33 National Marine Fisheries Service Fishery Bulletin First U.S. Commissioner established in 1881 of Fisheries and founder NOAA of Fishery Bulletin Abstract—A total of 69 specimens of The first data on the diet and reproduction of Fedorov’s lumpsucker (Eumicrotremus fedorovi) caught on the continental Fedorov’s lumpsucker (Eumicrotremus fedorovi) shelf and slope of Simushir Island in the northwest Pacific Ocean were dis- Ilya Gordeev (contact author)1,2 sected and studied for stomach con- 1 tents. The Fedorov’s lumpsucker was Kristina Zhukova found to feed mainly on the young of Svetlana Frenkel1 fish species, including the walleye pol- lock (Gadus chalcogrammus), northern Email address for contact author: [email protected] lampfish (Stenobrachius leucopsarus), and northern smoothtongue (Leuro- 1 Russian Federal Research Institute of Fisheries and Oceanography glossus schmidti), crustaceans, such as 17 V. Kransnoselskaya Street Themisto pacifica, Primno macropa, Moscow 107140, Russia calanoids, gammarids, mysids, and caprellids, and squid. Histological analy- 2 Lomonosov Moscow State University ses of ovaries revealed iteroparity, deter- GSP-1 Leninskije Gory minate fecundity, group-sync hronous Moscow 119991, Russia ovarian development, and total spawn- ing. Testes were of an unrestricted lobu- lar type. Chorion and thick zona radiata of Fedorov’s lumpsucker correspond to the condition of eggs in specimens of other fish species that release demer- sal eggs. Absolute fecundity values The genus Eumicrotremus, 1 of 6 gen- et al., 2009; Berge and Nahrgang, of Fedorov’s lumpsucker in our study era of Cyclopteridae (Scorpaeniformes: 2013), lumpsucker species feed on var- were significantly less than those that Cottoidei), includes 18 valid species ious crustaceans, juveniles of squid have been reported for other species (Froese and Pauly, 2020). This genus species, pteropods, juveniles of fish spe- of Cyclopteridae. The results of this is distributed mostly in the northern cies, and polychaetes. Lumpsucker spe- study provide the first data on this little known species of this family. Pacific Ocean. Four species inhabit cies feed intensively throughout most subarctic and Arctic areas: pimpled of the year and have been reported to lumpsucker (E. andriashevi), leather- make diurnal vertical migrations in fin lumpsucker (E. derjugini), Atlantic the water column to follow their main spiny lumpsucker (E. spinosus), and food item (hyperiids), and this move- Newfoundland spiny lumpsucker ment pattern explains their regular (E. terraenovae). The Fedorov’s lump- presence in open water (Chuchukalo, sucker (E. fedorovi) inhabits the waters 2006; Antonenko et al., 2009). of the northern Kuril Islands off the The reproductive biology of Cyclopte- eastern coast of Russia (Mecklenburg ridae has been previously examined in and Sheiko, 2003) and has been rarely studies of the lumpfish (Cyclopterus recorded as bycatch in the area of the lumpus) and smooth lumpsucker (Apto- Kuril Islands. Lumpsucker species cyclus ventricosus) (Cox and Anderson, spend most of their lives away from 1922; Davenport, 1985; Kennedy, 2018; the shore. They can be found 100 km Zhukova et al., 2018). Information on from shore in the open waters of the the reproductive processes of other Pacific Ocean, before they return to members of Cyclopteridae is scarce and shallow waters (200–300 m) to repro- fragmented. Lumpsucker species pro- Manuscript submitted 12 August 2020. duce (Orlov, 1994; Chuchukalo, 2006). duce clusters of demersal adhesive Manuscript accepted 11 March 2021. No information on the diet of Fedor- eggs and spawn in coastal waters (at Fish. Bull. 119:33–40 (2021). Online publication date: 8 April 2021. ov’s lumpsucker was available prior to depths down to 300 m). After spawning, doi: 10.7755/FB.119.1.5 this study. According to existing records males guard the fertilized eggs on the diet of other Eumicrotremus (Mecklenburg and Sheiko, 2003; The views and opinions expressed or species (Tabunkov and Chernysheva, Panchenko and Balanov, 2020). Female implied in this article are those of the 1985; Orlov, 1994; Melnikov, 1995; Pacific spiny lumpsucker (E. orbis) and author (or authors) and do not necessarily reflect the position of the National Kuznetsova, 1997; Chuchukalo et al., spinous lumpfish (E. soldatovi) have Marine Fisheries Service, NOAA. 1999; Roshchin, 2006; Antonenko been reported to have died after a single 34 Fishery Bulletin 119(1) spawning, and males have been observed to guard egg Corp., Tokyo, Japan) equipped with a Leica DC 100 digital clutches and then die when the eggs they were guarding camera (Leica Microsystems, Buffalo Grove, IL) was used complete development or hatch (Orlov, 1994). It is diffi- for imaging. Diameters of oocytes and intracellular struc- cult, therefore, to determine if lumpsucker species feed tures were measured by using the software ImageJ, vers. during their entire life cycles. However, other representa- 1.51 (Rasband, 2018). tives of Cyclopteridae, the Atlantic spiny lumpsucker, The maturity phases of each ovary and testis were clas- smooth lumpsucker, and lumpfish, can spawn several sified on the basis of the most advanced stage of germ cells times during their life cycles (Cox and Anderson, 1922; observed in histological sections, according to the scale Berge and Nahrgang, 2013; Zhukova et al., 2018). described by Guzmán et al. (2017). Ovaries were divided In this paper, we provide the first comprehensive data into 5 phases of development: onset of vitellogenesis, early on the stomach contents, gonadal development, and fecun- vitellogenic, mid- vitellogenic, late vitellogenic, and perio- dity of Fedorov’s lumpsucker and describe the biology and vulatory. Phase of testis maturity was determined on the reproductive processes of this little known species. basis of the presence or absence of male germ cells in a gonad: early recrudescence (spermatogonia and spermato- cytes), mid- recrudescence (spermatogonia, spermatocytes, Materials and methods and spermatids), late recrudescence (spermatogonia, sper- matocytes, spermatids, and spermatozoa), spermiating A total of 69 adult specimens of the Fedorov’s lumpsucker (spermatozoa prevail), and postspawning (spermatogo- were caught on the shelf and slope of Simushir Island, nia and residual spermatozoa). Oocyte development was located near the center of the Kuril Islands in the Sea of determinated by using the following stages and their asso- Okhotsk in the northwest Pacific Ocean, from 19 March ciated indicators: primary growth (PG, absence of cortical through 25 March 2017 during tows of the bottom trawl of alveoli and yolk granules), early developing (Vtg1, cortical the FV Anatoly Torchinov that targeted greenlings (Pleu- alveoli and scattered yolk granules along the outer region rogrammus spp.) at depths of 150–230 m. Specimens were of the cytoplasm), developing (Vtg2, yolk granules partly caught near Simushir Island within the area bounded by occupy the cytoplasm), fully vitellogenic (Vtg3, cytoplasm the following coordinates: 46°46′N and 151°56′E, 46°40′N completely filled with yolk), and maturing (M, yolk globule and 151°52′E, and 46°44′N and 151°46′E (Fig. 1). All 69 fusion and nucleus migration). specimens were frozen at −20°C immediately after cap- Absolute and relative fecundity were estimated by using ture and then transported to the laboratory at the Russian the gravimetric method (Murua and Saborido-Rey, 2003) Federal Research Institute of Fisheries and Oceanography for 5 frozen females (size: 74–95 mm TL and 25.4–60.1 g) in Moscow. The Fedorov’s lumpsucker examined in this study ranged in total length (TL) from 64 to 103 mm and weighed from 12.4 to 64.0 g. The 59 females caught were 64–103 mm TL (mean: 81.3 mm TL [standard deviation (SD) 1.23]) and 12.4–64.0 g (mean: 33.22 g [SD 1.36]), and the 10 males were 73–95 mm TL (mean: 84.7 mm TL [SD 2.50]) and 22.9–60.1 g (mean: 41.85 g [SD 5.00]). After a specimen was thawed, the food items were collected from its stomach, separated under a MicroMed MC-21 stereomicroscope (CIT Nelian, Moscow, Russia), and weighed to the nearest mil- ligram with analytical scales (R160P, Sartorius, Bohemia, New York). Fish specimens and food items were identified with the aid of Tuponogov and Kodolov (2014), Oku et al. (2017), and Voskoboinikova (2015). Gonads of 14 females and 2 males (size: 64–92 mm TL and 30.1–38.5 g) were fixed in 10% formalin, dehydrated, cleared with xylol, embed- ded in paraffin, sliced into sections 5 µm thick, and stained with hematoxylin and Ehrlich’s Figure 1 eosin. An Olympus BX45 microscope (Olympus Map showing the location (outlined with a black circle) where 69 adult Fedorov’s lumpsucker (Eumicrotremus fedorovi) were caught during 19–25 March 2017 off Simushir Island, located near the 1 Mention of trade names or commercial companies is center of the Kuril Islands in the Sea of Okhotsk in the northwest for identification purposes only and does not imply endorsement by the National Marine Fisheries Service, Pacific Ocean. NOAA. Gordeev et al.: The first data on the diet and reproduction ofEumicrotremus fedorovi 35 at the late vitellogenetic and periovulatory macroscopic almost 70% of stomachs and composed over 40% of the phases of gonadal maturity. A piece of ovarian tissue was total weight of boluses collected from the specimens with taken from the median portion of the gonad from each spec- food in their stomachs (65 of 69 specimens). imen. The subsample of each ovary, representing 5–10% of After walleye pollock, crustacean species were the most the gonad weight, was weighed, and all advanced oocytes frequent food items (Table 1). Hyperiids were represented (1.7–2.3 mm in diameter) in the subsample were counted. by only 2 species—Themisto pacifica and Primno macropa. The gonadosomatic index (GSI) and absolute (Fabs) and Copepods were represented by several species of Cala- relative (Frel) fecundity were estimated as follows: noida, including Neocalanus cristatus, Gaetanus minutus, Paraeuchaeta elongata, Onchocalanus magnus, Pseu- GSI = (GW × 100) / BW, (1) dochirella obtusa, Cornucalanus indicus, Scaphocalanus Fabs = (n × GW) / w, and (2) sp., and Neocalanus spp.
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