ISSN 0032-9452, Journal of Ichthyology, 2006, Vol. 46, No. 8, pp. 600–605. © Pleiades Publishing, Inc., 2006. Original Russian Text © V.V. Napazakov, V.I. Chuchukalo, 2006, published in Voprosy Ikhtiologii, 2006, Vol. 46, No. 5, pp. 630–635.

Feeding of Soft Sculpin Malacocottus zonurus (Psychrolutidae) in the Western Bering Sea V. V. Napazakov* and V. I. Chuchukalo Pacific Research Fisheries Center—TINRO-Tsentr, per. Shevchenko 4, Vladivostok, 690950 Russia *E-mail: [email protected] Received February 8, 2005

Abstract—The feeding of the soft sculpin Malacocottus zonurus dwelling on the shelf and in the upper part of continental slope of the western Bering Sea is studied from materials of trawl surveys in the years 1998–2000. Description of its food composition depending on the fish size is given. It is found that basically polychaetes, decapods, amphipods, mollusks, and fishes serve as its food. When the soft sculpin reaches a length of 15– 20 cm, its feeding type changes. DOI: 10.1134/S0032945206080078

The soft sculpin Malacocottus zonurus belongs to the family of tadpole sculpins (Psychrolutidae). It dwells in the near-bottom waters of the shelf and upper zone of the continental slope of the northern Pacific (Fedorov, 1973; Sheiko and Fedorov, 2000; Tokranov and Orlov, 2001a; Fedorov et al., 2003). Being the most massive representative of the family which, by Borets’s data (2000), includes 6 genera and 13 species in the Far Eastern seas, it can reach relatively high numbers in certain areas of this region. So, in 2000 in the KaraginOlutor area, its biomass made up 3.12% of the total biomass of the bottom ichthyocene (Gavrilov and Glebov, 2002). The available published data on its feeding are limited in most cases to food spectra, and they concern the other areas of the northern Pacific (Jewett et al., 1989; Mito et al., 1999; Chuchukalo et al., 1999; Tokranov and Orlov, 2001b; Yang, 2003). It is known that the soft

sculpin become prey of many predatory fishes. So, for example, there are noted cases of finding it in the food of the Simushire liparid Polypera simushirae (Orlov and Pitruk, 1996), Aleutian skate Bathyraja aleutica, spotted skate B. maculata, Matsubara skate B. matsubarai, blackcod Anoplopoma fimbria (Orlov, 1997a; 1997b), cod Gadus macrocephalus (Napazakov et al., 2001), threadnose skate B. parmifera (Chuchukalo and Napazakov, 2002), and halibut Hippoglossoides stenolepis (Orlov, 1998). From the results of three trawl surveys in the period 1998–2000, the authors of the present article consider the food spectra and estimate the daily rations and trophic status of the soft sculpin dwelling on the shelf and in the upper part of the continental slope of the western Bering Sea.

N 64° Gulf of Anadyr

62° Gulf of Karagin

200

Gulf of Olyutor 200

60°

1998 1999 2000 Isobath of 200 m

BERING SEA

58° 166°

168°

170°

172°

174°

176°

178°

180°

E

Places of sampling in 1998 (August–September), 1999 (September–October), and 2000 (October–November).

600

FEEDING OF SOFT SCULPIN MALACOCOTTUS ZONURUS (PSYCHROLUTIDAE)

601

Table 1. The food composition (% of weight) of the soft sculpin Malacocottus zonurus depending on the body length in the western Bering Sea in August–September, 1998 Size groups, cm

Food composition

10–15

Spongia Coelenterata Polychaeta Polychaeta fam. gen. sp. Nereis sp. Echiurida Echiurus sp. Euphausiacea gen. sp. Amphipoda Ampelisca sp. Anonyx sp. Amphipoda fam. gen. sp. Decapoda Pandalus borealis Argis crassa Caridea fam. gen. sp. Chionoecetes opilio Pagurus spp. @ Mollusca Yoldia amygdalea Yoldia sp. Macoma sp. Buccinidae gen. sp. Gastropoda gen. sp. Gonatopsis borealis Octopoda gen. sp. Ophiuroidea Ophiura sp. Ascidiacea fam. gen. sp. Asteroidea fam. gen. sp. Pisces Malacocottus zonurus Other fishes ‰ Average index of fullness, ‰ Number of stomachs, specimens Number of samples Portion of empty stomachs, %

15–20

20–25

– –

1.9 –

– 0.05

– 0.0

– –

– 3.7

5.4 0.4

10.2 2.0

55.7 –

30.9 –

2.3 4.5

– –

– 14.2 2.9

– 1.9 5.1

0.3 0.5 0.8

– – 1.0

17.7 – – 2.9 – –

– 3.9 47.7 – – 4.9

0.4 – 13.0 36.0 0.6 –

– – 12.3 10.5 2.2 –

1.5 – 0.7 – – 4.4 –

– – – – – – –

1.2 – – 5.0 + 16.6 2.3

– 11.7 – – – – 3.9

– – –

– – –

– – 243 22 2 9.1

– – 315 27 3 7.4

MATERIAL AND METHODS The collections of stomachs of soft sculpin carried out in three complex expeditions of TINRO-tsentr into the western Bering Sea in the months August–NovemJOURNAL OF ICHTHYOLOGY

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1.1 0.4 0.05 – 9.0 250 45 7 4.4

25–30

– – – 7.8 38.4 262 21 4 9.5

ber in the years 1998–2000 served as material for this article. The area of sampling in 1998–2000 included the lower part of shelf and upper part of the slope within the range from 71 to 638 m in the Olyutor and Karagin gulfs and Koryak coast (see figure).

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NAPAZAKOV, CHUCHUKALO

Table 2. The food composition (% of weight) of the soft sculpin Malacocottus zonurus depending on the body length in the Gulf of Olyutor in September–October, 1999 Food composition Actinia fam. gen. sp. Polychaeta Polychaeta gen. sp. Maldanidae gen. sp. Nephthys sp. Brada sp. Travisia sp. Lumbriconereis sp. Nereis virens Amphipoda Anonyx nugax Pardalisca cuspidata Rhachotropis aculeata Stegocephalus inflatus Stegocephalus sp. Gammaridae gen. sp. Mysidacea Amblyops sp. Decapoda Hippolytidae gen. sp. Crangon dalli Crangonidae gen. sp. Chionoecetes opilio Chionoecetes sp. Hyas coarctatus alutaceus Mollusca Bivalvia gen. sp. Gastropoda gen. sp. Cephalopoda gen. sp. Asteroidea fam. gen. sp. Ophiuroidea Ophiopholis aculeata Pisces Other components ‰ Average index of fullness, ‰ Number of stomachs, specimens Number of samples Portion of empty stomachs, %

Size groups, cm 5–10

10–15

15–20

–

–

–

19.1 – – – – – –

23.5 – 10.4 – – – –

29.8 5.3 21.2 – – – –

7.0 3.7 – 3.5 3.5 4.2 2.1

7.7 – 5.7 – – – 2.8

8.2 – 3.2 8.8 – 17.4

8.2 – – – 8.6 3.2

7.6 – – – 9.4 –

3.6 0.7 – 1.5 – –

10.7 – – – – –

–

–

–

–

6.2

20–25

25–30

9.1

–

20.6 – – 9.4 – 4.4

9.6 – 2.5 – 4.7 1.7

7.1 4.6 2.4 – – 4.7

4.6 – 1.5 0.7 – 5.4

– – – 14.4 – 2.8

– – – –

– – – –

– 0.9 2.4 –

33.0 5.7 1.5 1.4

50.3 – – –

– – 8.9 269 23 3 0

– 3.1 18.3 175 27 3 0

– – 4.6 190 20 2 5.0

2.8 – 4.5 277 26 2 0

– 2.8 2.8 144 9 2 0

The trawl surveys were carried out with the bottom trawl whose horizontal and vertical openings were respectively 16–17 and 5 m. The mesh size of the smallmeshed insertion was 10 mm.

The samples for feeding were processed in accordance with the VNIRO Manual for methods (1974) and TINRO Guide (1986). The length of individuals (fork length) and weight were measured to an accuracy of JOURNAL OF ICHTHYOLOGY

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Table 3. Food composition (% of weight) of the soft sculpin Malacocottus zonurus depending on the body length in the Karagin–Olyutor region in October–November, 2000 Size groups, cm

Food composition

15–20

Actinia fam. gen. sp. Polychaeta fam. gen. sp. Ctenophora fam. gen. sp. Echiurida Echiurus sp. Amphipoda Amphipoda fam. gen. sp. Hyperia sp. Anonyx nugax Decapoda Pandalus borealis Pandalus sp. Argis lar Chionoecetes opilio Pagurus sp. Mollusca Gastropoda gen. sp. Bivalvia gen. sp. Teuthida Octopodidae gen. sp. Ascidiacea fam. gen. sp. Ophiuroidea Ophiura sarsi Pisces gen. sp. Other components ‰ Average index of fullness, ‰ Number of stomachs, specimens Number of samples Portion of empty stomachs, % Daily ration, % of weight of the body

20–25

25–30

30–35

– 9.9 –

– – –

– 15.4 0.5

4.0 56.0 1.9

4.9

–

–

30.0

2.0 – 2.0

0.5 1.4 0.5

– – 5.3

0.1 – –

4.0 0.1 25.4 8.7 39.8

8.5 – 4.3 69.9 –

8.8 – – – –

– – – – –

0.2 0.7 0.4 1.4 –

– – – 5.8 –

– – – 6.9 –

– – – 5.0 3.0

0.4 0.1 – 213 54 7 9.3 3.6

– 3.6 5.5 334 25 3 16.0 –

– 61.3 2.0 287 22 3 22.7 –

1 cm and 1 g, respectively. The size groups were formed so that the group of 10–15 cm combines the individuals with a body length greater than 10 cm and includes the value of 15 cm exactly, and so on. The sample included the stomachs taken from individuals of the group of the same size from one trawl. The total mass of stomach contents and individual food components of each sample were weighed to an accuracy of 0.1 g. The ration was calculated by the Novikova methods (1949) modified by us (Chuchukalo and Napazakov, 1999). RESULTS AND DISCUSSION In 1998–2000 in the western Bering Sea in trawl catches, the soft sculpin was represented by individuals JOURNAL OF ICHTHYOLOGY

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– – – 373 10 1 0 –

with a length from 4.5 to 39 cm. They occurred in the depth range from 71 to 638 m, and maximum catches were noted at the isobaths from 200 to 344 m. To judge from our data, when the depth of fishing increased, the values of minimum length of the soft sculpin sequentially decreased: from 15.4 cm at depths up to 150 m to 8.9 cm at depths greater than 300 m. At the same time, the maximum fish length practically did not change. Both by the data of Chuchukalo et al. (1999) and by the data of Tokranov and Orlov (2001b), the maximum length of soft sculpin in the catches exceeded significantly the size limits (21 cm) specified in the publications by Borets (2000) and Novikov et al. (2000). Various benthic and nectobenthic animals (polychaetes, decapods, amphipods, mollusks, and fishes) serve

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as a food for soft sculpin in the western Bering Sea. In 1998, the individuals of 10-15 cm in length had various feeding, with echiurids, shrimp Pandalus borealis, and amphipods serving as its basic food. The echiurids and decapods were the basic ration for the individuals with a length from 15 to 20 cm. Decapods (mainly the juvenile Tanner crab Chinoecetes opilio), mollusks (mainly the northern squid Gonatopsis borealis), polychaetes, and fishes were a basic food in soft sculpin larger than 20 cm. In the soft sculpin with a length from 25 to 30 cm, we noted cannibalism (Table 1). In 1999, the soft sculpin also fed on benthic and nectobenthic organisms such as polychaetes, amphipods, decapods, mollusks, and fishes. The portion of mollusks in the composition of their food components increases and the portion of decapods and amphipods decreases when the fish length increases (Table 2). In 2000, soft sculpin as long as 20 cm mainly fed on decapods (chiefly hermit crabs) and polychaetes (Table 3). In addition, individuals larger than 20 cm fed actively on fish, and the Tanner crab predominated among decapods. The mysids, euphausiids, actiniae, ophiurans, and comb-jellies belong to the less significant food objects. The small species of mollusks and amphipods are important in the feeding of the younger age groups; with growth, the soft sculpin begins to consume more polychaetes, crabs, mollusks, and fishes. The noted age-dependent changes occur when the soft sculpin reaches a length of 20 cm, and those appear mainly due to the fact that crabs replace shrimp, and the portion of mollusks and fishes increases. In autumn in the western Bering Sea, the soft sculpin feeds actively. The average value of the index of fullness of stomachs (IFS) is within the range from 175 ‰, and the portion of empty stomachs is less to 373‰ than 20%. The daily ration of this species estimated by us made up 3.6% of the body weight of the fish of the size group of 15–20 cm (Table 3). The results of our investigation generally agree with the published data on the feeding of the soft sculpin from the other regions of the northern Pacific. So, as is known from the report by Mito et al. (1999) that in the eastern Bering sea the juvenile M. zonurus mainly feeds on polychaetes and gammarids; the Tanner crab (Chionoecetes tannery) and sea-cucumbers are present in the ration of the larger individuals. According to Yang’s data (Yang, 2003) in the area of the Aleutian Islands, polychaetes are the basic food constituting 43% of all contents of the soft sculpin stomachs. Shrimps and gammarids also fall into the group of important components constituting respectively 15 and 20% of the stomach content. The soft sculpin also consumes comb-jellies (5%), ophiurans (4%), and squids (2%). In the Pacific waters of southeastern Kamchatka and the northern Kurils, it mainly feeds on gastropods and octopodes (more than 50% by weight) and polychaetes

(16.8%) (Tokranov and Orlov, 2001b). In the northern parts of the Sea of Okhotsk, by the data of Chuchukalo et al. (1999), the soft sculpin has a broad food spectrum. Individuals smaller than 15 cm in length mainly eat polychaetes and mollusks; fishes of medium sizes feed on polychaetes and shrimps; and large individuals eat fish, shrimp, and mollusks (including the Commander squid Berryteuthis magister). Thus, the soft sculpin has a broad food spectrum in all the investigated regions. Our observations during the summer–autumn period in the years 1998–2000 showed that the juvenile (5–15 cm) mainly eats small benthic organisms, i.e., polychaetes and amphipods. When the soft sculpin reaches a length of 15–20 cm, its feeding type changes. In spite of the fact that the benthic objects are still included in its ration, certain nektonic and nektobenthic animals, fishes, octopodes, squids, and crabs begin to predominate in the food. ACKNOWLEDGMENTS The authors are grateful to N.A. Kuznetsova and A.M. Slabinskii, the research workers of the TINROtsentr, who took part in collecting the materials. The work is supported in part by the Russian Foundation for Basic Research (grant no. 03-04-49540). REFERENCES 1. L. A. Borets, An Annotated List of Fish from Far Eastern Seas (TINRO-Tsentr, Vladivostok, 2000) [in Russian]. 2. V. I. Chuchukalo and V. V. Napazakov, “On the Methods of Determining Diurnal Rations of Feeding and the Digestion Rate in Predacious and Benthos-Eating Fish,” Izv. Tikhookean. Nauchno-Issled. Inst. Rybn. Khoz. Okeanogr. 126, 160–171 (1999). 3. V. I. Chuchukalo, V. V. Lapko, N. A. Kuznetsova, et al., “Feeding of Bottom Fish on the Shelf and the Continental Slope of the Northern Part of the Sea of Okhotsk in Summer 1997,” Izv. Tikhookean. Nauchno-Issled. Inst. Rybn. Khoz. Okeanogr. 126, 24–57 (1999). 4. V. I. Chuchukalo and V. V. Napazakov, “Feeding and Trophic Status of Mass Species of Skates (Rajidae) from the Western Part of the Bering Sea,” Izv. Tikhookean. Nauchno-Issled. Inst. Rybn. Khoz. Okeanogr. 130, 422– 428 (2002). 5. V. V. Fedorov, “Ichthyofauna of the Continental Slope of the Bering Sea and Some Aspects of Its Origin and Formation,” Izv. Tikhookean. Nauchno-Issled. Inst. Rybn. Khoz. Okeanogr. 87, 3–41 (1973). 6. V. V. Fedorov, I. A. Chereshnev, M. V. Nazarkin, et al., Catalog of Marine and Freshwater Fish from the Northern Part of the Sea of Okhotsk (Dal’nauka, Vladivostok, 2003) [in Russian]. 7. Guide on Study of Feeding in Fish, Ed. by V. I. Chuchukalo and A. F. Volkov (TINRO, Vladivostok, 1986), p. 32 [in Russian]. 8. G. M. Gavrilov and I. I. Glebov, “Composition of Bottom Ichthyocenosis in the Western Part of the Bering Sea JOURNAL OF ICHTHYOLOGY

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Translated by G. B. Medveshchuk