Polar Biol (2001) 24: 299±302 DOI 10.1007/s003000100227
SHO RT N OTE
Jun Nishikawa á Atsushi Tsuda
Diel vertical migration of the tunicate Salpa thompsoni in the Southern Ocean during summer
Accepted: 20 December 2000 / Published online: 8 February 2001 Ó Springer-Verlag 2001
Abstract Diel vertical migrations (DVM) of a pelagic tunicate, Salpa thompsoni, were investigated to help elucidate their life-history strategy in the Southern Ocean. S. thompsoni began migration to the subsurface at midday when the solar radiation is largest, stayed in the phytoplankton-rich and rather bright layer (30± 120 m) for a relatively long time, and then moved up to the surface only during complete darkness. This DVM pattern would have an advantage in increasing the feeding opportunities for salps. Although the longer stay at a bright depth may also increase the risk of predation by potential visual predators, the overlap of the depths between salps and visual predators was considered to be low during the stay in the shallow layer. The unique DVM of S. thompsoni may be an adaptation to the oligotrophic environments of the oceanic Southern Ocean, and one of the characteristics that enable them to maintain large stocks in the ocean. There is no doubt that the pelagic tunicate, Salpa thompsoni, is one of the most thriving macrozooplankters in the oceanic region of the Southern Ocean, together with Euphausia superba. When we consider the reasons for the success of these macrozooplankters in the extreme conditions of the Southern Ocean pelagic realm, certain specialized adaptive strategies found in these animals stand out. Smetacek et al. (1990) suggested that E. superba have the unique adaptive strategy of utilizing ice algae for overwintering and that this enables the maintenance of large stocks. Higher recruitment levels for krill were correlated with larger sea-ice extenJ. Nishikawa (&) á A. Tsuda Ocean Research Institute, University of Tokyo, Minamidai, Nakano, Tokyo, 164-8639, Japan E-mail:
[email protected] Fax: +81-3-53516481 A. Tsuda Present address: Hokkaido National Fisheries Research Institute, Katsurakoi, Kushiro, Hokkaido 085-0802, Japan
sion and longer ice-cover duration (Siegel and Loeb 1995), thus supporting this suggestion. In S. thompsoni, however, biological information is still limited, and the mechanism by which salps maintain large stocks in the Southern Ocean has not been clari®ed. The goal of our work is to examine the strategy of S. thompsoni that enables them to thrive in the Southern Ocean. In this study, their detailed vertical distribution patterns are investigated, and potential advantages of the observed distribution patterns discussed. Successive net samplings were conducted at 64°20¢S, 140°00¢E, which are located to the north of the Antarctic Divergence (Fig. 1), using the ORI-VMPS (Vertical Multiple Plankton Sampler; mouth area 50 ´ 50 cm, 0.33 mm mesh; Terazaki and Tomatsu 1997), which can sample four layers every tow. Samplings were repeated eight times, from 500 m to the surface over 2 days (23 and 24 December 1994), near the surface-drifting buoy (Table 1). Salps in the zooplankton samples were counted and their abundances standardized to numbers m±2. In addition to the net samplings, vertical pro®les of water temperature, salinity and chlorophyll-a concentrations were obtained. Water temperature and salinity was measured with several CTD (SBE 9 plus with SBE 32 Carousel water sampler, SEA-BIRD Electronics) casts along the transect line on 140°E from 63°S to 65°S (Ocean Research Institute 1996). Water samples for measuring chlorophyll-a concentration were taken over 12 depth layers between 0 and 300 m. Chlorophyll-a concentrations were determined by the ¯uorometric method (Strickland and Parsons 1972). Water samples were ®ltered through a Whatman GF/F glass micro®ber ®lter and the pigments were extracted using N,Ndimethylformamide. The concentration of chlorophyll-a in the extracts was measured by ¯uorescence using a Turner Model 111 ¯uorometer on board. Solar radiation during the investigation period was measured with a pyranometer (S-185, Ishikawa Sangyo) mounted on deck. Large numbers of salps were observed throughout the entire investigation period. They were composed of a single species, S. thompsoni. The average density of salps
300
in the 0- to 500-m water column was 981 inds. m±2, and this varied between 156 and 2,297 inds. m±2 (Table 1). Clear nocturnal vertical migration was evident through the successional samplings (Fig. 2). S. thompsoni were mainly distributed in the upper 120-m layer during the night, where the abundance of food particles was relatively high as indicated by chlorophyll concentration, and below this depth during the daytime. The migration, however, did not follow the usual pattern: the upward migration started around midday when the level of solar radiation was highest, and the salps stayed in the 30- to 120-m, phytoplankton-rich layer a relatively long time. When the solar radiation fell to zero, the majority of the population came up to the surface.
Fig. 1 Water temperature (upper, °C) and salinity (lower, PSU) along 140°E. Position of a sampling station (triangle) and the area of the Antarctic Divergence (shaded) are indicated Table 1 Abundance of Salpa thompsoni in the 0- to 500-m water column collected with the ORI-VMPS Date (1994)
Time (hours)
Abundance (inds. m±2)
24 23 23 23 23 24 24 23
0120 0310 0615 0910 1200 1516 1813 2120
2297.4 307.6 240.7 156.4 479.6 1155.4 1206.9 2001.0
Dec. Dec. Dec. Dec. Dec. Dec. Dec. Dec.
The numerical density of S. thompsoni recorded in this study was as high as that reported previously in these areas (Nishikawa et al. 1995; Chiba et al. 1998). Nocturnal migration in S. thompsoni has been reported previously (Casareto and Nemoto 1986; Piatkowski et al. 1994). However, detailed study on their migration patterns has not been made. The timing of diel vertical migration (DVM) of zooplankton is primarily triggered by the daily change of the light (Haney 1988). The salp population started upward movement near the time when the solar radiation was strongest (Fig. 2), suggesting that the relative change in quantal intensity is a stimulus for initiating vertical migration, as demonstrated in marine copepods (Stearns and Forward 1984). The photo-behaviour of Antarctic salps is, however, still unclear; the swimming activity of mid-latitude species increased as light intensity diminished, and vice versa (Mackie and Bone 1977), but other species swim toward light sources (Madin 1990). It has been con®rmed to an extent from studies mainly on crustacean zooplankton that the adaptive advantage of the DVM by zooplankton is predator avoidance (from visual predators) (reviewed by Haney 1988; Lampert 1989). In S. thompsoni, to stay in the phytoplankton-rich and bright layer for a relatively long time would increase the feeding opportunity, and this would be adaptive in the oligotrophic environment of the oceanic Southern Ocean (El-Sayed 1984; Sakshaug and Holm-Hansen 1984; Heywood and Priddle 1987). However, this might also increase the risk of predation mortality by visual predators due to the longer daytime period during the austral summer. Although it is dicult to evaluate precisely whether this DVM pattern increases the predation risk during the stay in shallow, bright layers, it is likely that the overlap of vertical distributions between salps and their visual predators is a factor. Antarctic salps have been found in the guts of pelagic amphipods, ostracods, mysids, polychaetes, ®shes, and seabirds (Tickell 1964; Hopkins 1985; Harper 1987; Hopkins and Torres 1989; Hopkins et al. 1993), and ®shes and seabirds would be their visual predators. The mesopelagic ®shes, Electrona antarctica, Gymnoscopelus braueri, and Bathylagus antarcticus are recognized as salp predators (Hopkins 1985; Hopkins and Torres 1989; Hopkins et al. 1993), and they are all intensive nocturnal migrants (Torres et al. 1984; Lancraft et al. 1989). However, their peak abundances in vertical distribution during the night-time are below 160 m, except 0±300 m in Electrona antarctica (Lancraft et al. 1989), suggesting that the overlap of vertical distribution between salps and these ®shes may be small even if salps migrate up to the 30- to 120-m layer under the light. However, three albatrosses, Diomedea epomophora, D. melanophrys, and D. chrysostoma are known to attack salps from the air (Tickell 1964; Harper 1987). They are basically surface-seizing or shallow, plunging feeders (Oatley 1979; Harper et al. 1985), and most of their foraging is performed in the upper 10 m of water (Harper 1987; Prince et al. 1994). This suggests that the
301 Fig. 2 Vertical distribution of Salpa thompsoni (upper) and solar radiation (lower) as a function of time of day. ``Salp abundance'' indicates the relative abundance in each sampling period. The continuous and the broken line in arrows and the solar radiation curve indicate data taken on 23 and 24 December 1994, respectively. Total chlorophyll-a concentration is indicated on the right side of vertical distribution graphs
30- to 120-m layer would be a safe zone for salps against these predators. These gaps in the depth distribution between salps and their visual predators in the shallow, bright layer imply that the observed DVM behavior of S. thompsoni might not work to increase the predation mortality drastically, at least to these visual predators, although we do not know whether the observed DVM pattern was well adapted to predation avoidance or not. The gaps may be related to salps not being a major food source for these predators (e.g. Hopkins 1985). In conclusion, the observed DVM pattern in S. thompsoni would have the advantage of eective feeding in a food-rich layer, and this pattern may not increase markedly the predation pressure by the visual predators when they are distributed in the epipelagic layer under the sun during summer. More data on the DVM of S. thompsoni at various locations are necessary before drawing the conclusion that this DVM pattern is a common phenomenon in the Southern Ocean during the summer. However, the regional dominance of S. thompsoni may in part be supported by their unique vertical migration patterns, at least around the observed locations. Acknowledgements We are grateful to anonymous reviewers for critical reading of the manuscript. We also thank K. Kawaguchi, M. Terazaki and scientists aboard R/V Hakuho Maru for their cooperation and helpful discussions at sea. The captain, ocers and crew of R/V Hakuho Maru supported our study.
References Casareto BE, Nemoto T (1986) Salps of the southern ocean (Australian sector) during the 1983±84 summer, with special reference to the species Salpa thompsoni, Foxton 1961. Mem Natl Inst Polar Res Spec Issue 40: 221±239 Chiba S, Horimoto N, Satoh R, Yamaguchi Y, Ishimaru T (1998) Macrozooplankton distribution around the Antarctic Diver-
gence o Wilkes Land in the 1996 austral summer: with reference to high abundance of Salpa thompsoni. Proc NIPR Symp Polar Biol 11: 33±50 El-Sayed SZ (1984) Productivity of the Antarctic waters ± a reappraisal. In: Holm-Hansen O, Bolis L, Gilles R (eds) Marine phytoplankton and productivity. Lecture notes on coastal and estuarine studies, vol 8. Springer, Berlin Heidelberg New York, pp 19±34 Haney JF (1988) Diel patterns of zooplankton behavior. Bull Mar Sci 43: 583±603 Harper PC (1987) Feeding behaviour and other notes on 20 species of Procellariiformes at sea. Notornis 34: 169±192 Harper PC, Croxall JP, Cooper J (1985) A guide to foraging methods used by marine birds in Antarctic and Subantarctic seas. BIOMASS Handb 24: 1±22 Heywood RB, Priddle J (1987) Retention of phytoplankton by an eddy. Cont Shelf Res 7: 937±955 Hopkins TL (1985) Food web of an Antarctic midwater ecosystem. Mar Biol 89: 197±212 Hopkins TL, Torres JJ (1989) Midwater food web in the vicinity of a marginal ice zone in the western Weddell Sea. Deep Sea Res 36: 543±560 Hopkins TL, Ainley DG, Torres JJ, Lancraft TM (1993) Trophic structure in open waters of the marginal ice zone in the ScotiaWeddell con¯uence region during spring (1983). Polar Biol 13: 389±397 Lampert W (1989) The adaptive signi®cance of diel vertical migration. Funct Ecol 3: 21±27 Lancraft TM, Torres JJ, Hopkins TL (1989) Micronekton and macrozooplankton in the open waters near Antarctic ice edge zones (AMERIEZ 1983 and 1986). Polar Biol 9: 225±233 Mackie GO, Bone Q (1977) Locomotion and propagation of skin impulse in salps (Tunicata: Thaliacea). Biol Bull Mar Biol Lab Woods Hole 153: 180±197 Madin LP (1990) Aspects of jet propulsion in salps. Can J Zool 68: 765±777 Nishikawa J, Naganobu M, Ichii T, Ishii H, Terazaki M, Kawaguchi K (1995) Distribution of salps near the South Shetland Islands during austral summer, 1990±1991 with special reference to krill distribution. Polar Biol 15: 31±39 Oatley TB (1979) Underwater swimming by albatrosses. Cormorant 6: 31 Ocean Research Institute, University of Tokyo (1996) Preliminary report of the R/V Hakuho Maru Cruise KH94±4. Southern Ocean Expedition. Ocean Research Institute, University of Tokyo
302 Piatkowski U, Rodhouse PG, White MG, Bone DG, Symon C (1994) Nekton community of the Scotia Sea as sampled by the RMT 25 during austral summer. Mar Ecol Prog Ser 112: 13±28 Prince PA, Huin N, Weimerskirch H (1994) Diving depth of albatrosses. Antarct Sci 6: 353±354 Sakshaug E, Holm-Hansen O (1984) Factors governing pelagic production in polar oceans. In: Holm-Hansen O, Bolis L, Gilles R (eds) Marine phytoplankton and productivity. Lecture notes on coastal and estuarine studies, vol 8. Springer, Berlin Heidelberg New York, pp 1±18 Siegel V, Loeb V (1995) Recruitment of Antarctic krill Euphausia superba and possible causes for its variability. Mar Ecol Prog Ser 123: 45±56 Smetacek V, Scharek R, NoÈthig E-M (1990) Seasonal and regional variation in the Pelagial and its relationship to the life history cycle of krill. In: Kerry KR, Hempel G (eds) Antarctic ecosystems: ecological change and conservation. Springer, Berlin Heidelberg New York, pp 103±114
Stearns DE, Forward RBF Jr (1984) Copepod photobehavior in a simulated natural light environment and its relation to nocturnal vertical migration. Mar Biol 82: 91±100 Strickland JDH, Parsons TR (1972) A practical handbook of seawater analysis. Bull Fish Res Board Can 167 Terazaki M, Tomatsu C (1997) A vertical multiple opening and closing plankton sampler. J Adv Mar Sci Technol Soci 3: 127±132 Tickell WLN (1964) Feeding preferences of the albatrosses Diomedea melanophris and D. chrysostoma at South Georgia. In: Carrick R, Holdgate M, PreÂost J (eds) Biologie antarctique. Hermann, Paris, pp 383±387 Torres JJ, Lancraft TM, Weigle BW, Hopkins TL, Robinson BH (1984) Distribution and abundance of ®shes and salps in relation to the marginal ice-zone of the Scotia Sea. Antarct J US 19: 117±119
