JOURNAL OF PLANKTON RESEARCH j VOLUME 27 j NUMBER 11 j PAGES 1113–1125 j 2005 Interannual variability in a predator–prey interaction: climate, chaetognaths and copepods in the southeastern Bering Sea C. T. BAIER1* AND M. TERAZAKI2 1 2 NOAA/NMFS/AFSC, 7600 SAND POINT WAY, NE. BIN C 15700, SEATTLE, WA 98115-0070, USA AND OCEAN RESEARCH INSTITUTE, THE UNIVERSITY OF TOKYO,1-15-1 MINAMIDAI, NAKANO-KU, TOKYO 164-8639, JAPAN *CORRESPONDING AUTHOR: [email protected] Received June 6, 2005; accepted in principle August 25, 2005; accepted for publication September 28, 2005; published online October 5, 2005 Communicating editor: R.P. Harris The interaction of the chaetognath Sagitta elegans with the copepod community of the southeast Bering Sea middle shelf was examined in relation to environmental conditions during 1995–1999. Predation impact was estimated for 2 years, 1995 and 1997, using gut content analysis, experimentally derived digestion time (DT) and abundances of chaetognaths and prey. Pseudoca- lanus concentrations correlated with water temperature and Calanus marshallae with sea ice extent. Sagitta elegans were less abundant but individuals were larger in 1995, when C. marshallae predominated, compared to 1997, when Pseudocalanus and Acartia were the primary prey. Predation by S. elegans removed <1% standing stock dayÀ1 of Pseudocalanus or C. marshallae in 1995 and 1.7 to 2.3% of Pseudocalanus in 1997. The percent of the copepod community biomass required by chaetognaths was estimated to be <1% in 1995 compared with 8–12% in 1997. Calanus marshallae may be more vulnerable than Pseudocalanus to cumulative predation effects because of its reproductive strategy. The effect of chaetognath predation on the copepod community depends on which copepod species is predominant and its susceptibility to cumulative predation effects, as well as on daily predation impact, both of which varied between years with different climatic conditions. INTRODUCTION bloom occurs early in association with sea ice in March or April but is delayed until the water column stratifies in The southeast Bering Sea shelf is a highly productive May or June if ice retreats early or is absent (Stabeno region that supports an abundance of life, including mar- et al., 2001). Climatic variability during 1995–1999 was ine mammals, seabirds and commercially important fish. exceptional, spanning the range of ice extent and water The middle shelf in particular is an important habitat for temperature conditions observed over the southeast larval and juvenile fish, which provide forage for higher Bering Sea shelf during the past three decades (Wyllie- trophic levels (Napp et al., 2000). The Bering Sea is a high Echeverria and Wooster, 1998; Baier and Napp, 2003). latitude sea and a marginal ice zone, subject to great Understanding how copepod populations are affected seasonal and interannual fluctuations in environmental by climatic variability is an important step towards conditions. Sea ice dynamics dominate spring physical understanding the mechanisms that link climate and processes over the shelf. Sea ice is not formed in situ but higher trophic levels. Recent attention has focused on is formed in the northeast and pushed onto the southeast the importance of predation mortality on copepod popu- shelf by winds (Stabeno et al., 1998). Its presence, extent lations (Eiane et al., 2002; Hirst and Kiørboe, 2002). and persistence are highly variable. Sea ice dynamics Chaetognaths are abundant carnivores that feed on a directly affect the spring phytoplankton bloom: the variety of zooplankton and fish larvae, but their main doi:10.1093/plankt/fbi078, available online at www.plankt.oxfordjournals.org Published by Oxford University Press 2005. JOURNAL OF PLANKTON RESEARCH j VOLUME 27 j NUMBER 11 j PAGES 1113–1125 j 2005 prey are copepods (Feigenbaum and Maris, 1984). Sev- during which period temperature changed little and the eral studies have shown that chaetognath predation can water column was well mixed; this measurement was significantly affect populations of copepods (Szyper, intended to approximate that which zooplankton were 1978; Kimmerer, 1984; Stuart and Verheye, 1991). exposed to during their development prior to our May For example, Sameoto (Sameoto, 1973) estimated that sampling. These data and the timing of the bloom onset Sagitta elegans consumed 36% of annual secondary pro- were obtained from a subsurface biophysical mooring duction in Bedford Basin, making them the most impor- that was deployed in February of each year at Site 2 tant copepod predators there. Chaetognaths dominate (Stabeno et al., 2001) (Fig. 1). Water temperature was the zooplankton biomass over the southeast Bering Sea measured with either Seacat SBE 16-03 sensors or Min- inner shelf in late spring (Coyle and Pinchuck, 2002) and iature Temperature Recorders (MTR). WetLabs fluoro- around the Pribilof Islands in late summer (Schabetsberger meters at depths of 5–11 m generated a time series of et al., 2000; Ciannelli et al., 2004). Smith and Vidal fluorescence used to determine the timing of the spring (Smith and Vidal, 1986) found higher abundances of phytoplankton bloom (Hunt and Stabeno, 2002). Mean S. elegans in a cool year (1980) compared with a warm summer shelf-bottom temperature, which reflects condi- year (1981) and suggested that higher predation by tions during the previous winter, was measured using chaetognaths as well as lower temperatures may have temperature recording devices mounted on the head contributed to reduced numbers of small copepods over rope of bottom trawl gear, deployed during annual the middle shelf in 1980. Kotori (Kotori, 1976) estimated Alaska Fisheries Science Center bottom trawl surveys that the average abundance of S. elegans on the eastern of about 350 stations over the southeast Bering Sea Bering Sea shelf was 25 mÀ3, accounting for 0.4–60.5% shelf. The bottom trawl station grid extended from of the total zooplankton biomass in summer, and the 54.6 Nto61 N latitude and covered the outer and carbon requirement of the chaetognath community was middle shelf domains; only middle shelf temperatures 10% of secondary productivity. However, to our knowl- were used in our study (G. Walters, Seattle, personal edge there have been no quantitative studies of chaetog- communication). Ice cover along longitude 169 W was nath predation over the southeast Bering Sea shelf. digitized from weekly National Oceanic and Atmo- The present article builds upon a study of climate- spheric Administration (NOAA) ice charts (S. Salo, induced variability in populations of the copepod Calanus Seattle, personal communication). marshallae in the southeast Bering Sea (Baier and Napp, 2003). Here we examine the interaction of a predator, Zooplankton collections S. elegans, with the copepod community during years Zooplankton collections were made on the southeastern (1995–1999) with different climate conditions. Abun- Bering Sea middle shelf (Table I; Fig. 1). Samples were dances of chaetognaths and the dominant copepod spe- collected and experiments were conducted aboard the cies on the middle shelf were estimated during April and RV Miller Freeman. Zooplankton samples for interannual May of these years. Seasonal dynamics of chaetognaths comparisons were collected in April and May 1995– and their copepod prey were examined during February– 1999 using bongo or Tucker trawl (1996 only) tows. September 1998 and 1999. Diel feeding patterns were Additional samples collected in February, July and examined using data collected in May 2000. We quan- September 1998 and February and September 1999 were tified the effects of predation by the chaetognath S. elegans examined for seasonal patterns of abundance and cope- on copepods during April and May of 1995 and 1997. pod stage composition. At each station, temperature was sampled using a SeaBird 911+ CTD; these data were METHOD averaged over the depth of the water column. Bongo samplers were 60- and 20-cm diameter frames fitted with 333- and 153-mm mesh nets, respectively. The 20-cm Environmental sampling bongo was attached to the towing wire 1 m above the 60- Environmental variables including mean water tempera- cm frame (Incze et al., 1997). A SeaCat CTD was located 1 ture at 20 m, timing of the phytoplankton bloom, mean m above the 20-cm frame to supply real-time measurements summer shelf bottom temperature and sea ice extent of net depth. Double oblique tows were made 5–10 m were compared with patterns of zooplankton abun- above the bottom, at a speed of 2 knots with tow durations dance. Average water column temperature from CTD ranging from 6 to 9 min. Calibrated flowmeters were used to profiles at each station where chaetognaths were col- estimate the volumes filtered by each net. Clarke-Bumpus lected for feeding rate (FR) estimation were used in nets (153-mm mesh) were nested inside each 1-m2 Tucker digestion and FR calculations. The mean temperature trawl net (333-mmmesh).Thetrawlwastowedfrom5moff at 20 m depth was measured from March 14–April 30, the bottom to the bottom of the thermocline (net 1) and from 1114 C. T. BAIER AND M. TERAZAKI j INTERANNUAL VARIABILITY IN A PREDATOR–PREY INTERACTION Fig. 1. Locations of moored sensors (mooring 2) and zooplankton/CTD sampling stations for 1995–1999. the bottom of the thermocline to the surface (net 2) using and Identification Center, Szczecin, Poland. Chaetognaths wire angle and length of wire out to calculate gear depth. were identified to species only for 1995 and 1997, and S. Data from the depth-discrete Tucker trawl samples were elegans was the only species found. Subadult Acartia spp. and averaged over depth for comparison with bongo tows. All nauplii of all copepod species were excluded from the samples were preserved in 5% formalin : seawater. Samples counts, because these small stages were not quantitatively were enumerated, copepods identified and staged, and retained by the net mesh sizes used. Sorted subsamples chaetognaths separated out at the Polish Plankton Sorting were returned to Seattle.