Stomach content analysis of mesopelagic fish from the southern Kerguelen Axis

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Abstract

Mesopelagic fish represent an important trophic link between zooplankton and higher order predators in Southern Ocean food webs. Information on their feeding habits is still sparse, representing a key area of uncertainty in efforts to understand and model Southern Ocean food web dynamics. We used visual assessment of stomach contents to characterise the diets of three myctophids (Electrona antarctica, Gymnoscopelus braueri, Krefftichthys anderssoni) and one bathylagid (Bathylagus antarcticus) over the southern extension of the Kerguelen Plateau (‘southern Kerguelen Axis’), a highly productive area of both biological and economic importance in the Indian sector of the Southern Ocean. Diets of all four species were dominated by euphausiids, amphipods, copepods and fish. Bathylagus antarcticus also preyed upon a high proportion of soft-bodied organisms. There was strong evidence for dietary variability both within and between species, and this variability was driven by latitudinal variation in zooplankton assemblages. Size-based shifts in diet were apparent, with larger individuals of myctophid and bathylagid species consuming larger prey. Linear mixed effects models also demonstrated that the weight of prey consumed increased in relation to predator weight. Dietary information presented here advances our understanding of the mesopelagic components of Southern Ocean food webs, which will improve the development of food web models for the region.

Introduction

Mesopelagic fish are a critical component of global oceanic ecosystems (St. John et al., 2016). These small fish (predominantly < 20 cm body size) are ubiquitous in the ‘twilight zone’ (200–1000 m) of the open oceans and constitute a major part of the global fish biomass (Gjosaeter and Kawaguchi, 1980; Proud et al., 2018). Occupying a trophic position between zooplankton and higher predators, mesopelagic fish act as an important trophic link (Catul et al., 2011; Cherel et al., 2010; Lea et al., 2002, 2006; Pusch et al., 2004). They may also play an important role in global ocean biogeochemical cycling by transporting organic and inorganic carbon between depths (Hays, 2003; Hudson et al., 2014; Irigoien et al., 2014; Lehodey et al., 2015).

Within the Southern Ocean, the mesopelagic fish community is dominated by the Myctophidae and Bathylagidae families (Duhamel et al., 2014). Myctophids are thought to comprise the greatest biomass and species richness compared to any other Southern Ocean fish family (Duhamel et al., 2014; Kozlov, 1995). Bathylagids also represent a large biomass, being particularly abundant in the lower mesopelagic zone (400–1000 m) but found as deep as 4000 m (Duhamel et al., 2014). Due to the high biomass and high energy content of lipid-rich myctophids (Lea et al., 2002; Van de Putte et al., 2006), these fish are a critical component in the diets of higher order Southern Ocean predators (Bocher et al., 2001; Collins et al., 2008; Connan et al., 2007; Lea et al., 2006; Shreeve et al., 2009). Bathylagids have also been shown to be a key source of energy for Patagonian toothfish, which are the basis for a substantial commercial finfish fishery in the Southern Ocean (Gaskett et al., 2001; Goldsworthy et al., 2002). They are also likely to be key prey items for elephant seals and beaked whales (Pauly et al., 1998), and are important consumers of gelatinous zooplankton (Clarke et al., 2018).

Despite the ecological significance of Southern Ocean mesopelagic fish, remarkably little is known about their trophic ecology in most regions (Hulley and Duhamel, 2011; Murphy et al., 2012; Young et al., 2015). Relatively few studies have attempted to quantitatively characterise the diets of mesopelagic fish within Southern Ocean ecosystems (Pusch et al., 2004; Saunders et al., 2014, 2015c; Shreeve et al., 2009; Stowasser et al., 2012), with most only being semi-quantitative, and therefore of limited use to the development of food web models (Gorelova and Efremenko, 1989; Kozlov and Tarverdiyeva, 1989; Naumov et al., 1981; Pakhamov et al., 1996; Rowedder, 1979). Generally, Southern Ocean myctophids and bathylagids have been characterised as opportunistic foragers, predominantly feeding on various crustaceans such as copepods, amphipods and euphausiids (Hopkins and Torres, 1989; Lancraft et al., 1991; Lea et al., 2002; Pakhamov et al., 1996; Pusch et al., 2004), with dietary variability across space and time (Cherel et al., 2010; Pakhamov et al., 1996; Saunders et al., 2014, 2015a; Shreeve et al., 2009; Stowasser et al., 2012). Importantly, limited understanding of species abundance, as well as diet and trophodynamics of mesopelagic fish hinders our ability to conceptualise Southern Ocean food web dynamics and accurately represent mid-trophic level components within ecosystem models (Hill et al., 2012; Murphy et al., 2012; Young et al., 2015).

The Kerguelen Plateau is a highly productive area of both biological and economic importance in the Indian sector of the Southern Ocean. The region spanning from the subantarctic islands over the Kerguelen Plateau (Kerguelen, Heard and McDonald Islands), southwards to the Antarctic continent (hereafter termed the Kerguelen Axis) is thought to have a spatial transition in mid-trophic level regimes, with mesopelagic fish dominating trophic pathways in the north, towards a more krill-dominated ecosystem in the south (Hulley and Duhamel, 2011; Nicol and Raymond, 2012). Few studies have investigated the dietary composition of mesopelagic fish within the Kerguelen region, and of these, the spatial extent has largely been restricted to the northern Kerguelen Plateau (Cherel et al., 2010; Connan et al., 2010). Significant knowledge gaps remain regarding the dietary composition of key mesopelagic species around the southern Kerguelen Plateau, and how these diets may differ across northern (putatively fish-dominated) and southern (putatively krill-dominated) systems.

As part of the 2016 Kerguelen Axis marine ecosystem survey over the southern Kerguelen Plateau, the dietary composition of mesopelagic fish across a latitudinal gradient has recently been investigated using molecular sequencing techniques (Clarke et al., 2018) and stable isotope analysis (Woods et al., 2019). DNA sequencing of stomach contents showed myctophid diets were dominated by amphipods, euphausiids and copepods, whereas radiolarians and siphonophores contributed a much greater proportion for bathylagids. In both studies, size-based dietary shifts were apparent. Dietary DNA showed that larger mesopelagic fish were more likely to consume euphausiids, and also suggested regional differences in diet over the survey area. Due to methodological limitations, both studies were unable to extract detailed taxonomic and quantitative dietary information, and were unable to quantify the fish-based component of diets. Therefore, a study employing stomach content analysis represents a timely and complementary contribution, providing a more integrated and holistic understanding of mesopelagic fish trophic ecology in this region.

This study aims to characterise the dietary composition of four of the most common and widespread Southern Ocean mesopelagic fish species: three myctophids (Electrona antarctica, Gymnoscopelus braueri, Krefftichthys anderssoni), and one bathylagid (Bathylagus antarcticus). We use stomach samples of fish collected during surveys on the southern Kerguelen Axis, with this work forming part of the broader Kerguelen Axis research initiative to characterise ecosystems in this highly productive region. Variability in diet between species, and spatially between northern and southern regions of the survey area were investigated using traditional visual assessment of stomach contents. Species were sampled across a broad range of size classes to investigate the influence of predator size on predator and prey size relationships. This dietary information can be used to better understand spatial variation in food web structure in this region and the extent of size-based trophic structuring in this assemblage. This information can in turn inform future studies of how these dynamics may change in response to altered physical processes associated with climate change.

Section snippets

Sample collection

Mesopelagic community samples were collected in the austral summer of 2016 (22 January – 17 February) as part of the Kerguelen Axis ecosystem study on-board the R.S.V Aurora Australis. For this study we focus on mesopelagic fish that were collected from six sampling stations along the major south-to-north transect of the Kerguelen Axis. Three sampling sites were located in subpolar waters south of the Southern Boundary (SB) of the Antarctic Circumpolar Current (ACC) over the Princess Elizabeth

Dietary composition

Stomach contents of 372 fish were microscopically examined in the laboratory. The four species E. antarctica (n = 116), G. braueri (n = 74), K. anderssoni (n = 63) and B. antarcticus (n = 119) were opportunistically sampled from cod-end samples collected within each MIDOC station. Species were sampled across a broad range of size classes to investigate the influence of predator size on predator and prey size relationships (Fig. 2). Planktonic crustaceans were a key component of the fish dietary

Spatial trends in prey consumption

Results of this study show there was a clear latitudinal dichotomy in myctophid and bathylagid dietary composition. In general, euphausiids were the dominant prey item recorded in the southern survey area. In contrast, amphipods, copepods, fish and various soft-bodied organisms were the dominant prey items in the northern survey area. The latitudinal trends in dietary composition recorded by key mesopelagic fish are a likely reflection of zooplankton communities and lower trophic level

Conclusions

The present study provides important information regarding the diet and trophic interactions of four of the most abundant mesopelagic fish species within the southern Kerguelen Axis. These predators exploited a diverse range of zooplankton, and there was notable variation in diet between species. This study has demonstrated the mesopelagic fish community in the southern Kerguelen Axis play an important role in energy transfer through both krill-dependant and krill-independent trophic pathways.

Acknowledgements

We thank the captain and crew of the R.S.V Aurora Australis, as well as the researchers involved in the Kerguelen Axis voyage for their assistance with data collection and considerable efforts to facilitate this research. This research was supported by the Australian government under the (i) Cooperative Research Centre Program through the Antarctic Climate and Ecosystems Cooperative Research Centre (ACE CRC), (ii) Australian Antarctic Science Program (Projects 4343, 4344, 4347 and 4366), and

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