Mesozooplankton response to iron enrichment during the diatom bloom and bloom decline in SERIES (NE Pacific)

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Abstract

A mesoscale iron-fertilization experiment was carried out in the eastern subarctic Pacific during summer 2002. The iron patch was traced for 26 days after the enrichment, and the abundance and behavior of mesozooplankton was compared with those outside of the patch during the first half of the experiment (days 2–18) by Sastri and Dower [2006. Mesozooplankton community response during the SERIES iron enrichment experiment in the subarctic NE Pacific. Deep-Sea Research Part II.) and during the post-enrichment diatom bloom and its period of decline (days 15–26; this paper). The surface chlorophyll-a concentration in the patch was high between days 15 and 17 (6 mg m−3) and decreased to 1.4 mg m−3 at the end of the observation. Dominant zooplankton species in the upper 200 m were copepods: Eucalanus bungii, Pseudocalanus spp., Neocalanus plumchrus, N. cristatus, and Metridia pacifica. Species composition did not change significantly in the patch over the observation period. However, shallower distribution depths of E. bungii, N. cristatus and M. pacifica were observed in the patch during and after the diatom bloom. Especially, E. bungii was mainly distributed in the subsurface layer outside of the patch, but it was mainly in the surface mixed layer inside the patch, where it also had an enhanced development rate and increased biomass. We also propose the accumulation mechanism of zooplankton in the patch due to the upward immigration. Moreover, the abundance of the first copepodite stage of E. bungii and calyptopis larvae of euphausiids increased several fold in the patch compared to the densities outside the patch. The increases in both species are considered to be due to lowered mortality during the egg and naupliar stages, which was caused by lowered relative importance of eggs and nauplii in the diets of the suspension-feeding omnivores in the patch due to increased diatom abundance during the diatom bloom. Gut-pigment contents of dominant copepods in the patch increased 6–8 times, and the maximum values were observed during the bloom peak. The grazing impact on phytoplankton was low during the bloom period, but increased in the declining period of the diatom bloom.

Introduction

Several mesoscale iron fertilization experiments have been carried out in the major high-nitrate, low-chlorophyll (HNLC) regions to test the iron deficiency hypothesis (Martin and Fitzwater, 1988) and to investigate the ecosystem responses to iron addition (Martin et al., 1994; Coale et al., 1996; Boyd et al., 2000; Tsuda et al., 2003). In most experiments, phytoplankton standing stocks largely increased with iron addition accompanied by significant drawdown of pCO2 and macronutrients. The time scales of the iron-induced blooms ranged from a few days to over a month, presumably depending on the temperature, light availability and retention mechanisms of the bio-available iron concentration (Abraham et al., 2000; Tsumune et al., 2005). In HNLC regions, pico- and nano-phytoplankton are dominant throughout the year (e.g., Booth et al., 1993), and the production of these organisms is considered to be balanced with the grazing by microzooplankton (Strom and Welschmeyer, 1991; Tsuda and Kawaguchi, 1997). However, diatoms, micro-sized phytoplankton, became the most dominant taxa in the phytoplankton communities in the iron-enriched water masses, although pico- and nano-phytoplankton such as prymnesiophytes also show enhanced growth rates with iron addition (Gall et al., 2001; Suzuki et al., 2005; Tsuda et al., 2005a). The enhanced growth rate and increases in size and abundance of phytoplankton are considered to improve the food availability to meso-zooplankton.

In IronEX II (Coale et al., 1996), the abundance of small copepods increased due to the improved food availability and behavioral change (diel vertical migrators remaining in the surface layer during the daytime in the iron patch) during 1 week and then decreased in the later half of the experiment, presumably due to predation (Rollwagen Bollens and Landry, 2000). Arrested migration of mesozooplankton was considered as an important cause of the relatively small increase of phytoplankton abundance and small decrease in macronutrients and pCO2 in the enriched water of IronEx II (van Scoy and Coale, 1994; Banse, 1995; Cullen, 1995). In contrast, Southern Ocean mesozooplankton, which were dominated by large copepods, showed neither a detectable biomass change during the 2 week observation period, nor a significant contribution to the export flux from the euphotic layer (Zeldis, 2001). Moreover, in SEEDS which was conducted in the western subarctic Pacific, detectable changes in mesozooplankton biomass, vertical distribution, and diel vertical migration were not observed during the 2 week period (Tsuda et al., 2005b). However, abundance of the first copepodite stage of surface resident copepods (Neocalanus plumchrus and E. bungii) significantly increased after the formation of the diatom bloom in SEEDS. The increases of both species were considered to be due to lowered predation mortality during the egg and nauplius stages, which was caused by the increase in an alternative food source (diatoms).

Responses by mesozooplankton to diatom blooms induced by iron addition have been different in each experiment, which presumably is caused by differences in species composition of mesozooplankton and phytoplankton, and the seasonal timing of the experiments. More importantly, it is only possible to observe these functional and numerical responses by using ecosystem-scale experiments.

Similar species of mesozooplankton are distributed in both the Alaskan (AG) and western subarctic gyres (WSG) (Mackas and Tsuda, 1999). However, there are considerable differences between eastern and western subarctic Pacific in timing of the seasonal stratification (Parsons and LeBraseur, 1968), chlorophyll concentrations (Sugimoto and Tadokoro, 1997; Banse and English, 1999), phytoplankton taxonomic composition (Obayashi et al., 2001), iron deficiency indicated by photochemical quantum efficiencies of the algal photosystem II (Suzuki et al., 2002), and dust flux (Duce and Tindale, 1991). Moreover, some species of dominant copepods show different life cycles between the AG and WSG (Miller et al., 1984; Miller and Clemons, 1988; Tsuda et al., 1999, Tsuda et al., 2004).

The iron enrichment experiment in the eastern subarctic Pacific (SERIES) was carried out in the summer of 2002 with a relatively long observation period (26 d) that covered both the development and decline of the bloom (Boyd et al., 2004). Initially, iron fertilization caused an increase in prymnesiophytes, and then an increase in diatoms after the decline of prymnesiophyte bloom (Marchetti et al., 2006). Mesozooplankton responses during the first half of the experiment (D2–D18) are presented by Sastri and Dower (2006). They showed that species composition did not change throughout their observation period, but the abundance and biomass of E. bungii significantly increased in the patch. We focused on the functional and numerical responses of mesozooplankton during the iron-induced diatom bloom and its declining phase (D14–D26) by employing vertically stratified sampling to add to our knowledge of the effects of iron enrichment on marine ecosystems.

Section snippets

Materials and methods

A mesoscale in situ iron-enrichment experiment, SERIES (Subarctic Ecosystem Response to Iron Enrichment Study), was conducted in the Alaskan gyre of the North Pacific (50°20′N, 145°45′W) from 9 July to 4 August 2001 by R.Vs. J.P. Tully, El Puma and Kaiyo-Maru. The experiment consisted of two additions of iron as FeSO4 with an inert tracer gas, sulphur hexafluoride (SF6), over a 77 km2 patch on 9 July 2002. Day 1 (D1) is defined as the 24-h period starting at 00:00 10 July 2002. The iron-patch

Composition and biomass

Copepods accounted for 71% and 65% of the mesozooplankton biomass, inside and outside of the patch, respectively (Fig. 2), and the difference between inside and outside was significant (t-test for log-transformed data, p<0.05). Moreover, a significant increase in copepods biomass was observed for both inside and outside of the iron-patch. The slope of the biomass increase was higher inside than outside the patch. Euphausiids accounted for 8% and 10% of the mesozooplankton biomass, inside and

Community composition and seasonal timing

Copepods that show vertical migration as part of their ontogenetic development, especially E. bungii, accounted for the major part of the mesozooplankton biomass in this study. These copepods have annual or biennial life cycles in the subarctic Pacific (Miller et al., 1984; Miller and Clemons, 1988; Tsuda et al., 1999, Tsuda et al., 2004). Miller et al. (1984) suggested that main spawning period of E. bungii was the beginning of July and the peak abundance of young copepodites (C1 and C2) was

Acknowledgments

The authors express their thanks to the captains and crew members of the F.R.V. Kaiyo-Maru of the Fisheries Agency of Japan and all the participants of the cruise for their cooperation at sea. We are also grateful to Drs. D.L. Mackas, P.J. Harrison and anonymous reviewers for their helpful comments and suggestions. This research was supported by Global Environment Research Fund from the Ministry of the Environment of Japan.

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