Geographical expansion of Northeast Atlantic mackerel (Scomber scombrus) in the Nordic Seas from 2007 to 2016 was primarily driven by stock size and constrained by low temperatures
Introduction
The Northeast Atlantic mackerel (Scomber scombrus) stock is a widely distributed, highly migratory, temperate schooling pelagic fish of great commercial importance (Trenkel et al., 2014). Mackerel become mature at age 2–3 years old, spawn annually, and most of the stock is less than 12 years old (ICES, 2016). Mature individuals undertake a seasonal migration along a south-to-north axis currently ranging from Gibraltar to Svalbard, approximately from latitude 36°N to 78°N (ICES, 2013, Nøttestad et al., 2016a). Their migration cycle is characterized by over-wintering, followed by spawning in the south from January to July, whereas they feed in the north during summer and fall (Belikov et al., 1998, Uriarte and Lucio, 2001, Iversen, 2002, Jansen et al., 2012, Utne et al., 2012, Nøttestad et al., 2016a). Prior to the mid-2000s, mature mackerel summer (June–August) distribution was restricted to the Norwegian Sea (east of longitude 10°W and south of latitude 72°N), the North Sea, and the shelf west of Scotland (Fig. 1).
From the mid-2000s through to the present, mackerel summer distribution expanded in two directions from the traditional feeding area in the central Norwegian Sea. During one decade, mackerel distribution edge expanded westward, along the south coast of Iceland and towards the east coast of Greenland by approximately 1500 km, and northward towards Svalbard by approximately 500 km (Berge et al., 2015, Jansen et al., 2016, Nøttestad et al., 2016a). This expansion was first noticed by the Icelandic commercial fishery for Norwegian spring-spawning herring (Clupea harengus) as its mackerel by-catch increased from 20 t in 2002 to 1700 t in 2006 (Astthorsson et al., 2012). By the summer of 2007, mackerel presence east and southeast of Iceland became more noticeable (Nøttestad et al., 2007) and a direct mackerel fishery began in the eastern part of the Exclusive Economic Zone (EEZ) of Iceland (Astthorsson et al., 2012, Marine Research Institute, 2015). During the 20th century, there are a few reports of mackerel observations within the Icelandic EEZ from the commercial fleet and from historical records, however, the majority of observations were of a single individual fish (Lockwood, 1988, Astthorsson et al., 2012). This was a geographical distribution expansion but not a shift as mackerel density increased in the traditional feeding area in the Norwegian Sea and North Sea during the same period (Nøttestad et al., 2016a, van der Kooij et al., 2016).
Geographical distribution of migratory fish stocks is affected by abiotic and biotic environmental conditions, and population size as well as the individual's internal state mediated via motivations, constrains and feedbacks (Secor, 2015). Temperature is a major abiotic factor influencing geographical distribution of fish stocks in subarctic oceans (Drinkwater et al., 2014, Nye et al., 2014). Generally, in the northern hemisphere distribution shifts northward during warm periods and vice versa in cold periods (Sundby and Nakken, 2008, Nye et al., 2014). Furthermore, temperature can pose a direct constraint to a stock's distribution (Frank et al., 1996), as there is a physiological limitation to how cold/warm waters fish can tolerate (Brett, 1979). A major biotic factor is prey abundance and prey gradients, which have been positively linked to pelagic fish distribution during the feeding season (Broms et al., 2012).
It is well documented that fish stock size is frequently positively correlated to geographical distribution range (Lluch-Belda et al., 1989, Dragesund et al., 1997, Barange et al., 2009). Density-dependent habitat selection predicts that a population will expand into areas of lower habitat quality when stock size increase and retract into higher quality areas when stock size is small. MacCall´s basin model postulates that increasing intraspecific competition in a core area reduces habitat quality to be equal to the quality of marginal areas, motivating individuals to move into previously unoccupied marginal areas (Fretwell and Lucas, 1969, MacCall, 1990). The basin model thus predicts that density in the core area increases and that distribution range expands when stock size increases. Furthermore, that individual's somatic conditions are the same in the core area and in the marginal areas because habitat quality is the same (MacCall, 1990, Shepherd and Litvak, 2004).
Marine climate influences geographical distribution of fish stocks and its effects operate on many time-scales that range from immediate (Frank et al., 1996) to multidecadal (Sundby and Nakken, 2008) and are often concomitant with changing population size (Drinkwater et al., 2003; Drinkwater, 2006; Poloczanska et al., 2013). Climate change and multidecadal climate fluctuations like the subpolar gyre (Häkkinen and Rhines, 2004, Hatun et al., 2005), the Atlantic Multidecadal Oscillation (Schlesinger and Ramankutty, 1994), and the North Atlantic Oscillation (Hurrell, 1995) are linked to gradual changes in current circulation patterns and, in turn, nutrient concentrations (Hátún et al., 2017a) and sea temperature with cascading effects on productivity at all tropic levels (Drinkwater et al., 2003, Nye et al., 2014, Hátún et al., 2009, Hátún et al., 2016, Hátún et al., 2017b).
Temperature and prey availability are likely to influence mackerel distribution during the summer feeding season in the Nordic Seas. It is a temperate species, which relies on energy reserves collected during summer feeding as energy source for the over-wintering and spawning season (Lockwood, 1988, Olafsdottir et al., 2016). In the Nordic Seas, mackerel feed in the surface mixed layer, typically located in the upper 30–40 m and above the thermocline (Gødo et al., 2004, Nøttestad et al., 2016b). It is an opportunistic predator with a wide range of prey species (Langøy et al., 2012, Bachillier et al., 2016). Main prey is calanoid copepods, and to a lesser extent euphausiids, amphipods, other planktonic crustaceans, pelagic molluscs and fish (Prokopchuk and Sentyabov, 2006, Langøy et al., 2012, Óskarsson et al., 2016, Bachillier et al., 2016). Observations show that mackerel frequently occupy temperatures ranging from 8 °C to 14 °C during the summer feeding period (Utne et al., 2012, Nøttestad et al., 2007, Nøttestad et al., 2010, Nøttestad et al., 2011, Nøttestad et al., 2012, Nøttestad et al., 2013, Nøttestad et al., 2014, Nøttestad et al., 2015, 2016b, 2016c).
Recent work by Nøttestad et al. (2016a) suggested that the mackerel expansion in the Nordic Seas was positively related to stock size from 2007 to 2014, when stock size more than doubled. In the present paper, we expand this time series analysis to 1997–2016 and we also analyse the mechanisms behind the expansion. We assess how ambient temperature, prey abundance, and stock size influence mackerel summer distribution during range expansion from 2007 to 2016. Then we evaluate whether interannual temperature changes coincided with the sudden expansion in mackerel distribution by comparing temperature in the expansion areas before (1997–2006) and during (2007–2016) the expansion. Finally, we examine if habitat quality differs between the traditional feeding grounds in the Norwegian Sea and the recently invaded expansion areas. Somatic condition of individual mackerel, measured as relative mean weight-at-length, is used as proxy for habitat quality.
Section snippets
Study area
Oceanographic conditions in the Northeast Atlantic are influenced by topography and geostrophic currents coming from the south (temperate Atlantic waters) and from the north (cold Polar waters) and (Fig. 1). Atlantic water flows northwards into the Norwegian Sea, along the continental shelf edge towards Svalbard, and into the shelf area south and west of Iceland (Blindheim and Østerhus, 2005). Polar water flows southward along the east coast of Greenland with branches diverted into cyclonic
Geographical expansion and mackerel density
The total area occupied by mackerel in Nordic Seas during the summer feeding season, from 1997 to 2016, ranged from 0.4 to 2.5 million km2. The smallest area was in 1997, from 1998 to 2006 it was between 0.8 and 1.0 million km2, then the expansion began in 2007, peaked in 2014 at 2.5 million km2, and declined slightly in the last two years (Fig. 4a). The expansion coincided with a shift in COG and both parameters peaked in 2014 when total area was three-fold larger than the average total area
Temperature effect
Temperature directly constrained mackerel geographical distribution during the summer feeding season in the Nordic Seas during the expansion period from 2007 to 2016. Mackerel prefer temperatures ranging from 9 to 13 °C and where temperatures in the expanded areas were within that range resulted in both high mackerel presence and high mackerel density. Mackerel also occupied waters with temperatures ranging from 7 to 9 °C, although in this range while mackerel presence was still high, their
Conclusions
Our results suggested that mackerel geographical expansion during the summer feeding season in the Nordic Seas, from 2007 to 2016, was primarily driven by an increasing mackerel stock size and constrained by availability of preferred temperature habitat. This facilitated mackerel expansion into two major directions, COG shifted northward within the Norwegian Sea towards Svalbard by approximately 400 km, and westward by approximately 1650 km along the Irminger current south of Iceland and into
Acknowledgements
We thank the crewmembers participating in the many scientific surveys on research vessels and chartered fishing vessels, which provided the data for our study and were conducted by: Institute of Marine Research, Norway, Marine Research Institute, Iceland, the Faroe Marine Research Institute, Faroe Island, and Greenland Institute of Natural Resources, Greenland. We are grateful to the ICES Working Group on Widely Distributed Stocks and to NOAA/OAR/ESRL PSD, Boulder, CO, USA, for making available
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