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:
- We propose a new conceptual model for quantifying the dissolved
organic carbon (DOC), CO2, and particulate carbon (PC)
released by fish
- We quantified a detailed carbon budget for a marine model
zooplantivorous fish by feeding the fish radiocarbon-labeled living
zooplankton
- Using
the model and model fish- and literature-derived parameters,
mesopelagic fish were estimated vital sources of DOC and fast-sinking
PC
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