INTRODUCTION

Over the last 50 years, fishing has moved from the continental shelf areas toward the deeper waters. Therefore, the marine biota in these aquatic ecosystems, including fish comunities, is under threat across seas (Vinnichenko et al., 2005). Deep-water trawling is the least sustainable type of fishing. There are many examples of its results in fish stock depletion (Clark and Koslow, 2007; Pitcher et al., 2010). The principal requirements to data on fishing activity for the deep-water species are not different from the requirements to fishing deal for any other fish stocks, since it is necessary to know the life-cycle characteristics of the target species and afford to monitor the dynamics of its population (Francis and Clark, 2005). A considerable number of deep-water fish species have been overfished because of unavailable data on their life cycles. Therefore, fish stocks in many global ocean regions are depleted (Watling et al., 2011). In addition, it concerns the grenadier fish (Devine et al., 2012).

Grenadier fish are recorded practically in all the trawl and multi-level continental-shelf fishery systems worldwide, which includes the most frequent bycatches in deep-water fishing operations (Tuponogov, 1991, 2018; Tuponogov et al., 2008; Orlov and Tokranov, 2008, 2019). The giant grenadier Coryphaenoides pectoralis (Gilbert, 1892) (Gadiformes: Macrouridae) is caught in the Northern Pacific as both a bycatch species in commercial fishing for the Greenland turbot Reinhardtius hippoglossoides and the target species. It inhabits the bottom water layers. However, the species can be found in a wide depth range of 140–3500 m (Tuponogov and Novikov, 2016). Until the mid of 1970s, the giant grenadier fish were considered most abundant at depths of between 700–1100 m (Novikov, 1970, 1974). Later, the depth range was extended to 600–1700 m (Тupohogov, 1991, 2018; Tuponogov et al., 2008). Despite the increasing interest of fisheries enterpreneurs in this object and the development of fishing gear technology, many patterns of distribution and biology of the giant grenadier remain scarcely studied. The major reasons comlicating the studies are great water depths inhabited with the species and seabed complex environments, which makes it impossible for bottom trawling for fish stocks across the most habitat area (Tuponogov, 1991; Оrlov, 2007; Orlov and Tokranov, 2008; Tuponogov and Novikov, 2016). At present, the highest catches of the giant grenadier inhabiting the North Pacific zone are recorded in the Bering Sea (Clausen and Rodgveller, 2010; Тuponogov and Novikov, 2016; Rodgveller, 2020).

First information available in the literautre on biology and ecology of the giant grenadier inhabiting the Bering Sea appeared after the Bering Sea expedition in 1962 (Kaganovsky, 1965; Novikov, 1970, 1974). Later, a range of authors supplemented the research study outcomes for biology of the grenadier from the Bering Sea (Тuponogov and Kurennoy, 1986; Тuponogov, 1991, 2001; Orlov, 2003; Tuponogov et al., 2008; Orlov et al., 2007, 2012; Orlov and Tokranov, 2008, 2019; Тuponogov and Novikov, 2016). Considering the assignment of the greanadier to the longest-living species (Novikov, 1970, 1974; Тuponogov, 1991; Burton, 1999; Hutchinson and Anderl, 2012), the data for 1963–2020, used in this survey, can allow us to understand some aspects of its life cycle and distribution more completely.

The objectives of the research survey are to summarize the long-term data and to analyse the new data on the spatial distribution and the life cycle specificity of the giant grenadier inhabiting the Northwest Bering Sea.

MATERIALS AND METHODS

The survey was conducted based on the sampled material collected in the marine research and fishing expeditions undertaken by the All-Russia Research Institute of Fishery and Oceanography, Pacific Branch (TINRO) in the Bering Sea in 1963–2020. The data on 37 000 catches performed with the bottom and multi-depth trawls at depths of between 0–1200 m were processed (Figs. 1, 2). The information on the species size composition, sex ratio, and life cycle is provided for the Northwest Bering Sea, where the most catches were performed. The data on the sex ratio and sexual maturity in the giant grenadier are provided based on the sampled fish measurements and dissection of > 55 thousand specimens. The fish total length (TL) from the snout tip to the caudal-fin ray tip was measured.

Fig. 1.
figure 1

Distribution of TINRO trawl stations and exploratory fishing expeditions in the Bering Sea over 1963–2020 through the water depths relative to the trawl horizon-scale routing (THR): ()—sampling trawl. Here and in Figs. 3 and 4: ()—map chart of continental shelf.

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Fig. 2.
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Horizintal distribution of TINRO trawl-stations and exploratory fishing expeditions in the Bering Sea over 1963–2020: ()—bottom trawling to a depth of 0–1200 m.

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The gonad maturity stages were determined with the microscopy techniques according to a scale based on a range of visually different traits including the species size, body shape, color, elasticity, vascular development, and egg shape (Аlekseev and Alekseeva, 1996). In order to provide the verified data by dating the sexual maturity onset, all the females of >85 cm TL with gonads at maturity stage II and all the specimens with gonads at maturity stage VI–IIIa were combined with the females with gonads at maturity stage IIIa.

The produced data on captures were converted into the standard comparable values for distribution density in specimens/km2 with the Volvenko method (1998). It was made with formula: \(\frac{N}{A}\frac{p}{k} = \frac{{Np}}{{1.825{v}t \times 0.001ak}},\) where N—fish number per capture, specimens, A—area trawled, km2, t—duration of trawling, h; v—trawling speed, miles/h, 1.825—coefficient for conversion from miles to kilometers, а—horizontal trawl mouth opening, m, p—ratio of trawled hydrobiont stock height to vertical trawl opening (the p-value was taken equal to 1, cause of unavailable acoustic data for the target species and information on vertical trawl opening for certain trawl operations), and k—capture rate coefficient (k = 0.5 for the giant grenadier (Shuntov et al., 2006)).

Software Surfer v. 13.0.383 (Golden Software, USA) was used to build the map charts for the species distribution and occurrence. Diagrams showing the dinamics of male and female seasonal distribution in the water column were based on the depth-weighted average estimated as the sum of multiplication products of species densities (specimens/km2) and depths of trawling, assigned to the number of all the specimens sampled for research survey during a certain month. The depth-weighted average gives an idea about the maximum captures at certain depths for any given month within the indicated depth range. Ratios between the specimens with gonads at different maturity stages were estimated for each month throughout the range of water depth over the whole survey period. The graphs are created with the Python 3.0 (Python Software Foundation, USA) and the Matplotlib.

RESULTS

Giant grenadier distribution by different age groups. The giant grenadier is spread in the Bering Sea off the Commander and Aleutian Islands in the south toward Cape Navarin in the North. The largest aggregations of this species fish were found in the water areas over the Aleutian and Commander depression areas at the base of the continental shelf break and along the submarine Shirshov Ridge separating the Aleutian and Commander basins (Fig. 3a). The giant grenadier can be found in waters at depths from 99 m to the deepest layer of the explored depth zones within the surveys. Thus, the highest-density aggregations characterized by the median densities varying between 1800 and 2200 specimens/km2 are formed in the water layers at depths of between 500–1200 m along the continental slope. The fewer giant grenadier fish, which do not form any aggregations, can be found in the meso-bathypelagic zones at 140 to 1000 m depths of the water masses across the indicated depessions above the depths of between 500–4000 m (Fig. 3b).

Fig. 3.
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Distribution density of the giant grenadier Coryphaenoides pectoralis in the Bering Sea: (a) horizontal and (b) vertical distribution of density in the water column relative the trawl horizon-scale routing (THR).

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The fish larvae of ≤10.0 cm TL were recorded occasionally in the Central and Northwest Bering Sea (Fig. 4), in the bathypelagic zone at depths of between 160–300 m (Fig. 4d). Low frequencies of occurrence of such specimens are caused by the low capture rate coefficient and, probably, the complete destruction of soft tissues of juvenile fish caught by trawl gears.

Fig. 4.
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Distribution density of different-size specimens of the giant grenadier Coryphaenoides pectoralis in the Bering Sea: (а–c) horizontal distribution and (d–f) vertical distribution of density in the water column relative the trawl horizon-scale routing (THR). Fish total length (TL), cm: (а, b) < 30; (c, d) 30–40; (e, f) > 40.

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Fig. 4.
figure 5

(End.)

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The juvenile fish of a larger size (10.1–20.0 cm TL) are also found occasionally in captures, however, more frequently at a larger depth range (250–800 m), sometimes, occurring over the continental shelf break or, probably, caught in trawl samples or arrangements (Fig. 4d). These specimens are widely spread across the sea area (Fig. 4a).

The specimens of 20.1–30.0 cm TL are recorded more frequently and in larger numbers in the multi-depth trawl captures within the depth range similar to depths for inhabiting the specimens of 10.1–20.0 cm TL (Fig. 4d). They occur mainly in the water masses over the Commander and Aleutian depressions, which do not appear to form dense aggregations (Fig. 4a). Most juvenile fish are recorded at the depths of between 300–500 m. However, it should be noted that a white dot caused by the missing data on the juvenile density at 500–800 m water depths in the survey is observed (Fig. 1). Most specimens of 30.1–40.0 cm TL leave the water masses for the bottom layers over the continental slope to inhabit within a narrow water-depth range (500–800 m), while small numbers of them may be found in the mesopelagic zone (Figs. 4b, 4e).

The giant grenadier of >40 cm TL is distributed mainly in the bottom water layers above the continental shelf break followed by the Commander and Aleutian depressions and along the Shirshov Ridge at the depth range of 300 m to the maximum water depth achieved in the survey. The specimens of this size group tend to aggregate generally in the water masses along the continental slope. Such aggregations may vary in density from 1 to 2500 specimens/km2, while the density of specimens of this size group across the bathypelagic zone above >1500 m depth is no more than 25 specimens/km2 (Figs. 4c, 4f)

Dynamics of variation in gonadal maturation in a population portion of sexually mature fish. It has been shown above that the specimens of >40 cm TL transit to the bottom water lifestyle along the continental slope to reach sexual maturity correlated with growth. Thus, males and females reach sexual maturity at 65–70 and 70–80 cm in length, respectively (Fig. 5). Fig. 6a shows size composition of a population proportion of sexually mature fish.

Fig. 5.
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Dynamics of sexual maturity in females (a) and males (b) of the giant grenadier Coryphaenoides pectoralis in the Bering Sea: (―) immature specimens, (‑ ‑ ‑) mature specimens.

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Fig. 6.
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Size composition (a) and sex ratios for all the fish (b) and the specimens with gonads at maturity stage V (c) in the giant grenadier Coryphaenoides pectoralis in the survey bottom-trawl catches in the Bering Sea: (\(\blacksquare \))—males (average tota length of 55.3 cm), ()—females (88.1 cm).

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The percentage of female fish caught by bottom trawling along the continental slope sea floor is higher, at ratio 91 : 9 (Fig. 6b). In addition, the percentage ratio of males to females with gonads at maturity satge V comprises 35 : 65 (Fig. 6c).

The datasets over the total period of observations were monthly analyzed in order to understand thoroughly the spatial-temporal patterns of fattening and spawning in the population proportion of the sexually mature giant grenadier fish (Table 1, Fig. 7).

Table 1. Seasonal dynamics of sexually mature specimens of the giant grenadier Coryphaenoides pectoralis with gonads at different maturity stages in the survey bottom and different-depth trawl catches in the Northwest Bering Sea in 1963–2020
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Fig. 7.
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Seasonal dynamics of the sex ratio in the giant grenadier Coryphaenoides pectoralis and the weighted average depth of its occurrence: ((―)—all the fish, (- - -)—only fish with gonads at maturity stage V) in the Northwest Bering Sea in 1963–2020; above—all the fish, below—only fish with gonads at maturity stage V. See Fig. 6 for the rest of the legend.

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In the winter season, there are few giant grenadier specimens with gonads at maturity stage V. With respect to the female fish, the proportion of female specimens with gonads at maturity stages II and IIIa is larger, while there is small numbers of females with gonads at maturity stages IIIb and IV. The male fish with gonads at maturity stages III and IV were generally recorded. The sex ratio of fish specimens at the explored depths is biased toward females (Table 1, Fig. 7).

In the spring season, the females were dominant in catches at the average depth above 700 m (Fig. 7). However, if the female specimens with gonads at maturity stages II and IIIa were dominant in March, an increase in the female specimens with gonads at maturity stages IV, V, and VI can be observed in April and May. Thus, an increase in the number of females with gonads at maturity stage V may be associated with increasing the depth of trawling (Table 1). The number of male fish with gonads at maturity stage V also tends to increase from March to May with increasing the depth of trawling. Howerver, it is most likely associated with the first increased spawning activity in April–May. The male-to-female ratio is biased toward the males with increasing the depths of trawl operations, while the sex ratio between the specimens with gonads at maturity stage V remains at the same level.

In the summer season, any significant variations in ratios for specimens with gonads at different maturity stages are not observed, excluding a large proportion of males with gonads at maturity stage VI in June (Table 1), which tends to reduce throughout the summer months, exept August, when it slightly increases.

In the early autumn season (September), a proportion of the giant grenadier females ready to spawn with gonads at maturity stage V can reach 10–14%, while the proportion of females with gonads at maturity stage IV reduces at the reference sharp rise in the proportion of females with gonads at maturity stage VI (Table 1). With respect to the male fish, the proportion of male specimens ready to spawn with gonads at maturity stage V reaches 30–45%, despite a reduction in the total number of males in catches, which is associated with decreasing the depths of trawl surveys. The overall sex ratio between the giant grenadier males and females remains the same, while the sex ratios between the specimens with gonads at maturity stage V vary from month to month in this period. Thus, a proportin of females with gonads at this maturity stage is higher than that in the males in September–October (Fig. 7).

Spawning. The giant grenadier specimens with gonads at maturity stage V were recorded in catches throughout the year, excluding January and November, since the surveys were conducted no deeper than 700–750 m in these months. Therefore, this fact and an insignificant number of trawl operations cannot provide the opportunity to assess the spawning times and depths accurately. The male and female fish with gonads at maturity stage V were found at depths of between 600–1140 m. The proportion of females with gonads at maturity stage V comprises approximately ~1% throughout the year, tending to increase in the spring (May) and autumn (September) seasons to 9 and 14%, respectively. The males with gonads at maturity stage V can be also found thoughout the year. The proportion of such males is highest from April to October, comprising 24–77% (42%, on average), while the proportion in the winter season is lowest (Table 1). The sex ratio between the male and female fish with gonads at maturity stage V from February to August is biased toward males. Their proportion comprises 76%, on average. However, the proportions of spawning female fish in the autumn spawning activity intensified in September and October are higher than that in males, comprising 78 and 58% vs. 22 and 42%, respectively (Fig. 7).

DISCUSSION

Dustribution. The giant grenadier at different ontogenetic stages occupies different ecological niches within the entire Bering Sea from the Commander and Aleutian Islands in the south toward Cape Navarin in the north. The fertilized eggs of the giant grenadier are found in the water column above >400 m depth. It was shown with the deep-water survey extending from the Pasific side off the Kamchatka Peninsula to the Japanese Archipelago in 1976, the pollack surveys over the deepest parts of the Bering Sea and the Sea of Okhotsk (Tuponogov, 1991, 1997), and the Avacha Galf survey conducted lately (Buslov et al., 2006). The eggs are probably spread by the currents. In the observations published by Musienko as far back as 1963 and 1970 and Kashkina in 1965, they noted that the giant grenadier eggs, larvae of 14–18 TL, and juveniles were caught as every single specimen in the water masses above the depths of between 1000–3000 in the South Bering Sea off the Commander and Aleutian Islands. After hatching, the giant grenadier larvae and juvenile fish of <40 cm TL live the meso-bathypelagic lifestyle, spreading above the deepwater sea regions at the depth between 180 and 800 m, while most of them prefer the depths between 300 and 500 m, which do not appear to form any dense aggregations. Thus, the giant greanadier eggs and juveniles were previously found above the deep-water masses in the Avacha Gulf and above >400 m depth (Buslov et al., 2006; Saushkina, 2022). The species juvenil fish were recorded at the depths above 500 m in the Bering Sea (Novikov 1970, 1974; Аlferov, 2022; Alferov, 2022). With respect to the other sea regions, the species larvae were captured in the deepwater region of the Sea of Okhotsk (Tuponogov, 1991, 1997) and in the water masses at 530 m depth off the east coast of the Hokkaido Island (Endo et al., 2010). The giant grenadier juveniles may be carried by currents toward the shallow-water zones (Busby, 2005; Buslov et al., 2006). In addition, this pattern for juvenile fish distribution across the water masses is also typical for the other species of the family Macrouridae (Fukui and Tsuchiya, 2005).

The giant greandier fish reaching >40 cm TL start moving down toward the bottom layers. It was previously considered that settling on the bottom happens only after reaching 50–56 cm TL (Novikov 1970, 1974). The data based on the surveys show that later, the sexually mature specimens at a greater body length live the bottom lifestyle at depths in the range of 300 m to the maximum water depth achieved in the survey (1200 m) predominantly above the continental shelf break followed by the Commander and Aleutian depressions and along the Shirshov Ridge. These survey-based data meet the information on the depth range of 150–3500 m, indicated by the other researchers (Tuponogov, 1991, 2001; Orlov et al., 2012; Tuponogov and Kodolov, 2014; Tuponogov and Novikov, 2016). In the bottom water layer at the depths of between 500–4000 m, this species fish form the densiest aggregations, which median values vary from 1800 to 2200 specimens/ km2. In the water massess above the depths of between 500–4000 m, the giant grenadier can be found in the depth range of 140–1000 m in smaller numbers, which do not appear to form dense aggregations. The aggregation dense in the water masses over the continental slope may vary from 1 to 2500 specimens/km2, while the aggregation density of fish of >40 cm TL is not greater than 25 specimens/km2 in the bathypelagic zone over >1500 m depth. Thus, the similar results were previosly obtained (Shatunov et al., 2006). In addition, similar vertical migrations are typical of some other species of greandier fish at different stage of life cycle (Bergstad, 1990; D’Onghia et al., 2000).

Sex ratios. Comparing the weighted average depths of occurrence of the giant grenadier males and females, it becomes evident that femles are recorded in catches of bottom trawling at the water depths less than that for the male fish (Table 1). At the weighted average depths of less than 700 m below, the number of females is always larger than the male number. Their percentage ratio comprises approximately ~90 : 10. In addition, similar results were previously obtained based on the lower amount of data (Novikov, 1974; Tuponogov, 1991, 2001; Tuponogov et al., 2008; Orlov and Tokranov, 2008; Datsky, 2017). The dominance rate of females observed in the catches may be associated with the fact that males and females occupy different ecological niches (bathymetric ranges) in the deepwater habitat environments, which are only partiallly overlapped. In this context, the main habitats of the giant grenadier males probably occur at a range of depths down from 800 m, locating in the zone little accessable for bottom trawling, which is clearly shown with the example in May, when the proportion of males increased at the reference weighted average depth of >900 m, comprising 34% (Fig. 7). In addition, the other researchers (Novikov, 1970, 1974; Tuponogov, 1991) described the trend of increasing the proportion of males at the depths of >700–800 m. Moreover, the trend of increasing the male proportion with increasing the water depth probably remains across the habitats at a certain depth range, while the numerical superiority of males over spawning females can cause the occurrence of sexual competition. A similar pattern for a long-term presence of male fish on spawning grounds is typical of the pollack Gadus chalcogrammus (Shuntov et al., 1993; Fadeev and Ovsyznnikov, 2001) and the capelin Mallotus villosus (Velikanov, 2018).

The models for populations with such imbalanced sex ratios biased toward multiple males are typical of the roughhead grenadier Macrourus berglax, for instance, or the other species of grenadiers (Bergstad, 1990; D’Onghia et al., 2000).

Size composition. The giant grenadier males and females look slightly different from each other. However, sexually mature specimens of this species are different in the body size at the same age. Thus, the total length of males from the bottom trawls varies from 55  to 120 cm. The specimens of 75–90 cm TL represent the model group. Female fish is larger, comprising 50–180 cm TL, while the specimens of 80–105 cm TL are included into the model group. The survey-based datasets meet the statistics on ranges and maximum lengths previously indicated by Novikov (1970) and Tuponogov (1991, 2001) recording them up to 122 and 210 cm, respectively. Males and females reach sexual maturity at 65–70 and 70–80 cm TL, respectively, while Tuponogov (1991) indicated the female length-at-maturity of ~ 75 cm at which 50% of specimens reach sexual maturity.

Maturation. The maturing giant grenadier females and males use different habitats. Thus, the giant greandier females with gonads at early maturity stages (II and IIIa) can be found in catches throughout the year at the weighted average depth less than 650 m. Their proportion in the total number of females comprises 32–73%, while it tends to reduce with increasing the depth, which is probably caused by the fact that water massess at the depths of between 300–700 m along the continental slope provide habitats necessary for most female fish fattening. The proportion of females with gonads at maturity stage IIIb reaches the maximum values in catches from November to August (14–27%), while the minimum values are recorded in September, the period of spawning activities (up to 9%). The females with gonads at maturity stage IV can be found throughout the year. Their proportion comprises 14%, on average.

The proportion of males with gonads at maturity stages II and III is affected by significant variations from months to months, which is probably associated with variations in the explored depths in the surveys and statistical errors because of small sample sizes. The proportions of males with gonads in spawning (~32%, on average, at maturity stage V) and prespawning (~32% also, on average, at maturity stage IV) phases remain stable at high levels throughout the year. It should be noted that it is rather difficult to determine the male gonad maturity stage, since the morphological changes in testicular development are less exhibited than that in ovaries.

Spawning. Opinions of various researchers toward spawning dates between the giant grenadier populations are not equal. For instance, Novikov (1970, 1974) has indicated that spawning occurs throughout the year with increasing activity in the autumn–winter season. Tuponogov (1991) has later indicated that spawning takes place throughout the year, while its activity tends to increase in the spring–summer season. The other researchers refer to one or the other author’s concept (Buslov et al., 2006; Orlov, 2008; Datsky, 2017; Saushkina, 2022). In addition, the long-term period of spawning in the giant grenadier fish was also recorded in the East Bering Sea (Rodgveller et al., 2010).

CONCLUSIONS

The survey-based outcomes show that the giant grenadier spawning in the Bering Sea takes place throughout the year within the bottom layer, with two periods of peak spawning activity in the second half of a spring season and from the late summer season to the first half of an autumn season. Insignificant proportion of females tends to spawn in winter and summer seasons (up to 3%). Spawning activity increases in the spring season (up to 11% of female). This information coincides well with the data on the eggs from the giant grenadier recorded in the catches from the ichthyoplankton sampling nets in the deepwater horizon in the Avacha Gulf from the third ten-day period in April (Buslov et al., 2006) and the autumn season (up tp 19% females), which corresponds to the observations performed by Novikov (1970). Most males are ready to spawn throughout the year (on average, 32% males per month). Therefore, the number of male fish ready to spawn is larger than the female number throughout the year, except September and October. Considering the trend of increasing the proportion of males with increasing the water depth to >800 m, it may be supposed that giant greanadier spawning may be observed at greater depths, where ~90% male fish unaccounted from trawl surveys inhabit and the other ~60% females probably spawn. In order to clarify this assumption, the first author provided this published study collects additional information from the onboard observers for longline fishing for the giant grenadier at depths of between 800–1800 m at present. This additonal material should be collected at every 100-m depth in the depth range indicated above.

After spawning is complete, the females with gonads at mature stages VI and VI–IIIa can be found throughout the year, with two periods of peak quantity in April–May and in late August to early October. It is proven by the periods of spawning activity in the second half of a spring season and from the late summer season to the first half of the autumn season. In addition, increases in proportions of males spawned in June, August–September, and December can also indirectly indicate two spawning-season peaks indicated above (Table 1). The extended spawning season is also typical of the other species of the family Macrouridae. Thus, the spawning period in the species C. rupestris (Bergstad, 1990) and M. berglax (Murua and Motos, 2000), inahabiting the Atlantic Ocean, is extended for approximately half a year.