Influence of the late winter bloom on migrant zooplankton metabolism and its implications on export fluxes

Abstract

Studies on carbon active fluxes due to diel migrants are scarce and critical for carbon flux models and biogeochemical estimates. We studied the temporal variability and vertical distribution of biomass, indices of feeding and respiration of the zooplanktonic community north off the Canary Islands during the end of the late winter bloom, in order to assess vertical carbon fluxes in this area. Biomass distribution during the day presented two dense layers of organisms at 0–200 m and around 500 m, whereas at night, most of the biomass concentrated in the epipelagic layer. The gut pigment flux (0.05–0.18 mgC·m^− 2·d^− 1) represented 0.22% of the estimated passive export flux (POC flux) while potential ingestion represented 3.91% of the POC (1.24–3.40 mgC·m^− 2·d^− 1). The active respiratory flux (0.50–1.36 mgC·m^− 2·d^− 1) was only 1.57% of the POC flux. The total carbon flux mediated by diel migrants (respiration plus potential ingestion) ranged between 3.37 and 9.22% of the POC flux; which is three-fold higher than calculating ingestion fluxes from gut pigments. Our results suggest that the fluxes by diel migrants play a small role in the downward flux of carbon in the open ocean during the post-bloom period.

Introduction

Understanding the mechanisms involved in the production cycle of the subtropical waters is needed to elucidate the fate of organic matter produced in these large areas of the ocean. A process involved is the annually observed productive pulse named late winter bloom (Menzel and Ryther, 1961). In subtropical waters this bloom is due to erosion of the thermocline driven by surface cooling that enhances vertical diffusion of nutrients from below the mixed layer. Its influence in relation to the particle formation, transformation and flux is obvious. The late winter bloom in the Canary Island waters is fairly well known from the standpoint of plankton biomass and production (De León and Braun, 1973, Arístegui et al., 2001, Hernández-León et al., 2004). In general, primary production and chlorophyll a increase from January to March and decrease during April (Arístegui et al., 2001). Zooplankton biomass closely follows phytoplankton, developing through February, reaches a maximum in March and decreases in April. The evolution of zooplankton biomass and metabolic activity during this annual event is well described (Hernández-León et al., 2004). However, our knowledge of the influence of productive pulses on the active carbon flux mediated by diel vertical migration is scarce.

Vertical migration is a common feature in zooplankton communities and also one of the most important movements of biomass in the ocean (Atkinson et al., 1992, Buskey and Swift, 1983, Enright, 1977). A review by Hutchinson (1967) examines some hypothesis to explain the adaptive significance of vertical migration. The influence of sunlight, modified by other physical and biological factors, and the attempt to avoid visual orientating predators (Zaret and Suffern, 1976) are the most common explanations for this particular behavior. Other authors (Bollens and Frost, 1991, Frost, 1988, Gliwicz, 1986, Pinot and Jansá, 2001) support these conclusions. Diel-migrant zooplankton usually migrates to the surface to feed at night and returns to deeper layers at dawn (Lampert, 1989). By feeding in shallower layers and defecating, respiring, excreting and dying at depth, migrant organisms play a determining role in the vertical downward flux of particulate and dissolved matter in the water column (Longhurst et al., 1990, Longhurst and Harrison, 1988). This active flux is a complex mechanism composed by a sum of different components. The flux of particulate carbon due to the production of fecal pellets in the mesopelagic zone is the so-called “gut flux” (Angel, 1985, Hu, 1978). A more subtle transport to the mesopelagic zone is the vertical flux of dissolved carbon caused by the night time feeding at the shallower layers and the daytime respiration of the diel migrant biota at depth (Longhurst and Harrison, 1988, Longhurst and Harrison, 1989, Longhurst et al., 1990, among others). Several studies (Dam et al., 1995, Longhurst et al., 1989, Longhurst et al., 1990, Longhurst and Harrison, 1988, Steinberg et al., 2008, Yebra et al., 2005, Zhang and Dam, 1997) show that respiratory carbon from diel migrant biota below the epipelagic zone during daytime represents a significant pathway of downward transport of carbon compared to the gravitational vertical flux. The active flux also includes the fluxes due to mortality at depth (Dam et al., 1995), dissolved organic excretion (Steinberg et al., 2000) and predatory activity (Hernández-León, 1998, Hernández-León et al., 2001a, Hernández-León et al., 2002, Hernández-León et al., 2004). Nevertheless, the respiratory flux jointly with the gut flux are two main components of the biological pump in the ocean when compared to the passive or gravitational flux (Steinberg et al., 2000, Zhang and Dam, 1997).

The gut pigment flux can be calculated with the gut fluorescence method (Hernández-León et al., 2001b) while respiration of migrants can be assessed using an average value of respiration at depth (under 200 m depth) or, alternatively, measuring the electron transfer system activity (ETS, Packard, 1971) to obtain detailed profiles of in situ potential respiration at depth. The use of ETS activity to approach metabolic rates is not straightforward. However, it provides us with an in situ instantaneous cellular respiration rate much more accurate than simple estimations based on body size, abundance and temperature (Putzeys and Hernández-León, 2005). Therefore, determining the in situ potential respiration and the pigments contained in the gut of migrants we obtain an overview of the migrant community metabolic level during the study period.

Diet is the starting point of metabolism and it is clear that a diet shift could have an influence on the active carbon fluxes. Estimates of the carbon transported from surface to deep waters by diel vertical migration are rare and critical for carbon flux models and biogeochemical estimates. There are also few studies on the temporal development of the late winter bloom in oceanic waters of the subtropical gyre. None of them deals with the possible impact of a diet change on the biological pump efficiency. We determined the vertical distribution of mesozooplankton (200–1000 μm) biomass (as protein content), indices of gut fullness (gut fluorescence) and respiration (ETS activity) in order to calculate the contribution to carbon export flux by diel vertical migrants at the end of the late winter bloom north off the Canary Islands.