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Jun 18, 2023

Changing environmental conditions have altered the feeding ecology of two keystone Arctic marine predators

Scientific Reports volume 13, Article number: 14056 (2023) Cite this article Metrics details Environmental change in the Arctic has impacted the composition and structure of marine food webs. Tracking

Scientific Reports volume 13, Article number: 14056 (2023) Cite this article

Metrics details

Environmental change in the Arctic has impacted the composition and structure of marine food webs. Tracking feeding ecology changes of culturally-valued Arctic char (Salvelinus alpinus) and ringed seals (Pusa hispida) can provide an indication of the ecological significance of climate change in a vulnerable region. We characterized how changes in sea ice conditions, sea surface temperature (SST), and primary productivity affected the feeding ecology of these two keystone species over a 13- and 18-year period, respectively, in northern Labrador, Canada. Arctic char fed consistently on pelagic resources (δ13C) but shifted over time to feeding at a higher trophic level (δ15N) and on more marine/offshore resources (δ34S), which correlated with decreases in chlorophyll a concentration. A reduction in Arctic char condition factor and lipid content was associated with higher trophic position. Ringed seals also shifted to feeding at a higher trophic level, but on more pelagic resources, which was associated with lower SST and higher chlorophyll a concentrations. Years with abnormally high SSTs and reduced sea ice concentrations resulted in large isotopic niche sizes for both species, suggesting abrupt change can result in more variable feeding. Changes in abundance and distribution of species long valued by the Inuit of Labrador could diminish food security.

Climate change indicators over the last few decades reveal that Arctic ecosystems are changing at an increasing rate and into an unprecedented state1,2,3,4,5,6. Warming in the Arctic is occurring at a rate nearly 4 times faster than the global average1 leading to accelerating declines in average annual sea ice concentration, extent, and thickness2. Increased air temperatures and reduced sea ice are influencing other environmental factors, including sea surface temperature and primary productivity that are leading to alterations in Arctic marine food webs and animals ranges shifting northward3,4,5. Due to these changes, the Arctic is expected to experience a species turnover five times greater than the global average6.

Arctic marine food web dynamics are largely driven by sea ice conditions that impact primary production and biogeochemical processes7,8. The timing of sea ice break-up and the subsequent spring phytoplankton blooms initiates a period of high primary productivity that drives energy transfer throughout the food web during the summer months. Mid to upper trophic level species, such as Arctic char (Salvelinus alpinus) and ringed seals (Pusa hispida), rely heavily on the production supported by these spring phytoplankton blooms for periods of intense summer feeding9,10. Changes in sea ice conditions can therefore impact the feeding behavior of species that are intrinsically dependent upon the productivity resulting from sea ice break up, including Hudson Bay ringed seals and polar bears (Ursus maritimus)11. Climate change has also allowed for the northward expansion of forage fish, such as capelin (Mallotus villosus), which, are increasingly reported in the diets of both Arctic char and ringed seal12,13 as well as arctic seabirds, such as thick-billed murres (Uria lomvia)14. The geographic range expansion of capelin has reduced beluga whale (Delphinapterus leucas) consumption of Greenland halibut (Reinhardtius hippoglossoides) in favor of capelin during the summer months15, highlighting the complex nature of food web impacts associated with the intrusion of new species.

Arctic char and ringed seals are good indicators of ecological change in the Arctic because of their circumpolar distribution, high abundance, and their sensitivity to environmental conditions16,17. These species are also key components for the dietary, economic, and cultural needs of Inuit throughout the Arctic18,19. Sea ice conditions are important to both species as ringed seals utilize spring sea ice for molting, reproduction, and raising of their pups, while anadromous, iteroparous Arctic char migrate to the marine environment following spring sea ice break up to take advantage of favorable summer feeding, returning to the same freshwater systems in late summer/early fall to spawn and overwinter20,21. Sea ice break up initiates a period of intense feeding that is critical for the condition and survival of Arctic char and ringed seals, as they integrate lipids to prepare for winter and reproduction9,10. However, mismatches in timing have resulted in altered zooplankton production in response to earlier sea ice melt and phytoplankton blooms, which affects the foraging behavior of Arctic char and ringed seals, as well as their prey22,23,24,25,26,27.

Arctic char are a diverse species that consist of populations with varying life histories and variable feeding behavior28. In the marine environment they are opportunistic feeders with adaptable diets based on available prey, such as pelagic invertebrates and fish29. Much like Arctic char, ringed seals are known to have a diverse diet consisting of fish, pelagic invertebrates, and bivalves30,31. Ringed seal diets vary throughout the Arctic based on studies using dietary tracers32,33 and shifts in their feeding ecology to more pelagic energy pathways have been linked to changing environmental conditions10,33.

Stable isotopes of carbon (δ13C) and nitrogen (δ15N) are commonly used to make inferences about a consumer’s diet in aquatic systems. Based on relative isotopic fractionation processes, δ15N can be used to quantify trophic position of an organism, as it shows an increase of approximately + 3.8‰ per trophic level in Arctic systems34. Whereas δ13C can be used to infer food web carbon sources and relative contributions of inshore/benthic versus offshore/pelagic feeding preferences35. Similar to δ13C, sulfur stable isotopes (δ34S) do not have a large increase between prey and consumer but do vary between habitat and carbon source and are particularly useful in distinguishing between marine versus freshwater resources36,37. The use of two or more stable isotopes allows for the opportunity to look at isotopic niche size, which, can provide insight into the variability in the feeding behavior of a species or population over space or time38.

Isotopic incorporation rates (i.e., turnover) vary among tissues according to their metabolic activity. For example, tissues with high incorporation rates such as liver, blood, plasma, and fat track isotopic changes in diet closely (days to weeks), whereas tissues with low incorporation rates such as muscle integrate the isotopic signature over a longer time period, tracking the diet over a period of weeks to months39. On the other hand, inert tissues (e.g., feather and claws), incorporate the dietary signal when they are synthesized40. While the majority of studies on fish and marine mammals primarily analyze isotopic ratios in muscle tissue, seal claws provide a unique opportunity to temporally quantify diet by analyzing growth annuli along the claw, where alternating light and dark annuli correspond to seasonal growth or a 4-to-8-month period41, respectively. Ringed seal claws can include up to ten years of growth bands before tips begin being worn down. Once stable isotopes have been assimilated into claw bands, they remain unchanged42.

Given the increasing pace of environmental change in the Arctic, there is a need to better understand how this will impact important indicator species43,44, as well as marine food web structure and function45. There are a broad range of species undergoing dietary shifts that reflect the environmental and ecological change occurring in the Arctic. In this study, we assessed how changes in sea ice conditions, sea surface temperature (SST), and primary productivity influenced the diet of Arctic char over a 13-year period (2006–2019) and ringed seals over an 18-year period (2002–2020) in northern Labrador, Canada. First, we characterized the temporal dietary trends in both species using a combination of δ13C, δ15N, and δ34S in Arctic char muscle and ringed seal claws. We then assessed the influence of sea ice break up, SST, and primary production (chlorophyll a) on these dietary changes over time. Finally, to determine how Arctic char health was being impacted by environmental change, we assessed whether changes in diet and environmental conditions had impacted their condition and lipid content..

Our study took place in the Labrador Sea which represents a transition zone between the Arctic and Subarctic and may provide insights regarding what will occur at higher latitudes where Arctic char and ringed seals are also present. This region is influenced by the northwestern Labrador Sea, an area under the influence of both the cold southward flowing Labrador Current and a recirculation cell of the North Atlantic and West Greenland Current46. The study area was distributed along the coast of the Labrador Inuit Settlement Area (LISA) which comprises the majority of Labrador’s North Coast (Fig. 1) and is a region that is heavily utilized by the Inuit for hunting and fishing practices.

Map of study locations, where Arctic char (Nain) and ringed seals (Nain, Okak Bay, and Saglek fjord) were collected and the location of the Labrador Inuit Settlement Area (LISA), LISA marine zone, and Torngat Mountains National Park. WGC is the West Greenland Current and LC is the Labrador Current. Home ranges for Arctic char and ringed seals are shown and are as described in65 and66, respectively. The map was produced using QGIS 3.16.3 Hanover.

There were no differences in length (p = 0.83), weight (p = 0.61), δ13C (p = 0.49), or δ15N (p = 0.09) between male and female Arctic char. Condition factor and δ34S differed between males and females, however these results were influenced by 2014 and 2016 when only female char were collected. When 2014 and 2016 were removed, condition factor (p = 0.09; t-test) did not differ by sex, whereas δ34S in females (17.0 ± 0.1 ‰) (mean ± 1 SE) was higher than in males (16.8 ± 0.04 ‰) (t-test, p = 0.04). However, when analyzing individual years, δ34S did not differ between males and females. Based on these results, male and female Arctic char were grouped together prior to further analysis. Arctic char fork length and round weight varied by year (ANOVA, both p < 0.0001) with 2006 having the smallest fork lengths (342 ± 21 mm) and round weights (463 ± 91 g), and 2010 having the largest lengths (527 ± 45 mm) and weights (2157 ± 574 g) (Table 1). No relationship was found among the three stable isotopes (δ13C, δ15N, and δ34S) and age or body size for Arctic char (linear regression, p > 0.05).

No differences were found between ringed seal sample location and δ13C (p > 0.05) or δ15N (p > 0.05), thus locations were grouped together. Ringed seal sex did not have a significant influence on stable isotopes (δ13C or δ15N, p > 0.05) thus males and females were grouped together. No relationship was observed between seal age and δ13C (p = 0.34), but there was a positive relationship between age and δ15N (p = 0.003, R2 = 0.03), so all δ15N were age adjusted.

Arctic char isotopic niche volume varied by year (ANOVA, p < 0.0001) (Table 1). Of note, Arctic char isotopic niche volume was higher in 2009 and 2010 with respective sizes of 74.1‰3 and 94.3‰3, compared to all other years (mean = 3.7 ± 2.2‰3) (Fig. 2A). Ringed seal isotopic niche area varied by year (ANOVA, p < 0.0001) from a minimum in 2002 of 0.22‰2 to a maximum of 1.91‰2 ± 0.48 in 2007 (Table 2, Fig. 2B).

Arctic char isotopic niche volume varied across years with 2009 and 2010 having noteably larger niche volumes compared to other years (A). Ringed seal isotopic niche area varied across years (B).

No differences (t-test, p = 0.66) were found in baseline isotopic values for δ15N between 2010 and 2020, therefore no corrections were made to δ15N. We found no temporal trend in Arctic char δ13C (linear regression, p = 0.87) or isotopic niche volume (linear regression, p = 0.30), but δ15N and δ34S increased with year (p < 0.0001, R2 = 0.18; p < 0.0001, R2 = 0.41, respectively) (Fig. 3). Arctic char condition factor and percent lipid had a negative relationship with year (p < 0.0001, R2 = 0.19 and p = 0.02, R2 = 0.02, respectively). Ringed seal δ13C values decreased over time (p < 0.0001, R2 = 0.21) and δ15N had increased over time (p = 0.02, R2 = 0.02), whereas isotopic niche area had no temporal trends (p = 0.69) (Fig. 4). Ringed seal condition factor was greater in 2019 (84.5 ± 0.8) than in 2008 (75.1 ± 1.2).

There was no temporal trend in δ13C (A) but increasing trends in δ15N (p < 0.0001; R2 = 0.18) (B) and δ34S (p < 0.0001; R2 = 0.41) (C) were evident in Arctic char muscle from Nain, Labrador, Canada over time (2006 to 2019).

Stable isotope profiles in ringed seals harvested along the Labrador coast revealed that (A) δ13C decreased (p < 0.0001; R2 = 0.21) and (B) δ15N increased (p = 0.02; R2 = 0.02) between 2002 and 2020, indicating that seals have shifted to feeding more pelagically and at a higher trophic position over the study period.

Environmental variables within Arctic char and ringed seal home ranges are summarized in Tables 3 and 4, respectively. Within the home range of Arctic char there was an increase in seasonal loss of ice period (SLIP) and a decrease in chlorophyll a concentrations that were correlated with Arctic char δ15N values over the study period (Table 5). We found a negative relationship between Arctic char δ15N values and chlorophyll a concentration (p < 0.0001, R2 = 0.11), whereas we found a positive relationship with Arctic char δ15N values and SLIP (p < 0.0001, R2 = 0.21) (Fig. 5). Additionally, we found a negative relationship between δ15N and condition factor (p < 0.0001, R2 = 0.11) and δ15N and percent lipid (p = 0.04, R2 = 0.02) (Fig. 5).

Influence of environmental conditions on Arctic char δ15N (A,B) and influence of Arctic char δ15N on condition factor and percent lipid (C,D) in Nain, Labrador, Canada. Lower δ15N in Arctic char was associated with higher chlorophyll a (Chl-a) concentrations (mg/m3) (A). Higher δ15N in Arctic char was associated with a longer Seasonal Loss of Ice Period (SLIP) (B). Lower condition factor (C) and percent lipid (D) in Arctic char was associated with higher δ15N.

Within ringed seal home range we observed an increase in chlorophyll a concentrations (p < 0.0001, R2 = 0.29) and a decrease in SST (p < 0.0001, R2 = 0.16) over the 19 year study period that were correlated with ringed seal δ13C values (Table 6, Fig. 6A). Additionally, we found that chlorophyll a concentration decreased with increasing SST (p < 0.0001, R2 = 0.27, Fig. 6B).

Rising chlorophyll a (Chl-a) concentrations (green) and decreasing summer sea surface temperatures (SST, blue) measured within northern Labrador ringed seal home ranges from 2002 to 2020 (A). A decrease in Chl-a concentrations was found in years with greater SST (B). Ringed seals fed more pelagically (δ13C) with lower SST and higher Chl-a concentrations (C,D).

We observed a positive relationship between ringed seal δ13C values and SST (p = 0.01, R2 = 0.02, Fig. 6C), whereas we observed a negative relationship between δ13C values and chlorophyll a concentration (p = 0.0005, R2 = 0.05, Fig. 6D). We found no relationship between ringed seal isotopic niche area and any of the environmental variables.

Temporal trends of stable isotopes in Arctic char and ringed seals indicate that these two Arctic predators have undergone shifts in diet over the past two decades along the Labrador coast of Canada, which were related to changes in environmental conditions, particularly sea ice, sea surface temperature, and primary productivity. Carbon sources, based on δ13C, have become more pelagic/offshore in ringed seals, which likely reflects increasing seasonal open water primary productivity and is consistent with studies on this species from other areas of the Canadian Arctic9,50. No change in carbon sources based on δ13C in Arctic char were found, suggesting a continued reliance on prey with similar δ13C. Marine resources, based on δ34S, have increased in Arctic char. This increase likely reflects a combination of dietary choices, with an increase in capelin consumption as their abundance has increased51, and greater time spent in the marine environment associated with longer open water periods. These findings are consistent with recent studies on Arctic char in Cumberland Sound48. Both species showed increasing δ15N over time, suggesting feeding at a higher trophic position that could reflect greater consumption of forage fish, particularly capelin, whose populations have expanded northward. An extreme year for poor sea ice conditions because of variable ice coverage and abnormally high SSTs in 2010 resulted in large variability in stable isotopes in both species and values of isotopic niche volume in Arctic char that was orders of magnitude greater than the yearly mean value reflecting the dietary plasticity of both species. Despite this highly variable feeding behavior in 2010, the condition factor of Arctic char sampled was the highest of all years sampled.

While there were no temporal trends in Arctic char δ13C, there was variability between years and a significant shift to more pelagic resources (lower δ13C) in 2009 and 2010, when there was an abnormally long period of open water, poor ice conditions and high summer SSTs. The lack of a temporal trend in carbon source for the Arctic char may reflect a strong tie to feeding on pelagic forage fish [e.g., capelin, sand lance (Ammodytes spp.)] and zooplankton and little use of benthic resources10,51. Further, changes in water column primary productivity associated with ice changes may not have been large enough over the study period to significantly alter temporal trends in Arctic char carbon sources. Within Arctic marine food webs, there has been more pelagic feeding because of greater productivity compared to benthic regions52. This increase in primary productivity may help support large amounts of pelagic zooplankton that provide feeding opportunities to Arctic char. The large shift to more pelagic resources in 2010 suggests that continued reduction in sea ice could shift carbon sources for Arctic char, and potentially for other species consuming pelagic prey9,52. Such a large change in Arctic char isotopes for a single year does suggest an ability for this species to adapt their diet in the face of large environmental change. While Arctic char can dramatically change their feeding behavior for a given year, this does not necessarily mean that these changes are sustainable for Arctic char over a more extended period of time.

Labrador coast ringed seals shifted to a more pelagic diet over the past 18 years, based on decreasing trends in δ13C between 2002 and 2020, consistent with populations in other areas of the Arctic, including Hudson Bay and the Beaufort Sea9,50. Chlorophyll a concentration and SST were environmental drivers of δ13C in ringed seals. Both these environmental variables had a temporal trend over the study period. Increased chlorophyll a concentrations support a stronger phytoplankton carbon pathway53, explaining the shift in ringed seal feeding to more pelagic prey. Lower summer SSTs that occurred over the study period, possibly influenced by influxes of cold meltwater from the Arctic54, allow for greater phytoplankton abundance and grazing by Calanus sp.55 supporting more pelagic feeding by ringed seals. This phytoplankton carbon pathway includes forage fish, such as capelin and sand lance11, that are high in nutritional content and are proving to be an important component of ringed seal diets33,56.

Increasing δ15N in both Arctic char and ringed seals indicates that these species are feeding at higher trophic positions over the study period. This likely reflects an increase in forage fish consumption, namely capelin, that have become more abundant in the Arctic as it has warmed48,57. However, others found that δ15N did not increase in Arctic char in Cumberland Sound, despite capelin becoming a significant component of their diet48. Capelin abundance is largely driven by bottom-up regulation and is heavily influenced by sea ice conditions and primary productivity58. The capelin abundance along the Labrador coast has been increasing since the crash in the early 1990’s, and long-term commercial catches indicate that char habitat use and diet near Nain is varying annually in relation to capelin availability51. Arctic char have been shifting to a more piscivorous diet along the Labrador coast, driving this increase in trophic position, as forage fish occupy a higher trophic position than marine invertebrates10. Arctic char trophic position in this study was also higher in years with low chlorophyll a concentrations and when it takes longer for sea ice to completely break up. No temporal trends in the trophic position of ringed seals were observed in Greenland or Hudson Bay, although, consistent with our findings these studies found that higher ringed seal trophic position was associated with greater occurrence of capelin in diet21,59. Additional research is needed to better understand the relationship between δ15N and trophic position of Arctic char and ringed seals in Labrador, and piscivorous fish and marine mammals in general in a changing Arctic food web.

The use of marine resources has increased over the time of this study in Arctic char, reflected in increasing δ34S, indicating longer feeding periods and greater resource use in marine areas. Arctic char utilized more marine resources when the sea ice break up period (SLIP) took longer. These variable sea ice break up conditions may influence char to either enter the marine environment earlier and/or spend more time offshore. There was also a strong correlation between Arctic char δ15N and δ34S, which suggests that this shift to more marine resources is also associated with feeding at a higher trophic position. There is evidence that as Arctic char in northern Labrador feed more offshore, they consume more capelin51, which may result in higher δ15N and δ34S in their tissues. There has been limited use of δ34S in studies of Arctic char, but as demonstrated here, it can be useful in characterizing complex feeding behaviors of this anadromous species.

While, Arctic char isotopic niche size did not have a temporal trend, it was significantly larger in 2009 and 2010 compared to the other years. This large isotopic niche volume reflects the ability of individual Arctic char to adapt their diet within a year, reflecting their dietary plasticity as well as capability to adjust to abnormal environmental conditions. Similar to Arctic char, ringed seals had a larger isotopic niche area in 2010, where it was the second largest amongst all years. These findings suggest that there may have been ecosystem wide changes in the food web during this poor ice year with higher SST compared to other years. Despite there being changes in ringed seal isotopic niche area for this particular year, there were no temporal trends over our entire study period, which is consistent with the absence of temporal trends of isotopic niche area for ringed seals in Hudson Bay9.

The condition and lipid content of Arctic char decreased over the 13-year sampling period. These trends were commensurate with environmental conditions and the feeding behavior of Arctic char. Arctic char δ15N decreased with increasing chlorophyll a concentration and increased with SLIP. There was a negative relationship between SLIP and chlorophyll a concentration, possibly explained by intermittent ice coverage and limited light availability resulting in weak phytoplankton blooms. With a weak phytoplankton bloom, there is less food for pelagic invertebrates which may lead to Arctic char feeding on higher trophic level species, as well as an overall lower amount of prey biomass available with feeding higher in the food web. The shift in Arctic char feeding on higher trophic level species was connected to declines in condition factor and lipid content (Fig. 5). This reduction in char condition may also reflect reduced nearshore abundance or quality of preferred prey, leading to an increased energy expenditure to access offshore food resources. As there is a positive relationship between Arctic char δ15N and δ34S, there is a possibility that Arctic char have to travel further for their prey, exerting more energy traveling away from their freshwater habitat and into the marine environment.

Dietary shifts in Labrador Arctic char and ringed seals may be expected as climate change introduces new species into more northern regions with corresponding changes in competitive and predatory interactions altering food web structure60. Capelin moving in from the south have been shown to alter the predative interactions of beluga whales on Greenland halibut, with beluga whales shifting their feeding to capelin during the summer months13. An increase in trophic position for both species and a shift to more pelagic feeding by ringed seals, Closer to the carbon signatures that are found in Arctic char, could result in these two species competing more for food resources in the future. As both Arctic char and ringed seals shift to feeding at a higher trophic position, this may lead to increased concentrations of biomagnifying contaminants, such as mercury (Hg) and polychlorinated biphenyls (PCBs) over time61.

Climate warming and associated changes in ice and marine productivity within the Arctic may result in a shift in marine food webs and the invasion of subarctic species such as Atlantic salmon (Salmo salar)43,62. Our study provides evidence that both Arctic char and ringed seals have altered their feeding ecology over a 13- and 18-year period, respectively, in response to interannual variability in environmental conditions associated with climate warming. The parallel (i.e., δ15N trends) and contrasting (i.e., δ13C trends) changes observed across both species exemplify how species vary in their response to environmental change, which may have significant implications for shifts in competition/predation in Arctic marine food webs. These findings emphasize the importance of continued monitoring of stable isotope profiles in these valued and circumpolar species, as well as the need to improve our understanding of what is driving these shifts, particularly potential changes at lower trophic levels.

All samples were collected from subsistence-harvested anadromous Arctic char and ringed seals. Arctic char (n = 214, Table 1) were collected from around Nain from August–September (2006–2010 and 2013–2019, 12 years of data spanning 13 years) before they migrate back to freshwater to overwinter. Ringed seals (n = 53, Table 2) were harvested from three marine inlets in northern Labrador (Nachvak, Okak, and Saglek; 2008–2011 and 2019–2020) from September–October (Fig. 1). The 2008–2011 and 2019–2020 ringed seal claws provided a record from 2002–2011 and 2009–2020, respectively, which spanned an 18-year period.

Arctic char fork length (mm), round weight (g), and sex were recorded, muscle was taken near the dorsal fin and frozen until analysis. Otoliths were extracted for aging and analyzed by AAE Tech Services (La Salle, Manitoba, Canada). Following harvesting, ringed seal total length and girth were recorded, and the lower jaw and left fore flipper was extracted. Teeth were aged at Matson's Laboratory, USA, by longitudinally thin sectioning a lower canine tooth and counting annual growth layers in the cementum using a compound microscope and transmitted light. Flippers were frozen at −20 °C before having the digit I claw extracted for stable isotope analysis.

Dorsal muscle tissue from Arctic char was freeze dried at −48 °C and 133 × 103 mbar for 48 h. Dried muscle was crushed into a fine powder using surgical scissors and 400–600 µg of muscle tissue was weighed into tin capsules. Only adult ringed seals (≥ 6 years old) were used as they are known to undergo an ontogenetic shift in diet when they reach sexual maturity18,63. Claws from the first digit of the left fore flipper were removed using a scalpel for stable isotope analysis. The claw was detached from the bone by placing it in a water bath at 60 °C, cleaned using ethanol, and stored in deionized water42. Ringed seal claws can include up to 10 years of growth bands. Individual light and dark claw bands were cut using a surgical scalpel and 400–1000 µg of claw bands were weighed into tin capsules. Tin capsules with Arctic char muscle and ringed seal claw bands were analyzed for δ13C and δ15N by Delta V Thermoscientific Continuous Flow Mass Spectrometer (Thermo Scientific, Bremen, Germany) coupled to a 4010 Elemental Combustion System (Costech Instruments, Valencia, CA, USA). Muscle and nail band tissue was also weighed (5500–6000 µg) for δ34S into capsules and analyzed on a Delta V Plus Thermoscientific Continuous Flow Mass Spectrometer (Thermo Scientific, Bremen, Germany) coupled to a 4010 Elemental Combustion System. Isotopic ratios were reported as:

where, X is either 13C, 15N or 34S, R is the ratio 13C/12C, 15N/14N or 34S/32S, and the standards used were C from Vienna Peedee Belemnite (VPDB), N from atmospheric, or S from the Canyon Diablo troilite (CDT). The analytical precision [standard deviation (SD)] for NIST standard 1577c (bovine liver), an internal laboratory standard (tilapia muscle), USGS 40 and Urea (n = 50 for all) for δ13C and δ15N were < 0.20‰. The analytical precision for δ34S values from NIST 1577c, an internal laboratory standard, USGS 42, NIST 8555 and NIST 8529 (n = 118 for all) was < 0.25‰. The accuracy based on the certified USGS 40 sample (n = 50) showed a difference of 0.13 and -0.02‰ of the mean calculated values for δ13C and δ15N, respectively. NIST standards 8573, 8547, and 8574 for δ15N and 8542, 8573, 8574 for δ13C (n = 10 for all) were used to check the accuracy of the stable isotope analyses. The mean difference from the certified values were –0.09, 0.14, −0.06‰ for δ15N and 0.09, 0.01, and −0.08‰ for δ13C respectively. For δ34S, the accuracy using USGS 42 (n = 118) was within 0.12‰ of the mean calculated value.

Arctic char lipid percentage was determined on dried muscle tissue by performing a series of lipid extractions using a 2:1 mixture of chloroform: methanol using methods outlined in Bligh and Dyer64.

Environmental data were extracted in a Geotiff format within Arctic char and ringed seals home ranges as described in65 and66, respectively (Fig. 1) using QGIS (version 3.30.3, QGIS Development Team)67. Environmental data was extracted for 2006–2010 and 2013–2019 within the Arctic char home range and 2002–2020 within the ringed seal home ranges. The area used for Arctic char was based on migratory distribution, which is within 100 km of the catch location and proximity of their resident rivers 65, whereas for ringed seals the area was 196,886 km2 and was based on the minimal convex polygons of 95% of their space use 66.

Daily sea ice concentration (SIC), collected remotely from satellites, were acquired from the Sea Ice Index database at the National Snow and Ice Data Center website (https://nsidc.org/data/explore-data) at a 25 km × 25 km resolution and were used to determine the date of sea ice break up. Arctic sea ice is highly variable between years and dates can be selected to summarize sea ice retreat by using sea ice concentration68. We utilized a number of variables to characterize spring sea ice break up across species home ranges, including: day of opening (DOO), the last day SIC drops below 80% within the 25 km × 25 km pixel; day of retreat (DOR), the last day SIC drops below 15%; and, seasonal loss of ice period (SLIP), which is the number of days between DOO and DOR. Break up date was determined when 50% of the sampling points within the home range for ringed seals and Arctic char dropped below a variable’s defined SIC percentage.

Weekly chlorophyll a concentration (mg/m3) collected from AQUA/MODIS satellites from 2002 to 2020 was retrieved from the Nasa Earth Observations website at a 0.25° resolution. Some cells did not have chlorophyll a concentrations for a given week because of interference from cloud cover or sea ice. Since it was not possible to differentiate between cloud cover and sea ice for cells with no data, extrapolation was not attempted. Instead, mean chlorophyll a concentration was calculated based on the available data for that given week and was accepted for analysis if greater than 50% of the sampling points had data and was a week that followed sea ice break up. Weeks that had less than 50% sampling points with data were excluded as to not incur bias based on a limited number of sampling points with data. The week with the maximum chlorophyll a concentration was chosen to represent when the peak phytoplankton bloom occurred as this triggers periods of intense summer feeding.

Monthly SST (C) collected from AQUA/MODIS satellites from 2002 to 2020 was retrieved from the Nasa Earth Observations website at a 0.25° resolution to analyze summer SST following sea ice break-up. The data format was similar to the chlorophyll a data but at a monthly temporal resolution and extracted in the same manner as sea ice using QGIS. Mean summer SST was calculated using July, August, and September months as they are months with open water. The influence that summer SST has on feeding ecology of Arctic char and ringed seals was assessed during this period as this is when significant feeding takes place.

Statistical analyses were performed using RStudio (version 4.1.1, R Core Team 2021)69. Sex, age, fork length, round weight, and Fulton’s condition factor (based on fork length and weight using (K = 100 × weight/length3)47 of Arctic char were analyzed to determine which variables needed to be accounted for prior to temporal and environmental trend analysis of stable isotopes. The influence of sex on length, weight, condition factor, and stable isotopes (δ13C, δ15N, or δ34S) was assessed using two-sample t-tests. The influence of age on stable isotopes (δ13C, δ15N, or δ34S) was assessed by a one-way ANOVA, followed by Tukey tests to identify ages that differed. The influence of year on fork length and round weight of Arctic char was assessed by a one-way ANOVA, followed by Tukey tests to identify years that differed. As fish size varied by year, this highlighted the importance to assess the possible trends with size and δ13C, δ15N, and δ34S for each year using linear regression.

Location, sex, and age of ringed seals were analyzed to determine what factors needed to be accounted for prior to temporal and environmental trend analysis of δ13C and δ15N. The influence of location on stable isotopes (δ13C or δ15N) was assessed using one-way ANOVA. The influence of sex on stable isotopes (δ13C or δ15N) was assessed using two-sample t-tests. The influence of ringed seal age, as determined by the annuli along the claw, on stable isotopes (δ13C or δ15N) was assessed using linear regression. An age correction for ringed seal δ15N was required to standardize across ages as this stable isotope increased linearly with age, where:

where m is the slope of the relationship between age and δ15N.

No temporal trends (2002–2011) and little to no variability between years was observed for δ34S in the claws of ringed seals collected from 2008 to 2011, which is consistent with their predominant marine distribution and marine foraging behaviour18, therefore, claws collected in 2019–2020 were not analyzed for δ34S. Ringed seal condition was only determined for 2008 and 2019 by ((maximum girth (cm)/total length (cm)) × 100)18, as seals were not collected in most other years. Ringed seal condition between 2008 and 2019 was assessed using two-sample t-tests as these were the years when the majority of ringed seals were sampled (n = 13; n = 14). The influence of age on condition factor was also assessed for both years using linear regression and no trends (p > 0.05) were found.

The R package NicheROVER49 is capable of calculating an isotopic niche region beyond two dimensions and was used to calculate the isotopic niche volume of Arctic char using δ13C, δ15N and δ34S. The niche region is defined as the 95% probability region in multivariate space49. The influence of year on isotopic niche volume of Arctic char was assessed by a one-way ANOVA. Ringed seal isotopic niche area was calculated using δ13C and δ15N with Stable Isotope Bayesian Ellipses in R (SIBER)38 to calculate the standard ellipse area at a 95% probability using two stable isotopes, as δ34S did not vary between years for ringed seals. The influence of year on isotopic niche volume of ringed seals was assessed by a one-way ANOVA. As there were three stable isotopes used for Arctic char and two for ringed seals, isotopic niche size will be differentiated by volume and area for the respective species.

Calanus copepods from 2010 and 2020 were analyzed for δ15N to test for shifts in baseline isotopic values over time and assessed using two sample t-test. Relationships were assessed between δ13C, δ15N, δ34S, condition factor, percent lipid, and isotopic niche volume with year for Arctic char using linear regression. Relationships between δ13C, age corrected δ15N, and isotopic niche area with year for ringed seals was assessed using linear regression. Ringed seal condition was only determined for 2008 and 2019 by ((maximum girth (cm)/total length (cm)) × 100)18, as seals were not collected in most other years. Ringed seal condition between 2008 and 2019 was assessed using two-sample t-tests as these were the years when the majority of ringed seals were sampled (n = 13; n = 14).

Linear regression was used to examine relationships between environmental parameters (DOO, DOR, SLIP, SST, and chlorophyll a concentration) and Arctic char stable isotopes (δ13C, δ15N, δ34S), isotopic niche volume, condition factor, and percent lipid. Similarly, linear regression was used to examine the relationship between environmental parameters (DOO, DOR, SLIP, SST, and chlorophyll a concentration) and ringed seal stable isotopes (δ13C and age-adjusted δ15N) and isotopic niche area. Linear regression plots were developed to display significant relationships between environmental explanatory variables and both Arctic char and ringed seal biological response variables.

The datasets used and/or analysed during the current study are available from the corresponding author on reasonable request.

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Financial support was generously provided by the Northern Contaminants Program (NCP) through Crown-Indigenous Relations and Northern Affairs Canada (Project: ArcticNet Nunatsiavut Nuluak and Fine-scale temporal changes in mercury accumulation in Labrador ringed seals (Pusa hispida) using laser ablation technology on whiskers and claws: influence of a changing ice regime), the ArcticNet Canadian Network of Centres of Excellence, ArcticNet (Project: Towards a marine management plan for Nunatsiavut: Coastal ecosystem research in support of priority concerns of Inuit), Fisheries and Oceans Canada, Canada Research Chair program, and the University of Windsor. Thank you to the many people who assisted with field work, laboratory work and manuscript and grant writing including, Paul McCarney, Amber Gleason, Dr. Max Liboiron, Dr. Jody Spence, Katelynn Johnson, Lydia Paulic, Mitchell Hoyle, Carys Gallilee and Katerina Colbourne. We would like to express our sincere thanks to the crew of M.V. Whats Happening and to the community members of Nain, Nunatsiavut who have made this project possible.

School of the Environment, University of Windsor, Windsor, ON, Canada

Matthew A. Anderson, Aaron T. Fisk & Tanya M. Brown

Nunatsiavut Government, Nain, NL, Canada

Rodd Laing & Liz Pijogge

Ocean Wise, Vancouver, BC, Canada

Marie Noël

Putjotik Fisheries, Nain, NL, Canada

Joey Angnatok

Environment and Climate Change Canada, Burlington, ON, Canada

Jane Kirk

Environment and Climate Change Canada, Saskatoon, SK, Canada

Marlene Evans

Fisheries and Oceans Canada, West Vancouver, BC, Canada

Tanya M. Brown

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T.B., A.F., M.A., and M.N. designed the study. M.A., T.B., and A.F. drafted the main manuscript text. M.A. conducted laboratory work. M.A. generated figures and performed all data analyses. T.B., A.F., M.A., M.N., M.E., and R.L acquired funds. T.B., L.P., J.A., R.L., J.K., and M.E. obtained the samples for analysis. All authors were involved in the interpretation of results and writing and or editing the manuscript.

Correspondence to Tanya M. Brown.

The authors declare no competing interests.

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Anderson, M.A., Fisk, A.T., Laing, R. et al. Changing environmental conditions have altered the feeding ecology of two keystone Arctic marine predators. Sci Rep 13, 14056 (2023). https://doi.org/10.1038/s41598-023-39091-9

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Received: 25 January 2023

Accepted: 20 July 2023

Published: 28 August 2023

DOI: https://doi.org/10.1038/s41598-023-39091-9

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