Feeding Ecology of Odontaster validus under Different Environmental Conditions in the West Antarctic Peninsula

Simple Summary

Even though researchers have previously examined the diet of O. validus, the feeding ecology of this species of sea star is still poorly understood. To address this issue, we used a multifaceted approach to investigate the diet of O. validus from three systems with marked environmental differences of the northern Antarctic Peninsula. The results showed a significant divergence of O. validus δ¹⁵N–δ¹³C values among regions, suggesting a habitat-specific foraging behavior and confirming the ability of this species to switch resource utilization across differing habitat compositions, which may be a key survival response in the face of environmental change.

Abstract

To study how Odontaster validus can influence the spatial structure of Antarctic benthic communities and how they respond to disturbance, it is necessary to assess potential dietary shifts in different habitats. We investigated the diets of O. validus from Maxwell Bay and South Bay in the West Antarctic Peninsula. A multifaceted approach was applied including in situ observations of cardiac stomach everted contents, isotopic niche, and trophic diversity metrics. Results confirm the flexible foraging strategy of this species under markedly different environmental conditions, suggesting plasticity in resource use. The data also showed evidence of isotopic niche expansion, high δ¹⁵N values, and Nacella concinna as a common food item for individuals inhabiting a site with low seasonal sea ice (Ardley Cove), which could have significant ecological implications such as new trophic linkages within the Antarctic benthic community. These results highlight the importance of considering trophic changes of key species to their environment as multiple ecological factors can vary as a function of climatic conditions.

1. Introduction

One of the most abundant and conspicuous consumers of Antarctic ecosystems is the red sea star Odontaster validus [1,2]. Several aspects of O. validus ecology and biology have received attention, including its reproductive cycle [2,3,4,5], diet composition [6,7,8,9,10], population structure [2], and threats, such as disease [11] and increasing temperature [12,13,14,15]. Nonetheless, detailed data on the effects of food availability and trophic interactions are still scarce [5,16].

O. validus is a key species in Antarctic benthic communities [6,10], where it can exert different trophic roles [1,2,9] with different foraging tactics (i.e., omnivore, filter feeder, scavenger, herbivore, active predator, necrophagous, spongivore), allowing individuals to forage over a wide range of prey, including diatoms, amphipods, isopods, sponges, gastropods, bivalves, hydroid, sea star, sea urchin, detritus, nauplii, and algae [1,3,5,6,7,8,9]. Therefore, disentangling feeding behavior and associated trophic relationships is crucial to investigate the nature and magnitude of interactions in top-down and bottom-up regulation and to infer specific responses to habitat modification [17,18,19].

Stomach contents are often used to determine relative composition of prey species, but this method can be misleading because it does not necessarily describe what organisms can assimilate [20]. Analyses of stable isotopes of carbon and nitrogen is a powerful tool to provide time-integrated information on diet and habitat use. Stable isotopes of carbon and nitrogen (¹³C/¹²C, denoted as δ¹³C) vary across ecosystems and have the potential to trace biogeochemical processes and trophic interactions [21,22,23]. δ¹³C values distinguish the origins of organic matter [24], whereas the δ¹⁵N values are useful as a tracer for trophic levels [25]. It has been proposed that the variability of isotopic composition of a population or a species (i.e., its isotopic niche) can be used as a proxy to assess the trophic niche and, thus, the degree of individual specialization in consumers [26,27]. Advances in statistical analyses have made it possible to obtain a quantitative analysis of trophic ecology by metrics. More precisely, these metrics provide empirical and conceptual examples of trophic diversity, redundancy, and vertical and basal trophic structure [28,29].

Habitat modification of coastal Antarctic benthic communities is becoming increasingly common due to global warming [30,31,32]. Odontaster validus is highly dependent on benthic habitats as it responds rapidly to any kind of food falling to the seafloor, usually ingesting the entire food source within hours [19]. In fact, recent records show isotopic niche constriction in O. validus populations from sites with high activities of glacier meltwater and ice disturbance [16], as well as changes in size, coloration, nutrition, and reproductive effort as a result of primary production variability [2]. Accordingly, the foraging ecology of O. validus is closely linked to environmental conditions [2,15,16]; therefore, one might expect markedly differences in feeding ecology associated with context-specific habitat, especially around the northern Antarctic Peninsula where seasonal sea ice is dynamic and the distribution of resources is uneven [33,34].

Here, we quantitatively examined isotopic niches, trophic structure variation and the relative contribution of potential prey items in specimens collected from three systems with marked environmental differences of northern Antarctic Peninsula (low seasonal sea ice, high sea ice cover, and high activities of glacier meltwater and ice disturbance) to test hypotheses about O. validus dietary variation among regions. Additional analyses such as the relationships between disk radius and δ¹⁵N–δ¹³C values and composition of stomach contents were done to complement this study.

2. Materials and Methods

2.1. Study Sites

This study was conducted at two sites in Maxwell Bay (Marian Cove and Ardley Cove) on King George Island (South Shetland Archipelago), and one site on South Bay in Doumer Island (Palmer Archipelago) (Figure 1). Details of study sites are shown in

Table 1. Details of study sites. Salinity and seawater temperature gradient refer to surface waters (<10 m depth) throughout the year.

	Maxwell Bay		South Bay
	Marian Cove	Ardley Cove
Salinity gradient (psu)	33.8–34.1 [35]	33.97–34.14 [36]	34.2–34.7 [37]
Seawater temperature (°C)	−1.8–1.5 [35]	−1.4–1.8 [36]	−1.7–3.0 [38]
Physical disturbances (runoff)	High [35]	Low [36]	Low [37]
Total chlorophyll maxima (mg Chl-a m−3)	29.2 [39]		19.7 [39]
Annual sea ice extent	June–July [37]		June–November [37]

.

2.1.1. Marian Cove—High Activity of Glacier Meltwater and Ice Disturbance

Marian Cove is a rapidly warming and deglaciating small fjord mall (4.5 km in length, 1.5 km in width, and up to 120 m deep) where tidewater glaciers have retreated approximately 1.9 km over the last six decades [35]. Two zones can be distinguished in there including an inner cove, where maximal depths can reach 50 m (average = 30 m), and an outer deeper cove (>100 m) [35,40]. The present study focused on inner cove (0.2 km to glacier), where glacier break-up occurs throughout the summer months, introducing large volumes of turbid meltwater and icebergs into the cove [35,41,42,43]. Previous studies on the benthic faunal assemblages revealed a variety of filter feeders, including ascidians, sponges, and polychaetes associated to benthic diatom blooms [44,45].

2.1.2. Ardley Cove—Low Seasonal Sea Ice

Ardley Cove is a small area (2.5 km in length, 1.5 km in width, and up to 50 m deep) located in the innermost part of the Maxwell Bay (Figure 1A). Local hydrography is influenced mainly by marine water [36]. The benthic community of Ardley Cove is characterized by highly abundant and diverse macroinvertebrates and macroalgae, with a subtidal zone dominated by brown and red microalgae, several species of fishes, scavengers, grazers, sponges, bryozoans, and ascidians [46,47].

Another important characteristic in the study area is a physical and biogeochemical gradient between Ardley Cove and Marian Cove because of decreasing concentrations of suspended particulate matter and increasing temperature and salinity values with increasing distance from the meltwater sources [48,49].

2.1.3. South Bay—High Sea Ice Cover

South Bay is a small bay (2.6 km in length, 1 km width, and up to 222 m deep), largely covered by an ice cap with small subglacial discharge outflows and some ice calving around the fjord periphery [37]. Benthic habitats are characterized by rocky steep slopes and a marked shift from motile fauna at shallower areas (<10 m), to large sessile benthos at depths down to 30 m. Sites down to about 40 m depth appeared to be strongly affected by ice scouring, resulting in the occurrence of a marked patchiness in the distribution of communities [50].

2.2. Field Sampling

2.2.1. O. validus

Seventeen adults (arm length > 22 mm [1]) of O. validus, were collected per site during the austral summer 2017/2018 from subtidal sites (5–20 m depth). In Marian Cove, individuals were collected by hand whereas in Maxwell Bay, suction dredge sampling was the method of choice using a portable underwater venture suction dredge device equipped with a 20-µm mesh size. All organisms were measured to record arm length (distance from the mouth to the tip of the longest arm) and then sorted and frozen (−20 °C) until it was time to analyze them.

Four transects running perpendicular from the shore to a depth of 15 m were also surveyed to observe the in situ stomach contents of 15 adult O. validus. These observations were performed during 30-min surveys by SCUBA divers. Within each time interval, a total of 15 specimens were measurement and we flipped over every one to record if it was feeding (i.e., with stomach everted and a prey trapped within) and, if so, we wrote down which prey species were being consumed.

2.2.2. Potential Prey

In subtidal sites (depth < 30 m) at Ardley Cove and South Bay specimens of Gondogeneia antarctica, Nacella concinna, and Palmaria decipiens were collected by hand by SCUBA divers during the austral summer of 2018. The specimens were washed repeatedly with milliQ water and dried at 60 °C for 48 h.

2.2.3. Suspended Particulate Organic Matter (POM)

Water column POM data were obtained from water samples taken with 10-L go-flo bottle at 5-m during the austral summers of 2017 at Ardley Cove and South Bay. Water samples were filtered with GF-F glass fiber filters (47 mm diameter, 0.7 μm pore size), treated with 1M HCl, and rinsed with distilled water to eliminate carbonates.

2.3. Stable Isotope Analysis

In the laboratory, mollusk mantle, crustaceans (entire), and the tegument of each arm of O. validus were thawed with distilled water and oven-dried at 60 °C for 36–48 h, and then ground to a fine powder with a mortar and pestle. As sea stars’ and crustaceans’ endoskeletons are made of carbonates which, in turn, are more enriched with ¹³C than other tissue components, these tissues were acidified for the removal of carbonates by wetting the filters with 1 mL 0.5M hydrochloric acid (HCl). Lipids were extracted from all tissues with a chloroform/methanol (2:1) solution [51]. This was done because, compared to other molecules, lipids are depleted of ¹³C [52] and their concentration in tissues may vary between and within species.

Approximately 0.3–0.5 mg of tegument, mollusk mantle, and crustaceans (entire) were weighed in sterilized tin capsules and analyzed for dual stable carbon and nitrogen isotopes. All the consumers and benthic primary food sources were analyzed at the Pontificia Universidad Católica de Chile (Flash EA200 IRMS Delta Series, Thermo Scientific, Bremen, Germany), and the suspended POM was analyzed at the University of California, Davis, using a PDZ Europa ANCA-GSL elemental analyzer interfaced to a PDZ Europa 20–20 isotope ratio mass spectrometer (Sercon Ltd., Cheshire, UK).

Stable isotope ratios were reported in standard (δ) notation using the following equation:

δX = [(R_sample/R_standard) − 1] × 1000

(1)

where X is either ¹³C or ¹⁵N, R is the ratio of heavy to light isotopes, and the standard is either PDB for ¹³C or atmospheric N² for ¹⁵N. The reproducibility, as determined by the standard deviation of the internal standards, was ±0.18‰ and 0.30‰ for δ¹⁵N and δ¹³C, respectively.

2.4. Stomach Contents Analysis

The importance of the different prey items was evaluated calculating the frequency of occurrence (%F = number of stomachs containing prey i/total number of stomachs containing prey × 100) [53]. Prey were identified to the lowest possible taxonomic level on the basis of their digestion state.

2.5. Statistical Analysis

Permutational multivariate analysis of variance (PERMANOVA) [54,55], based on Bray–Curtis dissimilarity matrix (estimated probabilities were based on 999 permutations), was used to examine the divergence of O. validus δ¹⁵N–δ¹³C values among regions. A posteriori pairwise comparisons were used to determine significant differences among sites.

Absolute values of δ¹³C were used and all data were square root transformed prior to analyses to reduce the effects of outliers. We performed these analyses using the software Primer-7 [56]. An alpha level of 0.05 was used throughout to indicate statistical significance.

Trophic structure, in terms of trophic diversity and trophic redundancy of O. validus populations from the different regions, was investigated by calculating six quantitative community-wide Layman metrics using mean carbon and nitrogen isotope ratios of the consumers [29]. Trophic diversity is reflected by (1) δ¹⁵N range (NR) which represents the distance from the most depleted to the most enriched δ¹⁵N values between species and provides information regarding vertical trophic structure, (2) δ¹³C range (CR) is the distance from the most depleted to the most enriched δ¹³C values between species and represents the niche diversification with respect to the food sources; higher CR reflects the utilization of a broader spectrum of food sources; and (3) mean distance to centroid (CD), is the average Euclidean distance of each species to the centroid and provides information about the average degree of trophic diversity. Trophic redundancy, then, is characterized by (4) the mean nearest neighbor distance (MNND), which is the mean Euclidean distance in the bivariate isotopic space of each specimen to its nearest neighbor, and as such reflects a measure of overall density of species packing; (5) the standard deviation of nearest neighbor distance (SDNND), which is calculated as the standard deviation of these Euclidean distances and is a measure of the evenness of the spatial density and packing of the specimens in the isotopic space. Low MNND values (increased trophic redundancy) are an indication of populations with a large proportion of specimens with similar trophic ecologies, while low SDNND values suggest more even distribution of the isotopic niches [29]. In addition, both SEAC (the corresponding metric corrected for small sample size) and the Bayesian estimation of ellipse size SEAB were calculated to, respectively, represent the total niche space and to probabilistically compare the isotopic niches between regions [57,58]. Bayesian estimations of the isotopic niche and Layman metrics (based on 10⁵ successive iterations) were computed for each site and subsequent pairwise comparisons were computed with the SIBER package [27,57]. Pairwise comparisons of metrics between sites were calculated by comparing pairs of draws from the posterior distributions. If this percentage exceeded 95% or it was lower than 5%, the differences between metrics were considered as meaningful. All computations of metrics were done in R version 3.2.1. Finally, to estimate the relative contribution of prey items to O. validus, in each study site, we used the upgrade function simmr from the package Stable Isotope Mixing Models within R. This upgraded version contains a sophisticated mixing model that allows realistic assessments and discerning source contributions to a mixture [58]. Models were built over four Markov chains with 10,000 steps per chain and a burn-in of 1000 iterations. Data within each group fitted a normal distribution [59]. The model included the fractionation factor (Δ) suggested by McCutchan et al. [60] for different species (Δ¹³C, mean ± SD = 0.4 ± 1.2‰; Δ¹⁵N = 2.3 ± 1.6‰).

Potential prey items were selected according to studies analyzing stomach contents [1,3,5,6,7,8,9] and this study], although they may not give full coverage of the diet due to biases in sampling. δ¹⁵N–δ¹³C values of prey items from Marian Cove were obtained from Ahn et al. [61] (G. antarctica, P. decipiens, and suspended POM) and Choy et al. [62] (N. concinna).

Statistical analyses included a Kolmogorov–Smirnov test with the Lilliefors correction to explore whether O. validus δ¹⁵N–δ¹³C values followed normal distributions. Additionally, lineal regressions were used to examine how δ¹⁵N–δ¹³C values varied with the disk radius. These analyses were carried out with PASW Statistics (version 17.0 for Windows, SPSS, Chicago, IL, USA). Significance was assumed at 0.05.

3. Results

3.1. Divergence of O. validus δ¹⁵N–δ¹³C Values among Regions

A summary of PERMANOVA test and post hoc pairwise comparisons are shown in

Table 2. Summary of PERMANOVA test and post hoc pairwise comparisons.

PERMANOVA Test
	F	p
δ15N	16.695	0.001
δ13C	4.5288	0.016
Post Hoc Pairwise Comparisons
	Group	t	p
δ15N	Marian Cove, South Bay	5.0445	0.001
	Marian Cove, Ardley Cove	2.3037	0.034
	South Bay, Ardley Cove	5.1102	0.001
δ13C	Marian Cove, South Bay	3.3621	0.002
	Marian Cove, Ardley Cove	2.0963	0.037
	South Bay, Ardley Cove	0.6094	0.560

. We found significant differences in O. validus δ¹⁵N–δ¹³C among sites (Table 2; Figure 2). O. validus ¹³C values from South Bay was usually enriched in ¹³C compared with the individuals from Marian Cove and Ardley Cove (Figure 2A). Furthermore, in Ardley Cove O. validus were characterised by isotopic signatures enriched ¹⁵N (Figure 2B). Pairwise tests showed that O. validus δ¹³C values varied significantly between Marian Cove and Ardley Cove and South Bay and Marian Cove (Table 2).

3.2. Isotopic Niche and Trophic Structure of O. validus Populations among Regions

The generation of standard ellipses with the mean station-corrected δ¹³C and δ¹⁵N values of O. validus (Figure 3A) and the subsequent computation of SEAB (Figure 3B) showed that Ardley Cove O. validus population had the largest SEAB (mode = 0.6‰2, 95% credibility interval CI95 = 4.4–12.0‰2) followed by Marian Cove O. validus population (mode = 2.8‰2, CI95 = 1.6–4.6‰2). South Bay O. validus population had the lower SEAB (mode = 2.3‰2, CI95 = 1.3–3.9‰2). Overall, the trophic diversity (CR, NR, CD) and the trophic redundancy (MNND and SDNND values) differed among regions (Figure 4,

Table 3. Probability that the Layman metric and isotopic niche width (SEAB) of the row is smaller than that of the column.

δ13C Range (CR)
	Marian Cove	South Bay	Ardley Cove
Marian Cove		0.8870	0.0088
South Bay	0.1130		0.0018
Ardley Cove	0.9913	0.9983
δ15N Range (NR)
	Marian Cove	South Bay	Ardley Cove
Marian Cove		0.5418	0.2105
South Bay	0.45825		0.1853
Ardley Cove	0.7895	0.81475
Mean Distance to Centroid (CD)
	Marian Cove	South Bay	Ardley Cove
Marian Cove		0.8373	0.0009
South Bay	0.1628
Ardley Cove	0.9913	0.9968	0.0033
Mean Nearest Neighbor Distance (MNND)
	Marian Cove	South Bay	Ardley Cove
Marian Cove		0.7988	0.0365
South Bay	0.2013		0.0085
Ardley Cove	0.9635	0.9915
Standard Deviation of the Nearest Neighbor Distance (SDNND)
	Marian Cove	South Bay	Ardley Cove
Marian Cove		0.6910	0.0943
South Bay	0.3090		0.0470
Ardley Cove	0.9058	0.9530
Standard Ellipse Area Bayesian Estimations (SEAB)
	Marian Cove	South Bay	Ardley Cove
Marian Cove		0.6935	0.0028
South Bay	0.3065		0.0013
Ardley Cove	0.9973	0.9988

). The largest trophic diversity (CR~8.07, NR~3.93 CD~2.55) and absolute trophic redundancy values (MNND~0.66 and SDNND~0.42) were found in O. validus population from Ardley Cove, showing that this zone is characterized by a high trophic diversity and low trophic redundancy.

In contrast, the population from South Bay had the lowest absolute trophic diversity (CR~6.90, NR~1.3, CD~1.52) (Figure 4A–C) and redundancy values (MNND~0.52 and SDNND~0.29) (Figure 4D,E). The probabilities that the metrics of Ardley Cove were larger than those from other zones generally exceeded 0.7 (Table 3).

3.3. Exploring O. validus δ¹⁵N–δ¹³C Values with Disk Radius

Individuals from both Marian Cove and Ardley Cove regions showed positive linear relationships between disk radius and δ¹⁵N–δ¹³C values (Figure 5) indicating a shift in dietary source and trophic level with size, but no relation was found for O. validus from South Bay (Figure 5C,D).

3.4. Observing In Situ Cardiac Stomach Everted Contents of O. validus from Ardley Bay

All cardiac stomachs examined (n = 12) contained food items. A total of 9 different taxa and 6 species could be positively identified (Figure 6). The gastropod N. concinna was the main prey observed in stomachs (Fo = 34%), followed by amphipods (Fo = 17%) and Limatula hodgosoni (Fo = 13%). Polychaetes, Sterechinus neumayeri, Margarella antarctica, Littorinids, and the seastar Neosmilaster georgianus also constituted the O. validus diet.

3.5. Relative Contribution of Four Potential Prey to O. validus Diet

Overall, the simmr model output showed that different contributions of N. concinna, suspended POM, G. antarctica, and P. decipiens to O. validus diet across regions. O. validus at Marian Cove derived a high proportion of their diets (>60%) from the amphipod G. antarctica (Figure 7A). Individuals from South Bay showed a similar proportion of food sources, although N. concinna was slightly larger (Figure 7B). Conversely, O. validus at Ardley Cove derived over 40% of its isotopic signature from N. concinna and G. antarctica (Figure 7C). Details of O. validus stable isotope ratios and their potential prey are shown in

Table 4. Summary of the mean and standard deviation (mean ± SD) values of potential prey items and O. validus from each study site.

Study Site	Species/Source	δ13C (‰)	δ15N (‰)	N
Marian Cove	P. decipiens [61]	−23.1 ± 0.9	3.3 ± 0.8	2
	G. antarctica [61]	−19.2 ± 0.4	6.5 ± 0.4	6
	N. concinna [62]	−16.5 ± 1.5	5.0 ± 0.6	27
	Suspended POM [62]	−24.8 ± 1.2	3.3 ± 0.3	2
	O. validus	−19.2 ± 2.0	8.3 ± 0.5	17
South Bay	P. decipiens	−20.6 ± 0.4	4.5 ± 0.3	5
	G. antarctica	−18.8 ± 0.6	5.1 ± 0.4	5
	N. concinna	−14.1 ± 0.4	6.6 ± 0.2	5
	Suspended POM	−20.4 ± 1.2	3.3 ± 0.8	4
	O. validus	−16.9 ± 1.9	7.5 ± 0.4	17
Ardley Cove	P. decipiens	−18.5 ± 0.5	2.4 ± 0.0	5
	G. antarctica	−19.5 ± 0.2	5.8 ± 0.3	5
	N. concinna	−13.9 ± 0.7	6.9 ± 0.2	5
	Suspended POM	−19.8 ± 0.1	2.4 ± 0.0	2
	O. validus	−17.5 ± 2.8	9.1 ± 1.2	17

and Figure 7D–F.

4. Discussion

Our work shows a significant divergence of O. validus δ¹⁵N–δ¹³C values among regions, which confirms the flexible foraging strategy of this species under markedly different environmental conditions. These findings may have implications for food web models, as patterns of resource use documented among specimens from one site may not be applicable to a neighboring location.

Previous studies suggested important spatio-temporal dynamics of sea-ice cover related variations of basal resource inputs [15,63,64,65,66]. For instance, in regions where the persistence of sea ice is high, sympagic pelagic producers may support benthic organisms [15], whereas in regions free of sea ice most of the year, a mix of ice-derived materials, phytoplankton blooms and benthic sources occurs and sustains nearshore benthic communities with variable degrees of benthopelagic coupling [63,67]. The divergence of O. validus δ¹⁵N–δ¹³C values among regions reported here seems consistent with these findings, as high δ¹³C values and low δ¹⁵N values of O. validus from South Bay suggest that sympagic algae may be an important food source in an area where high sea ice concentration is present and where there is a long sea ice season. On the other hand, lower δ¹³C and higher δ¹⁵N values of O. validus from Maxwell Bay may be related to massive diatom blooms and high primary production rates recorded in the region [39] as phytoplankton blooms induce decreasing δ¹³C values in POM [68,69] and increase ¹⁵N values of surface waters as a result of the preferential consumption of ¹⁴N by phytoplankton. However, it is important to note that the high variability in these values, mainly in Ardley Cove, also suggest that O. validus assimilate a mixture of detrital and fresh organic matter derived from phytoplankton and macroalgae material, which is corroborated by Zenteno et al. [67].

The isotopic niche of O. validus from Ardley Cove was widest (also reflected by large NR and CR), likely because of high diversity of prey species in a region known for its complex trophodynamics and different primary food sources [36,67]. Similarly, detailed investigations in the outer section of Ezcurra Inlet (King George Island) show the widest isotopic niche of O. validus on a site with high benthos diversity. This corroborates current knowledge that the O. validus is a food generalist [1,2,9]. Furthermore, O. validus from Ardley Cove had the highest mean δ¹⁵N values and high reliance on sessile and mobile prey, indicating a prevalence of omnivory. Omnivory is a feeding strategy in which a consumer feeds at multiple trophic levels [70], which leads to an increase in connectance by adding weak links [71]. Theoretical and empirical evidence suggests that omnivory can stabilize food webs when trophic interactions are weak [71,72,73]. Consequently, the prevalence of omnivory of O. validus could have significant ecological implications within the Antarctic benthic community.

While the dietary niches of O. validus narrowed in Marian Cove and South Bay when compared to those of individuals in Ardley Cove, the degree of narrowing varied between both sites. In that respect, the isotopic niche width at South Bay was smaller than the isotopic niche width at Ardley Cove and Marian Cove, indicating a more restricted use of resources. This pattern is corroborated by the low CR values and a similar contribution of potential prey in individuals of South Bay. A more restricted use of resources may be context specific. For instance, in some regions, heterotrophic resources may be homogeneously distributed through the water column due to unique oceanographic regimes [74], which could be adjusting the proportion of each prey in a mixed diet with similar isotopic compositions and, thus, go undetected on bulk stable isotope analyses on a site where prey are predictable both temporally and spatially.

Isotopic niche width at Marian Cove was smaller than isotopic niche width at Ardley Cove, reflecting a more restricted use of resources and limited inter-individual differences, which is further confirmed by the low Layman metrics values (CR, CD and MNND). A similar pattern was observed in the inner Ezcurra Inlet Admiralty Bay (King George Island), where low trophic niche constriction occurs in a site with high turbidity, which could be associated with competition avoidance in a resource-limited system and intraspecific specialization of this species [16]. Interestingly, O. validus from Marian Cove feed opportunistically on mobile prey (G. antarctica), which could be linked to lower sessile prey availability due to the activities of glacier meltwater and ice disturbance in the study area [35,41,75,76]. These observations are consistent with what echinoderms do with ice disturbances, which has been recorded through monitoring carried out in other areas such as McMurdo Station [77].

Bayesian modeling offers a novel framework for quantifying the trophic plasticity and identifying the trophic strategies of O. validus. Specifically, our assessment of the contribution of prey is based on the assumption that the analysis of a relatively small number of items can be extrapolated to build generalizations of trophic ecology [67]. This approach can lead to biased conclusions because of a low sampling effort of other potential prey items (e.g., isopods, sponges, hydroid, sea star, sea urchin, detritus). Consequently, further work should be conducted to better understand the percentage of prey assimilation using multiple potential preys across regions, as well as the sources of variability to successfully apply this method within highly diverse systems.

Finally, size-based shifts in δ¹³C and δ¹⁵N values were evident in Marian Cove and Ardley Cove, with the increasing δ¹³C and δ¹⁵N values across disc radius. This shift can be explained by the replacement of smaller prey occupying lower trophic levels by larger and/or more carnivorous benthic prey in the diet during growth [16] and the ability to feed through different pathways in sites with different subsidies of basal resources. Unexpectedly, this shift was not observed in individuals from South Bay, possibly reflecting uniform foraging strategy regardless of age or a homogeneous supply of basal resources. These results show that O. validus is an omnivore that may modify its diet based on the profitability and abundance of its resources, either by switching prey or by adjusting the proportion of each in a mixed diet.

5. Conclusions

In summary, our work shows O. validus dietary variation among regions, suggesting that habitats shape potential dietary preferences in this species. Additionally, the high δ¹⁵N values and the prevalence of N. concinna as common food items for individuals inhabiting Ardley Cove may indicate that low seasonal sea ice durations directly influence O. validus trophic ecology, inducing a carnivore behavior, which in turn, may force the community to new trophic linkages. The ability of O. validus to vary resource utilization across differing habitat compositions may be a key response allowing their persistence and survival in the face of environmental change. However, fluctuations in resource availability and environmental changes could increase O. validus’ dietary complexity with implications for associated species.