Feeding Habits of the Mesopelagic Fish Gonostoma gracile in the Northwestern North Pacific
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1 Journal of Oceanography, Vol. 57, pp. 509 to 517, 2001 Feeding Habits of the Mesopelagic Fish Gonostoma gracile in the Northwestern North Pacific KAZUHISA UCHIKAWA 1 *, ORIO YAMAMURA 2 and YASUNORI SAKURAI 1 1 Graduate School of Fisheries Sciences, Hokkaido University, Hakodate, Hokkaido , Japan 2 Hokkaido National Fisheries Research Institute, Kushiro, Hokkaido , Japan (Received 10 September 1999; in revised form 7 February 2001; accepted 7 February 2001) The diet of Gonostoma gracile, a numerically abundant mesopelagic fish in the Subtropical Region and the Transition Domain of the northwestern North Pacific, was examined using 520 specimens collected during June July 1988, June 1995 and November The prey included mainly copepods, ostracods, amphipods and euphausiids. Copepods and ostracods were the most abundant, comprising approximately 70% of the total diet. There was little evidence of an ontogenetic dietary shift; Pleuromamma copepods were the most abundant prey for all size classes of fish ranging from 19 to 116 mm in standard length. The size range of prey increased with growth, but all fish sizes examined fed mainly on 1 4 mm long prey. Luminescent copepods and ostracods were the most abundant prey, suggesting that G. gracile detects its prey visually. Keywords: Gonostoma gracile, mesopelagic fish, diet, feeding habits, Pleuromamma, luminescent zooplankton, northwestern North Pacific. 1. Introduction The gonostomatid fish Gonostoma gracile (Günther) is abundantly distributed in the western North Pacific between 20 and 50 N (Grey, 1960; Kawaguchi, 1971, 1973; Miya et al., 1995), suggesting it may play an important role in this region s mesopelagic food web. Previous studies have examined the reproduction (Kawaguchi, 1967; Gorelova, 1981), and the horizontal and vertical distribution of this species (Kawaguchi, 1973). Feeding studies have also been conducted in the Kuroshio area and Suruga Bay (Kawaguchi, 1969), off the southern coast of Hokkaido (Gordon et al., 1985) and in the tropical western Pacific (Gorelova, 1981), but details of its feeding habits remain poorly known. In the present paper we report on the diet composition of G. gracile in the Subtropical Region and the Transition Domain of the northwestern North Pacific. 2. Materials and Methods Samples were collected during cruises of the T/S Hokusei-Maru during June July 1988 and June 1995, and of the T/S Oshoro-Maru during November A 2.5 m 2.0 m rectangular midwater trawl with a 333 µm mesh codend was towed obliquely at 3 knots (1.5 m s 1 ) * Corresponding author. uti@fish.hokudai.ac.jp Copyright The Oceanographic Society of Japan. at 15 stations between 0 and 600 m depth mainly at dusk and night. Gonostoma gracile was also collected at 13 stations by horizontal hauls of the same net at the same towing speed through scattering layers monitored by 24 khz echosounders (Fig. 1; Table 1). The depths of the horizontal hauls ranged from 100 to 430 m. A conductivity-temperature-depth probe (CTD) or expendable bathythermograph (XBT) cast was made at each sampling station. Fish samples were fixed in 10% buffered formaldehyde seawater solution at sea and transferred to 50% isopropyl alcohol in the laboratory. Stomach contents were examined under a stereomicroscope. Prey items were identified to the lowest taxon possible and counted. If possible, prey items were measured to the nearest 1 µm along the longitudinal axis (prosome length for copepods, total length without telson for amphipods, total length without terminal setae for euphausiids and total length for others). The diet of G. gracile was expressed as the percentage of each prey type of the total number of prey identified (Cn) and the percentage of stomachs in which each prey type was found (F). Prey selectivity was examined by comparing taxa compositions of the stomach contents with those of zooplankton captured concurrently in the oblique hauls at four stations (Table 1). The four samples represent the early summer and fall of the Transition Domain and the Subtropical Region, as defined by Favorite et al. (1976). 509
2 Fig. 1. Location of rectangular midwater sampling trawl in the northwestern North Pacific during cruises of the T/S Hokusei- Maru and T/S Oshoro-Maru; due to the close proximity of certain stations of the same cruise, only 20 of the 28 stations are depicted. Lines represent boundaries between the Subarctic Domain (SA), Transition Domain (TR) and Subtropical Region (ST); the Subarctic boundary was located between about 38 and N, and the northern boundary of the Transition Domain was located between about 43 and 46 N during sampling periods. Details of the station data are given in Table 1. Prey composition data were grouped by the different oceanographic areas and seasons, and compared with the relative abundances of zooplankton collected. Since few specimens were collected from the Subarctic Domain, they were excluded from the analyses. During both summer (June July 1988 and June 1995) and fall (November 1995), few similarly sized fishes were caught in both the Transition Domain and the Subtropical Region, so to compare the feeding habits between areas, data from all fish collected at other stations in the same area and season were pooled. The sampling stations were divided into four groups: Transition-summer (June 1988, 1995), Transitionfall (November 1995), Subtropical-summer (June July 1988, June 1995) and Subtropical-fall (November 1995). 3. Results 3.1 Length frequency distributions The sizes of Gonostoma gracile collected ranged from 19 to 116 mm in standard length (SL); the length frequency distribution was multimodal (Fig. 2). During both summer and fall, most of the fish smaller than 60 mm SL were caught in the Subtropical Region, whereas most larger than 60 mm SL were caught in the Transition Domain. Median sizes during summer were significantly larger than during fall in both the Subtropical Region and the Transition Domain (Mann-Whitney U test, p < 0.05). Fig. 2. Length frequency distribution of Gonostoma gracile by oceanographic areas during early summer and fall. 510 K. Uchikawa et al.
3 Table 1. Sampling data for the rectangular midwater trawl collections made during cruises of T/S Hokusei-Maru and T/S Oshoro- Maru. Stations were divided into Subarctic Domain (SA), Transition Domain (TR) and Subtropical Region (ST). Date Time Latitude (N) Longitude (E) Sampling depth (m) Area :30 19: ST :53 20: TR :33 19: SA :17 22: SA :24 20: TR :37 20: ST :07 20: ST :31 19: ST :02 10: ST :47 20: ST :42 20: SA :30 19: ST :25 20: ST * 18:18 19: ST :30 20: ST :17 19: TR :25 20: TR :13 18: TR :03 20: TR * 18:23 18: TR :04 19: TR :16 19: ST :25 18: ST :42 19: ST * 18:24 19: ST :57 21: ST * 3:38 5: TR :00 18: TR *Stations where zooplankton samples were examined. 3.2 Diet composition Of the 520 stomachs examined, 199 (38.2%) were empty. Only one individual showed signs of regurgitation and none had everted stomachs, suggesting that neither regurgitation nor stomach eversion biased the analyses. To analyze ontogenetic differences in the diet, specimens were divided into three body size classes: small (<40 mm), medium (40 < 60 mm) and large ( 60 mm). In all size classes, crustaceans formed the largest component ( % by number) of the diet and were dominated by copepods (Table 2). Prey included more than 24 copepod species, but the diet was dominated by only a few taxa. The most abundant family in all size classes was the Metridinidae, constituting % of the total number of prey identified and % of the total number of copepods. For the small size class, metridinid copepods of the genus Pleuromamma were the most abundant, constituting 25.5% of the prey identified and 46.1% of the copepods. Podopleans, such as Oncaea, were also abundant prey for the small size class, constituting 12.4% of the prey identified and 22.4% of the copepods. Pleuromamma was also the most abundant prey for the medium and large size classes, accounting for 12.2% of the prey and 33.3% of the copepods for the medium size class, and 24.5% of the prey and 32.0% of the copepods for the large size class. The genus Metridia composed 17.8% of the copepods in the medium size class. Neocalanus constituted 12.4% of the copepods ingested by the large size class, but less than 6% of the copepods in the smaller size classes. The other 14 copepod genera were less numerous in all size classes, constituting fewer than 8.9% of the copepods ingested (Table 2). The second most abundant prey group was the ostracods, most of which were represented by the genus Conchoecia. Ostracods constituted 38.0 and 35.2% of the total number of prey in the small and medium size classes, Feeding Habits of the Mesopelagic Fish Gonostoma gracile in the Northwestern North Pacific 511
4 Table 2. Diet of three size classes of Gonostoma gracile in the northwestern North Pacific Ocean. Cn: % of identifiable prey to the total number; F: % frequency of occurrence of identifiable prey. respectively, and 20.1% in the large size class (Table 2). Thus, 93.5% of the prey identified for the small size class, and about 70% of the diet of the medium and large size classes were composed of copepods and ostracods. Other abundant prey taxa for the medium and large size classes were amphipods (13.8 and 18.4%, respectively) and euphausiids (7.1 and 13.5%, respectively). Decapod crustaceans, polychaetes and tunicates were also ingested, but accounted for less than 1.5% of the total number of prey in each fish size class. Prey size overlapped substantially among the three fish size classes (Fig. 3); all classes preyed heavily on 512 K. Uchikawa et al.
5 Table 2. (continued). Feeding Habits of the Mesopelagic Fish Gonostoma gracile in the Northwestern North Pacific 513
6 1 4 mm long prey organisms. However, median prey size increased with growth and differed significantly among the three size classes (Kruskal-Wallis test, p < 0.001). Median prey size of the large size class was only 0.3 mm longer than that of the medium size class, and 1.3 mm longer than that of the small size class. However, the maximum prey size of the large size class was much Fig. 3. Size-frequency distribution of G. gracile prey for the three different fish size classes. longer (18 mm) than that of the medium class (11 mm). In the small size class, prey smaller than 1 mm long composed 29% of the diet by number; 71% of this prey size group was composed of podopleans such as Oncaea. The medium and large size classes did not consume prey smaller than 1 mm long (Fig. 3). Of the prey larger than 4 mm long, 70% were euphausiids and amphipods in the medium and large size classes. 3.3 Prey selectivity All Transition-summer, Subtropical-summer and Subtropical-fall samples had similar diets, with copepods ( %) and ostracods ( %) as the two most abundant prey. In the Transition-fall sample, copepods (30.1%) and amphipods (30.1%) were equally abundant, followed by euphausiids (27.7%) and ostracods (8.4%). Although fish specimens in this sample were smaller than those in the other samples, they consumed larger prey. Of the identifiable copepods, Pleuromamma was the most numerous ( % of the prey identified) in the four samples (Table 3). Table 4 shows the composition of crustacean zooplankton collected at the four stations by the oblique tows. As described above, G. gracile fed almost exclusively on crustaceans, so only crustaceans were examined in this analysis. Copepods were the most numerically abundant, comprising more than ca. 70% of the total number of crustaceans in the four samples. Copepods were especially numerous in the Transition-summer sample, where they composed 97.3% of the total number. Ostracods constituted only a small proportion (<3.7%) of all samples, although they occurred more abundantly in the stomachs. The composition of crustacean zooplankton changed seasonally in the Transition Domain; the relative abundance of amphipods and euphausiids increased from summer to fall, i.e., from 0.7 to 10.7% for amphipods and from 0.9 to 12.0% for euphausiids. Since Table 3. Diet composition (Cn %) of Gonostoma gracile in the early summer and fall in the Transition Domain and the Subtropical Region; Subtropical-summer (ST-S), Subtropical-fall (ST-F), Transition-summer (TR-S), Transition-fall (TR-F). ST-S ST-F TR-S TR-F (N = 183) (N = 151) (N = 87) (N = 83) Mean fish size mm SL (mean ±S.D.) 45.6 (±15.0) 35.3 (±12.9) 71.2 (±17.6) 67.4 (±15.5) Prey group Copepoda Pleuromamma Ostracoda Amphipoda Euphausiacea Other Crustacea Polychaeta 9.1 Tunicata K. Uchikawa et al.
7 Pleuromamma was the most abundant prey taxon, we sorted Pleuromamma, comparing the proportion of Pleuromamma in the diet and the net samples. This varied 70-fold in the catches (Table 4), but only 3-fold in the diet (Table 3), a trend that was more evident when comparing the proportion of Pleuromamma in the total number of copepods. This proportion varied 200-fold ( %) in the net samples, but was fairly constant ( %) in the stomach contents. 4. Discussion A potential source of bias in the results of the present study arises from different rates of prey digestion. Softbodied organisms, such as larvaceans and eucalanid copepods, may be vulnerable to rapid digestion. By contrast, the abundant prey taxa, the copepod genus Pluromamma, are easily identified even in rather digested states, because species in this genus have a darkly pigmented metasomal organ. However, Hopkins and Baird (1981) stated that soft-bodied, non-crustacean prey could in some cases be recognized even in the intestines of midwater fishes. Additionally, we observed that copepods other than Pluromamma have exoskeletons that resist digestion, and that taxonomic characteristics of families or genera persist in well-digested states. For example, we could identify the soft-exoskeleton copepod Eucalanus even when its exoskeleton was considerably damaged. Thus, biases resulting from differential digestion rates of prey items do occur to some degree, but the diet composition in Table 2 represents reliable estimates for Gonostoma gracile collected in our study, and biases would not seriously affect the conclusions we discuss below. G. gracile is a typical crustacean feeder, preying mainly on copepods and ostracods. Fish larger than 40 mm SL also consumed euphausiids and amphipods. The median size of prey eaten by the three size classes of Table 4. Crustacean composition (%) of zooplankton samples collected with Gonostoma gracile in June and November in the Transition Domain and the Subtropical Region. Abbreviations for oceanographic areas and seasons as in Table 3. Zooplankton taxa ST-S ST-F TR-S TR-F Copepoda Pleuromamma Ostracoda Amphipoda Euphausiacea Decapoda Mysidacea < <0.1 <0.1 Unident. Crustacea 0.1 <0.1 G. gracile shifted with growth (Fig. 3). Prey smaller than 1 mm, such as podopleans, were consumed only by the 20 < 40 mm fish, whereas amphipods and euphausiids increased in importance with growth (Table 3). In many mesopelagic fishes, smaller individuals feed mainly on copepods and ostracods, whereas larger ones shift toward euphausiid-based diets (Tyler and Pearcy, 1975; Scotto di Carlo et al., 1982; Young and Blaber, 1986; Lancraft et al., 1988). However, in the present study, copepods and ostracods were the most abundant prey taxa for all size classes. In addition, the prey size spectra overlapped substantially among the three size classes, suggesting that although maximum prey size increased with growth, the ontogenetic dietary shift appears to be limited. In other words, this nonmigratory gonostomatid fish preys on a wide size rage throughout its life history, which would seem to demonstrate adaptive behavior in an ambush-type feeder. Seasonal variation in the diet was low in the Subtropical Region but high in the Transition Domain. This variation was not due to any difference in fish size, since the difference was contrary to the ontogenetic pattern expected from differences in fish size. Rather, the variation was probably due to the seasonal dynamics of the zooplankton community, because the relative abundances of amphipods and euphausiids during fall were higher than during summer in the Transition Domain. Pleuromamma was the most abundant prey taxon in the spatio-temporally different samples. The proportion that Pluromamma formed of the total number of copepods in the diet was disproportionate to the proportion in the trawl net. Pleuromamma undertakes a strong diel vertical migration (Ambler and Miller, 1987; Bennett and Hopkins, 1989), while G. gracile does not, remaining at m depth at night (Kawaguchi, 1973). So the relative abundance of Pleuromamma at the depths inhabited by G. gracile was underestimated due to the presence of epipelagic zooplankters in the samples. However, the proportion of Pleuromamma in the total number of copepods in the net varied widely from 0.1 to 20.2%, while the proportion in the fish stomachs varied only from 40.5 to 51.4%, suggesting that G. gracile feeds on Pleuromamma regardless of its relative abundance. The occurrence of ostracods in the diet (13 38%) was also disproportionate to the numbers in the trawl samples (<4%). We conclude that G. gracile feeds preferentially on Pleuromamma and ostracods. Similar results have been reported in previous studies of a number of midwater fishes, including gonostomatid, myctophid and sternoptychid species (e.g., Merrett and Roe, 1974; Hopkins and Baird, 1977, 1981, 1985; Clarke, 1980; Kinzer and Schulz, 1985; Lancraft et al., 1988; Sameoto, 1988). Feeding Habits of the Mesopelagic Fish Gonostoma gracile in the Northwestern North Pacific 515
8 All metrinid copepods, including Pleuromamma and Metridia, and probably all conchoeciid ostracods, are luminescent (Herring, 1985, 1988). G. gracile feeds preferentially on these zooplankters. Furthermore, Metridia was an abundant prey item for 40 mm SL fish, and Oncaea, a genus of densely pigmented copepods (Clarke, 1980), was abundant for <40 mm fish, suggesting that G. gracile feeds selectively on luminescent or densely pigmented crustaceans. This suggests in turn that visual detection is an important feeding mode of G. gracile. It has been proposed that some mesopelagic fishes feed preferentially on more visible, densely pigmented crustaceans (Clarke, 1980, 1982). Scotto di Carlo et al. (1982) also reported that two myctophid species feed selectively on bioluminescent copepods, including Pleuromamma. Light signals can easily be detected and located at considerable distances in deep water (Young, 1983), where they may serve as good signals for locating prey. However, predation on luminescent organisms can be dangerous for predators if the luminescent zooplankters attract other predators after they are ingested (this is termed the burglar alarm hypothesis by Burkenroad (1943)). The body and digestive tract of G. gracile are covered with thick black pigment, which suggests that this might be an adaptation to conceal ingested luminescent prey (McAllister, 1967). Additionally, Gartner et al. (1997) suggested that, at depth, nonmigratory zooplanktivores are less active than migratory zooplanktivores. These nonmigrant mesopelagic fish seem to adopt an ambush predation strategy (Borodulina, 1972; DeWitt and Cailliet, 1972). In the dark, G. gracile may wait passively and capture bioluminescent crustaceans that flash in their vicinity. Acknowledgements K. Uehara, R. Tamura and the captains, officers and crews of T/S Hokusei-Maru and T/S Oshoro-Maru helped us with sampling at sea. We thank J. R. Bower for his helpful comments on the manuscript and N. Shiga for assistance in the laboratory. We are also grateful to H. Ogi, S. Sakano, K. Shimazaki and A. Yamaguchi for their helpful discussions. References Ambler, J. W. and C. B. Miller (1987): Vertical habitat-partitioning by copepodites and adults of subtropical oceanic copepods. Mar. Biol., 94, Bennett, J. L. and T. L. Hopkins (1989): Aspects of the ecology of the calanoid copepod genus Pleuromamma in the eastern Gulf of Mexico. Cont. Mar. Sci., 31, Borodulina, O. D. (1972): The feeding of mesopelagic predatory fish in the open ocean. J. Ichthyol., 12, Burkenroad, M. D. (1943): A possible function of bioluminescence. J. Mar. Res., 5, Clarke, T. A. (1980): Diets of fourteen species of vertically migrating mesopelagic fishes in Hawaiian waters. Fish. Bull. U.S., 78, Clarke, T. A. (1982): Feeding habits of stomiatoid fishes from Hawaiian waters. Fish. Bull. U.S., 80, DeWitt, F. A., Jr. and G. M. Cailliet (1972): Feeding habits of two bristlemouth fishes, Cyclothone acclinidens and C. signata (Gonostomatidae). Copeia, 1972, Favorite, F., A. J. Dodimead and K. Nasu (1976): Oceanography of the Subarctic Pacific Region, Int. North Pac. Fish. Comm. Bull., 33, Gartner, J. V., Jr., R. E. Crabtree and K. J. Sulak (1997): Feeding at depth. p In Deep-Sea Fishes, ed. by D. J. Randall and A. P. Farrell, Academic Press, London. Gordon, J. D. M., S. Nishida and T. Nemoto (1985): The diet of mesopelagic fish from the Pacific coast of Hokkaido, Japan. J. Oceanogr. Soc. Japan, 41, Gorelova, T. A. (1981): Notes on feeding and gonad condition in three species of the genus Gonostoma (Gonostomatidae). J. Ichthyol., 21, Grey, M. (1960): A preliminary review of the family Gonostomatidae, with a key to the genera and the description of a new species from the tropical Pacific. Bull. Mus. Comp. Zool. Harvard, 122, , Figs Herring, P. J. (1985): Bioluminescence in the crustacea. J. Crust. Biol., 5, Herring, P. J. (1988): Copeod luminescence. Hydrobiologia, 167/168, Hopkins, T. L. and R. C. Baird (1977): Aspects of the feeding ecology of oceanic midwater fishes. p In Oceanic Sound Scattering Prediction, ed. by N. R. Anderson and B. J. Zahuranec, Plenum Press, New York. Hopkins, T. L. and R. C. Baird (1981): Trophodynamics of the fish Valenciennellus tripunctulatus. I. Vertical distribution, diet, and feeding chronology. Mar. Ecol. Prog. Ser., 5, Hopkins, T. L. and R. C. Baird (1985): Aspects of the trophic ecology of the mesopelagic fish Lampanyctus alatus (Family Myctophidae) in the eastern Gulf of Mexico. Biol. Oceanogr., 3, Kawaguchi, K. (1967): Biology of Gonostoma gracile (Gonostomatidae) I. Morphology, life history and sex reversal. Inform. Bull. Planktol. Japan, Commemoration Number of Dr. Matsue, 1967, Kawaguchi, K. (1969): Ecological studies on meso- and bathypelagic micronektonic fishes in the western North Pacific Ocean. Ph.D. Thesis, Univ. Tokyo, Tokyo, 221 pp. (in Japanese). Kawaguchi, K. (1971): Gonostomatid fishes of the western north Pacific. Japan. J. Ichthyol., 18, Kawaguchi, K. (1973): Biology of Gonostoma gracile Günther (Gonostomatidae) II. Geographical and vertical distribution. J. Oceanogr. Soc. Japan, 29, Kinzer, J. and K. Schulz (1985): Vertical distribution and feeding patterns of midwater fish in the central equatorial Atlantic. I. Myctophidae. Mar. Biol., 85, Lancraft, T. M., T. L. Hopkins and J. J. Torres (1988): Aspects of the ecology of the mesopelagic fish Gonostoma elongatum (Gonostomatidae, Stomiiformes) in the eastern Gulf of Mexico. Mar. Ecol. Prog. Ser., 49, K. Uchikawa et al.
9 McAllister, D. E. (1967): The significance of ventral bioluminescence in fishes. J. Fish. Res. Bd. Can., 24, Merrett, N. R. and H. S. J. Roe (1974): Patterns and selectivity in the feeding of certain mesopelagic fishes. Mar. Biol., 28, Miya, M., M. Yamaguchi and M. Okiyama (1995): Midwater fishes off the Pacific coast of Boso Peninsula, central Japan: species composition, abundance, biomass, and zoogeographic affinities. Japan. J. Ichthyol., 42, Sameoto, D. D. (1988): Feeding of lantern fish Benthosema glaciale off the Nova Scotia Shelf. Mar. Ecol. Prog. Ser., 44, Scotto di Carlo, B., G. Costanzo, E. Fresi, L. Guglielmo and A. Ianora (1982): Feeding ecology and stranding mechanisms in two lanternfishes, Hygophum benoiti and Myctophum punctatum. Mar. Ecol. Prog. Ser., 9, Tyler, H. R. and W. G. Pearcy (1975): The feeding habits of three species of lanternfishes (Family Myctophidae) off Oregon, USA. Mar. Biol., 32, Young, J. W. and S. J. M. Blaber (1986): Feeding ecology of three species of midwater fishes associated with the continental slope of eastern Tasmania, Australia. Mar. Biol., 93, Young, R. E. (1983): Oceanic bioluminescence: an overview of general functions. Bull. Mar. Sci., 33, Feeding Habits of the Mesopelagic Fish Gonostoma gracile in the Northwestern North Pacific 517
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