The estimation of metabolism in the mesopelagic zone: Disentangling deep-sea zooplankton respiration
Introduction
Export flux from the epipelagic to the mesopelagic zone through the so-called biological pump in the ocean is driven by (1) passive or gravitational sinking of particulate organic matter, (2) physical mixing of particulate and dissolved organic matter, and (3) the active transport of carbon performed by diel vertical migrants (Buesseler et al., 2007). As an important component of this biological pump, zooplankton and micronekton ingest organic carbon in the epipelagic zone and then release it in the mesopelagic layer through respiration (Longhurst et al., 1990), egestion (Angel, 1989), excretion (Steinberg et al., 2000), and mortality (Zhang and Dam, 1997). Metabolism, mortality, and gut flux are thus the main physiological mechanisms of active flux. Mortality are rather difficult to estimate but it could be assessed from growth assuming steady-state conditions, and estimating it from respiration rates assuming normal values of assimilation and gross growth efficiencies (Ikeda and Motoda, 1978). Similarly, feeding could also be inferred from respiration (Ikeda and Motoda, 1978). Thus respiration rates are, therefore, of paramount importance to estimate the role of these organisms in exporting carbon to the mesopelagic layer.
Values of respiratory flux are obtained from the biomass of migrant organisms (night minus day biomass values in the epipelagic zone), and respiration rates measured in migrant organisms captured at night in the epipelagic zone. These values are, then, converted to respiration at depth using empirical or published Q10 values (e.g., Le Borgne and Rodier, 1997). Alternatively, values from published equations relating respiration, body size, and temperature (e.g., Ikeda, 1985, for zooplankton) are also used. The former approach was applied in the seminal papers by Longhurst et al., 1990, Dam et al., 1995, but most authors assessing respiratory flux used the equation given by Ikeda (1985) (e.g., Zhang and Dam, 1997, Al-Mutairi and Landry, 2001). Assuming a short or long-range migration also introduces a significant source of error because temperature vary with depth. Zhang and Dam (1997) used the mean temperature from 200 to 400 m depth (as the daytime residence of migrants) to estimate respiration rates from the equation by Ikeda (1985). However, they also estimated 23% lower values of respiratory flux considering the average temperature in the 200–1000 m water column.
Another approach to estimate respiration at depth is the measurement of the activity of enzymes related to respiration in the cell. The electron transfer system (ETS) activity is a methodology normally used to derive respiratory values at depth (e.g., Hernández-León et al., 2001, Yebra et al., 2005, Putzeys et al., 2011, Yebra et al., 2018, Hernández-León et al., 2019). Organisms are captured at different layers in the epi- and mesopelagic zone using multiple opening-closing nets, and stored in liquid nitrogen (−196 °C) once on board. As enzyme activity is stable during the time spent in the net haul (Gómez et al., 1996), it is assumed that measured activity is related to respiration at depth once corrected for temperature. Organisms are collected during day and night giving information about their range of migration and temperature experienced during residence at depth. However, the enzymatic proxy needs calibration with known respiration rates. The respiration to ETS (R/ETS) ratio normally varies between 0.5 and 1, mainly depending on the food availability to organisms (Hernández-León and Gómez, 1996). R/ETS ratios of 0.5 are commonly used to give conservative respiratory flux estimates.
Here, these different approaches (Q10, equations based on temperature and body size, and enzymatic activities) were used to estimate respiration by diel vertical migrants at depth in a transect along the tropical and subtropical Atlantic Ocean. We performed respiration measurements on rather large (migrant) copepods captured at night in the epipelagic zone, measuring their ETS activity, and relating both measurements to obtain the R/ETS ratio. We also obtained individual biomass and ETS activity in the mesopelagic zone in order to estimate respiration using different equations in the literature, and also converting ETS activity using different R/ETS ratios. The objective of the present study was to compare the different approaches to assess respiration at depth in order to estimate respiratory flux in the ocean.
Section snippets
Sampling
Zooplankton used for experiments was collected in a oceanographic transect performed on board the R.V. “Hespérides” during the “Migrants and Active Flux In the Atlantic ocean” (MAFIA) cruise along the tropical and subtropical Atlantic Ocean. The research vessel sailed from Salvador de Bahía (Brazil) to the Canary Islands (Spain) from March 31st to April 29th, 2015 (Fig. 1). Organisms were captured in the epipelagic layer at night using a WP-2 plankton net (UNESCO, 1968) in vertical hauls
Results
The oceanographic characteristics of the Atlantic transect were described elsewhere (Olivar et al., 2017). In short, a marked gradient of temperature was observed from the South Equatorial Counter Current off Brazil to the Canary Current as expected (Fig. 2a). Oxygen distribution (Fig. 2b) showed an Oxygen Minimum Zone (OMZ) along the transect with sharp minimum values in the mesopelagic zone in the North Equatorial Current (Station 8), Guinea Dome (Station 9), and the upwelling zone off
Discussion
Migrant biomass and respiration rates at depth are obligate parameters to measure in order to estimate respiratory flux, an important component of active flux in the ocean. Migrant biomass is relatively straightforward to measure as it is the difference between nighttime and daytime biomass in the epipelagic layer assuming no avoidance of the net by organisms. However, respiration rates at depth are complex to estimate as their measurement requires capturing organisms at depth during day or at
Acknowledgements
This work was supported by projects “Migrants and Active Flux in the Atlantic Ocean” (Mafia, CTM2012-39587-C04-01), and “Biomass and Active Flux in the Bathypelagic Zone” (Bathypelagic, CTM2016-78853-R) from the Spanish Ministry of Economy and Competitiveness. This article is a publication of the Unidad Océano y Clima of the Universidad de Las Palmas de Gran Canaria, a R&D&i CSIC-associate unit. We would like to thank two anonymous reviewers for their suggestions and comments. The authors also
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2021, Journal of Experimental Marine Biology and EcologyCitation Excerpt :Estimates of active flux are typically made by measuring biomass of the migratory community then applying mass-specific and temperature scaling factors (i.e., Q10 relationships) to experimentally calculated oxygen consumption rates, as well as organismal nitrogen and carbon excretion rates (e.g., Kiko et al., 2020; Le Borgne and Rodier, 1997). However, depth-dependent metabolic rates are driven not only by temperature differences, but also by differences in swimming activity and oxygen availability (Bianchi et al., 2013; Hernández-León et al., 2019b; Herrera et al., 2019). Daily cycles in feeding activity would also be expected to affect metabolic rates through specific dynamic action, the metabolic costs of assimilating nutrients and incorporating them into biomass (Kiørboe et al., 1985).