Reproductive Strategies in Female Polar and Deep-Sea Bobtail Squid Genera Rossia and Neorossia (Cephalopoda: Sepiolidae)
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Polar Biol (2008) 31:1499–1507 DOI 10.1007/s00300-008-0490-4 ORIGINAL PAPER Reproductive strategies in female polar and deep-sea bobtail squid genera Rossia and Neorossia (Cephalopoda: Sepiolidae) V. V. Laptikhovsky · Ch. M. Nigmatullin · H. J. T. Hoving · B. Onsoy · A. Salman · K. Zumholz · G. A. Shevtsov Received: 7 April 2008 / Revised: 18 June 2008 / Accepted: 30 June 2008 / Published online: 18 July 2008 © Springer-Verlag 2008 Abstract Female reproductive features have been investi- Introduction gated in Wve polar and deep-sea bobtail squid genera Rossia and Neorossia (R. macrosoma, R. moelleri, R. paciWca, CuttleWsh of the family Sepiolidae, commonly known as N.c. caroli and N.c. jeannae). These species are character- “bobtail squid”, inhabit tropical, temperate and polar waters ized by asynchronous ovary maturation, very large eggs of all oceans. The family has three subfamilies including (>10% ML), fecundity of several hundred oocytes, very the oceanic and pelagic Heteroteuthinae and the benthic high reproductive output, and continuous spawning with Sepiolinae and Rossiinae which inhabit continental shelf low batch fecundity. This adaptive complex of reproductive and slope waters. Sepiolinae are common on tropical and traits evolved in these small animals as an optimum strat- temperate shelves and on the upper part of the continental egy for polar and deep-water habitats. slope (down to depths of about 400 m). Rossiinae are gen- erally associated with cold water. They occur on polar Keywords Neorossia · Rossia · Spawning · shelves and in deep seas between 200 and 2,000 m, usually Reproduction · Polar · Deep-sea deeper than 500 m, though not south of the Antarctic Polar Front (Reid and Jereb 2005). Because species belonging to the Sepiolinae occur in rel- V. V. Laptikhovsky (&) atively shallow waters, are easy to catch and are reared Falkland Islands Fisheries Department, FIQQ 1ZZ, quite successfully in aquaria, reproduction in sepiolids is P.O. Box 598, Stanley, Falkland Islands e-mail: [email protected] best studied in this subfamily (Arnold et al. 1972; Boletzky 1975, 1983a, b; Bergstrom and Summers 1983; Gabel- Ch. M. Nigmatullin Deickert 1995; Yau and Boyle 1996; Bello and Deickert AtlantNIRO, 5 Dm.Donskoy 236000 St Kaliningrad, Russia 2003; Salman and Önsoy 2004). Fecundity in Sepiolinae is H. J. T. Hoving generally several hundred eggs and the number of eggs laid CEES, Ocean Ecosystems, University of Groningen, at a spawning event (batch size) varies from 1 to 176. Egg P.O. Box 14, 9750 AA Haren, The Netherlands length is 2–4 mm and spawning is continuous with decreas- ing intensity, though some individual females in captivity B. Onsoy Fisheries Faculty, Mugla University, Kotekli, Mugla, Turkey have been reported as single spawners (Gabel-Deickert 1995). A similar continuous spawning pattern was found in A. Salman Heteroteuthinae (Hoving et al. 2008). Faculty of Fisheries, Ege University, In contrast, little is known about the female reproductive 35100 Bornova, Izmir, Turkey biology of Rossiinae, except that they produce relatively K. Zumholz large eggs (egg length 7–12 mm) (Okutani and Sasaki Leibniz-Institute of Marine Sciences, IFM-GEOMAR, 2007). One female Rossia paciWca was kept in captivity Düsternbrooker Weg 20, 24105 Kiel, Germany and laid two batches of 50 and 35 eggs each. The laying of W G. A. Shevtsov the rst and the second batch was separated by an interval TINRO-Centre, 4 Shevchenko Alley, 690950 Vladivostok, Russia of 3 weeks and the female died after the last eggs were 123 1500 Polar Biol (2008) 31:1499–1507 spawned (Summers 1985). Pre-spawning large females of North Atlantic and the Arctic Ocean northward to 82°N this species may have 50–200 well-developed oocytes in from northeast Canada to the Laptev Sea between 17 and the ovary (Summers and Colvin 1989; Shevtsov and 250 m (Nesis 2001; Reid and Jereb 2005). Rossia paciWca Mokrin 2000). The western Mediterranean mature female Berry, 1911 inhabits the North PaciWc from Japan and Cali- Rossia macrosoma may have 120–150 large yolk oocytes fornia to the Bering Strait between 30 and 1,350 m (Nesis in their ovaries and ripe eggs are laid in clusters of 30–40 1989; Reid and Jereb 2005). The species Neorossia caroli (Gabel-Deickert 1995; Reid and Jereb 2005). Data on the (Joubin, 1902) is the most bathyal sepiolid and is also the ovulation pattern and actual fecundity are absent for both most common cephalopod between 1,000 and 2,000 m the species, because smaller eggs were never taken into (Reid and Jereb 2005). The species consists of two subspe- consideration during fecundity analysis. Recent research on cies (Reid and Jereb 2005): N.c. caroli (Joubin, 1902) that the female reproductive biology of Neorossia caroli from inhabits the East Atlantic from Iceland to Namibia from 40 the western Mediterranean (Cuccu et al. 2007) demon- to 1,744 m; and N.c. jeannae (Nesis et al., 2001) which strated that mature females have between 24 and 611 occurs around the Falkland Islands between 474 and 670 m. oocytes while more than 100–200 oocytes are present in An egg mass of R. paciWca was sampled onboard RV immature bobtail squid. An egg clutch deposited on a piece “Kayo Maru” on 24 November 1997. The vessel was oper- of hard substrate consisted of 13 eggs. Following the classi- ating a bottom trawl between 61°06Ј–61°34ЈN and Wcation proposed by Rocha et al. (2001) the spawning pat- 179°15Ј–178°12ЈE (depth range 210–280 m). tern of N. caroli is continuous. To increase the knowledge Captured animals were preserved whole in 6–10% for- of reproductive strategies within the family Sepiolidae this malin. In preserved squid, the dorsal mantle length (ML) paper provides information on the fecundity, ovary devel- was measured to be within 1 mm, and total body mass opment, female reproductive strategies and spawning pat- (BM) was estimated to be within 0.1 g. Animals were terns of Wve Rossiinae species and subspecies (genera assigned as immature, maturing, mature and spent animals Rossia and Neorossia). (Table 2). The ovary and accessory glands were weighed to be within 0.0001 g. All oocytes from the ovary and the ovi- duct were separately counted and measured along the major Materials and methods axis to the nearest 0.1 mm. The gonadosomatic index (GSI) was calculated as a ratio between the gonad mass (GM) to A total of 64 females belonging to Wve species and subspe- the BM (GSI = (GM/BM) £ 100) and the reproductive cies of the polar and deep-sea bobtail squid genera Rossia system index (RSI), as a ratio between reproductive sys- and Neorossia were collected in the diVerent geographical tem mass (RSM), and BM (RSI = (RSM/BM) £ 100) areas (Fig. 1; Table 1). From the North Atlantic, we exam- (Bakhayokho 1983; Gabr et al. 1998). Total number of ined Rossia macrosoma (delle Chiaje, 1830) and Rossia oocytes in the ovary and ripe eggs in oviduct was consid- moelleri Steenstrup, 1856. R. macrosoma inhabits waters ered to be the potential fecundity (PF). The number of fol- from East Greenland and Iceland to the Mediterranean Sea licular sheaths together with PF, minus the number of and Northwest Africa and occurs at depths between 30 and ovulated ripe eggs was assumed to represent maximum 900 m (Reid and Jereb 2005). R. moelleri occurs in the potential fecundity, MPF. Relative fecundity (RF) was Fig. 1 Position of sampling N N sites of R. moelleri (diamonds), 60° Rossia macrosoma and 50° Neorossia c.caroli (circles), Rossia paciWca (squares) and 40° N.c. jeannae (crosses) 30° ATLANTIC PACIFIC 20° 10° 0° 10° 20° OCEAN 30° 40° 50° S W 90° 70° 50° 30° 10° 10° 30° 50° 70° 90° 110° 130° 150° 170° E 123 Polar Biol (2008)31:1499–1507 Table 1 Locality data for female Rossia spp and Neorossia spp examined Species N Date Mantle length, Body mass, Vessel Locality Position Fishing gear Depth (m) ML (mm) BM (g) Rossia 21 II–X 1991–1993 24–59 5.9–89.4 RV “Koca Piri Rejs” Aegen and 34°26Ј–40°28ЈN Bottom trawl 180–340 macrosoma Mediterranean Seas 24°50Ј–34°51ЈE R. moelleri 11 II–XI 2003–2006 26–44 6.6 –38.7 RV “Walter Hervig” Greenland Arctic 61°38Ј–66°40ЈN Bottom trawl 91–400 30°34Ј–58°31ЈW R. paciWca 5 VIII–XII 1995–1196 61–86 90–195 FV “Kayo Maru” Bering Sea 60°40Ј–61°45ЈN Bottom trawl 176–455 178°E–179°45ЈW – 2 VIII–X 1995 25–41 9.7–28.2 RV “TINRO” Sea of Japan 42°37Ј–46°56ЈN Pelagic trawl 200 and 200 133°12Ј–139°15ЈE Neorossia 3 VII–X 1992 27–36 9.5–19.2 RV “Koca Piri Rejs” Aegen and 38°04Ј–39°50ЈN Bottom trawl 450–480 caroli caroli Mediterranean Seas 24°35Ј–25°58ЈE N. caroli jeannae 22 IX–XI 2006–2007 25–63 6.6–163.3 FVs “Antonio Nores”, Subantarctic waters oV 45°18Ј–59°56ЈS Bottom trawl 733–845 “Manuel Angel Nores” the Falkland Islands 52°15Ј–59°46ЈW sheaths had degenerated. had sheaths the follicular and empty spawning been during released already had eggs) 200–700 it (probably of most that cating indi- eggs 106–155 only was females spawning advanced increasedwith female length (Fig. (Fig. 382–837 was recorded. were not (Fig. ovulation becomesperiodthe relativelyin short high the prior eggs of large number the although and maturity, tion matura- of atallstages predominating with small oocytes Rossia macrosoma. Results weight. egg individual an to of RF product as the culated was cal- (PRI) investment reproductive ofpotential Index calculated(RFto BM MPF of the ratio as = MPF/BM).