1. Introduction
Deep benthic, marine habitats are poorly understood ecosystems that consist of species and communities which are difficult to research but require careful management [
1,
2,
3,
4]. Sablefish,
Anoplopoma fimbria (Pallas 1814); and shortraker rockfish,
Sebastes borealis (Barsukov 1970) are syntopic fish species that inhabit the continental shelf and slope of the North Pacific Ocean [
5,
6]. They have similar ecologies and are among the most abundant large-bodied predators in deepwater benthic habitats [
7,
8]. Although they are syntopic and commonly caught in the same general locations,
A. fimbria is more associated with soft, muddy flats, whereas
S. borealis is more often associated with slopes and with boulders or rocky outcrops [
9,
10,
11]. Both species are long-lived and large-bodied (
A. fimbria, 94 years maximum age and 114 cm total length;
S. borealis, 157 years maximum age and 120 cm total length), and they exhibit low recruitment [
3,
5,
6,
12,
13].
Anoplopoma fimbria and
S. borealis support economically valuable fisheries. For 2022, in Alaska, commercial landings of
A. fimbria totaled 25 million kg and were valued at USD 147 million.
Sebastes species collectively amounted to 76.8 million kg and USD 32 million [
14]. Neither species is currently considered overfished; however, they occupy relatively low tiers (based on conservation threat) on available stock information ranked by the North Pacific Fishery Management Council and have not been evaluated by the IUCN [
15,
16]. With not many data available on either species, many aspects of their basic ecology, upon which management decisions are based, remain unclear [
1,
17]. Understanding the trophic connections and interactions among similar, co-occurring species is particularly important to inform potential management and conservation decisions [
18].
One way to inform trophic interactions between these two species is to characterize and compare their isotopic trophic niches [
19]. The isotopic niche, when quantified using δ
15N and δ
13C stable isotope ratios, provides a measurement of trophic position (δ
15N), a comparable measurement of the energy flow pathway (δ
13C), and a bivariate measure of niche breadth (or size) by combining estimates of variation from both carbon and nitrogen axes [
20,
21]. We can infer trophic levels within a food web based on δ
15N isotope ratios [
22,
23]. When consumers assimilate resources, they incorporate more of the heavier isotope, δ
15N (compared to the lighter isotope δ
14N) in their tissues [
24]. Thus, the δ
15N/δ
14N ratio increases with each trophic level at a relatively consistent rate of about 3–4‰ [
23]. In marine systems, a more enriched δ
13C ratio suggests that a population is feeding in a benthic (detrital) energy pathway, while a less enriched δ
13C ratio suggests a population is feeding in a more pelagic (phytoplankton) energy pathway [
25]. Niche breadth descriptions provide estimations of the variation associated with the isotopic niche within a population. In marine ecosystems, organisms exhibit complex and interdependent trophic interactions and dynamics [
26,
27]. Primary producers and apex predators have particularly large effects on food webs because their removal can result in cascading impacts across trophic levels (i.e., bottom-up and top-down effects) [
28,
29,
30]. Data on trophic interactions and the positioning of organisms within a food web (i.e., the trophic niche) are essential for the preservation of healthy ecosystems and understanding how environmental changes impact food webs.
Food web, isotopic, and dietary studies on
A. fimbria and
S. borealis are limited, and the most quantitative study to date is focused on juvenile
A. fimbria [
22].
Sebastes borealis individuals collected from western Alaska to the northern Kuril Islands consumed squids, crabs, shrimp, krill, and fish [
6]. Similarly, adult
A. fimbria from Washington and Oregon coasts and the Gulf of Alaska consumed cephalopods, crustaceans, and fish [
31,
32]. From available diet information, it is difficult to determine the trophic relationship between these two co-occurring species. Both species are categorized as opportunistic feeders, such that diet may vary by fish size, prey availability, depth of collection, and habitat [
33,
34]. Both
A. fimbria and
S. borealis are distributed sympatrically across a wide range in the North Pacific Ocean [
5,
6]. Estimates of adult diets of these species have been collected from relatively few locations, with none close to southeast Alaska. More quantitative and comparable data are needed to capture the long-term diet, ecological niche, and potential trophic interactions of adults of these two species. The dietary niche studies that have been published provide valuable, but only qualitative, information about trophic niche and potential trophic interactions between species.
To determine potential trophic interactions of co-occurring A. fimbria and S. borealis, we characterized and compared their isotopic niches using stable isotope analysis of carbon and nitrogen from two distinct habitats in southeastern Alaska marine waters. Specifically, we compared the mean position of the isotopic niche between species and locations to determine overlap and potential for competitive interactions. Secondly, we compared isotopic niche breadth between species and locations to determine the relative size of the isotopic niche between species and locations. Finally, we assessed the relationship between stable isotope ratios and body size in the sample to evaluate the effect of size variation on their isotopic niche. In essence, we tested the null hypothesis that there are no significant differences in the mean position, breadth, and overlap of the isotopic niche of A. fimbria and S. borealis between the two locations.
4. Discussion
We document strong similarity in isotopic niche position and substantial overlap between
A. fimbria and
S. borealis in the inside location compared to the coastal location. In addition, isotopic niche breadth is relatively small in both
A. fimbria and
S. borealis in the inside location. This arrangement of overlapping, but small isotopic niches is consistent with results from a previous study of rockfishes (
Sebastes spp.) in a nearby inside location [
42]. The trophic position (as indicated by δ
15N) of the deepwater
A. fimbria and
S. borealis in our study is comparable to the highest trophic position observed in the demersal rockfishes (see values for
S. ruberrimus), but the energy pathway (as indicated by δ
13C) is more depleted, by about 2‰, indicating a more pelagic source of energy compared to the demersal rockfishes in the Suchomel et al. [
42] study. Although our data are limited to only two geographical locations, variation in niche metrics between locations suggests that the competitive relationship between
A. fimbria and
S. borealis may depend on local conditions and is likely to vary throughout the sympatric range of these species.
Greater separation of the isotopic niche of
A. fimbria and
S. borealis on the δ
13C axis and greater niche breadth of
A. fimbria in the coastal location suggests less potential for resource competition in the coastal location. Why would isotopic niches and potential competitive interactions differ between inside and coastal locations? Several possibilities exist to explain this observed variation among locations. First, differences could result from variation in the available prey base between the two locations. Greater diversity of available prey or more abundant prey in the coastal location could allow both isotopic niche separation between species and greater niche breadth in
A. fimbria. Although we have no direct comparison of the diversity and abundance of prey between inside and coastal locations, the locations differ in substantial ways. The coastal location was characterized by a sloping shelf and water and nutrient flow driven by multiple coastal currents combined with winds [
43]. In contrast, the inside location was more isolated, with the currents driven by tidal movements, wind, and freshwater input [
44]. Southeastern Alaska waters experience variation in strength of upwelling which drives differences in productivity and energy availability [
45], potentially resulting in different diversity and abundance of resources among locations. Additionally, locations could differ in availability of suitable habitat and associated differences in available prey. Although these two species occur at similar depths and are often caught on the same longline or recreational fishing gear, they inhabit distinct deepwater microhabitats [
7,
8].
Anoplopoma fimbria populations are typically associated with deep, soft, and muddy flats [
9], whereas
S. borealis are most often associated with rocky slopes or structures [
10]. More research directed at prey diversity and availability among microhabitats in deep marine areas is needed to determine the validity of these suggestions.
In addition to potential differences in diversity and availability or abundance of prey resources, other factors may account for observed differences in isotopic niches between locations. Basal trophic biomass such as primary producers or detritus may differ in the level of nitrogen isotope ratios among locations [
46,
47]. Differences in basal-level isotopic ratios may cascade up the food web to create higher nitrogen isotope levels in top predators in some areas. This process may explain the consistently higher nitrogen isotopic position of both species in the inside location relative to the coastal location. The inside location may have more terrestrial-based detrital input because it is surrounded by terrestrial landscapes and may have many sources of terrestrial inputs (i.e., rivers and streams) compared to the coastal location. Although this mechanism may account for the difference in trophic level observed between locations, it does not inform the greater isotopic overlap and lower niche breadth or the potential for competition in the inside location.
Another concern is that isotopic ratios can vary through time as well as space. If this variation is random and not a function of seasonal or other environmental differences, then the observed variation could result from random variation in isotopic ratios, potentially exacerbated by smaller sample sizes in
S. borealis. Although isotopic ratios can vary through time, this variation is unlikely to be random. Several studies have demonstrated that isotopic ratios reflect environmental variation among and within locations [
47,
48]. Both species in this study are exceptionally long-lived vertebrates, and it is thus unlikely that muscle tissue in slow-growing adults exhibits rapid turnover in stable isotope ratios. Samples of both species in both locations were obtained over the same summer period in the same year; thus, even if seasonal variation in isotopic ratios occurs, it is unlikely to be an explanation for differences observed between species and locations in this study. Another potential confounding factor between locations is the difference in mean body size of samples of
S. borealis. In some species of fishes, isotopic ratios vary with body size, such that differences in isotopic ratios could result from differences in body size between samples [
49,
50]. However, this is an unlikely explanation for our observed differences. All our samples were adult specimens, and total length varied only in
S. borealis between locations. However, the relationship between total length and isotopic ratios of carbon and nitrogen was significant only in
A. fimbria and only in the inside location. Thus, there is no indication in our data that variation in body size of samples could lead to the differences observed among locations. Considering all these potential explanations for observed variation, we suggest that variation in prey diversity, availability, or abundance between locations seems to be the most likely explanation for observed differences in isotopic niche. Further studies on differences among locations in isotopic ratios observed in these two species are needed to determine the causal factors behind our observed differences.
Trophic niche breadth and overlap of niches between species as measured by stable isotope ratios may not reflect measures of trophic niche derived from dietary analysis [
51,
52]. Dietary trophic niche breadth characterizes the taxonomic diversity of prey items found in stomachs, and thus is limited to specimens with identifiable prey items (i.e., specimens with empty or unidentifiable prey in stomachs are excluded) and recently ingested prey [
53,
54]. Isotopic trophic niche measures of niche breadth and overlap reflect trophic level and energy pathway but do not reflect taxonomic variation among prey [
24,
25,
41,
55,
56,
57]. Because of the potential for prey items to differ taxonomically yet have similar isotopic signatures, our strength of inference about niche breadth and overlap between these species is limited [
53,
58]. Importantly, isotopic niche measures allow the determination of a quantifiable niche position in the overall food web that is not available from dietary trophic niche measures. Thus, these two methods measure different aspects of the trophic niche. In this study, we are confident that the isotopic niche positions relative to trophic level and energy pathway are well-representative of the trophic relations of these species. Our measures of niche breadth and overlap and inferences about potential competition may not reflect niche breadth and overlap based on taxonomic measures in dietary studies. Further studies that incorporate both dietary and isotopic analysis are required to determine how well these measures obtained from the two different methods relate. Combining these methods could provide important data about prey diversity, abundance, and composition, and substantially increase our understanding of the trophic ecology of these two species [
59].
Previous studies on the dietary niche of
A. fimbria and
S. borealis primarily focused on relative frequency of diet items and prey types, characterizing similar food resources for both species as fish, cephalopods, and crustaceans [
33,
34,
60]. In contrast, we focused on measuring trophic niche metrics by using stable isotopes rather than specific prey items or dietary sources. However, previous diet studies are consistent with isotopic niche characterizations in our study. The only other study using stable isotope analysis performed on either of our focal species was a study on diets of juvenile
A. fimbria (ages 0–1) [
22]. Juveniles were collected from a small bay off the coast of Baranof Island, Alaska, an area which is close, and most similar, to our coastal area. In this study, juvenile δ
15N mean isotopic ratios were lower than adult
A. fimbria in our study by about 1‰, whereas δ
13C mean values were more depleted than for adults in our study [
22]. The differences in δ
13C between juveniles [
22] and adults in our study may be attributed to habitat differences; juveniles in Callahan et al. were collected from depths of 25–75 m, but adults in our study were obtained from depths of 600–700 m. In addition, the absence of lipid correction for δ
13C values in the study on juveniles could also cause more depleted δ
13C values in fishes with high lipid content like
A. fimbria. Juvenile
A. fimbria exhibited a lower trophic level compared to adults (our study), suggesting a possible ontogenetic niche shift between juvenile and adult stages. Further research that includes both juvenile and adult size classes sampled from the same location is needed to provide verification and deeper understanding of changes in isotopic niche associated with ontogeny.
In rapidly changing environments, such as high-latitude marine systems, the collection of reference data provides a framework for determining the effects of future climate or demographic changes in populations [
22]. By establishing a species-specific reference for the isotopic niches of
A. fimbria and
S. borealis, future researchers can more accurately compare and predict the impact of environmental and anthropogenic factors on these species. Historically, the approach of using previously collected reference points has provided valuable context for conservation and management efforts. For instance, reference data collected over time on the abundance of blue sharks in the Mediterranean allowed for comparative analysis that estimated population declines of 97% [
61], indicating an urgency for immediate action to preserve the species. In addition, historical reference values collected on humpback whale abundance paired with recent research estimated a population decline of about 7000 individuals in just nine years [
62]. These examples, along with many others, shed light on the crucial role of quantitative reference data in informing conservation decisions and understanding ecological dynamics.
Anoplopoma fimbria and
S. borealis co-occur over large geographic ranges along the continental slope in the Northeast Pacific from southern California to Japan [
10]. Further research could potentially reveal even larger levels of variation in isotopic niches across this wide range. In addition, our results imply that the stable isotope metrics for both species could be site-specific and based on the surrounding environment. To determine if these results generalize to a broader pattern, additional data should be taken from multiple locations and across years. By incorporating data on primary production to provide basal trophic level information and including multiple locations with stable isotope values of the same species, we could create a trophic niche isoscape analogous to those using trace-level isotopes to determine movement patterns in other marine and freshwater species. Strontium isoscapes created to determine cutthroat trout (
Oncorhyncus clarkii lewisi) movements over their lifetime provide a comprehensive picture of resource use and movement [
63]. In a similar study of Pacific salmon, strontium isotope mapping revealed insights about their ecology and life histories not previously attainable due to their migratory nature [
64]. With additional reference points across time and location for
A. fimbria and
S. borealis, a trophic isoscape based on carbon and nitrogen stable isotopes could be created to better inform ongoing decisions about their conservation and management in the future.