Introduction

The family Nototheniidae is the most diverse of the Antarctic fish, consisting of 14 genera and 56 endemic species to the Southern Hemisphere (Nelson et al. 2016). The majority of notothenioids occur in Antarctica, but some species range northward to such regions such New Zealand, Macquarie Island, Chile, and Argentina (Nelson et al. 2016). This is the case of the genus Dissostichus, composed by two commercially important species: D. eleginoides and D. mawsoni (Collins et al. 2010). The Patagonian toothfish (or Chilean sea bass) D. eleginoides (Online Resource 1) inhabits the southern tip of South America (Argentina and Chile), sub-Antarctic Indian Ocean islands, and Pacific Macquarie Island (Cousseau and Perrota 2013). It was usually captured as a by-catch species in trawl fisheries off the South American continental shelf or by long-line fisheries targeting large adult Patagonian toothfish in deep water (Collins et al. 2010), but actually more than 95% of the catches are supported by directed trawl fisheries (Di Marco et al. 2019). In Argentina, the distribution is related with sub-Antarctic waters in the outer edge of the continental shelf, Malvinas/Falklands Islands, and continental slope up to 35°S and 2500 m depth (Cousseau and Perrota 2013). Maturity is attained earlier by males, between 80 and 90 cm (Prenski and Almeida 2000; Laptikhovsky et al. 2006; Collins et al. 2010). The species appeared to be moderately fast growing and long-lived reaching at least 50 years (Horn 2002) and two meters in total length (Cousseau and Perrota 2013).

The diet of the Patagonian toothfish was studied in Kerguelen (Duhamel 1981) and Crozet Islands (Duhamel and Pletikosic 1983), South Georgia and Shag Rocks (Zhivov and Krivoruchko 1990; McKenna 1991; Garcia de la Rosa et al. 1997; Pilling et al. 2001; Xavier et al. 2002; Barrera-Oro et al. 2005; Collins et al. 2007), Macquarie Island (Goldsworthy et al. 2002), Malvinas/Falklands Islands (Arkhipkin et al. 2003), Argentinean continental shelf (Garcia de la Rosa et al. 1997), and central and south Chile (Murillo et al. 2008; Sallaberry-Pincheira et al. 2018). However, feeding habits of the Patagonian toothfish from the eastern end of the Argentinean continental shelf to the west surroundings of the Burdwood/Namuncurá Bank in the southern Atlantic Ocean (53–55°S) have not been investigated to date. In this context, the general objective of the present work was to examine the diet of the Patagonian toothfish by analyzing the stomach contents of specimens captured aboard the factory trawler Centurión del Atlántico during September and October 2017 and 2018. The specific objectives were as follows: (a) quantify the diet composition of the Patagonian toothfish in the Southwest Atlantic Ocean (53°S–55°S), (b) determine the trophic level, (c) evaluate the effect of total length, sex, maturity, depth, and region on the diet, and (d) analyze prey–predator total length relationships.

Material and methods

Study area

The study is on the southernmost Patagonian shelf break in South America (53°–55°S, 351–1073 m depth) located in the western zone of Burdwood Bank/Namuncurá MPA (Fig. 1). The top of the Burdwood Bank/Namuncurá MPA is a large plateau of 80–150 m depth situated in the south of the Malvinas/Falklands Islands and to the east of Argentinean continental shelf break and Beagle Chanel, separated from them by deep water, 500–2000 m depth (Van Mieghem and Van Oye 1965). The Burdwood Bank/Namuncurá MPA includes a non-coastal marine-protected area created in 2013 considered an oceanic hot spot of benthic biodiversity (Schejter et al. 2016). Based on the distribution patterns of several groups of marine organisms, the study area is located within the Magellanic biogeographic province which occupies most of the southern Patagonian shelf (South of 43°S) (Perillo et al. 2006). Following the cold waters of the Malvinas Current, this assemblage of species extends its distribution towards outer, northern, and deeper areas of the shelf and slope (Perillo et al. 2006).

Fig. 1
figure 1

Map of the study area showing the sample sites where specimens of Patagonian toothfish Dissostichus eleginoides were collected in each region (E: east region, W: west region) aboard the commercial fishing vessel Centurión del Atlántico to study the diet in the southwest Atlantic Ocean

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Sample collection

The Patagonian toothfish Dissostichus eleginoides specimens were collected during September and October 2017 and 2018, between 53° and 55° S, and from 351 to 1073 m depth aboard the commercial fishing vessel Centurión del Atlántico (Fig. 1). Fishing was conducted in each sampling site (Fig. 1) using an Ergesund 716 bottom trawl net with rock hopper gear (200 to 150 mm mesh size in the body of the net, 120 mm mesh size in the cod end, 9 m vertical opening and 22 m horizontal aperture). The specimens captured from the Burdwood Bank/Namuncurá MPA surroundings were measured to the nearest cm (TL, total length), weighted (to the nearest 0.01 kg), and sexed. Sexual maturity (mature or immature) was determined for females according to the ovary condition and the presence of yolk eggs, whereas male maturity was determined by the size and color of testes (Macchi and Pájaro 2003). The stomachs were excised, opened, and the prey items found were identified to the lowest possible taxonomic level, counted, and weighed using an electronic scale Marel M1100 series, with an accuracy of 0.01 kg.

Statistical analysis

The parameters a and b of Weight–Length Relationship (WLR) were estimated by the least square method from logarithmically transformed data, and the degree of fit between weight and length variables was measured by the correlation coefficient (r2) (Crawley 2005). This varied from 1, when the regression explains all of the variation, to 0, when the regression explains none of the variation (Crawley 2005). The exponent b provided information on fish growth: if b = 3 then growth is isometric, if > 3 is positive allometric growth, and < 3 is negative allometric growth (Froese et al. 2011).

The stomachs sampled were randomized 100 times, and the accumulation prey curve was plotted as a function of stomach number with their 95% confidence intervals in order to assess whether the number of stomachs analyzed was sufficient to accurately describe the diet of each group of specimens of Patagonian toothfish D. eleginoides considered in the dietary analysis (Ferry and Cailliet 1996; Cortés 1997).

The vacuity index (VI) was estimated as the percentage of empty stomachs in the sample (Moura et al. 2008) to evaluate the rate of feeding activity and to reveal whether the specimens ate on the site or not. The contribution of each prey to the diet of Patagonian toothfish D. eleginoides was evaluated by calculating the percentage frequency of occurrence (%F, the total number of stomachs in which a given prey was found expressed as percentage of the total number of stomachs with food), the percentage of number (%N, the total number of a given prey as percentage of the total number of prey found), the percentage of weight (%W, the weight of a given prey as percentage of the total weight of prey found). These three parameters were integrated into the Index of Relative Importance: IRI = %F × (%N + %W) (Pinkas et al. 1971), expressed in percentage (%IRI; Cortés 1997). In addition to the traditional %IRI, the Prey-Specific Relative Importance Index (PSIRI) (Brown et al. 2012) was used to quantify the diet which is calculated according to the following formula:

$$\% \hbox{PSIRI} = \frac{{\% \hbox{F} \times \left( {\% \hbox{PN} + \% \hbox{PW}} \right)}}{2}$$

where \(\% \hbox{PN = }\frac{{\% \hbox{N}}}{{\% \hbox{F}}}\) and \(\% \hbox{PW = }\frac{{\% \hbox{W}}}{{\% \hbox{F}}}\) This index was recently introduced and recommended to replace %IRI for its demonstrated more balanced treatment of the relative measures of prey quantity. Moreover, the %PSIRI is additive with respect to taxonomic levels, such that the sum of %PSIRI for species will be equal to the %PSIRI of the family containing those species (Brown et al. 2012).

The trophic level (TR) was estimated for the Patagonian toothfish D. eleginoides following the method proposed by Cortés (1999) as follows:

$$\hbox{TR} = 1 + \left( {\sum\limits_{j = 1}^{n} {\hbox{P}_{j} \times \hbox{T}r_{j} } } \right).$$

where Trj is the trophic level of each prey item j and Pj is the percentage of weight (%W) of each prey item j in the diet of Patagonian toothfish D. eleginoides, and n is the total number of prey items. The Trj were obtained from the literature (Ebert and Bizzarro 2007; Sea around us 2019). The TR was calculated for adults and juvenile specimens.

To test the hypotheses that the diet of the Patagonian toothfish D. eleginoides was influenced by TL, sex, maturity stage, depth, and region, we used Generalized Linear Models (GLM) and the information theory selection criteria (Venables and Ripley 2002). The number (counts) of the main prey items of the Patagonian toothfish (pelagic fish, demersal fish, cephalopods and shrimp Acanthephyra pelagica) were used as dependent variables. This kind of numerical data has many zeros, a variance much greater than the mean, and it exhibits a negative binomial distribution (Crawley 2005). All these issues allowed to build GLM with negative binomial error distribution and a log link (Crawley 2005). The independent variables selected to explain the consumption of the main prey were as follows: total length (TL, cm), sex, maturity stage (juvenile, adults), depth, and region (east, west). Models including a quadratic term of TL (TL2) as independent were also fitted in order to test a curvilinear relationship between TL and the consumption of any prey. Models with all possible combination of two independent variables were constructed. A theoretical model without an independent variable was also fitted to test the hypothesis that none of the independent variables selected in this work influenced the consumption of any prey (Lucifora et al. 2009). Akaike’s information criterion (AIC) and Akaike’s weight (w) were used to compare and rank a total of the 21 competing models and to estimate which of them best fit the data (Franklin et al. 2001; Johnson and Omland 2004). The model with the lowest AIC was selected and plotted (Franklin et al. 2001; Johnson and Omland 2004). All analyses were performed using R program 3.3.1, 64 bits (https://www.R-project.org).

The relationships between the total length of predator and prey were evaluated by analyzing the presence of more than a single slope across the whole distribution of the response variable by fitting quantile regression models (Koenker and Bassett 1978; Cade and Noon 2003). The total length of pelagic and demersal fish consumed was used to test the hypothesis that prey size increased in accordance with the size of the Patagonian toothfish D. eleginoides. Regressions of 10, 50, and 90% quantiles were fitted to test the minimum, medium, and maximum increase of prey size consumed with increasing TL of the predator, respectively (Cade and Noon 2003). The analyses were performed with quantreg R package (Koenker 2007).

Results

From a total of 441 specimens sampled, 318 (VI: 27.89%) ranging from 38 to 190 cm TL (Fig. 2a) contained food in their stomachs. The VI was 27.69% and 28.26% in the west and east region, respectively. The WLR indicated that the Patagonian toothfish had isometric growth (b = 3) (Fig. 2b). The sample sizes were sufficient to describe diets in all groups considered and to make statistical analyses as the cumulative prey curves reached an asymptote (Online Resource 2). The Patagonian toothfish D. eleginoides fed mainly on fish, followed by cephalopods and other invertebrates (Table 1). Among fish, the most important were the morid cod Notophycis marginata, myctophids, large rattail Macrourus holotrachys, notothenids Patagonotothen ramsayi, hoki Macruronus magellanicus, and small rattail Coelorinchus fasciatus (Table 1). One case of cannibalism was registered in one Patagonian toothfish of 190 cm and 79.66 kg that consumed another specimen of 107 cm and 11.16 kg. The cephalopods were mainly represented by the squid Onykia ingens and the small-sized squid Doryteuthis gahi (Table 1). The most important within the other invertebrate group was the bathypelagic shrimp Acanthephyra pelagica (Table 1). The trophic level (TR) of the Patagonian toothfish D. eleginoides was 4.57. Juveniles specimens showed a TR of 4.22, whereas adults TR was 4.78.

Fig. 2
figure 2

a Total length frequency distribution of the Patagonian toothfish Dissostichus eleginoides with food in the stomachs, collected to study the diet in the southwest Atlantic Ocean, b Relationship of weight with total length (TL) of the Patagonian toothfish D. eleginoides showing exponential and isometric growth

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Table 1 Diet composition of the Patagonian toothfish Dissostichus eleginoides off Southwest Atlantic Ocean expressed by the percentage frequency of occurrence (%F), the percentage of number (%N), percentage of weight (%W), the percentage of Index of Relative Importance (%IRI), and the percentage of the Prey-Specific Relative Importance Index (%PSIRI)
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The pelagic fish were the main prey of intermediate size predators in the east region (Fig. 3a, Table 2), whereas demersal fish were more heavily consumed in the west region and by juvenile specimens (Fig. 3b, Table 2). The cephalopods were more consumed by adult specimens in the west region (Fig. 3c, Table 2). The bathypelagic shrimp Acanthephyra pelagica was more important in the diet of intermediate size Patagonian toothfish, and it was more important in the east region (Fig. 3d, Table 2).

Fig. 3
figure 3

Generalized linear models (GLMs) fitted for the number of the main prey of the Patagonian toothfish Dissostichus eleginoides off Southwest Atlantic Ocean, selected using Akaike’s information criterion, which explain changes in the consumption of a pelagic fish, b demersal fish, c cephalopods, and d shrimp Acanthephyra pelagica. The GLMs have negative binomial error distribution and a log link

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Table 2 Best generalized linear models that explain the consumption of the most important prey of the Patagonian toothfish Dissostichus eleginoides off Southwest Atlantic Ocean
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The minimum, medium, and maximum values of the total length of the pelagic fish consumed by the Patagonian toothfish D. eleginoides were independent of the TL of the predator (slope of the quantil 10% = 0.00; p = 1; slope of the quantil 50% = 0.02; p = 0.58; slope of the quantil 90% = −0.03; p = 0.38; Fig. 4a). On the other hand, minimum, medium, and maximum values of the total length of the demersal fish consumed by the Patagonian toothfish D. eleginoides were positively correlated with the TL of the predator (slope of the quantil 10% = 0.16; p < 0,001; slope of the quantil 50% = 0.37; p < 0,001; slope of the quantil 90% = 0.60; p < 0,001; Fig. 4b).

Fig. 4
figure 4

Quantile regressions of the total length of a pelagic fish and b demersal fish, with the total length of the Patagonian toothfish Dissostichus eleginoides off Southwest Atlantic Ocean. The dotted, solid, and dashed lines represent 10%, 50%, and 90% quantile regressions, respectively

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Discussion

The Patagonian toothfish Dissostichus eleginoides in the austral shelf break off the Southern Atlantic Ocean (Burdwood Bank/Namuncurá MPA surroundings, 53–55°S) foraged predominantly on pelagic and demersal fish. The diet also included cephalopods and other invertebrates such as shrimps. These results are in accordance with those reported for Patagonian toothfish in Kerguelen (Duhamel, 1981), central and southern Chile (Murillo et al. 2008; Sallaberry-Pincheira et al. 2018), Malvinas/Falkland Islands (Arkhipkin et al. 2003), Argentine continental shelf (Garcia de la Rosa et al. 1997), and in South Georgia and Shag Rocks (McKenna 1991; Barrera-Oro et al. 2005; Collins et al. 2007). However, other studies differed and showed higher consumption of crustaceans in Crozet Islands (Duhamel and Pletikosic 1983) and in South Georgia and Shag Rocks (Zhivov and Krivoruchko 1990; Garcia de la Rosa et al. 1997; Pilling et al. 2001; Xavier et al. 2002) and higher proportion of cephalopods in Macquarie Islands (Goldsworthy et al. 2002). These comparisons suggested an opportunistic or adaptive foraging behavior for the Patagonian toothfish D. eleginoides with diets influenced by the distinct prey availability in each region. Only one case of cannibalism was previously reported, where the remnants of a juvenile Patagonian toothfish were found in the stomach of one animal (Arkhipkin et al. 2003). Here, cannibalism accounted 26.14% in weight, as one Patagonian toothfish of 190 cm and 79.66 kg consumed another of 107 cm and 11.16 kg.

The trophic level of Patagonian toothfish indicated that it was tertiary consumer, or top predator (TR > 4), throughout the analyzed ontogeny. In addition, the trophic level of Patagonian toothfish increased with ontogeny from 4.22 in juveniles to 4.78 in adults. This was in accordance with previous studies which indicated that for most marine species, TR increased with length of the predator (Stergiou and Karpouzi 2002; Ebert and Bizzarro 2007). Given the different functional trophic groups identified in the Mediterranean Sea, the Patagonian toothfish could be classified as carnivorous with preference for fish and cephalopods (Stergiou and Karpouzi 2002). Since exploited marine ecosystems are characterized by a decline of the mean TR in landings (Pauly et al. 1998), the monitoring of the TR, the food web structure, and fisheries landings will be the most appropriate future management. It was already demonstrated the fishing down the food webs phenomenon by fisheries operating on the other species of the genus, the Antarctic toothfish D. mawsoni, along the Antarctic continental margin (Ainley and Pauly 2014).

The present work reported regional variations in the diet of the Patagonian toothfish: the pelagic fish and bathypelagic shrimp Acanthephyra pelagica were more consumed in the east region, whereas demersal fish and cephalopods were more consumed in the west one. These regional differences could be related to distinct differences in the prey availability between the two regions. The myctophids and bathypelagic shrimp A. pelagic exhibited a meso and bathypelagic distribution, reaching depths of about 2000 and 3500 m, respectively (Boschi et al. 1992; Catul et al. 2011); thus, they were more abundant in the eastern region and more consumed by the Patagonian toothfish there. Conversely, demersal fish and cephalopods are abundant species at the continental shelf end and shelf break (Brunetti and Ivanovic 1992; Brunetti et al. 1998; Cousseau and Perrota 2013) and more heavily consumed by Patagonian toothfish in the west region. Differences in the specific composition of the toothfish diet between Shag Rocks and South Georgia have been previously reported (Barrera-Oro et al. 2005; Collins et al. 2007). This pattern suggested a flexible and adaptive feeding behavior of the Patagonian toothfish that fed upon pelagic fish and crustaceans in a region, changing to feed on cephalopods and demersal fish where this type of prey increases its availability.

Ontogenetic dietary changes associated with total length and maturity stage of the Patagonian toothfish were confirmed. Pelagic fish and the bathypelagic shrimp Acanthephyra pelagica had the greatest importance in the diet of intermediate-sized Patagonian toothfish. Demersal fish were more heavily consumed by juveniles, and cephalopods were more consumed by adult specimens. In South Georgia Collins et al. (2007) reported that diet changed with size, with an increase in myctophid fish and krill as toothfish grow and disperse. The ontogenetic diet shifts appeared to be a universal phenomenon in fish as a consequence of the morphological changes that accompany growth (increasing mouth dimensions and stomach capacity, improvement in their locomotion ability, etc.) and allow to capture a broader range of prey size and types (Wootton 1990). Moreover, the preference of sexually mature specimens for cephalopods could have a positive effect on spawning and egg quality, since high concentration of polyunsaturated fatty acids were detected in this mollusk, mainly docosahexaenoic acid (DHA) and eicosapentaenoic acid (EPA) (Watanabe et al. 1984; de Moreno et al. 1998; Salman et al. 2007). This hypothesis has been previously proposed for the common hake Merluccius hubbsi, and suggested that the most marine bony fish diet switch to cephalopods registered is driven by these essential lipids for spawn and for the survival and growth of eggs and larvae, rather than functional limitations e.g., gape size (Macchi et al. 2013).

There was a positive relationship between the total length of the demersal fish consumed by the Patagonian toothfish D. eleginoides and the predator TL. The size of prey also increased with fish size in South Georgia and Shag Rocks, with a greater range of prey sizes consumed by larger fish (Collins et al. 2007). However, the total length of the pelagic fish consumed in the present work was independent of the TL of the predator. The lack of a positive relationship between predator and prey may be due to the morphological trait (size range) of each ecological prey type or to the biased range of Patagonian toothfish that fed on pelagic fish. For example, pelagic fish herein consumed represented narrow TL range (6–30 cm) in comparison with demersal fish (10–107 cm). In addition, the demersal fish were predated throughout ontogeny. On the other hand, the pelagic fish were heavily consumed by intermediate-sized Patagonian toothfish. These results reinforce the hypothesis that juveniles exhibited a bento-pelagic behavior, utilizing lipid deposits and reducing skeletal mineralization to attain near-neutral buoyancy in the absence of a swim bladder (Collins et al. 2010; Nelson et al. 2016). The Patagonian toothfish migrate into deeper water as they grow, and adults live in deep water (1000-2000 m) where they feed, moving only slightly shallower during the spawning season in July–August (Collins et al. 2010).