Estimation of carbon released by mesopelagic fish in the global open ocean using a carbon release model and model fish-derived parameters
Qingxia Liu1, 2, 3, 6†, Linbin Zhou1, 3, 6†, Yun Wu4, Xuejia He5, Na Gao1, and Li Zhang1, 3, 6*
1CAS Key Laboratory of Tropical Marine Bio-resources and Ecology, Guangdong Provincial Key Laboratory of Applied Marine Biology, South China Sea Institute of Oceanology, Chinese Academy of Sciences, Guangzhou 510301, China
2 Guangdong Provincial Key Laboratory of Fishery Ecology and Environment, South China Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences, Guangzhou 510300, China
3 Southern Marine Science and Engineering Guangdong Laboratory (Guangzhou), Guangzhou 511458, China
4 School of Environment Science and Engineering, Nanjing University of Information Science & Technology, Nanjing 210044, China
5 Research Center of Harmful Algae and Marine Biology, Jinan University, Guangzhou 510632, China
6 University of Chinese Academy of Sciences, Beijing 100049, China
*Corresponding author: Li Zhang (zhangli@scsio.ac.cn)
These authors contributed equally to this work.
Key Points:
Abstract
The role of zooplanktivorous mesopelagic fish in the ocean carbon cycle is attracting increasing attention. However, little information is available regarding the carbon budget of marine zooplanktivorous fish, let alone that of mesopelagic fish. Here, we propose a carbon release model that divides fish-released carbon into two parts (based on the source: ingested food and the fish body) and three forms (as dissolved organic carbon (DOC), CO2, and particulate carbon (PC)). By feeding a model marine zooplanktivorous fish, marine medaka (Oryzias melastigma ), a radiocarbon-labeled living rotifer, Brachionus plicatilis , we quantified a detailed carbon budget for the fish. The results indicate that 53%–75% of the ingested food carbon was not assimilated but was released mainly as DOC (48%–59%), followed by CO2(30%–40%) and PC (11%–13%). The release (/efflux) rates of fish body carbon changed from 0.12 to 0.053 d-1 when daily food rations shifted from 2.2% to 4.3% of the fish biomass. DOC, CO2, and PC accounted for 39%–42%, 40%–45%, and 16%–18% of the carbon released from the fish body, respectively. By using the carbon release model and the parameters derived from the model fish and from the literature, we estimate that mesopelagic fish in the global open ocean produce 1.34–15.2, 0.95–10.8, and 0.35–3.97 Pg C/y of DOC, CO2, and PC, respectively. Our results show that marine zooplanktivorous fish can transform substantial fractions of their daily ingested food and released body carbon into DOC and that mesopelagic fish may be important sources of DOC and fast-sinking PC in the ocean.
1 Introduction
Increasing attention is being paid to the roles played by fish in the ocean carbon cycle. Small-sized (< 6 cm) mesopelagic fishes (most of which are zooplanktivorous fish) are very abundant in the mesopelagic layer (from 200 to 1000 m in depth) of the open ocean and dominate the world’s total fish biomass. Recent surveys indicate that the biomass of these mesopelagic fish could be one order of magnitude higher than a previous estimate of ~1000 million tons in the global open ocean (Davison et al., 2013, 2015; Irigoien et al., 2014; Proud et al., 2019). Increasing evidence indicates that these fish can mediate carbon export to deep waters by performing diel vertical migration and producing fast-sinking fecal pellets (Boyd et al., 2019; Pershing et al., 2010; Saba & Steinberg, 2012; Trueman et al., 2014). In addition, mesopelagic fish, as a globally important source of marine calcium carbonate, may play a key role in the marine inorganic carbon cycle (Salter et al., 2017; Wilson et al., 2009).
Nevertheless, the contribution of zooplanktivorous fish to the ocean carbon cycle is still poorly quantified. Bioenergetics is the study of the balance between the energy supply from food and energy expenditure (Cho et al., 1982); it can describe the fate or allocation of consumed food to growth, respiration, and waste products (e.g., exudates and feces) (Ney, 1993 and reference therein). Thus bioenergetics has been used for the study of fish contributions to the ocean carbon cycle (Davison et al., 2013). Much effort has been invested in examining and analyzing the allocation of consumed food to growth and respiration. In contrast, less attention has been paid to the “waste carbon” released by fish (Ney, 1993 and reference therein), although waste carbon is key for understanding the roles of fish in the ocean carbon cycle. In fact, the bioenergetics model cannot exactly describe all the carbon dioxide (CO2) and waste carbon released by fish, especially at small time scales such as the daily scale, because part of the CO2 and waste carbon may come from the fish body rather than ingested food in fish gut (e.g., a fish without any food in its gut will continue to release CO2 and waste carbon come from only the fish body). In addition, the allocation of fish food carbon to CO2 through respiration and to dissolved organic carbon (DOC) from the excretion and leakage of fish feces has seldom been measured directly. To the best of our knowledge, the proportion of food carbon released as DOC and the release of fish body carbon as CO2, DOC, and feces have not yet been quantified. The lack of such data concerning the carbon budget of zooplanktivorous fish impedes our understanding of the roles of small fish, such as mesopelagic fish, in the ocean carbon cycle (Davison et al., 2013; Saba & Steinberg, 2012). For example, due to the lack of data, fish-released DOC was not considered in a pioneering estimation of carbon export mediated by mesopelagic fish in the northeastern Pacific Ocean (Davison et al., 2013), and piscivorous or freshwater fish-derived variables have to be used in the models for marine fish (Bachiller et al., 2018; Ney, 1993).
The previous studies inspired us to propose that the daily carbon released by a fish could be divided into two parts on the basis of its source, from either ingested food or the fish body. It is possible to extrapolate from the carbon release parameters of a model fish in order to estimate the carbon released by mesopelagic fish. Power-law scaling functions have been reported to describe the relationship of carbon turnover rates of fish with fish mass and temperature (Weidel et al., 2011), and the daily food rations and metabolic rate of mesopelagic fish are also fish mass- and temperature-dependent (Davison et al., 2013; Gillooly et al., 2001). The fate of the ingested food can be simply considered to be either assimilated by the fish or released as CO2, DOC, and particulate carbon (PC), and the lost fish body carbon will be released as CO2, DOC, and PC. Theoretically, if we know the allocation of ingested food and the body carbon released from a mesopelagic fish to CO2, DOC, and PC at a certain temperature, we could estimate the total carbon released by the fish at any temperature or by another fish of a different size. In fact, as discussed above, such data are lacking. It is difficult to obtain such data for wild mesopelagic fish in situ, and as well as in the laboratory, as rearing mesopelagic fish in the laboratory is still a technical challenge (Martin et al. 2020). This leads us to consider estimating the carbon released by mesopelagic fish by extrapolating it from the carbon release parameters of a model fish with a similar feeding habitat and body size as the mesopelagic fish. Marine medakaOryzias melastigma may be a good choice for such a model fish. It has been widely used as a model fish in ecological and ecotoxicological studies (Bo et al., 2011; Kong et al., 2008; Mu et al., 2015). More importantly, marine medaka resembles mesopelagic fish ecologically, as it feeds on zooplankton and has a body size (in centimeters) comparable to that of zooplanktivorous mesopelagic fish (Davison et al., 2013; Irigoien et al., 2014).
Therefore, to estimate the contribution of mesopelagic fish to the ocean carbon cycle, we first proposed a conceptual model dividing fish-released carbon into two parts, i.e., food carbon release and body carbon release, based on the source (from either ingested food in the fish gut or tissues in the fish body), and into three forms, DOC, CO2 and PC. Second, by feeding the model fish a radiocarbon (14C)-labeled living rotiferBrachionus plicatilis , the three forms of carbon released from14C-labeled ingested food and14C-labeled fish body were quantified. Finally, on the basis of the conceptual model and by using carbon release parameters derived from the model fish and parameters (e.g., mesopelagic fish biomass and daily food rations of mesopelagic fish) from the literature, we estimated the carbon release from mesopelagic fish in the global open ocean. Our results indicate that mesopelagic fish play an important role in the active export of not only PC but also DOC and CO2 to the depths of the ocean.
2 Materials and Methods