaction: Validation study and application to tissues, bloodstains, andhair forensic samples from California. California Fish and Game 84:159–169.

Gowans, S., and H. Whitehead. 1995. Distribution and habitat partitioning by smallodontocetes in the Gully, a submarine canyon on the Scotian Shelf. Canadian Journal ofZoology 73:1599–1608.

Hale, P. T., A. S. Barreto and G. J. B. Ross. 2000. Comparative morphology and distributionof the aduncus and truncatus forms of bottlenose dolphin Tursiops in the Indian andWestern Pacific Oceans. Aquatic Mammals 26:101–110.

Heithaus, M. R., and L. M. Dill. 2002. Food availability and tiger shark predation riskinfluence bottlenose dolphin habitat use. Ecology 83:480–491.

Hicks, B. D., D. J. St. Aubin, J. R. Geraci and W. R. Brown. 1985. Epidermal growth in thebottlenose dolphin, Tursiops truncatus. Journal of Investigative Dermatology 85:60–63.

Hoelzel, A. R. 1998. Genetic structure of cetacean populations in sympatry, parapatry, andmixed assemblages: Implications for conservation policy. Journal of Heredity 89:451–458.

Hoelzel, A. R., and G. A. Dover. 1991. Genetic differentiation between sympatric killerwhale populations. Heredity 66:191–195.

Hoelzel, A. R., M. Dahlheim and S. J. Stern. 1998a. Low genetic variation among killerwhales (Orcinus orca) in the eastern North Pacific and genetic differentiation betweenforaging specialists. Journal of Heredity 89:121–128.

Hoelzel, A. R., C. W. Potter and P. B. Best. 1998b. Genetic differentiation betweenparapatric ‘nearshore’ and ‘offshore’ populations of the bottlenose dolphin. Proceedings ofthe Royal Society of London, Series B 265:1177–1183.

Hoelzel, A. R., J. Hey, M. E. Dahlheim, C. Nicholson, V. Burkanov and N. Black. 2007.Evolution of population structure in a highly social top predator, the killer whale.Molecular Biology and Evolution 24:1407–1415.

Irvine, A. B., M. D. Scott, R. S. Wells and J. H. Kaufmann. 1981. Movements and activitiesof the Atlantic bottlenose dolphin, Tursiops truncatus, near Sarasota, Florida. FisheryBulletin 79:671–678.

Kelly, J. F. 2000. Stable isotopes of carbon and nitrogen in the study of avian and mammaliantrophic ecology. Canadian Journal of Zoology 78:1–27.

Kemper, C., P. Gibbs, D. Obendorf, S. Marvanek and C. Lenghaus. 1994. A review of heavymetal and organochlorine levels in marine mammals in Australia. Science of the TotalEnvironment 154:129–139.

Kiszka, J., B. Simon-Bouhet, L. Martinez, C. Pusineri, P. Richard and V. Ridoux. 2011.Ecological niche segregation within a community of sympatric dolphins around atropical island. Marine Ecology Progress Series 433:273–288.

Kiszka, J., B. Simon-Bouhet, C. Gastebois, C. Pusineri and V. Ridoux. 2012. Habitatpartitioning and fine scale population structure among insular bottlenose dolphins(Tursiops aduncus) in a tropical lagoon. Journal of Experimental Marine Biology andEcology 416–417:176–184.


Klatsky, L. J., R. S. Wells and J. C. Sweeney. 2007. Offshore bottlenose dolphins (Tursiopstruncatus): Movement and dive behavior near the Bermuda Pedestal. Journal ofMammalogy 88:59–66.

Kr€utzen, M., E. Valsecchi, R. C. Connor and W. B. Sherwin. 2001.Characterization of microsatellite loci in Tursiops aduncus. Molecular Ecology Notes1:170–172.

Kr€utzen, M., L. M. Barr�e, L. M. M€oller, M. R. Heithaus, C. Simms and W. B. Sherwin. 2002.A biopsy system for small cetaceans: Darting success and wound healing in Tursiops spp.Marine Mammal Science 18:863–878.

Lavery, T. J., N. Butterfield, C. M. Kemper, R. J. Reid and K. Sanderson. 2008. Metals andselenium in the liver and bone of three dolphin species from South Australia, 1988–2004. Science of the Total Environment 390:77–85.

Lowther, A. D., R. G. Harcourt, S. D. Goldsworthy and A. Stow. 2012. Population structureof adult female Australian sea lions is driven by fine-scale foraging site fidelity. AnimalBehavior 83:691–701.

Mann, J., and B. Sargeant. 2003. Like mother, like calf: The ontogeny of foraging traditionsin wild Indian Ocean bottlenose dolphins (Tursiops sp.). Pages 236–266 in D. M.Fragaszy and S. Perry, eds. The biology of traditions: Models and evidence. CambridgeUniversity Press, Cambridge, U.K.

Meador, J. P., D. Ernest, A. A. Hohn, K. Tilbury, J. Gorzelany, G. Worthy and J. E. Stein.1999. Comparison of elements in bottlenose dolphins stranded on the beaches of Texasand Florida in the Gulf of Mexico over a one-year period. Archives of EnvironmentalContamination and Toxicology 36:87–98.

Mendez, M., H. Rosenbaum and P. Bordino. 2008. Conservation genetics of the franciscanadolphin in Northern Argentina: Population structure, by-catch impacts, andmanagement implications. Conservation Genetics 9:419–435.

M€oller, L. M., J. Wiszniewski, S. J. Allen and L. B. Beheregaray. 2007. Habitat type promotesrapid and extremely localised genetic differentiation in dolphins. Marine and FreshwaterResearch 58:640–648.

M€oller, L., F. Valdez, S. Allen, K. Bilgmann, S. Corrigan and L. Beheregaray. 2011. Fine-scalegenetic structure in short-beaked common dolphins (Delphinus delphis) along the EastAustralian Current. Marine Biology 158:113–126.

Moritz, C. 2002. Strategies to protect biological diversity and the evolutionary processes thatsustain it. Systematic Biology 51:238–254.

Munoz-Fuentes, V., C. T. Darimont, R. K. Wayne, P. C. Paquet and J. A. Leonard. 2009.Ecological factors drive differentiation in wolves from British Columbia. Journal ofBiogeography 36:1516–1531.

Nater, A., A. M. Kopps and M. Kr€utzen. 2009. New polymorphic tetranucleotidemicrosatellites improve scoring accuracy in the bottlenose dolphin Tursiops aduncus.Molecular Ecology Resources 9:531–534.

Natoli, A., A. Birkun, A. Aguilar, A. Lopez and A. R. Hoelzel. 2005. Habitat structure andthe dispersal of male and female bottlenose dolphins (Tursiops truncatus). Proceedings ofthe Royal Society of London, Series B 272:1217–1226.

Parra, G. J. 2006. Resource partitioning in sympatric delphinids: Space use and habitatpreferences of Australian snubfin and Indo-Pacific humpback dolphins. Journal ofAnimal Ecology 75:862–874.

Parsons, E. C. M. 1999. Trace element concentrations in the tissues of cetaceans from HongKong’s territorial waters. Environmental Conservation 26:30–40.

Parsons, K. M., J. W. Durban, D. E. Claridge, D. L. Herzing, K. C. Balcomband L. R. Noble. 2006. Population genetic structure of coastal bottlenosedolphins (Tursiops truncatus) in the northern Bahamas. Marine Mammal Science 22:276–298.

Patterson, E. M., and J. Mann. 2011. The ecological conditions that favor tool use andinnovation in wild bottlenose dolphins (Tursiops sp.). PLOS ONE 6:e22243.


Patterson, D., and C. Witt. 1992. Hydraulic processes in Moreton Bay. Pages 25–39 in O. N.Crimp, ed. Moreton Bay in the balance. The Australian Littoral Society, Moorooka,Australia.

Perrin, W. F., B. W€ursig and J. G. M. Thewissen. 2002. Encyclopedia of marine mammals.Academic Press, San Diego, CA.

Peterson, B. J., and B. Fry. 1987. Stable isotopes in ecosystem studies. Annual Review ofEcology and Systematics 18:293–320.

Pilot, M., W. Jedrzejewski, W. Branicki, V. E. Sidorovich, B. Jedrzejewska, K. Stachura andS. M. Funk. 2006. Ecological factors influence population genetic structure of Europeangrey wolves. Molecular Ecology 15:4533–4553.

Pimm, S. L., and M. L. Rosenzweig. 1981. Competitors and habitat use. Oikos 37:1–6.Post, D. M., C. A. Layman, D. A. Arrington, G. Takimoto, J. Quattrochi and C. G. Monta~na.

2007. Getting to the fat of the matter: models, methods and assumptions for dealingwith lipids in stable isotope analyses. Oecologia 152:179–189.

Pritchard, J. K., M. Stephens and P. Donnelly. 2000. Inference of population structure usingmultilocus genotype data. Genetics 155:945–959.

Qu�erouil, S., J. Kiszka, A. R. Cordeiro, et al. 2013. Investigating stock structure andtrophic relationships among island-associated dolphins in the oceanic waters of theNorth Atlantic using fatty acid and stable isotope analyses. Marine Biology 160:1325–1337.

Quinn, R. H. 1992. Fisheries resources of the Moreton Bay region. Queensland FishManagement Authority, Brisbane, Australia.

Rosel, P. E., L. Hansen and A. A. Hohn. 2009. Restricted dispersal in a continuouslydistributed marine species: common bottlenose dolphins Tursiops truncatus in coastalwaters of the western North Atlantic. Molecular Ecology 18:5030–5045.

Rosenzweig, M. L. 1981. A theory of habitat selection. Ecology 62:327–335.Rosenzweig, M. L. 1991. Habitat selection and population interactions: The search for

mechanism. American Naturalist 137:25–28.Rubenstein, D. R., and K. A. Hobson. 2004. From birds to butterflies: Animal movement

patterns and stable isotopes. Trends in Ecology and Evolution 19:256–263.Rueness, E. K., N. C. Stenseth, M. O’Donoghue, S. Boutin, H. Ellegren and K. S. Jakobsen.

2003. Ecological and genetic spatial structuring in the Canadian lynx. Nature 425:69–72.

Sacks, B. N., S. K. Brown and H. B. Ernest. 2004. Population structure of California coyotescorresponds to habitat-specific breaks and illuminates species history. Molecular Ecology13:1265–1275.

Sacks, B. N., D. L. Bannasch, B. B. Chomel and H. B. Ernest. 2008. Coyotes demonstratehow habitat specialization by individuals of a generalist species can diversify populationsin a heterogeneous ecoregion. Molecular Biology and Evolution 25:1384–1394.

Sargeant, B. L., J. Mann, P. Berggren and M. Kr€utzen. 2005. Specialization and developmentof beach hunting, a rare foraging behavior, by wild bottlenose dolphins (Tursiops sp.).Canadian Journal of Zoology 83:1400–1410.

Schoener, T. W. 1986. Resource partitioning. Pages 91–126 in J. Kikkawa and D. J.Anderson, eds. Community ecology: Pattern and process. Blackwell Scientific,Melbourne, Australia.

Sellas, A. B., R. S. Wells and P. E. Rosel. 2005. Mitochondrial and nuclear DNA analysesreveal fine scale geographic structure in bottlenose dolphins (Tursiops truncatus) in theGulf of Mexico. Conservation Genetics 6:715–728.

Shinohara, M., X. Domingo-Roura and O. Takenaka. 1997. Microsatellites in the bottlenosedolphin Tursiops truncatus. Molecular Ecology 6:695–696.

Silber, G. K., and D. Fertl. 1995. Intentional beaching by bottlenose dolphins (Tursiopstruncatus) in the Colorado River Delta, Mexico. Aquatic Mammals 21:183–186.

Sk�ulason, S., and T. B. Smith. 1995. Resource polymorphisms in vertebrates. Trends inEcology and Evolution 10:366–370.


Smolker, R. A., A. F. Richards, R. C. Connor and J. W. Pepper. 1992. Sex differences inpatterns of association among Indian Ocean bottlenose dolphins. Behaviour 123:38–69.

Smolker, R. A., A. F. Richards, R. C. Connor, J. Mann and P. Berggren. 1997. Sponge-carrying by Indian Ocean bottlenose dolphins: Possible tool-use by a delphinid.Ethology 103:454–465.

Stavros, H.-C. W., G. D. Bossart, T. C. Hulsey and P. A. Fair. 2007. Trace elementconcentrations in skin of free-ranging bottlenose dolphins (Tursiops truncatus) from thesoutheast Atlantic coast. Science of the Total Environment 388:300–315.

Torres, L. G., and A. J. Read. 2009. Where to catch a fish? The influence of foraging tactics onthe ecology of bottlenose dolphins (Tursiops truncatus) in Florida Bay, Florida. MarineMammal Science 25:797–815.

Torres, L. G., P. E. Rosel, C. D’Agrosa and A. J. Read. 2003. Improving management ofoverlapping bottlenose dolphin ecotypes through spatial analysis and genetics. MarineMammal Science 19:502–514.

Wilson, B., P. M. Thompson and P. S. Hammond. 1997. Habitat use by bottlenose dolphins:Seasonal distribution and stratified movement patterns in the Moray Firth, Scotland.Journal of Applied Ecology 34:1365–1374.

Wiszniewski, J., S. J. Allen and L. M. M€oller. 2009. Social cohesion in a hierarchicallystructured embayment population of Indo-Pacific bottlenose dolphins. AnimalBehaviour 77:1449–1457.

Wiszniewski, J., L. Beheregaray, S. Allen and L. M€oller. 2010. Environmental and socialinfluences on the genetic structure of bottlenose dolphins (Tursiops aduncus) insoutheastern Australia. Conservation Genetics 11:1405–1419.

W€ursig, B., and T. A. Jefferson. 1990. Methods of photo-identification for small cetaceans.Report of the International Whaling Commission (Special Issue 12):43–52.

W€ursig, B., and M. W€ursig. 1977. The photographic determination of group size,composition, and stability of coastal porpoises (Tursiops truncatus). Science 198:755–756.

Yang, J., T. Kunito, S. Tanabe, M. Amano and N. Miyazaki. 2002. Trace elements in skin ofDall’s porpoises (Phocoenoides dalli) from the northern waters of Japan: An evaluation forutilization as non-lethal tracers. Marine Pollution Bulletin 45:230–236.

Yordy, J. E., R. S. Wells, B. C. Balmer, L. H. Schwacke, T. K. Rowles and J. R. Kucklick.2010. Life history as a source of variation for persistent organic pollutant (POP) patternsin a community of common bottlenose dolphins (Tursiops truncatus) resident to SarasotaBay, FL. Science of the Total Environment 408:2163–2172.

Received: 14 February 2013Accepted: 8 June 2014


habitat and resource partitioning among indo-pacific bottlenose dolphins in moreton bay, australia

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