Capelin (Mallotus villosus) is an important trophic node in many Arctic and sub-Arctic ecosystems. In Godthåbsfjord, West Greenland, the zooplankton community has been shown to change significantly from the inner part of the fjord, which is impacted by several glaciers to the shelf outside the fjord. To what extent this gradient in zooplankton composition influences capelin diet during their summer feeding in the fjord is yet unknown. To investigate this, we analysed stomach content of capelin (8–14 cm) sampled using a pelagic trawl at three stations in outer (GF3), mid (GF7) and inner (GF10) part of Godthåbsfjord in May and August 2013. In May, the copepod nauplii numerically dominated the diets, but euphausiids contributed > 92% by carbon mass at all stations. In August, calanoid copepods were the most important prey numerically and by carbon mass. Smaller copepod species became more important towards the inner stations, whereas the large Calanus species dominated in the outer stations. There was also a trend in decreasing stomach carbon content towards the inner stations, and on the individual level, variation in stomach content was strongly negatively related to the proportion of small copepods in the diet. This suggests that the inclusion of small copepods in the diet cannot compensate for the absence of larger euphausiids and copepods. Therefore, any change in the ecosystems that favours these at the expense of larger zooplankton and euphausiids is likely to impact capelin feeding negatively with consequences for the whole ecosystem.
Warming of the Arctic region, including Greenland, has resulted in increasing freshwater run-off into the coastal marine environment (Bamber et al. 2012; Sejr et al. 2017). This input of freshwater greatly influences the marine physical environment (Mortensen et al. 2013), and contributes to distinct gradients in primary production, zooplankton composition and higher trophic levels (Arendt et al. 2010; Arimitsu et al. 2016; Calbet et al. 2011; Meire et al. 2016).
Capelin (Mallotus villosus Müller) is a small planktivorous fish of the Osmeridae family with a circumpolar distribution in the northern hemisphere, however, recent research suggest that capelin in the Pacific ocean is another species (Mecklenburg et al. 2018). It is an important part of many high latitude marine ecosystems as the pivotal point in wasp-waist ecosystems (Cury et al. 2000; Hop and Gjøsæter 2013). Their high abundance in many ecosystems enables them to exert an intense predation pressure on zooplankton (Hassel et al. 1991), thereby converting zooplankton biomass into fish biomass. Capelin themselves are in turn an extremely important prey resource for both marine mammals and fish (Vilhjalmsson 2002) and consequently play an important role in transferring energy from lower to higher trophic levels.
The west-Greenland capelin is distributed from the southern tip of Greenland, 59°N–72°N, inhabiting both fjords and near shore shelf areas. Despite its continuous distribution, it has been suggested that there may be separate populations in the area (Bergstrøm and Vilhjálmsson 2008). There are no present reliable population size estimates, but a ubiquitous presence all along west Greenland and high local densities (Bergstrøm and Vilhjálmsson 2008) suggests that it has the same ecological role and importance as in other Atlantic ecosystems. This is also supported by studies on capelin (Hedeholm et al. 2010, 2012) and predators that rely on capelin (Friis-Rødel and Kanneworff 2002).
The nutritional value of wasp-waist species such as capelin has been shown to depend on the composition of their diet, which shows considerable spatial and temporal variation that reflects the availability of zooplankton species (Hedeholm et al. 2012; Orlova et al. 2002). The quality of zooplankton as prey in terms of energy density and total energy content differs between species, typically with smaller copepod species having less accumulated lipid per weight unit than larger ones (Kattner and Hagen 2009). Capelin energy content, as expressed in their growth, condition and energy density, appears to be linked to these prey quality differences (Hedeholm et al. 2011) and reflect prey abundance (Gjøsæter et al. 2002). The effects of zooplankton abundance and quality changes on capelin condition can propagate to apex predators through reduced foraging gain of capelin predators [i.e. the Junk Food Hypothesis, Österblom et al. (2006)]. This has been shown in particular for the major capelin predator, Atlantic cod (Gadus morhua L.) (Sherwood et al. 2007) but also in marine birds that depend on capelin to supply their chicks with sufficient energy (Davoren and Montevecchi 2003).
Freshwater driven gradients are prominent in the zooplankton community in the Godthåbsfjord, SW Greenland (64°N). Here smaller copepods species (e.g. Microsetella spp., Oithona spp., Pseudocalanus spp.) dominate in the inner part of the fjords, most strongly impacted by glacial meltwater, but are replaced by larger species, primarily Calanus spp., towards the mouth of the fjord and on the shelf (Arendt et al. 2010; Tang et al. 2011). Similarly, krill shows a clear shift in species composition and abundance from the freshwater-influenced inner parts towards the ocean (Agersted and Nielsen 2014). Biomass of krill, especially Thysanoessa raschii and Meganyctiphanes norvegica, peaks in the central and inner parts of the fjord exceeding the biomass of copepods. Tang et al. (2011) linked the metazooplankton communities to specific water masses in the fjord suggesting that changes in the extent and distribution of these water masses will affect the abundance and distribution of zooplankton in the fjord. Moreover, for M. norvegica, where no fertilised females are found in the fjord, it is suggested that the fjord population is maintained by freshwater driven advection of individuals from the shelf area (Agersted and Nielsen 2014). The relationship between freshwater input and species composition implies that continued warming of the region both directly and through accelerated melting of the Greenland Ice Sheet can alter the zooplankton community (Agersted and Nielsen 2014; Arimitsu et al. 2016).
In this study, we examine the diet of capelin along a transect from the inner part of Godthåbsfjord to the mouth of the fjord to investigate whether the observed gradients in freshwater input and the zooplankton community is reflected in the diet of zooplanktivorous fish inhabiting glacier influenced Arctic fjords. We discuss the potential impact of climate change on the zooplankton community and the energy intake and condition of capelin, and consequently the transfer of energy to the highest trophic levels in the Godthåbsfjord.
Materials and methods
Study site and sampling
The Godthåbsfjord system covers a surface area of 2013 km2 and has an average depth of ~250 m with several sills located near the entrance to the fjord (Fig. 1) (Mortensen et al. 2011). Based on hydrographic observations Godthåbsfjord has previously been divided into two regional domains: the outer sill region and the main fjord basin (Mortensen et al. 2011). Figure 2 shows a length transect of the temperature and salinity from the mouth of the fjord to the inner part of the fjord close to the glaciers obtained during this study using SBE19plus CTD profiler. In May, salinities in the upper 250 m in the fjord were high with only limited stratification as freshwater input to the inner part is low at this time due to limited snow- and ice melt. The outer part of the fjord (the outer sill region, GF1–GF4) is characterised by strong tidal mixing leading to uniform salinity and temperatures throughout the water column. During August, the fjord is strongly impacted by large input of glacial meltwater creating a strongly stratified system. The impact is most pronounced in the inner fjord stations (GF9–GF12), where salinity drops to ∼10 psu in the upper 5–10 m. Towards the mouth of the fjord, the stratification gradually weakens due to intense tidal mixing and fjord geometry where water must pass through a < 5 km narrow entrance.
Capelin were sampled in Godthåbsfjord on 5–12 May and 19–23 August 2013 from RV “Sanna” operated by Greenland Institute of Natural Resources. Samples were obtained from 30 min pelagic trawl (5-mm cod end) hauls at 3–4 nm h−1 conducted between 11 a.m. and 6 p.m. at three locations in the fjord. GF3 (64°07N, 51°53W) is located in the outer sill region at the mouth of the fjord; GF7 (64°25.5N, 51°30.6W) is in the middle part of the fjord and GF10 (64°36.6N 50°57.5W) is localised in the main basin of the fjord at the entrance to the inner fjord branch and is influenced by the tidal outlet glacier (Fig. 1). The distance between GF3 and GF10 was approximately 75 km. The trawling depth was determined by the depth distribution of the capelin as observed on the echo sounder and varied between 80 and 120 m.
Immediately after sampling the size distribution at each location (total length, 2-cm intervals) was determined from all sampled capelin or a subsample of at least 100 individuals. Stomachs and guts from a random subsample of approximately 15 fish per cm size interval were dissected out and stored in formaldehyde (6%) saltwater. Stomachs from each size interval were preserved together.
The stomachs were rinsed in water and examined under a stereomicroscope. Food items in the intestine were not included in the analysis as they were highly digested. Stomach contents were identified to the lowest possible taxonomic level, but was often restricted to class or order due to digestion. Prey body lengths were measured from calibrated pictures for all prey groups except copepods, where prosome length was measured, and then converted to live body carbon content based on published equations (Table 1).
Prey items were grouped in major categories Amphipods, Euphausiids, Calanus spp., other copepods, Nauplii, Copepod eggs, etc. The copepods were further divided into Calanus finmarchicus, Calanus glacialis, Calanus hyperboreus, Calanus sp., Pseudocalanus sp., Metridia lucens, Metridia longa, Microcalanus pusillus and Unknown.
The similarity in diet composition between stations, months and capelin size groups was visualised using hierarchical clustering based on Brey–Curtis similarity square root transformed mass proportions of major prey categories as well as separately on individual copepod species in order to examine the impact of the spatial structure of the copepod community on capelin diet. Discriminant analysis (SIMPER) was performed on carbon mass to determine what prey items were responsible for the dissimilarity between stations. The analyses were performed using PRIMER v. 5 (Clark and Warwick 2001).
Two-way ANOVA followed by Tukey HSD post-hoc test was used to test for differences in mean capelin size among stations and months. Differences in median stomach content between stations and months were tested using Mann–Whitney tests followed by paired comparisons. All tests were performed in SPSS and preceded by tests of their assumptions.
Capelin were caught at all stations in May and August and 142 stomachs containing 4972 prey items were examined. Of these, only two stomachs were categorised as empty (Tables 2, 3). The mean size of capelin varied between 9.6 cm on GF10 in August to 11.9 cm on GF10 in May (Fig. 3) and differed significantly between all stations and months, except between GF3 and GF7 in May (Two-Way ANOVA, F(5,1727) = 220.9, p << 0.001, Tukey HSD post hoc). The average size of capelin at the three stations were larger in May compared to August, when fish larger than 12 cm were rare and small fish (< 10 cm) became more common in the catch. In May, there was a trend towards larger capelin at the inner station, though this trend reversed in August.
Numerically, copepod eggs and nauplii dominated the diet in May (Table 2) followed by the euphausiids and, at the inner station GF10, the copepod M. longa. In contrast, calanoid copepods, mainly C. finmarchicus and Pseudocalanus sp., were numerically abundant in the diet in August (Table 3). The numerical importance of C. finmarchicus was highest at GF3 and decreased towards the inner fjord, whereas Pseudocalanus sp. showed the opposite pattern.
In May, the euphausiids, especially T. raschii, made up more than 95% of the carbon mass of the diet in all size groups and stations, the remainder being mainly calanoid copepods (Fig. 4). The diet was more varied in August. The diet carbon mass was dominated by copepods at the outer station, GF3. The large calanoid copepods made up between 63 and 80% of the carbon mass of the diet and the group of unidentified copepods contributed between 15 and 25%. There was a gradual shift in diet carbon composition towards GF7 and GF10. In the size group 12–14 cm, copepods were almost completely replaced by euphausiids at these stations, whereas the group “Other copepods”, consisting of the smaller species, increased in mass towards the more freshwater-influenced GF10 in the size groups 8–12 cm. Hence, in August there was a clear station as well as capelin size effect on the composition of diet carbon, which was not observed in May.
The cluster analysis identified two major clusters of stations, months and size groups (Fig. 5). The first cluster consisted of all sizes and stations from May and the largest fish from GF7 and GF10 in August indicating their common dependence on euphausiids. The similarity between any two May samples was more than 90% and same sizes were more similar than any two size groups at the same station. The second major cluster consisted of the remaining seven of the August groups. Here the GF3 size groups separated out from the other stations at ca 65% similarity due to the importance of Calanus species in the diet. Also, the two GF10 size groups clustered together whereas the two GF7 groups were separated due to the importance of euphausiids in the diet of the 10–12 cm size group.
Discriminant analysis (SIMPER) was used to estimate what prey groups contributed to the diet dissimilarity between stations. The SIMPER analysis showed that carbon mass in pooled size groups showed low average dissimilarities between stations ranging from 18.5 to 42.1% in May (Table 4). The main contributor to the diet carbon differences between stations in May were the euphausiids, followed by Calanus sp., Nauplii and Other copepods. The average dissimilarity was highest in the comparisons involving GF3, primarily driven by lower contribution of euphausiids and higher contribution of nauplii at this station compared to GF7 and GF10. In August, average dissimilarities between stations increased to 53.2–55.7% and were due to differences in the importance of Calanus sp., Other copepods, Unidentified copepods and Euphausiids (Table 4). In all comparisons, Calanus sp. was the main contributor to the differences due to their decreasing carbon contribution towards the inner fjord. The opposite pattern was seen for euphausiids.
In short, the prey group carbon composition suggests minor differences between sizes and stations in May due to the general reliance on euphausiids. In August, there is clear separation between clusters of stations and sizes. Copepods are important for smaller fish and the Other copepods, consisting of smaller copepods, become more important towards the inner fjord (GF10) which is most influenced by melting glaciers.
The carbon contribution from the different copepod species in the diet varied among stations in May (Fig. 6). The smaller copepods species, especially M. longa, became more important towards the inner stations and in the smaller size group fish. In the largest size group (12–14 cm), C. glacialis and C. finmarchicus were important at GF3 and GF7, whereas C. finmarchicus was replaced by C. hyperboreus at the innermost station, GF10. In the size group 10–12 cm, C. glacialis was less important and the importance of C. hyperboreus increased. In August, the diversity of copepods in the diet increased as more of the smaller species were encountered. C. finmarchicus contributed between 27 and 64% of the diet carbon and was the most important copepod species at all stations and size groups except at GF10 in the 8–10 cm size group where Pseudocalanus sp. was more important. C. glacialis was primarily found at GF03 and to lesser extent at GF10. Of the smaller species, Pseudocalanus sp. was the most important especially at station GF7 and GF10.
The clustering based on carbon contribution from the different copepod species showed that all but one sample from May clustered together with more than 68% similarity (Fig. 7). The last sample group, GF10, size 10–12 cm, separated from all other groups at 26% similarity. All GF03 sample groups from August clustered more closely with the May sample groups than with the other of the August groups (63% similarity) probably due to a common dependence on larger Calanus species. One exception was GF10 8–10 cm, which clustered with the May GF3 samples. The August groups consisting of all GF7 and the 10–12 cm fish from GF10 separated from the May and GF03 groups from August at 51% similarity.
The SIMPER analysis of species composition in May showed average dissimilarities between stations from 81 to 90% with the inner- and outmost stations being most dissimilar (Table 5). The difference between stations were primarily driven by differences in the contribution of M. longa and the three large Calanus species, where C. finmarchicus contributed most to diet carbon at the GF03 and the C. hyperboreous and C. glacialis contributed most at GF10. The dissimilarity between stations decreased in August (64–87%), but the difference was still largest between GF03 and GF10. C. finmarchicus was by far the most important contributor to differences between stations, followed by Unknown copepods, C. glacialis and Pseudocalanus sp.
In summary, importance of the different copepod species differed between stations in May and August. The differences were related to the contribution of small copepod species, which increased towards the meltwater-influenced stations. For the larger Calanus species C. finmarchicus was abundant at the outer station GF03 but was replaced by C. glacialis and C. hyperboreus at GF7 and GF10.
The average carbon mass for each month and station varied between 0.31 to 5.17 mg per individual in the size group 8–10 cm, 0.65–16.49 mg in the 10–12 cm size group and 5.04–31.61 mg in the 12–14 cm size group. There were no significant differences in median stomach content between stations in the 8–10 cm size group (MW = 4.8, p = 0.089), despite a clear decreasing trend towards the meltwater-influenced head of the fjord in August (Fig. 8). In the 10–12 cm size group, there was a significant difference among stations and months (MW = 15.4, p = 0.009) and Bonferroni corrected paired comparisons showed significant differences between GF7 in May and GF7 and GF10 in August. Again, there was a clear decreasing trend in carbon mass towards station GF10 in August. There were no differences between stations in May. In the 12–14 cm size group there was a significant difference between stations and months (MW = 13.5, p = 0.019), although the only significant comparison was between GF7 in May and GF7 in August. In contrast to the smaller size groups there was no clear trend in average stomach carbon content along the transect in this largest size group.
The variation in stomach content between the individuals was best modelled by the proportion of “Other copepods” in the diet. A significant (F(1,83) = 148, p < 0.001) linear function of log-transformed proportions (Log(Carbon mass) = 1.01 * Log (prop of “Other Copepods”) + 2.22) explained 64% of the variation in diet carbon mass in the fish that had eaten “Other copepods” (85 of 142 fish) (Fig. 9). This is a strong indication that the absence of larger prey lead to a reduction in the food intake rate of the capelin.
The present study documents strong spatial and temporal variation in the diet of a keystone zooplanktivorous fish, the capelin, in a fjord system impacted by melting of the Greenland Ice Sheet.
Capelin life history
Relatively little is known about the life history of capelin in West Greenland. The stock is not surveyed systematically, but seems to migrate less than other stocks (Friis-Rødel and Kanneworff 2002). The capelin are primarily dispersed in the fjords and adjacent coastal waters, although schools are observed in offshore areas where adult capelin dominate survey catches (Bergstrøm and Vilhjálmsson 2008). The juveniles are primarily found in the fjords and coastal waters (Bergstrøm and Vilhjálmsson 2008; Sørensen 1985). There are no data on the distribution of capelin within the Godthåbsfjord, but the acoustic recordings and the consistent catches obtained during the sampling suggest that they are found throughout the fjord.
The maturing adult capelin migrate to the fjords during winter, and arrive at the spawning sites in late April and spawn until June moving progressively from deep in the fjords to near-coastal regions. So far, only beach spawning has been documented in Greenland. There appears to be some degree of semelparity, with all males and some females presumably dying in connection with spawning (Friis-Rødel and Kanneworff 2002; Sørensen 1985). Hence, the May sample presumably consists by both immature and mature individuals whereas the August sample will be dominated by immature individuals. This absence of individuals that have spawned and died between May and August is apparent in the overall length distribution and consistent with the finding that spawning capelin in Godthåbsfjord are generally around 11–13 cm large (Hedeholm et al. 2010). In short, immature and maturing fish appear to be found in most of the fjord throughout the year and become supplemented with a smaller group of mature fish migrating in from the near-coastal regions in preparation for spawning. Overall, the lack of substantial migrations in and out of the fjord suggests that the capelin in the Godthåbsfjord are critically dependent on the prey availability in the fjord.
The overall diet composition of the capelin sampled in Godthåbsfjord resembles observations in other Arctic and sub-Arctic systems, i.e. a mix of primarily large calanoid copepods (C. finmarchicus, C. glacialis, C. hyperboreous and M. longa), euphausiids, amphipods and a few smaller copepod species (Astthorsson and Gislason 1997; Dalpadado and Mowbray 2013; Hedeholm et al. 2012; Orlova et al. 2010). The proportions of these groups in the diet appear to be driven by the size of the capelin and the relative availability of the different groups in the different areas and periods. This suggests that the diet composition is linked to environmental and climatic factors that determine the occurrence of these prey items.
Most studies recognise the size related shift from calanoid copepods to euphausiids as the capelin grows larger (Dalpadado and Mowbray 2013; Hedeholm et al. 2012; Huse and Toresen 1996). There appears to be a notable shift around 11–12 cm where euphausiids become dominant, although our study suggest that this may occur earlier if large copepod prey is scarce as observed in early May in Godthåbsfjord (Teglhus et al. 2015). This is also found in the comparative study on capelin from Newfoundland and the Barents Sea (Dalpadado and Mowbray 2013). Here the Partial Filling Index (PFI) with regard to euphausiids increased from ca. 20 in capelin < 12 cm to ca. 50 in capelin > 12 cm in the Barents Sea, but remained below 5 in both size groups in Newfoundland with no indication in increasing importance of euphausiids with size. Hence, larger copepods may also constitute the main food of larger capelin in areas and periods when euphausiids are scarce (McNicholl et al. 2016). This suggests that the switch from copepods to the larger euphausiids is driven by optimization of energy gain rather than functional limitations with regard e.g. gape size (Lazzaro 1987; Werner and Hall 1974).
Capelin in the Godthåbsfjord also preyed on a variety of smaller non-Calanus copepod species. These were numerically important and made a significant contribution to the diet carbon mass in August. The main species were Pseudocalanus sp., M. longa and M. lucens. These species were also found to be important in Placentia Bay, Newfoundland (O'Driscoll et al. 2001), around Iceland (Astthorsson and Gislason 1997) and on the West-Greenland shelf (Hedeholm et al. 2012). The importance of the smaller copepods to the capelin diet appears to be dependent on the availability of larger Calanus species. If larger Calanus are absent, capelin seems to feed opportunistically on these smaller copepod species.
Amphipods were of little importance in the Godthåbsfjord, whereas they were important along a West-Greenland shelf transect from 60 to 70°N where they constituted ca. 20% of the diet by weight (Hedeholm et al. 2012). This is consistent with a 5-year analysis of zooplankton distribution in the fjord that revealed that amphipods only form a very small fraction of the zooplankton (Arendt et al. 2013). Around Newfoundland they constituted a significant part of the diet and were more frequent than euphausiids (O'Driscoll et al. 2001). In general, it appears that the amphipods are important in colder areas, such as Newfoundland compared to the Barents Sea and Godthåbsfjord (Dalpadado and Mowbray 2013; Orlova et al. 2010).
Non-crustacean food was generally absent from the diet of Godthåbsfjord capelin except a small contribution from appendicularia in August. This is in contrast to the importance of groups such as appendicularia, chaetognaths and pteropods in other studies (Huse and Toresen 1996; O'Driscoll et al. 2001). This may be due to the more episodic blooms of these groups, compared to crustacean zooplankton, that allow capelin to feed intensively on these in some areas and periods. Hassel et al. (1991) showed large variation in the biomass of chaetognaths and pteropods in different water masses in the Barents Sea and Dalpadado and Mowbray (2013) found that the importance of appendicularia varied considerably among stations off the coast of Newfoundland. Hence, the absence of the non-crustacean groups may be due to low abundance during our sampling periods. Alternatively, the importance can have been underestimated due to faster digestion of these prey groups compared to crustacean prey.
Spatial and temporal variation in diet composition
The spatial and temporal variations in the diet composition of the capelin reflect the different zooplankton communities observed in earlier studies of the Godthåbsfjord (Swalethorp et al. 2015). Arendt et al. (2010) made a transect from the offshore Fyllas Bank to the glaciers in May 2006. They showed a clear difference in the copepod biomass composition from the mouth of the fjord (~GF3) which was dominated by large Calanus species, to the central fjord (~GF7) where Pseudocalanus sp. and M. longa dominated and to the glacier influenced stations (GF10 and further in) where M. longa contributed > 75% of the biomass in 300 and 200-µm mesh size plankton nets. In 45-µm nets, Microsetella sp. became dominant at the innermost stations. A study by Tang et al. (2011) confirmed that spatial differences remain important during the summer months (July/August 2008) in Godthåbsfjord and identified seven different water masses, which each had a distinct zooplankton composition. In June 2010, Agersted and Nielsen (2014) found that the biomass of euphausiids increased more than two orders of magnitude from the area around GF03 towards GF7 and GF10, where the euphausiid biomass made up more than 85% of the combined biomass of euphausiids and copepods from 0 to 100 m depth. The Arctic species, T. raschii was the most dominant at most stations examined within the fjord.
Despite the overall similarity in copepod distribution in Arendt et al. (2010) and Tang et al. (2011), there were also notable differences probably related to the temporal development of the copepod community from May to August. The Greenland Ecosystem Monitoring program (GEM, https://g-e-m.dk) has since 2007 performed monthly zooplankton investigations at GF3. An extract of zooplankton data from the GEM database reveals a consistent pattern across the years. In 2013, the combined abundance of copepodites stages CIII-CV and adults of the three Calanus species increased from 52 individuals m−2 on May 12 to 813 individuals m−2 on July 23. Similarly, the abundance of Pseudocalanus sp. increased from < 250 individuals m−2 prior to June to 2195 individuals m−2 on June 19. The increase from low abundances prior to June and to a peak in late summer was also seen in most other copepod species. Hence, the capelin diet composition with regard to copepods is likely to reflect both a relatively stable horizontal distribution and an annual cycle of copepod abundance also observed in other West-Greenland shelf areas (Madsen et al. 2001) as well as in the diet of Northern sandeel (Ammodytes dubius) on Fyllas Bank outside Godthåbsfjord (Danielsen et al. 2016). The cluster analysis supports this with a clear separation of the stations in clusters defined by month and then by station, especially when it comes to major diet groups, but also with regard to the copepod composition although the division here is less stringent.
With regards to non-Calanus copepods, there was a good agreement between the observed distribution and their dietary importance. M. longa and Pseudocalanus sp. were abundant in the central and inner fjord (Arendt et al. 2010; Tang et al. 2011), GF7 and GF10, where they also constituted important prey items. In the SIMPER analysis, M. Longa was the most important contributor to the copepod diet differences between station GF10 and GF3, and GF10 and GF7 in May. In August, Pseudocalanus sp.. replaced M. longa as the most important non-Calanus species in the diet and made a significant contribution to diet differences between GF03, where it was rare, and GF7 and GF10 where it contributed considerably to the diet. Overall, there was an increasing importance of small copepods from the outer station GF3 towards the inner glacier influenced stations in line with the observed distribution of the copepods.
The spatio-temporal importance of the Calanus species appear primarily governed by the reproductive cycle of the copepods, their advection from the shelf and their vertical distribution. All three Calanus species, probably adults preparing for reproduction, were found in small numbers in the diet at GF3 in May. In August, higher abundances were observed further into the fjord and in the diets at GF7 and GF10. These are likely the early copepodite stages from the reproduction in early summer (Madsen et al. 2001).
Interestingly, C. hyperboreus was not found in the diets on GF7 and GF10 in August, which may be due to their vertical distribution, which Tang et al. (2011) found to be below 400 m at these stations. Similarly, M. longa was abundant in the zooplankton in August, but in contrast to May contributed little to the diet. This may also reflect temporal changes in the peak vertical distribution of M. longa that changed from 100–150 m in May to < 50 m in August, which was shallower than the depth of the sampled capelin. Hence, temporal and spatial variability in the vertical distribution of both prey and predator is important to consider when assessing the potential importance of different copepod species.
The euphausiids, primarily T. raschii, were by far the most important prey group in May and in the 12–14 cm capelin on GF7 and GF10 in August. The dominating role of euphausiids in May is likely linked to the low abundance of the large Calanus species in the fjord until later in the summer. The lack of euphausiids at station GF3 in August is also in line with the low abundance observed here (Agersted and Nielsen 2014). Given the abundance of krill at the GF7 and GF10 in August, it is intriguing that the capelin < 12 cm primarily rely on the Calanus and Pseudocalanus sp. In the smallest size group (8–10 cm), this may be due to gape limitation, but the 10–12 cm group have no problems consuming euphausiids in May. It does suggest that it is energetically more favourable for the smaller capelin to eat copepods when they are there, but that they can eat larger euphausiids when they are absent as in May.
The clear zonation of the zooplankton community in the Godthåbsfjord is not unique, but rather appears to be a feature of many Arctic fjord systems and they often share the same characteristics (Arimitsu et al. 2016; Hop et al. 2002). In Kongsfjord, Svalbard, the highest abundances of euphausiids were also found in the inner glacial meltwater-influenced parts of the fjord (Dalpadado et al. 2016), where they were associated with high chlorophyll concentrations. Also in Kongsfjorden, Walkusz et al. (2009) found distinct copepod communities related to different water masses. The temporal and spatial occurrence of these species, which include the three large Calanus species, Pseudocalanus sp. and M. longa, resembles the pattern from Godthåbsfjord and suggest a common phenology and water mass affinity in these Arctic and sub-Arctic fjord systems. Moreover, the diet composition of capelin in May and August 2013 mirrors the temporal and spatial distribution of the different species in Godthåbsfjord 2006, 2008 and 2013 indicating that the distribution pattern of copepods and euphausiids is stable over the years.
Ecological consequences of changing feeding opportunities
The relation between the spatio-temporal occurrence of zooplankton and the diet of capelin suggest that changes in the fjord environment will have an impact on the feeding and thereby condition of capelin, which may cascade through the food web (Astthorsson and Gislason 1998).
We found a tendency of reduced stomach carbon content from the mouth of the fjord to the inner part in August (Fig. 8). At an individual level, we also found a strong negative relation between the proportion of small copepod species in the diet and stomach carbon content (Fig. 9), suggesting that capelin are not able to compensate for the lack of large prey and, therefore, feeding on these smaller species is correlated with lower energy intake. The difference in stomach carbon content between fish feeding on larger vs smaller prey may to some extent be overestimated as digestion, and hence gut evacuation rates of smaller prey items may be faster (Knutsen and Salvanes 1999).
The inner part of the fjord is characterised by high primary production both in spring (Meire et al. 2016) and during summer, when upwelling of nutrients driven by marine-terminating glaciers, increases the nutrient supply and primary production (Meire et al. 2017). Both during spring and summer, the circulation in the Godthåbsfjord is characterised by a dominant outflow in surface layer (0–50 m) and inflows at deeper depths (Mortensen et al. 2014). This circulation regime causes a conveyer belt where the phytoplankton is displaced away from the glaciers. In the inner part of the fjord, small zooplankton species such as Microsetella norvegica, Oithona similis and Oncaea spp. (Tang et al. 2011) still dominate the zooplankton community although they were rare or lacking in the diet of capelin. In addition to their small size, the lipid content and composition of these copepods differs from the larger Calanus species, which further reduce their suitability as prey for capelin (Kattner and Hagen 2009; Lischka and Hagen 2007). Hence, it appears that the food web close to the glaciers, which is characterised by high abundances of euphausiids and small copepods, may be detrimental to the feeding of capelin sizes not able to prey efficiently on euphausiids. Larger zooplankton peak further downstream in the central and outer fjord, feeding on the exported production of the inner part (Meire et al. 2016; Tang et al. 2011; Teglhus et al. 2015) creating better feeding conditions in these regions for capelin smaller than 12 cm.
O'Driscoll et al. (2001) found that capelin feeding on smaller zooplankton had a smaller size-at-age compared to those who were feeding on larger, more lipid rich prey. This link between prey species and lipid accumulation was also found by Orlova et al. (2010) who furthermore argued that a muscle fat content of 7.5% was necessary to facilitate next year’s reproduction. Finally, Astthorsson and Gislason (1998) suggested a link between temperature, zooplankton abundance and capelin growth in which zooplankton biomass was a limiting factor for capelin growth. Hence, there is good evidence that the availability of large lipid rich prey is crucial for the nutritional condition and value of capelin. This is also the case for many other planktivorous fishes such as herring and sandeels (Danielsen et al. 2016; Mollmann et al. 2005; Prokopchuk and Sentyabov 2006).
Euphausiids play a key role as the main prey for capelin in Godthåbsfjord and several other areas as euphausiids consists of a larger biomass compared to copepods. This role is especially important in spring and early summer when the calanoid copepod communities are dominated by nauplii and early copepodite stages. The importance of euphausiids led Obradovich et al. (2013) to formulate the euphausiid hypothesis that propose that the lack of recovery of the Newfoundland and Labrador capelin stocks after the collapse in the 1990s is due to absence of euphausiid prey. Consequently, climate related changes in abundance of the different euphausiid species, as seen in the Barents Sea (Orlova et al. 2010), are likely to have a major impact on the population dynamics of capelin around Greenland. For the Godthåbsfjord system, Agersted and Nielsen (2014) predict that increases in freshwater outflow and increasing temperatures is going to favour Atlantic euphausiids at the expense of Arctic species such T. raschii. How this will affect capelin, for whom T. raschii at the present constitute the major prey item is uncertain. Capelin is a crucial trophic node in many sub-Arctic ecosystems, and as a main prey item for a wide range of marine top-predators, reduced capelin growth and condition is likely to translate into reduced energy intake of these predators. Following the collapse of the Newfoundland capelin stocks, the common murre (Uria aalge), an important avian predator on capelin, delayed breeding and delivered smaller and lower quality capelin to their chicks, which resulted in poor condition of the chicks (Davoren and Montevecchi 2003). Recently, the recovery of cod stocks in the same areas has been linked to the parallel recovery of the capelin stock (Rose and O'Driscoll 2002; Rose and Rowe 2015). Hence, there is good evidence that changes to the capelin feeding ecology has an impact far beyond the capelin itself and may affect the population dynamics of top-predators.
In conclusion, the spatial and temporal differences in capelin diets reflects the known distribution of the prey items along the freshwater gradient from the glaciers to the mouth of the fjord and the temporal development of the zooplankton community in West-Greenlandic waters. The importance of euphausiids and large calanoid copepods for capelin energy intake is evident and abundant small copepod species are not able to compensate for the lack of these prey items. We expect that ongoing global changes will continue to lead to increasing freshwater run-off and changes in the zooplankton community composition in the Godthåbsfjord and in a number of similar Arctic and sub-Arctic fjord systems. Our results suggest that this will affect capelin feeding ecology and condition, and through capelin, impact most of the top-predators in Godthåbsfjord.
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We gratefully acknowledge the contributions of the Arctic Research Centre (ARC), Aarhus University. Support was also provided by the Canada Excellence Research Chair (CERC). Financial support was provided by the Greenland Self-government and the Greenland Climate Research Centre (GCRC). We acknowledge the MarineBasis-Nuuk programme, part of the Greenland Ecosystem Monitoring (GEM), for contributing to the sample collection. Data from the Greenland Ecosystem Monitoring Programme were provided by the Greenland Institute of Natural Resources, Nuuk, Greenland in collaboration with Department of Bioscience, Aarhus University, Denmark. This work is a contribution to the Arctic Science Partnership (ASP) and GEM. The authors thank the crew of the RV ‘Sanna’ for sampling assistance
Funding was provided by Greenland Self-government and Greenland Climate Research Centre (GCRC).
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The authors declare that they have no conflicts of interest.
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All procedures performed in studies involving animals were in accordance with the ethical standards of the institution or practice at which the studies were conducted.
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Grønkjær, P., Nielsen, K.V., Zoccarato, G. et al. Feeding ecology of capelin (Mallotus villosus) in a fjord impacted by glacial meltwater (Godthåbsfjord, Greenland). Polar Biol 42, 81–98 (2019). https://doi.org/10.1007/s00300-018-2400-8
- Glacial meltwater