Marine chemistry variation along Greenland’s coastline indicated by chemical fingerprints in capelin (Mallotus villosus) otoliths
Introduction
In recent years, there has been widespread focus on the effects of climate change on the Arctic biosphere. The Arctic is home to an ecosystem of flora and fauna that has adapted to extreme climatic conditions and is susceptible to climatic change. The effects of climate change in the Arctic are well documented, witnessed by shifts in inland and sea ice coverage, shrinking of glaciers, and more extreme temperatures and weather phenomena (see Doney et al., 2011 for a general review on climate change in the arctic marine environment). Decreasing ice coverage has, however, also expanded the access to fish resources. It is anticipated that the abundance of major commercial species such as cod, tuna, mackerel and halibut in the Arctic will increase in the coming years, as environmental changes in their traditional distribution areas will force them to migrate polewards (see e.g. Drinkwater, 2005; Dulvy et al., 2008; Engelhard et al., 2014; Fossheim et al., 2015; Hughes et al., 2015; Jansen et al., 2016; Mackenzie et al., 2014; Perry et al., 2005).
A species that has changed distribution and productivity during the recent years of increased temperatures is the small pelagic fish capelin (Mallotus villosus) (Carscadden et al., 2013; Jansen et al., 2021). In the northeast Atlantic, capelin distribution has shifted towards west and north in recent years, likely resulting in increased presence in Greenlandic waters. In Greenland, this has led to increased commercial interest (ICES, 2018). Capelin has a circumpolar distribution, and is an important species in the arctic marine food web because of its status as prey for many fish, birds and mammals (e.g. Atlantic cod, Greenland halibut, Atlantic salmon, seals, whales, and seabirds) (Friis-Rodel and Kanneworff, 2002; Præbel et al., 2008).
Genetically, the capelin is divided into four major regional groups: West Pacific, East Pacific, Newfoundland, and Northeast Atlantic & West Greenland (Præbel et al., 2008). In addition, a recent genetic study has shown that capelin from Canada and West Greenland (Nuuk, Disco and Uummannaq) are reproductively isolated (Cayuela et al., 2020). In Greenland, the distribution of capelin extends from Kap Farvel (59°43’ N) up along the east- and west coast to at least Ittoqqortoormiit (70°29’ N) in the East and Upernavik (72°47’ N) in the West. Growth differences and inter-fjord genetic variations have been suggested for west coast capelin, whereas the stock composition of capelin spawning in east Greenland has never been studied (Friis-Rodel and Kanneworff, 2002; Hedeholm et al., 2010; Vilhjálmsson, 2002). During the spawning season, large schools of capelin appear along the coast in Greenland’s fjords to spawn in shallow water in coastal sediments. Males are generally larger than females and are believed to be semelparous, whereas females may spawn during multiple seasons. Post spawning, surviving capelin migrate away from the shore and are found in deeper parts of the fjords and along outer banks and adjacent offshore areas. Their exact whereabouts outside the spawning season are not known. Capelin have the ability to perform long-distance migration (Carscadden et al., 2013). However, no indications of such behavior have been found among fjord-spawning capelin in Greenland, although the research effort has been very limited (Friis-Rodel and Kanneworff, 2002; Sørensen and Simonsen, 1988).
Large-scale commercial fishing takes place in most of the NW- and NE Atlantic. Catches have been stable in recent years with ∼293,000 tons taken from ICES subareas 5 and 14 and Division 2.a west of 5 °W (average catch 2016–2018 in Iceland and Faroes grounds, East Greenland, and Jan Mayen area) and ∼23,000 tons taken from NAFO Subarea 2 and divisions 3 K L, off the east coast of Newfoundland (average catch 2015–2017)(DFO, 2018; ICES, 2019). The West Greenland (NAFO Subarea 1) population is not monitored and the population size is unknown. Capelin fishing in West Greenland has historically been limited to inshore, small-scale fisheries for bait and local consumption. A trial fishery has been attempted, but a large-scale, commercial fishery has never been established (Friis-Rodel and Kanneworff, 2002; Pers. Comm. Anders Bjørn Larsen, Directorate for Fisheries (APNN), Government of Greenland. 7 April 2020). The West Greenland capelin stock is considered an untapped resource with great commercial potential, but due to its central role in the marine ecosystem, a sustainable management plan is necessary before a potential large-scale fishery can be considered. Currently, biological information on population structure, spatial distribution and stock dynamics is inadequate to provide viable stock management advice. The recent changes in capelin distributions in the North Atlantic, likely brought on by environmental changes, has increased the need for further studies regarding spatial dynamics in Greenland (ICES, 2018).
In this study, capelin otolith microchemistry is utilized to identify chemical signatures related to spawning locations. Fish otoliths (ear stones) are carbonate structures in the inner ear that grow throughout a fish’s life. Otoliths are typically composed of ∼96 % carbonate, ∼3 % protein matrix, and contain ∼1 % of trace elements. Some trace elements are proxies for specific relationships or processes, because incorporation of these elements into the otoliths is regulated by environmental and/or physiological factors (Campana, 1999; Elsdon and Gillanders, 2004; Kerr and Campana, 2014). Environmental factors include temperature, salinity, pH, pollution, oxygen content and geological input (e.g. Hüssy et al., 2020; Izzo et al., 2016). Physiological factors are typically related to growth, metabolic rate, consumption, and reproduction (e.g. Sturrock et al., 2015). In addition, elements are filtered by several internal “gateways” that are encountered on the path from ambient water through blood stream and endolymph to ultimately being incorporated onto the otolith surface (Campana, 1999).
Otolith microchemistry has proven useful at identifying population structures, tracking migration patterns, and differentiating between fish stocks based on spatial variations in physicochemical conditions of ambient water (e.g. Campana, 2005; Elsdon et al., 2008; Thorrold et al., 1998). Otolith microchemistry analysis is typically applied to species living in fresh- or brackish environments (often diadromous), where water chemistry can vary significantly across short distances, and where element sources can be back-tracked (e.g. Bradbury et al., 2011; Gillanders, 2005; Wells et al., 2003). The method has also been applied successfully in the marine environment to distinguish fish from spatially separate areas (e.g. Campana et al., 1994; Heidemann et al., 2012; Moreira et al., 2018; Proctor et al., 1995; Rooker et al., 2001). The main criterion is that the targeted areas show contrasting physical and/or chemical conditions that result in distinct otolith trace element signatures. This can prove particularly challenging to identify in an open system marine setting, where multi-directional flow and larger water volumes typically lead to homogenization of water chemistry.
A few recent studies have investigated capelin otolith microchemistry in Canadian waters. These studies have focused on connectivity between spawning habitats and the otolith chemistry of early life stages (pre-hatch, larval, or juvenile) (Davoren et al., 2015; Davoren and Halden, 2014; Lazartigues et al., 2016; Loeppky and Davoren, 2018) and of adults (Davoren and Halden, 2014). In Greenland, water chemistry along the outer coastline is governed by several ocean currents with different thermohaline characteristics, as well as influx of freshwater from sea ice, glaciers and rivers. This forms a stratified and chemically diverse environment where multiple water bodies mix and form thermohaline stratification (see Straneo and Cenedese, 2015 for a review). In the fjords, water characteristics are governed by limited water exchange with the open ocean combined with substantial, seasonal influx of freshwater from rivers and glaciers, resulting in a vertical salinity profile that is increasingly brackish towards the surface (Buch, 2002). Sediment input also plays a part in shaping local water chemistry, particularly near rivers and glaciers (Sommaruga, 2015). Thus, there are considerable horizontal and vertical variations in the ambient water chemistry, both in the fjords and along the outer coast, which may form distinct chemical signatures in fish otoliths from different areas along the coast.
This study aims to provide elemental signature baselines from otoliths of adult capelin to characterize chemically distinct regions along Greenland’s marine coastline, using otolith edge chemistry that represents areas in the general vicinity of sampling locations. We hypothesize that chemically distinguishable areas can be identified on the basis of large-scale and local hydrographic variations. Using information on hydrography, geography, and capelin biology in Greenland, sampling localities are grouped into three overarching regional groups – Northwest, Southwest and East – as presumptive separators of chemical disparity along the coast. Differences in otolith microchemistry between these groups are examined with the aim of providing chemical baselines for future investigations of capelin stock dynamics. With this study, we hope to lay the basis for a greater understanding of capelin spatial dynamics in Greenland, thereby aiding the effort to develop a sustainable management plan.
Section snippets
Sample selection and preparation
Spawning capelin were collected in 2017 from 18 localities situated along the coast of Greenland (Fig. 1; Table 1), spanning from north-western Upernavik across Tasiusaq in south to Ittoqqortoormiit in eastern Greenland. Sampling sites were selected to constitute a wide geographic distribution. Nevertheless, as very few spawning locations are known in East Greenland, the majority of individuals were collected in West Greenland. In each of the preselected areas, the exact sampling locations were
Size and sex
Fish lengths vary with sex and geography (Fig. 3). At age 4, females are somewhat smaller than males, but as shown by VIF-analysis the correlation between length and sex is negligible. Correlation between length and locality is similar for the two sexes: Fish lengths are generally larger in the northwest (1-NW) (except for locality 7) and in the east (3-East) than in the southwest (2-SE). The largest fish are found at eastern locality 19.
Element distributions
Initial univariate tests are aimed at recognizing trends
Discussion and conclusions
This study has identified two well-defined, chemically distinct groups (1-NW and 2-SW) of spawning aggregations of capelin along the Greenland west coast. The LDA analyses detect only minor overlap between the two groups, and LDA/QDA classification success is high. Group 3-East, however, cannot be considered a chemically distinct or homogeneous unit, as the two localities 19 and 20 show significant disparity for several elements. LDA/QDA classification success is also relatively low. Perhaps,
Funding
This work was supported by Royal Greenland, Polar Seafood, The BANK of Greenland, and DTU Aqua.
CRediT authorship contribution statement
Peter Fink-Jensen: Conceptualization, Methodology, Validation, Formal analysis, Investigation, Resources, Data curation, Writing - original draft, Writing - review & editing, Visualization. Teunis Jansen: Conceptualization, Methodology, Formal analysis, Resources, Writing - review & editing, Supervision, Project administration, Funding acquisition. Tonny Bernt Thomsen: Methodology, Investigation, Resources, Writing - review & editing. Simon Hansen Serre: Methodology, Formal analysis,
Declaration of Competing Interest
The authors report no declarations of interest.
Acknowledgements
We would like to thank the local Greenlandic fisherman that provided samples for this study and Sofie Ruth Jeremiassen (GINR) for facilitating the contact to the fishermen. We wish to thank the lab assistants at DTU Aqua for their assistance with sample preparation, as well as lab technicians Mojagan Alaei and Olga Nielsen at GEUS for their assistance with microchemical analysis. We also wish to thank Christoffer Moesgaard Albertsen of DTU Aqua and Bo Markussen of Department of Mathematical
References (74)
- et al.
Strontium and barium uptake in aragonitic otoliths of marine fish
Geochim. Cosmochim. Acta
(2000) - et al.
Juvenile fish habitat across the inner Danish waters: Using otolith chemistry to discriminate between hybridising con-familials and contiguous, coastal habitat
Estuarine, Coastal and Shelf Science
(2019) Otolith elemental composition as a natural marker of Fish stocks
Stock Identification Methods
(2005)- et al.
A comparison of recent changes in distribution of capelin (Mallotus villosus) in the Barents Sea, around Iceland and in the Northwest Atlantic
Prog. Oceanogr.
(2013) - et al.
Connectivity of capelin (Mallotus villosus) between regions and spawning habitats in Newfoundland inferred from otolith chemistry
Fish. Res.
(2014) - et al.
Does otolith chemistry indicate the natal habitat of Newfoundland capelin Mallotus villosus?
J. Exp. Mar. Bio. Ecol.
(2015) - et al.
Fish otolith chemistry influenced by exposure to multiple environmental variables
J. Exp. Mar. Bio. Ecol.
(2004) Using elemental chemistry of fish otoliths to determine connectivity between estuarine and coastal habitats
Estuar. Coast. Shelf Sci.
(2005)- et al.
Length measurement methods of Atlantic mackerel (Scomber scombrus) and Atlantic horse mackerel (Trachurus trachurus) – current practice, conversion keys and recommendations
Fish. Res.
(2018) - et al.
Accurate trace element analysis of speleothems and biogenic calcium carbonates by LA-ICP-MS
Chem. Geol.
(2012)