Foraging habits in a generalist predator: Sex and age influence habitat selection and resource use among bottlenose dolphins (Tursiops truncatus)
Article first published online: 30 MAY 2014
© 2014 Society for Marine Mammalogy
Marine Mammal Science
Volume 31, Issue 1, pages 155–168, January 2015
How to Cite
Rossman, S., Berens McCabe, E., Barros, N. B., Gandhi, H., Ostrom, P. H., Stricker, C. A. and Wells, R. S. (2015), Foraging habits in a generalist predator: Sex and age influence habitat selection and resource use among bottlenose dolphins (Tursiops truncatus). Marine Mammal Science, 31: 155–168. doi: 10.1111/mms.12143
- Issue published online: 22 DEC 2014
- Article first published online: 30 MAY 2014
- Manuscript Accepted: 13 APR 2014
- Manuscript Received: 13 JAN 2014
- Dolphin Quest
- Earthwatch Institute
- Disney Worldwide Conservation Fund
- Morris Animal Foundation's Betty White Wildlife Rapid Response Fund
- National Marine Fisheries Service
- The U.S. Environmental Protection Agency
- International Whaling Commission
- National Science Foundation
- bottlenose dolphin;
- Tursiops truncatus;
- stable isotopes;
- foraging ecology;
- habitat use;
- individual specialization;
- Sarasota Bay
This study examines resource use (diet, habitat use, and trophic level) within and among demographic groups (males, females, and juveniles) of bottlenose dolphins (Tursiops truncatus). We analyzed the δ13C and δ15N values of 15 prey species constituting 84% of the species found in stomach contents. We used these data to establish a trophic enrichment factor (TEF) to inform dietary analysis using a Bayesian isotope mixing model. We document a TEF of 0‰ and 2.0‰ for δ13C and δ15N, respectively. The dietary results showed that all demographic groups relied heavily on low trophic level seagrass-associated prey. Bayesian standard ellipse areas (SEAb) were calculated to assess diversity in resource use. The SEAb of females was nearly four times larger than that of males indicating varied resource use, likely a consequence of small home ranges and habitat specialization. Juveniles possessed an intermediate SEAb, generally feeding at a lower trophic level compared to females, potentially an effect of natal philopatry and immature foraging skills. The small SEAb of males reflects a high degree of specialization on seagrass associated prey. Patterns in resource use by the demographic groups are likely linked to differences in the relative importance of social and ecological factors.
The use of particular food resources or habitats by members of a population impacts the intensity of intraspecific competition, social interactions, and risk of predation or parasitism (Bolnick et al. 2003). Further, a wealth of recent literature documents that ecological inequality within a population results in differential use of the total resource pool (e.g., habitat or prey type) by individuals or assemblages within that population (Bolnick et al. 2003, Newsome et al. 2009, Torres and Read 2009). Such intraspecific variation in resource use can confer both benefit and detriment to the long-term viability of a population. For example, differential habitat use among assemblages within a population can result in increased population viability amid the loss of a specific habitat type (Tyler and Rose 1994). However, loss of a habitat upon which all or most juveniles are dependent would likely result in population decline, emphasizing the importance of studying variation in resource use among demographic groups (Dahlgren et al. 2006). The impact on certain demographic groups, and thus population viability, is of particular concern for wildlife populations in close proximity to human development because resources within these communities are more likely to experience disturbance (e.g., habitat loss, competition with humans for resources). Marine mammals are of particular interest as they are large predators that often inhabit metropolitan coastal areas where habitats have undergone degradation and increased fishing pressure.
The bottlenose dolphins (Tursiops truncatus) of Sarasota Bay (SB), Florida, represent a model system to study patterns in resource use within and between demographic groups. SB dolphins are year-round, multigenerational residents that have been intensively studied for nearly five decades (Wells et al. 1987; Wells 2003, 2014). Previous stomach content studies of stranded deceased dolphins from the SB population (Barros and Wells 1998, Berens McCabe et al. 2010) provide estimates of diet that reflect recently ingested prey. Additionally, dolphin foraging has been assessed using molecular prey detection on fecal samples (Dunshea et al. 2013). Unlike stomach content analysis, molecular prey detection is not limited to salvaged individuals. However, the time period represented by the molecular data is similarly short. Together stomach content data and molecular prey detection are excellent indicators of the prey species commonly consumed by SB bottlenose dolphins. Yet, to date, there is no information on potential differences in resource use among demographic groups within the long-term resident community.
Carbon and nitrogen stable isotope analysis of bottlenose dolphin tissues complements stomach content and molecular techniques by providing information on habitat use, trophic position, and diet over a long time period (half-life of months for skin and years for muscle) (Newsome et al. 2010). The foraging habits of a large number of individuals can be obtained because, in addition to tissues from salvaged animals, analysis can be conducted on biopsies from extant members of the population. Unique types of information can be derived from stable isotope data. Carbon isotope values (δ13C) are indicators of primary production at the base of the food web. δ13C values differentiate seagrass from phytoplankton and nonseagrass habitat (mangrove and open bay) (Peterson and Fry 1987). For Sarasota Bay bottlenose dolphins, high δ13C values indicate frequent foraging in seagrass habitat (Rossman et al. 2013). Nitrogen isotope values (δ15N) generally increase by 3‰–4‰ with each step in the food chain, offering a good indicator of trophic level (Peterson and Fry 1987); although, recent studies indicate trophic dynamics may be lower for high trophic level organisms (Hussey et al. 2014). The information provided by stable isotope analysis is particularly valuable for cryptic foragers such as bottlenose dolphins who capture and consume prey underwater. Because of the ecological information derived from stable isotope approaches, mass-balance models using multiple isotopes are well established tools for determining the relative contribution of various prey sources to a population's diet (Harrigan et al. 1989, Phillips et al. 2005).
Recently, dietary assessments using stable isotopes have been advanced via the development of Bayesian mass balance models. By incorporating variability in prey and consumer isotope values, Bayesian diet modeling programs, such as Stable Isotope Analysis in R (SIAR) (Jackson et al. 2011) have a unique advantage over earlier mass balance models (Harrigan et al. 1989, Phillips et al. 2005). Unlike the earlier models that report the fractional contribution of prey to the diet as a range, Bayesian models provide a true probability distribution for each prey item (Parnell et al. 2010).
While SIAR provides an estimate of the average contribution of each prey item to the diet, the degree of variation within a population or demographic group is also an important descriptor of foraging ecology. Stable isotope Bayesian ellipses in R (SIBER) (Jackson et al. 2011) uses δ13C and δ15N values to construct ellipses that represent two dimensional equivalents of the standard deviation. While these ellipses were originally intended to compare isotopic variability among species within a community they can also be used to quantify variability within and between demographic groups and to infer differences in habitat use and trophic diversity.
In this study we assess resource use (diet, habitat use, and trophic level) among male, female, and juvenile bottlenose dolphins (demographic groups). We first compare diet among the groups using stable isotope-based Bayesian dietary estimation. We then compare variation in resource use among the groups via stable isotope Bayesian standard ellipses. These tools provide important insight into a cryptic forager and the manner in which the unique ecology of the demographic groups relates to resource use at the population level.
SB is a complex series of shallow bays (<4 m deep, 40 km long) on the central west coast of Florida, communicating with the Gulf of Mexico through narrow, deep passes separating a series of narrow barrier islands. The study area encompasses a diverse array of habitats, including seagrass meadows, mangrove fringing forests, human-altered shorelines, and open bay (Rossman et al. 2013). Fish commonly found in the diet of bottlenose dolphins were collected for isotopic analysis during fish abundance surveys 2009–2012 (Table 1) (Barros and Wells 1998, Berens McCabe et al. 2010, Dunshea et al. 2013). In total, 15 species and 234 individual samples were processed for isotope analysis. Sampling targeted fish between 100 and 300 mm, the size range most often found in stomach contents of bottlenose dolphins (Barros and Wells 1998). Bottlenose dolphin skin samples were obtained from a community of ca. 160 individuals, mostly of known age and sex that are resident to SB (Wells 2003, 2009). Skin samples were taken during health assessments when dolphins were briefly captured, biopsied, and released (Wells et al. 2004). In the field, tissues were stored in liquid nitrogen and retained frozen prior to analysis. Isotope values for bottlenose dolphin muscle tissue used to determine the trophic enrichment factor (TEF) were taken from Rossman et al. (2013). Because muscle data derive from stranded, deceased dolphins it is independent from the skin samples used for diet estimation in SIAR.
|Species||Common name||δ13C||δ15N||n||SCA||DNA||Prey cluster|
|Elops saurus||ladyfish||−17.5 ± 1.6||11.7 ± 1.1||11||0.013*||0.059*||1|
|Centropomus undecimalis||snook||−16.1 ± 0.7||11.1 ± 1.0||3||0.024||0.020||1|
|Leiostomus xanthurus||spot||−16.7 ± 2.1||10.3 ± 1.4||24||0.029||0.085||1|
|Caranx hippos||crevalle jack||−15.5 ± 1.5||11.5 ± 0.5||4||0.012*||0.009*||2|
|Cynoscion nebulosus||spotted seatrout||−14.3 ± 1.7||11.5 ± 1.7||27||0.013*||0.0230*||2|
|Lutjanus synagris||lane snapper||−14.6 ± 1.1||8.7 ± 1.1||9||0.002*||0.000*||3|
|Gerreid sp.||mojarra||−13.8 ± 1.0||7.8 ± 0.7||16||0.006*||0.003*||3|
|Orthopristis chrysoptera||pigfish||−14.3 ± 0.9||9.3 ± 0.8||27||0.020||0.008||3|
|Sciaenops ocellatus||red drum||−14.1± 1.2||9.4 ± 0.8||4||0.002*||0.000*||3|
|Archosargus probatocephalus||sheepshead||−14.9 ± 1.6||9.0 ± 0.8||15||0.018||0.028||3|
|Opsanus beta||Gulf toadfish||−13.8 ± 1.1||8.7 ± 2.2||14||0.327*||0.110*||3|
|Mugil cephalus||striped mullet||−12.9 ± 1.6||9.9 ± 4.0||15||0.022||0.008||3|
|Lagodon rhomboides||pinfish (seagrass)||−13.7 ± 1.2||8.0 ± 1.3||27||0.309||0.456||3|
|Lagodon rhomboides||pinfish (non-seagrass)||−16.1 ± 1.2||9.0 ± 0.7||20||4|
|Opisthonema oglinum||threadfin herring||−17.5 ± 1.7||9.2 ± 0.4||11||0.039*||0.003*||4|
|Harengula jaguana||scaled sardine||−16.2 ± 2.2||9.4 ± 1.4||7||0.0001||NA||4|
White muscle tissue from fish and bottlenose dolphin skin were freeze-dried, lipid extracted, and homogenized to a fine powder in a high-energy ball mill (SPEX SamplePrep) and a 1 mg aliquot of homogenate was transferred to tin capsules for stable carbon and nitrogen isotope analysis. Isotope values were determined using an elemental analyzer (Eurovector) interfaced to an Isoprime mass spectrometer (Elementar). Isotope values are expressed as:
where X represents 13C or 15N, and R represents the abundance ratios: 13C/12C or 15N/14N respectively. In-house standards used for δ13C and δ15N were calibrated with respect to international scales V-PDB and air respectively. In-house precision was ±0.2‰ for δ13C and δ15N values.
To delineate factors impacting prey fish isotope values, we assessed the influence of standard length, habitat, season, and location on δ13C and δ15N values of each of five prey fish species whose sample size was sufficient for general linear modeling (GLM). These species included spot, Leiostomus xanthurus; spotted seatrout, Cynoscion nebulosus; pigfish, Orthopristis chrysoptera; pinfish, Lagodon rhomboides; and sheepshead, Archosargus probatocephalus. The variable habitat included three levels: seagrass, mangrove, and open bay. Tukey's HSD was used to test for pairwise differences in mean δ13C or δ15N value between habitats. For the variable “season,” fish were grouped based on the calendar date of capture: spring (21 April–6 June), summer (21 June–20 September), fall (21 September–20 December), and winter (21 December–21 April). For the variable location, latitude and longitude were combined into a single variable via principal components analysis (PCA). The first PCA, retained for modeling efforts as the variable “location,” explained 97% of the variation in latitude and longitude. All statistical analyses were conducted in R 3.0.1 (R Development Core Team 2013).
Bottlenose dolphin demographic groups were defined as follows: males (>6 yr of age), females (>6 yr of age), and juveniles (2–6 yr of age). Dolphins younger than 2 yr of age are not included in health assessments and, thus, not represented in this study. Nearly all calves leave their mothers around 6 yr of age, thus the age ranges for males and females (>6 yr of age) only reflect foraging by males and females independent from their mothers (Wells 1991). The package, Stable Isotope Analysis in R (SIAR) 4.2 (Parnell and Jackson 2013) was run within R 3.0.1 (R Development Core Team 2013) to provide dietary estimates for each bottlenose dolphin demographic group. SIAR requires isotope values for consumers, isotope values of prey species, and a TEF. Because SIAR cannot differentiate prey items with similar isotope values (Phillips et al. 2005), we used a k-means cluster analysis to group prey fish into four clusters. The resulting clusters differed by trophic level and/or source of primary production at the base of the food web. The TEF value used in this study was based on stomach content data, molecular prey detection, prey isotope values, and muscle isotope values of stranded deceased dolphins from SB. First, a weighted average δ13C value of bottlenose dolphin diet was calculated as follows:
Where δ13Cd is the average carbon isotope value of bottlenose dolphin diet, Fi is the fractional contribution of diet item i based on stomach content analysis or molecular prey detection (Barros and Wells 1998, Berens McCabe et al. 2010, Dunshea et al. 2013), and δ13Ci is the average carbon isotope value of diet item i as reported in this study. To determine the δ13C TEF the isotope value of the bottlenose dolphin diet (δ13Cd) was subtracted from the average SB dolphin muscle δ13C value (Rossman et al. 2013). The same method was then applied to determine the TEF for δ15N. With only two TEF values we could not provide an estimate of variance associated with trophic fractionation which was assumed to be negligible compared to other sources of isotopic variation. Because the TEF derives from isotope values of bottlenose dolphin muscle and the dietary estimates used isotope values of skin, the TEF determination was independent of data used in Bayesian dietary estimation.
Stable isotope Bayesian ellipses in R (SIBER) including standard ellipse areas were produced using SIAR (Jackson et al. 2011). To test for significant differences we ran 100,000 Markov-chain Monte Carlo iterations for SEAb and constructed 95% credible intervals around the mean of each subgroup. The probability that there was a significant difference in SEAb between demographic groups was determined by calculating the proportion of times the posterior estimate for one demographic group was smaller than another (Turner et al. 2010). We considered the two SEAb to be significantly different when no more than 5% of the posterior estimates for one group were smaller than those of another group (α = 0.05). For graphical representations we used standard ellipse areas controlled for small sample size (SEAc).
We assessed isotope values of prey species constituting 81% (stomach content analysis) or 84% (molecular prey detection) of bottlenose dolphin diet (Barros and Wells 1998, Berens McCabe et al. 2010, Dunshea et al. 2013). Species average δ13C values ranged from −17.5‰ (ladyfish, Elops saurus, and threadfin herring, Opisthonema oglimum) to −12.9‰ (striped mullet, Mugil cephalus), and average δ15N values ranged from 7.8‰ (mojarra, Gerreid sp.) to 11.7‰ (ladyfish) (Table 1). Habitat, length, season, and location did not significantly influence the isotope values of pigfish, spot, sheepshead, or spotted seatrout. Pinfish δ13C values were significantly related to habitat and location (F2, 42 = 36.09, P < 0.001, F1, 42 = 5.20, P = 0.028, respectively). δ13C values decreased from northwest to southeast and from seagrass (mean ± standard deviation: −13.7‰ ± 1.2‰) to open bay (−15.5‰ ± 1.0‰) to mangrove habitat (−17.1‰ ± 1.0‰) (seagrass vs. open bay: P < 0.001, seagrass vs. mangrove: P < 0.001, mangrove vs. seagrass: P < 0.001). Length and season did not appear to influence pinfish δ13C values. Pinfish δ15N values demonstrated a significant relationship with habitat and length (F2, 42 = 6.43, P =0.004, F1, 42 = 5.80, P = 0.021, respectively) but not location or season. δ15N values of pinfish increased with length and were higher in open bay vs. seagrass habitat (9.3‰ ± 0.5‰ vs. 8.0‰ ± 1.3‰, P = 0.003). δ15N values from mangrove pinfish (8.6‰ ± 0.7‰) did not significantly differ from those of seagrass or open bay.
The k-means cluster analysis of prey fish isotope values combined fish species that shared a common food web base (δ13C values) and trophic level (δ15N values) (Fig. 1). High δ13C values are indicative of seagrass based food webs (e.g., seagrass grazing pinfish, −13.7‰) and low δ13C values are associated with open bay and mangrove primary production (e.g., clupeids whose food web is generally phytoplankton based: threadfin herring, −17.5‰, scaled sardine, Harengula jaguana, −16.2‰). Cluster 1, contained high trophic level nonseagrass prey and included snook (Centropomus undecimalis), ladyfish, and spot. Cluster 2 consisted of high trophic level prey associated with seagrass and consisted of seatrout and crevalle jack (Caranx hippos). Cluster 3 included low trophic level, seagrass-associated species and consisted of Gulf toadfish (Opsanus beta), seagrass pinfish, pigfish, red drum (Sciaenops ocellatus), lane snapper (Lutjanus synagris), sheepshead, mojarra, and striped mullet. Cluster 4 contained low trophic level nonseagrass associated prey and consisted of threadfin herring, nonseagrass pinfish, and scaled sardine. Because pinfish isotope values significantly differed between habitats, pinfish were separated by habitat prior to the cluster analysis. This resulted in cluster 3 containing seagrass pinfish and cluster 4 containing nonseagrass pinfish with low δ13C values (open bay and mangrove). The mean isotope values and associated standard deviation for all species within a cluster were used to estimate cluster averages and standard deviation, which were implemented as sources in the Bayesian dietary estimation.
The weighted average δ13C and δ15N of SB bottlenose dolphin diet based on the relative contribution of prey from stomach content analysis or molecular prey detection was −14.2‰ and 8.9‰ and −14.5‰ and 8.9‰, respectively (Barros and Wells 1998, Berens McCabe et al. 2010, Dunshea et al. 2013). Given the average isotope value for bottlenose dolphin muscle (−14.4‰ and 10.8‰ for δ13C and δ15N, respectively) the TEF estimate based on stomach content analysis was −0.1‰ for δ13C and 2.0‰ for δ15N. The TEF estimate based on molecular prey detection was 0.1‰ for δ13C and 2.0‰ for δ15N. The TEF used in this study was an average of the two values: 0.0‰ for δ13C and 2.0‰ for δ15N.
The mean skin isotope values, reported as mean ± standard deviation, for the three demographic groups were similar to one another: juveniles (δ13C = −14.9‰ ± 0.9‰, δ15N = 10.6‰ ± 0.6‰, n = 14), females (δ13C = −14.6‰ ± 1.3‰, δ15N = 11.2‰ ± 0.9‰, n = 14) and males (δ13C = −14.2‰ ± 0.4‰, δ15N = 10.7‰ ± 0.7‰, n = 14) (Fig. 1).
The results of the Bayesian mass balance model, given as mean ± standard deviation, showed that juveniles consumed prey cluster 3 in the highest proportion (0.58 ± 0.09) (Fig. 2) followed by cluster 4 (0.31 ± 0.11), cluster 1 (0.06 ± 0.05), and cluster 2 (0.05 ± 0.05). Females consumed cluster 3 in the highest proportion (0.60 ± 0.11), followed by cluster 4 (0.20 ± 0.12), cluster 2 (0.11 ± 0.08), and cluster 1 (0.09 ± 0.07). Males consumed prey cluster 3 in the highest proportion (0.71 ± 0.07) followed by cluster 4 (0.14 ± 0.08), cluster 2 (0.09 ± 0.06), and cluster 1 (0.06 ± 0.05).
Females had the largest SEAb at 3.59‰2 (95% CI: 2.15‰2–6.00‰2) followed by juveniles at 1.93‰2 (95% CI: 1.10‰2–3.21‰2), and males at 1.29‰2 (95% CI: 0.77‰2–2.14‰2) (Fig. 3). The SEAb of males was significantly smaller than that of females (P = 0.003) but not juveniles (P = 0.144). The SEAb of juveniles was significantly smaller compared to the SEAb of females (P = 0.046). SEAc was calculated for graphical representations of standard ellipse area (Fig.3).
Male, female, and juvenile bottlenose dolphins possess unique combinations of ecological, physiological, and social constraints (Wells 2003, 2014), all of which may impact how these different demographic groups find and consume prey. We probed differences in the foraging ecology of these three groups using stable isotope analysis and Bayesian modeling. Because our analyses included a large number of prey species (15) we performed cluster analysis to group prey. This resulted in ecologically significant clusters differentiated by source of primary production at the food web base and/or trophic level.
Our Bayesian mass balance modeling benefited from a TEF estimate that was, (1) based on prey data specific to the SB bottlenose dolphin food web, (2) independent of our skin isotope data used in SIAR, and (3) derived from two independent estimates of population diet, one based on stomach content analysis and the other on molecular prey detection (Barros and Wells 1998, Berens McCabe et al. 2010, Dunshea et al. 2013). In using the average isotope value of muscle to produce a TEF that was later applied to Bayesian modeling based on skin data, we assumed that the TEF of muscle and skin were similar. This assumption is consistent with the findings of Borrell et al. (2012) and Fernández et al. (2011), who documented identical average δ13C and δ15N values for skin and muscle from cetaceans. For SB bottlenose dolphins, the mean δ13C and δ15N isotope values of skin and muscle differed by <0.1‰.
The average TEF values calculated in this study were 0‰ for δ13C and 2.0‰ for δ15N. While our δ15N TEF is low compared to the often cited average of 3.4‰ (Post 2002), a growing body of literature documents widespread variability in TEF across and within taxa (McCutchan et al. 2003, Lecomte et al. 2011). Our values are in agreement with a low δ15N TEF expected for a consumers with a high protein diet and who utilize marine environments (Vanderklift and Ponsard 2003).
Results from the Bayesian mass balance model indicate that all bottlenose dolphin demographic groups predominantly depend on low trophic level, seagrass-associated prey fish (prey cluster 3). Among the clusters, prey cluster 3 contains the largest number of species including both prey fish frequently small (e.g., pinfish, pigfish, and mojarra) and more massive prey items (e.g., mullet). Prey cluster 3 is likely the most important dolphin diet because seagrass serves as an excellent foraging habitat, supporting high densities of prey fish and providing safety from predators in SB (e.g., bull sharks) (Barros and Wells 1998, Gannon et al. 2009, Mann et al. 2000, McHugh et al. 2011). Our findings are consistent with those of Barros and Wells (1998) documenting seagrass as an important habitat for bottlenose dolphins. In addition to prey cluster 3, juveniles, in particular, appeared to consume low trophic level, nonseagrass prey (cluster 4) to a larger extent than male or females. This may be related to physiological and behavioral constraints that are unique to juveniles. The acquisition of foraging skills by calves is likely a slow process; upon nutritional weaning (typically in second year of life), calves may not yet possess skills associated with complex foraging behavior typical of adults. For example, the detection and capture of prey species associated with structures (e.g., Gulf toadfish) or fast-moving high trophic level fish may be too difficult for young dolphins (Berens McCabe et al. 2010). The small gape size of juveniles may work in conjunction with undeveloped foraging skills to constrain diet to small, easily detectable, low trophic level prey, such as all members of prey cluster 4 and pinfish, pigfish and mojarra in prey cluster 3. However, the finding that high trophic level prey were not a large contributor to the diet of any demographic group is consistent with the observation that high trophic level prey species occur in only low abundances and may be too energetically costly for consumption at the population level.
An increasing body of literature suggests that variation in resource use within and between individuals of a population is an important ecological parameter that has profound implications for conservation biology (Bolnick et al. 2003, Johnson et al. 2009). To assess variation in the foraging behavior between male, female, and juvenile bottlenose dolphins, we used SEAb as a quantitative indicator of variation in resource use (Jackson et al. 2011). Male and female bottlenose dolphins appear widely divergent in their diversity of resource use. Males possess a significantly small SEAb, nearly one fourth the size of the female SEAb. The small SEAb size indicates that differences in foraging habits among males are small. Even though most male bottlenose dolphins possess home ranges larger than those of females (Wells 2003, Urian et al. 2009) and have access to numerous habitat types, the position and small size of the male standard ellipse indicates a predominant reliance on seagrass-associated prey. This may occur because seagrass habitat has one of the highest densities of prey fish of any habitat (Gannon et al. 2009) often including numerous large prey species (e.g., mullet), which generally provide more calories compared to smaller fish. Because gape size can be a constraint, the larger gape size of males offers an advantage. More importantly, consuming large prey allows males, relative to females and juveniles, to maximize their caloric intake while minimizing energy expenditure.
In contrast to the males, the large SEAb of females indicates broader foraging habits. The large SEAb predominately derives from the wide range of δ13C values, an indicator of habitat use (i.e., seagrass vs. open water). This suggests that individual female dolphins consistently utilize a subset of available habitats (habitat specialization). Observations of SB bottlenose dolphins suggest a high degree of habitat specialization among females. For example, females occupy smaller home ranges compared to males (Wells 2003, Urian et al. 2009). For reproductively active females, habitat familiarity, predator avoidance, and proximity to familiar female associates favor a small home range and place limitations on foraging habitat. Thus, some females in the SB population may specialize on prey from seagrass habitats while others may consume prey associated with phytoplankton based food webs. Thus, it appears that while most males specialize on seagrass-associated prey, females may specialize on a variety of habitats or prey resources. Furthermore, female bottlenose dolphin habitat selection appears correlated with trophic level. Females who forage in seagrass also consume lower tropic level prey compared to females who forage in open water. This likely results from seagrass associated female dolphins utilizing the abundant low trophic level prey commonly found in seagrass habitat. While low trophic level species are found in open water (e.g., clupeids) they do not substantially contribute to the diet of female bottlenose dolphins as indicated by SIAR results, stomach content analysis and molecular prey detection (Barros and Wells 1998, Berens McCabe et al. 2010, Dunshea et al. 2013).
Samples obtained during health assessments are, out of necessity, generally from dolphins traveling in shallow habitats. This possibly introduces a bias favoring individuals who frequently utilize seagrass, a common habitat type for shallow water. However, a bias of this nature would likely impact males and females similarly yet, we document an SEAb for females significantly larger than that of males.
Juveniles possessed an intermediate SEAb between males and females. Relative to females, the ellipse for juveniles is similar in spatial orientation but smaller in total area. The shape of the ellipse for juveniles is contracted in δ13C and lower in δ15N compared to females. The similarity in shape between the female and juvenile ellipses is likely the result of maternal habitat selection and/or the high degree of philopatry demonstrated by calves newly independent of their mother (McHugh et al. 2011). The lower δ15N values suggest that juveniles feed at a lower trophic level than females possibly resulting from limitations of a small gape size and less developed foraging skills.
Bottlenose dolphins have traditionally been described as opportunistic generalists (Shane et al. 1986). However, recent studies have demonstrated that bottlenose dolphins do not indiscriminately capture and consume prey; instead, they specialize on a subset of available prey, especially soniferous fishes (Berens McCabe et al. 2010), yet the manner in which dietary variability and specialization is partitioned within dolphin populations remains uncertain. In this study, we found an ecologically significant disparity in the diversity of resource use by male and female bottlenose dolphins, with females accounting for the majority of the variation in foraging habits at the population level. Differences in resource use among male, female, and juvenile bottlenose dolphins likely resulted from trade-offs associated with social interactions, predator avoidance, and energetic needs related to body size, activity levels, and reproductive condition. This dichotomy in resource use may have impacts for conservation and management. Because specialization in resource use within a population impacts social interaction and exposure to habitat degradation, certain subsets of the population may be more likely to strand as the result of disturbance. This is because individuals who utilize a particular foraging habitat may be predisposed to stranding or increased mortality if nutritional stress results from habitat loss or disturbance (Johnson et al. 2009). In addition, an elevated mortality risk may result from increased exposure to pathogens or diseased individuals, phenomena that may be promoted by some types of foraging specialization. Consequently, foraging habits may play a critical role in understanding the ecology of phenomena such as unusual mortality events (Gulland and Hall 2007).
We thank the many Mote Marine Laboratory and Chicago Zoological Society staff members, interns, and volunteers who made this work possible by providing logistical support and assistance in the field. We especially thank the Sarasota Dolphin Research Program's (SDRP) fish survey team, including Damon Gannon, Sunnie Brenneman, Sandy Camilleri, Katie Brueggen, along with Larry Fulford who provided much needed help for collection of samples from fish, and Mote Marine Laboratory's Stranding Investigations Program staff for samples from dolphin carcasses. The collection of samples during dolphin health assessments was greatly facilitated by SDRP staff, students, and collaborators, and especially Blair Irvine, Michael Scott, Brian Balmer, Jason Allen, Katie McHugh, and Aaron Barleycorn. We would like to thank undergraduate research assistants who aided in sample preparation and analysis Ramona Beckman and Sam DeCamp (Michigan State University). Samples from live dolphins were collected under a series of National Marine Fisheries Service Scientific Research Permits since 1984 and Mote Marine Laboratory IACUC approvals. Prey fish samples were authorized by the Florida Fish and Wildlife Conservation Commission (Special Activity License nos. 04SR-809 and 11-0809-SR) and Mote Marine Laboratory IACUC approvals. Sample collection from Sarasota Bay resident dolphins was supported by Dolphin Quest, Earthwatch Institute, Disney Worldwide Conservation Fund, Morris Animal Foundation's Betty White Wildlife Rapid Response Fund, National Marine Fisheries Service, The U.S. Environmental Protection Agency, and the International Whaling Commission. This material is based upon work supported by the National Science Foundation Graduate Research Fellowship under Grant No. (0802267) as well as Marine Mammal Commission Contract #E4047334. Any use of trade, firm, or product names is for descriptive purposes only and does not imply endorsement by the U.S. Government, Mote Marine Lab, Chicago Zoological Society or Michigan State University.
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