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Deep-Sea Research I 61 (2012) 123–130

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Deep-Sea Research I

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Ontogenetic vertical migration of grenadiers revealed by otolith microstructures and stable isotopic composition

Hsien-Yung Lin a, Jen-Chieh Shiao a,n, Yue-Gau Chen b, Yoshiyuki Iizuka c a Institute of Oceanography, National Taiwan University, Taipei, Taiwan, ROC No. 1, Sec. 4, Roosevelt Road, Taipei, 10617 Taiwan, ROC b Department of Geosciences, National Taiwan University, Taipei, Taiwan, ROC No. 1, Sec. 4, Roosevelt Road, Taipei, 10617, Taiwan, ROC c Institute of Earth Sciences, Academia Sinica, Nangang, Taipei, Taiwan No. 128, Academia Road, Sec. 2, Nankang, Taipei 115, Taiwan, ROC article info abstract

Article history: Otolith d18O and d13C of six species grenadiers were analyzed to reconstruct the historical Received 28 July 2011 residing depths and metabolic activity. During the larval to juvenile stage, Spicomacrurus kuronumai, Received in revised form Hymenocephalus lethonemus, and Bathygadus nipponicus gradually migrated from the mixed layer to the 7 December 2011 thermocline downward over a vertical distance 4140 m after which they moved within a narrow Accepted 10 December 2011 vertical range for the remaining life. The downward migration distance was less than 65 m during the Available online 22 December 2011 larval stage of Hymenocephalus sp. and Coryphaenoides acrolepis, which showed a second descent period Keywords: from the thermocline to deeper water as juveniles. Coryphaenoides marginatus stayed at the lower Grenadiers thermocline during the larval stage and the juveniles migrated downward in a relative short distance Otolith stable isotope around 100 m and settled in deeper water (4600 m), followed by irregular movements over a vertical Ontogenetic vertical migration range of about 200 m during juvenile and adult stages. The otolith d13C profile suggested that fishes Life history (S. kuronumai, H. lethonemus, and B. nipponicus) with a longer migration distance had a higher metabolic rate in their early life-history stages than in the later stages. However, the metabolic rate did not vary for those fishes (H. sp., C. acrolepis and C. marginatus) living within a narrow vertical range during their larval to adult stages. The otolith microchemistry suggested that ontogenetic downward migration was an important strategy for grenadiers linking the life stages between pelagic larvae and benthic settlement. Furthermore, the migration timing and distance for the pelagic larvae varied between species and habitats. S. kuronumai, H. lethonemus, H. sp. and C. acrolepis might metamorphose and settle at the same time, B. nipponicus metamorphosed during migration and C. marginatus migrated as juveniles. & 2011 Elsevier Ltd. All rights reserved.

1. Introduction sea floor and the buoyant eggs float to the thermocline where the larvae are hatched. The larvae grow near the thermocline and Global catches of deep-sea fishes have steadily increased from then descend to adult living depth. Some surveys (Stein, 1980; 2% of the total oceanic catches in 1975 to 33% in 2000 (Garibaldi Endo et al., 1992; Busby, 2005; Fukui and Tsuchiya, 2005; Fukui and Limongelli, 2003). Most deep-sea fisheries take place on et al., 2008, 2010; Endo et al., 2010) of grenadier eggs and larvae continental slopes or seamounts, such as the fisheries for orange agree with the life cycle proposed by Marshall (1973). However, roughy (Hoplostethus atlanticus), black scabbard fish (Aphanopus the early life history is only described for some species of carbo), redfish (Sebastes mentella), blue ling (Molva dypterygia), grenadiers based on limited survey data for certain life stages Greenland halibut (Reinhardtius hippoglossoides), and the grena- (Busby, 2005; Endo et al., 2010). For most grenadiers species, the diers (Cohen et al., 1990; Clark, 2001). available catch records are insufficient to reconstruct their life Nearly all grenadiers are benthopelagic fishes and can be history from larval to adult stage. Therefore, an alternative found in all ocean basins but rarely in the high Arctic. Most method is required to offer robust data for better understanding grenadiers inhabit depths from 100 m to more than 6000 m but the migratory life history of grenadiers. most occur at depths between 200 m and 2000 m (Cohen et al., The otolith is a calcified structure in the inner ears of fishes 1990). Marshall (1973) suggests that grenadiers spawn near the that functions as a part of sensory organ. The periodic formation of growth increments and environmental signals recorded in the otolith serve as a powerful tool for studying life history of n Corresponding author. Tel.: þ886 2 33663227; fax: þ886 2 33663744. teleosts. The otolith increments and checks can provide informa- E-mail address: [email protected] (J.-C. Shiao). tion for daily age determination (Pannella, 1971) and life history

124 H.-Y. Lin et al. / Deep-Sea Research I 61 (2012) 123–130 events such as hatching, settlement and metamorphosis (Hislop nipponicus, Hymenocephalus lethonemus, H. sp., Coryphaenoides et al., 2001; Morioka et al., 2001; Plaza et al., 2001; Hirakawa marginatus, and C. acrolepis were collected in October 2010 off et al., 2007). For deep water fish, the periodic structures in the the southwestern coast of Taiwan by the research vessel ‘‘Ocean otolith including yearly and daily increments have been validated Researcher I’’ (Table 1, Fig. 1). The specimen of H. sp was not by marginal growth analysis (Moku et al., 2001; Swan and intact and morphological characteristics of the remaining carcass Gordon, 2001), radioactive signals (Andrews et al., 1999), tagging only allowed identification to genus name. Hydrological data, (Dougherty, 2008), and rearing (Morales-Nin et al., 2005). Settle- including salinity and temperature, were measured in situ with a ment marks of the otoliths were found in some deep-sea larval or SeaBird Conductivity-Temperature-Depth recorder (SBE 9/11 juvenile fishes such as the greater forkbeard, Phycis blennoides plus, SeaBird Inc., USA, Fig. 2). (Casas and Pineiro, 2000) and greeneye, Chlorophthalmus albatrossis (Hirakawa et al., 2007). Accessory growth centers in otoliths are formed during the larval metamorphosis of 2.2. Otolith preparation Gadiformes (Morales-Nin and Aldebert, 1997), walleye pollock, Theragra chalcogramma (Brown et al., 2001) and ling, Genypterus Sagittal otoliths were dissected from the fish after the mea- blacodes (Morioka et al., 2001). In European hake (Merluccius surement of standard length, preanal length, and weight of the merluccius), accessory growth centers represent larval metamor- grenadiers. Otoliths were embedded in epofix resin (Struers, phosis and settlement on the sea floor (Arneri and Morales-Nin, Demark) and ground on the sagittal plane till the primordium 2000; Morales-Nin et al., 2005). was exposed by the grinding machine (Buehler, Metaserv 2000, The chemical composition of the otolith records environmen- Evanston, IL, USA). Then, the otoliths were polished and treated tal signals and physiological status, which are very useful for with 8% EDTA (ethylene diamine tetra-acetate) for 20–40 s. understanding the autoecology of fishes (Campana, 1999). Otolith Otolith images were taken by a compound microscope (Olympus d18O is influenced by salinity, water d18O values and water BX-51) equipped with a digital camera (DP-71, Olympus) using temperature. The deposition of otolith d18O is in equilibrium reflected and transmitted light. Otoliths were coated with gold with ambient water and the fractionation factor is water tem- and observed under a scanning electron microscope (SEM, JSM- perature dependant (Kalish, 1991; Campana, 1999). Several stu- 6360LV, Japan). The otolith growth increments around the core dies suggest that aragonite d18O is inversely related to the area were interpreted as putative daily increments since they ambient water temperature with a slope of approximately were not validated for these deep-water fishes. A dark and light 0.20 to 0.23 (Grossman and Ku, 1986; Radtke et al., 1998; growth increment was defined as a daily growth increment. Høie et al., 2004), although the intercepts significantly differ The other sagittal otolith of the same fish was prepared in the between species (e.g., Patterson et al., 1993; Thorrold et al., same way as described above for stable isotope analysis. Otolith 1997). Oxygen isotopic composition has been extensively used powders were collected by a computerized micromill (Merchantek, to study natal origin (Shiao et al., 2010), fish migration (Shephard USA) along several segmented lines that followed the otolith et al., 2007; Shiao et al., 2009), and age determination (Weidman growth zones marked on the real-time computer image from the and Millner, 2000) of fishes. Otolith d13C represents a mixture of dietary carbon and dissolved inorganic carbon (DIC). Approxi- mately 17–30% of otolith C is metabolically derived, while the rest is derived from DIC (Høie et al., 2003; Solomon et al., 2006). Metabolism, diet, and trophic level (Schwarcz et al., 1998, Jamieson et al., 2004) may have more prominent effects on otolith d13C than does DIC, which shows little variability across latitude in the open ocean (1%, Kroopnick, 1980). The objective of this study is to reconstruct the migratory life history of six species of grenadiers by analyzing otolith microstructure and isotopic composition. The results can evaluate previous studies on the life cycles of grenadiers and are also helpful to understand the ontogenetic vertical migration, historical residence depth, and metabolic activity of the deep-sea fishes.

2. Materials and methods

2.1. Fish collection

Specimens of Spicomacrurus kuronumai were collected in June Fig. 1. Sampling site: southwestern coast of Taiwan (SWT) and northern area of 2008 in the northern area of the South China Sea; Bathygadus South China Sea (NSCS).

Table 1 Grenadiers sampling for otolith analysis. Fishes were collected in June, 2008 in the northern South China Sea and October, 2010 off southwestern Taiwan.

Species Number Preanal length (cm) Longitude (E) Latitude (N) Depth (m) Date

Spicomacrurus kuronumai 3 3.0/3.3/3.1 116158.950 20159.280 300 June 2, 2008 Hymenocephalus lethonemus 1 3.3 120106.030 22125.570 600 October 7, 2010 Hymenocephalus sp. 1 2.3 120106.030 22125.570 600 October 7, 2010 Coryphaenoides acrolepis 2 2.3/2.5 120106.030 22125.570 600 October 7, 2010 Coryphaenoides marginatus 2 8.8/6.9 120106.030 22125.570 600 October 7, 2010 Bathygadus nipponicus 2 9.3/4.8 120106.030 22125.570 600 October 7, 2010 Author's personal copy

H.-Y. Lin et al. / Deep-Sea Research I 61 (2012) 123–130 125

Fig. 2. Temperature and salinity proﬁles from the sampling locations in the northern area of the South China Sea (NSCS, panel a) and southwestern coast of Taiwan (SWT, panel b).

camera on top of the micromill. The micromill software interpo- NBS19 standard: lated new lines between two adjoining segmented lines according R R to the number of samples wanted. The round tip of the drill d ¼ sample standard 1000ð%Þð1Þ R (H23RS, Comet, Germany) was 200 mm in diameter. Milling depth standard was set to approximately 200 mm. Otolith powders, weighting 40– where R is the ratio of 18O:16Oor13C:12C in the sample or 50 mg, were collected from the margin to the core along the longest standard. axis of the sagittal plane, with sampling interval gradually increas- Otolith d18O fractionation specific to grenadiers is still ing from approximately 100 mmto150mm while sampling path unknown. Since the relationship between water temperature gradually decreasing from 150 mmto50mm. Milled samples were and otolith d18O is best described by the inorganic calcite then collected sequentially between each of the lines. After each equation as suggested by Campana (1999). We use the inorganic milling, the otolith image was recorded. The temporal resolution calcite equation developed by Kim and O’Neil (1997) to estimate for the early life stage represented by each sample varied from otolith d18O from water d18O and temperature (as a proxy of approximately 2 weeks to 2 months depending on the species. depth, Fig. 3). The equation is modified to reflect aragonite (otolith) which is enriched in 18O by 0.6% relative to calcite during precipitation at 25 1C(Tarutani et al., 1969).

18 18 3 2.3. Stable isotopic analysis d Ootod Ow ¼ 3:710:206T ð CÞð2Þ 18 18 18 In this equation, d Ooto is the otolith d O value, d Ow is the The oxygen and carbon isotopic compositions were analyzed 18 water d O (in the VPDB scale), and T is the water temperature. using a Finnigan MAT 253 mass spectrometer (Thermo Electron 18 d Ow can be described by the equation from salinity in Luzon Corporation, Germany). The CO gas for isotope measurements 2 Strait (Lin, 2000): was produced by reaction with pure orthophosphoric acid at 18 70 1C in an automated on-line system (Kiel carbonate device IV, d Ow ¼13:2þ0:39S, ð3Þ Kiel, Germany) with acid added to the sample in individual 18 reaction vials. The long term reproducibility of the Finnigan where S is the salinity. d Ow is reported in the VSMOW (Vienna MAT 253 is better than 70.082% for d18O and better than Standard Mean Ocean Water) scale that can be converted to the 70.054% for d13C (one standard deviation) for an internal VPDB scale by the equation (Friedman and O’Neil, 1977): carbonate standard (40–50 mg) based on replicate measurements 18 18 d Owðon the VPDB scaleÞ¼0:99978ðd Ow on the VSMOW scaleÞ0:22: (n¼92) during this experimental period. ð4Þ All isotopic values were reported relative to standards by the International Atomic Energy Agency, Vienna. Otolith d18O and The residing depth of the ﬁsh is estimated from measured d13C values were reported in standard notation relative to the otolith d18O value based on the proﬁle of depth and predicted Vienna Pee Dee Belemnite (VPDB) through calibration against the otolith d18O(Fig. 3). Høie et al. (2004) reported that the precision Author's personal copy

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Fig. 4. The otolith microstructure of Spicomacrurus kuronumai showed a distinct check (arrowhead) at approximately 50 day after hatching, which corresponds to the settlement of pelagic larval to benthic habitat. Scale bar¼1000 mm.

Fig. 3. Predicted otolith d18O(d18Ooto) from CTD proﬁles from the southwestern coast of Taiwan (SWT) and northern area of the South China Sea (NSCS). of temperature estimates derived from otolith d18O values was approximately 71 1C for single otolith analyses.

3. Results

3.1. Spicomacrurus kuronumai and Hymenocephalus lethonemus

A clear check mark appeared in the middle of the otolith (Fig. 4) and the mean (7SD) daily increment width was larger (15.771.0 mm) inside the mark and became smaller (6.670.4 mm) beyond the mark. Within this check mark, 52, 57 and 49 rings were counted in S. kuronumai and 81 rings were counted in H. lethonemus. Otolith d18O gradually increased from the core (0.064%70.19, n¼3 for S. kuronumai; 0.268%, n¼1 for H. lethonemus) to the first peak around the check mark Fig. 5. Otolith d18O (panel a) and d13C (panel b) profiles of Spicomacrurus (1.397%70.23 for S. kuronumai; 2.064% for H. lethonemus), then kuronumai (thin line, three samples) and Hymenocephalus lethonemus (bold line, the values varied in a narrow range to the otolith edge (Fig. 5a). one sample). The arrowheads represent the position of otolith check marks. S. kuronumai showed a steep increase in otolith d13C from the core to the check mark and a second increase near the otolith edge. Otolith d18OofB. nipponicus steeply increased from 0.245% and 13 H. lethonemus showed a continuous increase in otolith d C from 0.227% at the cores to 1.596% and 1.804% at the first translucent the core to the edge (Fig. 5b). zones (n¼2, Fig. 8a). Otolith d13CofB. nipponicus also steeply increased from the core to the first translucent zone then 3.2. Bathygadus nipponicus, Coryphaenoides marginatus and remained at the same level or increased a second time between C. acrolepis the first translucent zone and the edge (Fig. 8b). Otolith d18OofC. acrolepis (n¼2) slightly increased from The polygonal nucleus was surrounded by accessory growth 0.967% and 1.665% at the cores to 1.334% and 2.021% at an centers (77 and 76 day, Fig. 6) and at least one translucent zone accessory growth center (116 and 126 day). The values remained appeared in the otoliths of B. nipponicus (148 and 155 day, Fig. 7). at levels around 2.087% and 1.874% from the translucent zones Author's personal copy

H.-Y. Lin et al. / Deep-Sea Research I 61 (2012) 123–130 127

Fig. 6. The otolith core area of Bathygadus nipponicus surrounded by a polygonal nucleus and discontinuous zone (arrowhead). The arrow indicates the translucent zone. Scale bar¼200 mm.

Fig. 8. Otolith d18O (panel a) and d13C (panel b) proﬁles of Bathygadus nipponicus. The arrowheads indicate the locations of discontinuous zones and arrows represent the translucent zones in the otolith.

Fig. 7. Otolith of Coryphaenoides acrolepis. The arrow indicates the translucent zone. Scale bar¼1000 mm.

(263 and 250 day) to the otolith edges (Fig. 9a). Otolith d13C for C. acrolepis varied in a small range between 3.5% to 4.0% (Fig. 9b). Otolith d18O proﬁles for two C. marginatus were 1.631% and 1.829% in the core and remained at this level until the accessory growth center (84 and 80 day), then increased to 2.030% and 2.394% at the translucent zone before gradually decreasing between 1000–3000 mm from the core and then increasing again to 2.0–2.5% at the otolith edge (Fig. 10a). Otolith d13C for C. marginatus remained around 4.3% during the early life stage, then gradually increased to 2.5% at the otolith edge (Fig. 10b). One individual showed an abrupt drop in otolith d13C around 800–1200 mm from the core.

3.3. Hymenocephalus sp.

The otolith nucleus of Hymenocephalus sp. was also surrounded by accessory growth centers (56 day) and a check mark appeared near the edge of the otolith (147 day, Fig. 11). The increment width was larger (12.5770.25 mm) inside the check and became smaller (7.3770.46 mm) beyond the check mark. Otolith d18O for H. sp. was 0.375% in the core, 0.623% at the accessory growth center, and 1.755% at the check mark (Fig. 9a). H. sp. showed a gradual increase in otolith d13C from 6.0% at Fig. 9. Otolith d18O and d13C proﬁles of Coryphaenoides acrolepis (thin line) and the core to 5.0% (700–2100 mm) and a slight decline to 5.5% Hymenocephalus sp. (bold line). The discontinuous zones (arrowhead) and trans- at the otolith edge (Fig. 9b). lucent zones (arrow) are marked. Author's personal copy

128 H.-Y. Lin et al. / Deep-Sea Research I 61 (2012) 123–130

important life history strategies that link pelagic larval and demersal adult stages of the grenadiers. The use of otolith d18O as a proxy for water temperature revealed that the larval or juvenile settlement on the sea floor corresponds to the first translucent zone of B. nipponicus and C. marginatus and the check mark of S. kuronumai, H. lethonemus and H. sp. The distance of vertical sinking during larval and juvenile stages varied between approximately 150–350 m depending on the species. It is still unclear when the otolith check mark and accessory growth centers are formed during the ontogenetic development of the grenadiers. If the structure was formed during the larval metamorphosis, we hypothesized that S. kuronumai, H. lethonemus, H. sp., and C. acrolepis might metamorphose from larva to juvenile during settlement on the sea floor, B. nipponicus finished larval metamorphosis during the sinking process and C. marginatus migrated and settled as juveniles. After settlement on the sea floor, B. nipponicus stayed at constant depth while juvenile C. marginatus migrated to deeper waters. Different patterns showing vertical downward migration for grenadiers were summarized in a conceptual diagram (Fig. 12). Grenadiers are widespread benthopelagic fishes which have ribbon-like distributions around the oceanic rim (Merrett, 1989). The adult fishes live within relatively narrow bathymetric ranges on the continental slope to the abyssal floor. S. kuronumai is a shallower-dwelling macrourid living at 350 to 500 m depth. The short pelagic larval stages of S. kuronumai indicate a rapid development from larva to juvenile accompanying a gradual descent to deeper water. In contrast, the deeper-dwelling species C. pectoralis (600 to 1500 m depth) has a longer pelagic larval Fig. 10. Otolith d18O (panel a) and d13C (panel b) profiles of Coryphaenoides stage of around 4 years (Orlov and Tokranov, 2008). The different marginatus. The discontinuous zones (arrowhead) and translucent zones (arrow) are marked. lengths of the pelagic stage between species might reflect different distances between the feeding habitats of pelagic larvae and demersal stages. All species examined except C. acrolepis showed much lower otolith d18O during the early life stage than at other stages. C. acrolepis is found on the northern Pacific continental slope in water depths of 300 to 3700 m. Stein (1980) collected the smallest larvae of C. acrolepis in shallower water between the sea surface and 200 m depth, while post-larvae were collected at 500 m and juveniles at 650 to 800 m depth. Otolith d18Ooftwo C. acrolepis juveniles (about 8 cm) showed ontogenetic descent in the distance about 150–200 m. Mulcahy et al. (1979) also analyzed otolith d18O of adult C. acrolepis (67–84 cm) that suggested a migration from 600 to 2000 m during the adult stage. d18O values in the otolith core suggested that larval C. marginatus lived at depths around 400 m, deeper than the 100 m found

epipelagic zone larva Fig. 11. Hymenocephalus sp. shows the discontinuous zone (arrowhead) and check (arrow). Scale bar¼1000 mm. larva juvenile juvenile 4. Discussion mesopelagic zone adult

Depth juvenile This study revealed by otolith microstructure and stable isotopic analysis the ontogenetic downward migration by grenadiers. The results supported previous oceanographic surveys and demersal habitats provided new insights into the migratory life history of the continental slope grenadiers. Marshall (1973) suggested that grenadiers reproduced near the sea floor and the fertilized eggs then floated to the mixed layer or thermocline. The hexagonal ornamentation on the egg Fig. 12. A conceptual diagram showing different patterns of vertical downward surface was believed to inhibit the ascent rate of buoyant eggs migration for grenadier larvae and juveniles. The larvae may metamorphose (Robertson, 1981; Merrett and Barnes, 1996). The rise of eggs to during sinking or at the same of settlement on the sea floor. The migrating the thermocline and the downward migration of the larvae are distance varies among the species. Author's personal copy

H.-Y. Lin et al. / Deep-Sea Research I 61 (2012) 123–130 129 by Fukui et al. (2008). C. marginatus are distributed at depths different life traits, such as those found in this study, is an between 250 m and 790 m from southern Japan to the East China adaptive strategy for larval grenadiers to reach different adult Sea (Okamura, 1970). At lower latitudes, larval C. marginatus may living depths and to occupy deep-sea environments all around the reside at deeper depths to avoid higher water temperatures world. nearer to the surface. Otolith d13C represents a mixture of dietary carbon (Nonogaki et al., 2007; Elsdon et al., 2010), dissolved inorganic carbonic Acknowledgments 13 isotope (d CDIC, Weidel et al., 2007), and a metabolic contribu- 13 tion (Høie et al., 2003; Solomon et al., 2006). d CDIC shows very We thank C.H. Wang for assistance with isotopic analysis of minor or only little variability with water temperature and water samples and the crew of R/V Ocean Researcher I for their latitude in the open ocean (1%, Kroopnick, 1980) and the help during the surveys. We are also grateful to B.M. Jessop for variation is also fairly small (usuallyo0.5%) in deeper waters useful comments. This study was financially supported by the (Gislefoss et al., 1998; Bostock et al., 2010). Carbon fractionation National Science Council, Taiwan (NSC100-3113-M-002-002). is also controlled by biological (kinetic) effects. Consequently, the carbon isotope levels can reflect the metabolic condition of fishes References (Hidalgo et al., 2008). Therefore, the large variation (up to 4%)in 13 otolith d C during the early life stage of S. kuronumai, Andrews, A.H., Cailliet, G.M., Coale, K.H., 1999. Age and growth of the Pacific H. lethonemus, and B. nipponicus appears largely influenced by grenadier (Coryphaenoides acrolepis) with age estimate validation using an ontogenetic effects e.g., metabolic rate or foods, rather than improved radiometric ageing technique. Can. J. Fish. Aquat. Sci. 56, 13 13 1339–1350. d CDIC. The otolith d C profile suggested that the grenadiers Arneri, E., Morales-Nin, B., 2000. Aspects of the early life history of European hake were active feeders with a high metabolic rate during their early from the central Adriatic. J. Fish Biol. 56, 1368–1380. life stage (Merrett and Haedrich, 1997). Adolescent to adult Bostock, H.C., Opdyke, B.N., Williams, M.J.M., 2010. Characterising the intermedi- ate depth waters of the Pacific Ocean using d13C and other geochemical grenadiers forage in colder and deeper water and have a lower tracers. Deep Sea Res. Part I 57, 847–859. metabolism (Smith, 1978). Bradbury, I.R., Snelgrove, P.V.R., 2001. Contrasting larval transport in demersal fish Otolith d13C profiles of H. sp. and C. acrolepis suggested a less and benthic invertebrates: the roles of behavior and advective processes in variable metabolism from larvae to adolescence consistent with determining spatial pattern. Can. J. Fish. Aquat. Sci. 58, 811–823. Brown, A.L., Busby, M.S., Mier, K.L., 2001. Walleye pollock Theragra chalcogramma the narrow range of water temperature experienced. Juvenile during transformation from the larval to juvenile stage: otolith and osteolo- C. marginatus migrated to a depth of around 600 m then irregu- gical development. Mar. Biol. 139, 845–851. larly moved upward and downward after bottom settlement. The Busby, M.S., 2005. An unusual macrourid larva (Gadiformes) from San Juan Island, 13 Washington, USA. Ichthyol. Res. 52, 86–89. small variance of otolith d C(o1%) indicated a stable metabo- Campana, S.E., 1999. Chemistry and composition of fish otoliths: pathways, lism during the larval and juvenile stages of C. marginatus. Their mechanisms and applications. Mar. Ecol. Prog. Ser. 188, 263–297. metabolism gradually decreased as they moved to deeper water. Casas, J.M., Pineiro, C., 2000. Growth and age estimation of greater fork–beard 13 (Phycis blennoides Brunnich, 1768) in the north and northwest of the Iberian One C. marginatus showed a dramatic drop in d C during the Peninsula (ICES Division VIIIc and IXa). Fish. Res. 47, 19–25. juvenile to young adult stage, probably caused by a short period Clark, M., 2001. Are deep–water fisheries sustainable? – the example of Orange of stress (Høie et al., 2004). roughy (Hoplostethus atlanticus) in New Zealand. Fish. Res. 51, 123–135. Cohen, D.M., Inada, T., Iwamoto, T., Scialabba, N., 1990. FAO species catalogue Vol Efficient colonization of the open ocean by deep-sea fish such 10 Gadiform fishes of the world (Gadiformes). An annotated and illustrated as grenadiers involves a reproductive strategy that produces catalogue of cods, hakes, grenadiers and other Gadiform fishes known to date. many small pelagic eggs (Crabtree and Sulak, 1986; Duarte and FAO Fisheries Synopsis No. 125, Vol. 10, FAO, Rome. Crabtree, R.E., Sulak, K.J., 1986. Contribution to the life history and distribution of Alcaraz, 1989). Most larval grenadiers are collected from semi- Atlantic species of the deep-sea fish genus Conocara (Alepocephalidae). Deep enclosed seas or waters close to the coast but very few at mid- Sea Res. 33 (9), 1183–1201. ocean floors. Larval grenadiers feed in the lower layer of the Dougherty, A.B., 2008. Daily and sub-daily otolith increments of larval and seasonal thermocline where plankton tends to accumulate juvenile walleye pollock, Theragra chalcogramma (Pallas), as validated by alizarin complexone experiments. Fish. Res. 90, 271–278. (Marshall, 1965). This layer, with relatively warm temperatures Duarte, C.M., Alcaraz, M., 1989. To produce many small or few large eggs: a size- and rich food, is a good nursery ground for rapidly growing larvae, independent reproductive tactic of fish. Oecologia 80, 401–404. especially for young grenadiers which lack large yolk reserves Elsdon, T., Ayvazian, S., McMahon, K.M., Thorrold, S.R., 2010. Experimental evaluation of stable isotope fractionation in fish muscle and otoliths. Mar. (Merrett, 1989). However, the distance and timing of ontogenetic Ecol. Prog. Ser. 404. 195–205. downward migration can vary among different adult habitats, as Endo, H., Yabe, M., Amaoka, K., 1992. A rare macrourid alevin of the genus found in this study, and different larval vertical distributions can Hymenocephalus from the Pacific Ocean. Jpn. J. Ichthyol. 39 (3), 265–267. Endo, H., Nakayama, N., Suetsugu, K., Miyake, H., 2010. A larva of Coryphaenoides play an important role in larval transport and dispersal (Bradbury pectoralis (Gadiformes: Macrouridae) collected by deep-sea submersible from and Snelgrove, 2001; Leis, 2010). off Hokkaido, Japan. Ichthyol. Res. 57, 272–277. This study used otolith d18O to construct the historical resi- Friedman, I., O’Neil, J.R., 1977. Compilation of stable isotope fractionation factors of geochemical interest. In: Fleisher M, Chap KK (Eds.) Data of Geochemistry, dence depths of grenadiers from larval to adult stages. The 6th edn. US Geol Surv Prof Pap 440: 1–12. methodology is suitable for fast growing species or developmen- Fukui, A., Tsuchiya, T., 2005. Pelagic larvae of Ventrifossa garmani (Gadiformes: tal stages with larger otolith daily increment such as early life Macrouridae) from Suruga Bay and offshore waters of Japan. Ichthyol. Res. 52, 311–315. period. The method is also helpful to validate some otolith Fukui, A., Tsuchiya, T., Sezaki, K., Watabe, S., 2008. Pelagic eggs and larvae of microstructures, which reflect certain life history events, for Coryphaenoides marginatus (Gadiformes: Macrouridae) collected from Suruga example the settlement on the sea floor. However, it is still Bay, Japan. Ichthyol. Res. 55, 284–293. difficult to elucidate life histories of long-lived deep sea fishes Fukui, A., Takami, M., Tsuchiya, T., Sezaki, K., Igarashi, Y., Kinoshita, S., Watabe, S., 2010. Pelagic eggs and larvae of Coelorinchus kishinouyei (Gadiformes: Macro- during the slow-growing stage e.g., adults, due to the limited uridae) collected from Suruga Bay, Japan. Ichthyol. Res. 57, 169–179. temporal resolution of this technique. Nevertheless, all fishes Garibaldi, L., Limongelli, L. 2003. Trends in oceanic captures and clustering of large examined herein showed ontogenetic downward migration but marine ecosystems: two studies based on the FAO capture database. 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