The Importance of Mesozooplankton Diel Vertical Migration for Sustaining a Mesopelagic Food Web

We used extensive ecological and biogeochemical measurements obtained from quasi-Lagrangian experiments during two California Current Ecosystem Long-Term Ecosystem Research cruises to analyze carbon fluxes between the epipelagic and mesopelagic zones using a linear inverse ecosystem model (LIEM). Measurement constraints on the model include 14C primary productivity, dilution-based microzooplankton grazing rates, gut pigment-based mesozooplankton grazing rates (on multiple zooplankton size classes), 234Th:238U disequilibrium and sediment trap measured carbon export, and metabolic requirements of micronekton, zooplankton, and bacteria. A likelihood approach (Markov Chain Monte Carlo) was used to estimate the resulting flow uncertainties from a sample of potential flux networks. Results highlight the importance of mesozooplankton active transport (i.e., diel vertical migration) for supplying the carbon demand of mesopelagic organisms and sequestering carbon dioxide from the atmosphere. In nine water parcels ranging from a coastal bloom to offshore oligotrophic conditions, mesozooplankton active transport accounted for 18% - 84% (median: 42%) of the total carbon supply to the mesopelagic, with gravitational settling of POC (12% - 55%; median: 37%) and subduction (2% - 32%; median: 14%) providing the majority of the remainder. Vertically migrating zooplankton contributed to downward carbon flux through respiration and excretion at depth and via consumption loses to predatory zooplankton and mesopelagic fish (e.g. myctophids and gonostomatids). Sensitivity analyses showed that the results of the LIEM were robust to changes in nekton metabolic demands, rates of bacterial production, and mesozooplankton gross growth efficiency. This analysis suggests that prior estimates of zooplankton active transport based on conservative estimates of standard (rather than active) metabolism should be revisited. Contribution to the Field Understanding the flows of carbon within the ocean is important for predicting how global climate will shift; yet even after decades of research, the magnitude with which the ocean sequesters carbon is highly uncertain. One reason behind this uncertainty is that a variety of mechanisms control the balance between carbon input and carbon output within the ocean. The topic of this work is to inspect the role of biological organisms in physically transferring organic carbon from the surface to the deep ocean. As opposed to other mechanisms—such as sinking particles, the biological transfer of carbon is difficult to measure directly and is often quite variable, leading to large uncertainties. Here we use an extensive set of in situ observations off the coast of southern California to model the flow of carbon through the ecosystem. The model determined that in our study area nearly half of the total transfer of carbon from the surface ocean to deep was carried out by zooplankton that swim up to the surface each night to feed. This finding has direct implications for global carbon budgets, which often underestimate this transfer of carbon.

annually. This is consistent with previous modeling exercises based on zooplankton behavior Table 1. Overview of conditions for each cycle along with the attributed classifications: upwelling, transition region, and nutrient limited.
The fate of active export flux is important for understanding the ecological impact of this communities. Model results suggested that the carbon demand was equal to <1% -4% (median: be met by carbon flux from the surface layer, the most likely sources of which are sinking 5 8 4 particle flux (which we experimentally measured using two independent approaches) and active transport is more likely to support mesopelagic fish and gelatinous predator communities.

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Although sinking particles can efficiently support bacterial production (as they are likely directly 5 8 9 colonized by particle-attached bacteria), many fish and gelatinous zooplankton are predators that myctophids' prey.

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Mesopelagic sources of mortality have implications for the fitness of vertical migrators. It 5 9 9 is often assumed that DVM is ecologically advantageous when the costs associated with not 6 0 0 feeding during the day and actively swimming to depth are offset by the benefits of reduced that their excretion and respiration occur primarily in the epipelagic. The comparable mortality experienced by vertically-migrating mesozooplankton in the as a lifestyle because if these organisms were present at the surface during the day then they 6 1 9 might experience substantially greater predation than in the mesopelagic.

Sensitivity Analysis and Ecological Connections
The ecosystems generated in the 9 model runs were as varied as the cruise measurements: including observations from dynamic coastal blooms to quiescent oligotrophic communities. All Supplemental Figure 1) with 95% CI from the MCMC random walk. Whether this result can be 6 2 6 considered a model bias or is derived from possible systematic differences between 14 CPP and 6 2 7 true net primary production (Marra, 2009;Milligan et al., 2014;Minas et al., 2002 median) and total export flux by 11%. Since passive particle flux is constrained by observations, 6 4 5 passive flux increased by 0% -12% (median: 4%) while active transport by mesozooplankton increased by 0% -56% (median: 26%). Active transport by nekton was also elevated (0% -14%,  The results were also robust to changes in other observations. When the nekton metabolic 6 5 0 estimates were halved, export by vmMYC was reduced by 51% (inter-cycle median), a change of 6 5 1 < 5 mg C m -2 d -1, while other forms of export were unchanged. Increasing the upper limit of 6 5 2 mesozooplankton GGE from 30% to 40% led to a ~20% increase in mesozooplankton active  LIEMs are a powerful tool for assimilating diverse in situ measurements and constraints particularly powerful because it allows information from the mesopelagic to constrain epipelagic 6 5 9 food web flows and vice versa. Compared to most previously published LIEMs, the model presented here includes many more in situ rate measurements, made possible by the suite of than/less than constraints derived from biomass measurements, leading to correspondingly 6 6 5 higher uncertainty. This highlights a need for studies that simultaneously quantify the activity of 6 6 6 many different plankton functional groups. Since a LIEM is fundamentally a data-regression technique, our results are emergent from structure. Thus, we believe the resulting model solutions to be descriptive of the dominant in situ 6 7 0 processes in the CCE LTER study region. However, it is important to note that there was large 6 7 1 uncertainty associated with some model flows, and that this uncertainty could be quantified using 6 7 2 the MCMC approach (Supp. recover ecosystem rates (Saint-béat et al., 2013;Stukel et al., 2012). Even more important is its 6 7 5 ability to generate confidence intervals that realistically represent the uncertainties in model cycle P0810-6, we found that the 95% confidence interval for HNF ingestion of detritus was 5 -6 7 8 127 mg C m -2 d -1 , providing no real knowledge of whether or not this connection was an 6 7 9 important part of the ecosystem. However, for Cycle P0810-5, we found that mesopelagic 6 8 0 mesozooplankton predation on small vertical migrators was 233 -423 mg C m -2 d -1 (95% CI) and hence have a high degree of confidence that this flow was substantial at this location. Investigation of the confidence intervals can thus inform which conclusions can be considered  Reports of active transport by vertically migrating biota have long suggested that these 6 8 8 organisms can transport a globally significant amount of carbon to depth. However, most early 6 8 9 studies suggested that active transport was substantially less important than passive flux of oligotrophic BATS station off Bermuda, Dam et al. (1995) found that respiration by including dissolved organic nitrogen (DON). In fact, vertical migrators were found to perform 6 9 5 15% -66% of the total nitrogen transport. Hansen and Visser (2016) estimated that across the 6 9 6 North Atlantic active transport by mesozooplankton may constitute 27% of total export. In 6 9 7 addition to zooplankton, vertical migrations by micronekton can also lead to significant export  Using a conservative approach, Longhurst (1990) estimated that active export by zooplankton waters, which is similar to our results where the LIEM suggests that mesozooplankton 7 0 6 respiration at depth is 9% -113% (median: 34%) that of passive export. Global modeling 7 0 7 estimates have suggested that active transport may be responsible for 14% (Archibald et al., alone. More recent results, have been suggesting increased importance for active transport, regions, but was 2-fold higher than passive flux in eutrophic areas of the tropical and subtropical 7 1 5 Atlantic. Our results that total active transport (zooplankton and nekton) may be responsible for 7 1 6 18% -84% (median: 42%) of total carbon export in the CCE are thus somewhat higher than expectations (e.g., mesopelagic carbon demand, euphotic zone new production, 7 2 0 mesozooplankton energy partitions). We thus suggest that active transport in high biomass 7 2 1 regions may be more important, in fact, than some previous studies suggest, and we recommend that rely on standard (rather than active) estimates of zooplankton metabolic rates. of the remainder (i.e. mesopelagic export efficiency is < 10%). Notably, 3 of the 4 cycles with constrain the role of mesozooplankton in export production. 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