Phenodeviants of the Lumpfish Cyclopterus Lumpus (Cyclopteridae) and Their Survival S

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ISSN 0032-9452, Journal of Ichthyology, 2019, Vol. 59, No. 6, pp. 954–957. © Pleiades Publishing, Ltd., 2019.

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Phenodeviants of the Lumpfish Cyclopterus lumpus (Cyclopteridae) and Their Survival S. M. Rusyaeva, *, J. Kennedyb, and A. M. Orlovc, d, e, f, g aKamchatka Directorate for Technical Support of Maritime Supervision, Petropavlovsk-Kamchatsky, Russia bMarine and Freshwater Research Institute, Reykjavik, Iceland cRussian Federal Research Institute of Fisheries and Oceanography (VNIRO), Moscow, Russia dSevertsov Institute of Ecology and Evolution, Russian Academy of Sciences, Moscow, Russia eDagestan State University, Makhachkala, Republic of Dagestan, Russia fTomsk State University, Tomsk, Russia gCaspian Institute of Biological Resources, Dagestan Scientific Center, Russian Academy of Sciences, Makhachkala, Republic of Dagestan, Russia *e-mail: [email protected] Received May 27, 2019; revised July 9, 2019; accepted July 10, 2019

Abstract—Deviations in the development of the caudal peduncle in the lumpfish Cyclopterus lumpus are described. Data on abiotic and biotic conditions of lumpfish’s existence in the North Atlantic are generalized. The importance of a unique niche of lumpfish in the marine ecosystem, which allows fish with greatly reduced swimming abilities (functions) to survive, is shown in the case of specimens with skeletal abnormalities.

Keywords: lumpfish Cyclopterus lumpus, deviant, survival, pollution, oxygen, predators, North Atlantic DOI: 10.1134/S0032945219060146

The lumpfish Cyclopterus lumpus is a valuable com- aboard the research vessels of the Polar Research mercial species for fishery in the North Atlantic. Institute of Marine Fisheries and Oceanography Lumpfish is caught during the prespawning period for (PINRO) and the Marine and Freshwater Research caviar production; its annual supply to the world mar- Institute (Reykjavik, Iceland) in the Norwegian and ket varies from 3800 to 6000 t (Johanesson, 2006). Barents seas in 2002 and 2018 (Table 1, Fig. 1). Unfor- Lumpfish are not schooling fish, but they form aggre- tunately, their preservation and morphological analy- gations during feeding and spawning periods (Daven- sis were impossible in laboratory conditions and their port, 1985). The species is characterized by sexual study was limited to taking photographs and external dimorphism, which is expressed in its size; females are examination. considerably larger than males (Andriyashev, 1954). The data on the species morphology are limited to In addition, we used the material on the study of descriptions of typical specimens (Lampart-Kałużni- lumpfish larvae obtained as a result of incubating arti- acka and Heese, 2000; Kudryavtseva and Karamushko, ficially fertilized eggs (41000 eggs) in a 1-m in depth 2005). Despite the available data on different anatomi- netted cage installed in the sea in May 2004. cal anomalies in fish (Dawson, 1964, 1966, 1971; Daw- son and Heal, 1976), there is no information in the lit- RESULTS AND DISCUSSION erature regarding phenodeviants of lumpfish. The aims of this work are to document the data on Three specimens of lumpfish with an unusual body considerable anatomical anomalies and changes in the shape were caught in the Norwegian and Barents seas body shape of lumpfish affecting the dynamic charac- in 2002 and 2018. The caudal peduncle in specimen teristics of deviant specimens and to find possible one is shortened; the caudal fin is absent (Fig. 1a). The causes of their occurrence. caudal fin in specimen two (Fig. 1b) is composed of several rays in the form of corolla; the visible part of the caudal peduncle is absent; rays of the fin are MATERIALS AND METHODS attached to a massive part of the body. The caudal fin The study is based on three phenodeviant speci- and caudal peduncle are completely lacking in specimens of lumpfish caught in the course of trawl surveys men three (Fig. 1c).

954 PHENODEVIANTS OF THE LUMPFISH 955

Table 1. Characteristic of materials on the lumpfish Cyclopterus lumpus used in the paper Depth Length (TL), No. Region (coordinates) Date of capture Weight, g Sex of trawling, m cm 1 Norwegian Sea July 2002 0−20 ~25−30 – Male (?) (~68°00′−71°00′ N ~14°00′ E−3°00′ W) 2Barents Sea September 25−50 27 1050 The same (71°33′ N 47°00′ E) 2002 3 Norwegian Sea July 2018 0−34 22 – '' (66°05′ N 7°20′ W) TL is the total length.

Specimens two and three are sexually mature deviations during the embryonic period. The embryo- males, TL 27 and 22 cm, that usually corresponds to genesis of lumpfish occurs under natural conditions the age of 6–7 years (Kudryavtseva, 2008). The sex of and is guarded by a male that aerates the egg batch by specimen one was not identified. splashing water onto eggs using gills during 30–45 days (Mochek, 1973). Low oxygen content is probably a When analyzing deviations in the development of critical factor in lumpfish embryogenesis (Davenport, marine fishes' caudal fins and cases of a shortened fish 1983). It has been found that different body deformi- body, the researchers have identified the following ties in lumpfish larvae occur during incubation at reasons: effect of pollutants (Sloof, 1982; Bengtson warmer water temperatures (Imsland et al., 2019). et al., 1985; Westernhagen, 1988; Jawad, 2004); effect It should be noted that the effect of temperature on of storms (mechanical effect) on fish eggs that develop matter and energy transformations in the early onto- in the sublittoral zone (Pertseva-Ostroumova, 1961); genesis of lumpfish is complex and results, for exam- deterioration of oxygen conditions in part because of ple, in incomplete resorption of protein from the yolk high egg density (Turner and Farley, 1971; sac under increasing temperature and decrease in the Devauchelle et al., 1986); effect of extreme tempera- efficiency of utilization of the protein resorbed from tures (Milton, 1971; Koo and Jonhston, 1978). In all the yolk sac for the embryo growth (Novikov, 2000) cases, the researchers considered variants of the cau- that, in our opinion, does not exclude deviations in the dal peduncle deformities (deviations in the direction, body-shape development. Over the past two decades, decrease in the bone thickness). Our specimens have a under conditions of elevated temperatures in the shortened caudal peduncle without deviations in its North Atlantic Ocean (Saba et al., 2016), the increase direction. in the frequency of deviations may be suggested in fish An important (and initial) point of our study is the capable to a lesser degree of spatial and temporal finding of lumpfish larva with a shortened caudal changes in the spawning grounds. peduncle (a photo is not available; the specimen was There are experimental data on the negative effect similar to specimen two in the body shape) as a result of pollutants on embryogenesis and development of of experiments on artificial fertilization and passive lumpfish larvae (Hustad, 2008). Thus, in our view, the incubation of eggs without a male that caused 25% effect of pollutants on lumpfish spawning in the sub- mortality of embryos. This experiment, in our opin- littoral zone and a wide spectrum of physical and ion, is the key to understanding the occurrence of chemical conditions throughout their range provide

(a) (b) (c)

Fig. 1. Specimens of the (а–с, nos. 1–3) lumpfish Cyclopterus lumpus with a typical absence of the caudal peduncle (numbering is according to Table 1, photos taken by I. Prokopchuk, S.M. Rusyaev, and J. Kennedy).

JOURNAL OF ICHTHYOLOGY Vol. 59 No. 6 2019 956 RUSYAEV et al. high probability for the occurrence of deviations to trawl fishing, while food unattractiveness of males during the lumpfish’s embryonic period. decreases the risk of attacks by predatory pinnipeds Morphological anomalies of specimen one caught during the spawning period and increases the proba- in the Norwegian Sea may be the result of injury by bility of existence of male deviants. The answer to the fishing gear or predator attacks. Nevertheless, this question about the dependence of caudal peduncle specimen indicates the ability of lumpfish to survive anomalies on the sex (taking into account sexual poly- despite extremely reduced locomotor function. It morphism of lumpfish) and the effect of elevated water should be noted in this regard that some fishes temperature in the North Atlantic on the increase in attacked by predators (which survived) may increase the probability of anomalies’ occurrence in some fish their chances to survive due to their increased migra- species remains unanswered. Our conclusions con- tion activity, selectivity of habitats, etc. (Gunter and cerning possible reasons for manifestation of the Ward, 1961). The fact that all specimens were captured described anomalies in lumpfish are preliminary and with a pelagic trawl in the epipelagic parts of the Nor- require further studies. wegian and Barents seas where the biomass of predators is smaller than in the near bottom horizons possi- ACKNOWLEDGMENTS bly indicates a selective behavior of fish exhibiting the lowest locomotor function. We are grateful to Irina Prokopchuk (PINRO) for the help in collecting and processing the material on lumpfish The risk of tail injury in lumpfish up to the age of in the course of trawl surveys of fish in the Barents and Nor- 2 years seems to be the least. Larvae and fries of lump- wegian seas. fish are not found in the diet of young predators that also use the littoral complex of the Barents and Nor- wegian seas in their feeding (Fjøsne and Gjøsæter, COMPLIANCE WITH ETHICAL STANDARDS 1996). Juvenile lumpfish are not detected in the diet of the immature saithe Pollachius virens in fjords of the Conflict of interests. The authors declare that they have Kola Peninsula (Dolgov, 2005), which is the most no conflicts of interest. common fish in bays of the Kola Peninsula and Statement on the welfare of animals. All applicable inter- Northern Norway. national, national, and/or institutional guidelines for the care and use of animals were followed. 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