Notes: WW, wet weight; P SW, time spent in surface
waters; P MW, time spent in mesopelagic waters;T SW, mean temperature in surface waters;T MW, mean temperature in mesopelagic waters;R SW, daily food ration in surface waters;R MW, daily food ration in mesopelagic waters;FC , food carbon; BC , body carbon;Ke , body carbon release rate;
DOC,
dissolved organic carbon; CO2, carbon dioxide; PC,
particulate carbon. Data in brackets are ranges corresponding to the
above mean values.
a, The total WW of the mesopelagic fish in the open ocean between 40°N
and 40°S was assumed to be 109–1010t, and the WW of the mesopelagic fish in other regions between
40°N–70°N and 40°S–70°S was assumed to be
0.3×109–1010 t (Lam & Pauly, 2005;
Irigoien et al., 2014). The biomass of DVM and NM mesopelagic fishes
were calculated by assuming 30%–50% of the mesopelagic fish undergo
diel vertical migration (Davison et al., 2015; Klevjer et al., 2016).
b, Davison et al., 2015; Davison et al., 2013
c, Davison et al., 2013; Irigoien et al., 2014
d, Kaeriyama & Ikeda, 2004; Max et al., 2012
e, Davison et al., 2013
f, Harris et al., 2000
g, Childress & Nygaard, 1973
4 Discussion
4.1 Carbon release from marine fish
Existing knowledge regarding the food carbon allocation and body carbon
release (/turnover) of marine fish is limited. The carbon AE of marine
fish has seldom been reported.
The proportion (7%–8%) of PC released from the food carbon of marine
medaka was in the range (0.8%–9.7%) of those of seven carnivorous
marine fishes fed fish (Ammodytes personatus ) pieces (Tang et
al., 2003) and was comparable to that (8.2%–9.7%) of
the
detritivorous fish Liza haematocheila (Kang et al., 2007, 2010).
The K e (0.053–0.12 d-1) of
marine medaka measured in this study was within the range (0.0044–0.14
d-1) of reported carbon turnover rates for fish muscle
tissue (Weidel et al., 2011). Our results showed that most (40%–45%)
of the replaced and released body carbon was released in the form of
CO2, indicating that respiration is the largest loss
route for the released body carbon. The proportion was at the lower end
of the reported values (44.3%–79.4%) for carnivorous marine fishes
(Tang et al., 2003). The measured CO2 from body carbon
in our study may be only part of the total carbon used for respiration
because some catabolized carbon (in the form of bicarbonate) is excreted
in fish intestines,
forms
precipitated carbonates, and is finally released as fecal pellets
(Salter et al., 2017; Wilson et al., 2009). Providing that the entire
measured PC released from the body carbon was precipitated carbonates in
fish feces, we could estimate that up to 58%–61% (59.5% on average)
of the released body carbon was used for respiration. In fact, according
to our conceptual model, the carbon used for marine medaka respiration
was from not only replaced (and released) fish body carbon but also from
ingested food. In other words, the daily respiration rate of mesopelagic
fish could be derived from the daily release rate of CO2from food and that from released body carbon (Text S6).
The mesopelagic fish respiration rates derived from the model fish
marine medaka are consistent with recent understanding
about the power-law relationship of
the mesopelagic fish respiration rate to the fish wet mass and habitat
temperature
(Text
S6; Figure S3).
Using
74 data points (each of which includes the respiration rate of
myctophids, one of the most biomass dominant groups of mesopelagic fish,
the temperature and the fish WW) from five studies, a power-law equation
was developed to calculate the WW-specific respiration rate from fish WW
and ambient temperature (Belcher et
al., 2019). By using this equation, we calculated the daily respiration
rates of 0.5-g mesopelagic fish at the different ambient temperatures
(3, 8, 9, and 25°C) used in our estimation. The daily respiration rates
calculated by using the equation were not different from the daily
CO2 release rates derived from the model fish (paired
t-test, p > 0.1; Figure S3).In addition, significant
power-law relationships exist between the calculated daily respiration
rates, and the model fish-derived daily CO2 release
rates (Figure S3).This consistency
justifies our use of carbon release parameters derived from marine
medaka to extrapolate the carbon release of wild mesopelagic fish.
Our results showed that substantial proportions of the ingested food
carbon and the lost body carbon of the model fish are released as DOC.
To our knowledge, the DOC excreted by marine fish has not yet been
directly measured in previous studies.
In addition, the release of DOC from fish feces has not yet been
reported. The contribution of fecal leakage to the measured
DO14C was not examined in the present study.
Contradictory results have been reported about the contribution of fecal
pellets to DOC released from zooplankton. Substantial DOC released from
fecal pellets of zooplankton has been reported (Thor et al., 2003;
Urban-Rich, 1999), but some studies show that the leaching of DOC from
fecal pellets of zooplankton was insignificant compared to the DOC
released through excretion
(Steinberg et al., 2000). We do not think that the leakage of fish feces
(if it exists) would contribute much to the DO14C
measured in the present study; PC in feces only accounted for a small
proportion (7%–8%) of the food carbon release (Figure 5), and the
release rates of the DOC did not peak during the first 2–4 h of the
depuration, when the release rates of feces peaked (Figure 4d, e).
However, why a substantial proportion (46%–49%) of the released DOC
was COC (Figure S2) is still open for discussion.
4.2 Estimated carbon release from mesopelagic fish in the open
ocean
Assuming a mean global primary production of 59.2 Pg C/y (41–77 Pg C/y)
as the scaling basis (del Giorgio and Duarte 2002), our estimation shows
that the DOC (1.34–15.2Pg C/y), CO2 (0.95–10.8 Pg
C/y), and PC (0.35–3.97 Pg C/y) released by mesopelagic fish in the
open ocean were 2.3%–25.7%, 1.6%–18.2%, and 0.6%–6.7% of the
global primary production, respectively. Our estimation of the global
CO2 released by mesopelagic fish was comparable to an
estimation that the carbon consumed in by mesopelagic fish respiration
was approximately 10.5% ± 7.8% of the primary production along a
global investigation transect (Irigoien et al., 2014).The upper limit of
the estimated CO2 released by mesopelagic fish was
comparable to the amount of carbon consumed by mesozooplankton
respiration (13.0 Pg C/y) in global oceans (Hernández-León & Ikeda,
2005). The amount of PC in fecal pellets released by mesopelagic fish
was approximately 1/20 to 1/2 of the amount of fecal carbon (with upper
limits of
6.2–6.8
Pg C/y) released by mesozooplankton in epipelagic oceans (Steinberg &
Landry, 2017).
By
assuming that half of the daily food carbon release of DVM mesopelagic
fish occurred in deep waters, the active carbon export mediated by the
DVM mesopelagic fish (0.54–8.86
Pg
C/y) was estimated to be comparable to or even higher than the carbon
export mediated by DVM zooplankton (1.04 ± 0.26 Pg C/y) (Archibald et
al., 2019). The contribution of DVM micronekton (mainly dominated by
fish) to respiratory flux has been reported to be similar to that of DVM
zooplankton in the northeastern Atlantic Ocean (Ariza et al., 2015).
The
high biomass of mesopelagic fish, which is comparable to or even higher
than the biomass of mesozooplankton in global oceans, may explain the
high carbon release from mesopelagic fish. The global mesopelagic fish
biomass
(1.3–13
Pg WW or 0.11–1.1 Pg C) used in our estimation is comparable to or even
higher than the global mesozooplankton biomass (0.26 Pg C) in the
epipelagic ocean (0–200 m in depth) (Hernández-León & Ikeda, 2005),
where most zooplankton are distributed. In fact, mesopelagic fish
biomass is likely higher than mesozooplankton biomass at low latitudes.
For example, recent studies show that the biomass of mesopelagic fish is
approximately
1.51–29.38
g C/m2 in the open oceans between 40°N and 40°S, and
2.09–3.10 g C/m2 in the southern California current
ecosystem, whereas the epipelagic mesozooplankton biomass is only
0.15–1.3 g C/m2 at the same latitudes (Davison et
al., 2015;
Hernández-León
& Ikeda, 2005; Irigoien et al., 2014).
Our estimation of the active export of DOC by mesopelagic fish
(0.28–4.59 Pg C/y) was comparable to the estimates of the global export
of DOC below 74 m by mixing (2.31 ± 0.60 Pg C/y) (Roshan & DeVries,
2018) and indicates that DVM mesopelagic fish are an important source of
not only ammonium
(Bianchi
et al. 2014) but also DOC for the mesopelagic layer. This may explain
the dissolved organic matter anomalies concurrent with migrating animals
(mainly fish) in the mesopelagic layer (Boyd et al., 2019) and support
the argument that the supply of significant amounts of labile DOC from
mesopelagic fish sustains a microbial growth efficiency in the
mesopelagic layer that is twice as high as that at the surface of the
Red Sea (Calleja et al. 2018).
The present estimation of the active export of PC by mesopelagic fish
(0.07–1.14 Pg C/y) is lower than a recent estimation of the global
magnitude of carbon export by the mesopelagic migrant pump (0.9–3.6 Pg
C/y), which is mediated mainly by mesopelagic fish (Boyd et al., 2019),
but is comparable to an estimation of the active carbon export by
vertically migrating marine fish (0.19 Pg C/year) (Aumont et al. 2018).
4.3 Uncertainties in the estimation of carbon released from
mesopelagic fish
Our estimation of the carbon released from mesopelagic fish is
undeniably still far from precise. This is an opportunity to
thoughtfully examine the values coming from lab experiments and the
other inputs to the extrapolation analysis and to offer specific advice
on future research topics. Uncertainties may come from the use of
parameters derived from marine medaka and from the literature, including
the estimation of mesopelagic fish biomass, the vertical migration
behavior of mesopelagic fish, the use of only a single food for the
model fish, the allocation of ingested food carbon to release, and the
exclusion of varying metabolic rates and Ke s of
fish during different activities. Better information about these factors
will help to improve the estimations.
Our estimation of the carbon released from mesopelagic fish is strongly
dependent on the mesopelagic fish biomass. The substantially varying
estimates of global mesopelagic fish biomass lead to much uncertainty.
The mesopelagic fish biomass used in our estimation (1.3–13 Pg) is
similar to a recent estimate of global mesopelagic fish biomass of
1.8–16 Pg (Proud et al., 2019). The large variation in the estimates of
mesopelagic fish biomass could be the most important factor accounting
for the large ranges (covering one order of magnitude) in the estimated
DOC, CO2, and PC released by mesopelagic fish in the
present study (Figure 8). In fact, the estimates of mesopelagic fish
biomass used in our estimation and in Proud et al. (2019) are based on
the acoustic method. Methodological uncertainties from the acoustic
method (e.g., interference from siphonophores) are the major cause of
variation in the
estimation
of mesopelagic fish biomass
(Proud
et al. 2019). In addition, the lack of acoustic data about mesopelagic
fish at high latitudes may further undermine the estimation of
mesopelagic fish biomass in the global open ocean. Early studies based
on trawling document that the density of mesopelagic fish at high
latitudes could be
several
fold higher than that at low latitudes (Lam & Pauly, 2005). A recent
study based on global observations from a satellite-mounted lidar also
shows that the total DVM animal biomass is higher in the more-productive
high-latitude oceans (Behrenfeld et al., 2019). Therefore, constraining
the uncertainty of the acoustic method and
performing
more surveys based on multiple methods and covering a broader area,
especially those at high latitudes, are needed to more precisely
determine the biomass of global mesopelagic fish.
The ratio of DVM mesopelagic fish to total mesopelagic fish was based on
two recent studies at low latitudes, from 40 °N to 40 °S, and in the
southern California current system (Davison et al., 2015; Klevjer et
al., 2016). Little is known about the proportion of DVM mesopelagic fish
at high latitudes. It may be reasonable to assume that the DVM
mesopelagic fish at low latitudes spend 12 h of diurnal time in the
upper ocean and another 12 h of nocturnal time at mesopelagic depths.
However, diurnal and nocturnal times at high latitudes vary
significantly in different seasons. Little is known about seasonal
variations in vertical-migration behavior or about mesopelagic fish
biomass at high latitudes. More observations at high latitudes are
needed, and recent progress in satellite observations of DVM animal
biomass may facilitate such work (Proud et al. 2019).
The use of parameters derived from the model zooplanktivorous fish
marine
medaka to extrapolate the allocation of ingested food and the released
body carbon of mesopelagic fish may lead to uncertainties. However, the
extrapolation is reasonable, at least for the moment.
First,
the model fish marine medaka ecologically resembles mesopelagic fish,
especially because both the model fish and most mesopelagic fish live on
zooplankton, and they have similar body sizes (in centimeters). Second,
it is still a technical challenge to catch and rear living mesopelagic
fish in the lab
(Belcher
et al., 2019), making it difficult (if not impossible) to measure the
“actual” carbon release parameters of mesopelagic fish. Third, very
little (if any) data on the carbon release of marine zooplanktivorous
fish (let alone mesopelagic fish) were available before our study,
making it difficult to find appropriate data in the literature to fit
our model. As discussed above,
the
consistency of the model fish-derived respiration rates of mesopelagic
fish with those from the literature provides strong support for our
extrapolation (Text S6; Figure S3). Undoubtedly, more experimental work
is needed to examine the carbon release parameters of other
zooplanktivorous fish, especially mesopelagic fish, if possible.
The use of only rotifers as the food for the fish may lead to the
underestimation of the fraction of ingested food allocated to fish
feces. Only rotifers were used as living zooplankton food for the marine
medaka, and no other zooplankton, such as copepods, the main natural
food for mesopelagic fish, was used to feed the fish. One of the main
reasons for this is that it is still a challenge to rear enough living
copepods or other zooplankton to feed fish and complete experiments. The
fish may allocate the carbon of ingested food differently depending on
the zooplankton
types
in their diet. For example, the exoskeletons of copepods may lead to an
increased fraction of feces, as the chitin in the exoskeletons cannot be
digested by most fish (Durbin & Durbin, 1981, Pinnegar & Polunin,
2006). Therefore, more lab experiments that feed zooplanktivorous fish
(including marine medaka) copepods and other zooplankton are needed to
examine the carbon release parameters of zooplanktivorous fish.
Although
our model fish-derived respiration rates for mesopelagic fish are
consistent with those from the literature (Text S6; Figure S3), the
estimated allocation of ingested food carbon and lost body carbon to
respiration and release as CO2 by mesopelagic fish might
be underestimated because metabolism during feeding and diel swimming
between the upper ocean and mesopelagic depths were not considered in
the present estimation. According to our experimental designs,
CO2 release from food was counted only after the
feeding; no intense swimming occurred after the feeding because the
individual fish had been placed in small beakers for the depuration. The
active, feeding metabolic rate can be four times the standard metabolic
rate of resting, inactive fish (Davison et al., 2013; Smith & Laver,
1981); therefore, our estimation, which did not consider the fish
metabolism during feeding and swimming, may underestimate the
CO2 released from the ingested food of the mesopelagic
fish. For the same reason, the derived Ke s and
related CO2 release rates of mesopelagic fish might also
be underestimated. Thus, future work is needed to examine the release
rates for the model fish during different activities, such as swimming.
In contrast, the decrease in K e with the increase
in the daily food ration indicates that the K e of
marine medaka used for the estimation might be overestimated. According
to our pilot studies, 1000 and 2000 rotifers were enough to fill the
experimental fish stomachs 38% and 75% full, respectively. However, as
a daily food ration for a marine medaka with WW of approximately 0.08 g
and living at 25°C, 1000 rotifers is below the maintenance level for
fish growth, and the high K e (0.12
d-1) indicates that substantial body carbon was used
for catabolism. The decreased K e (0.053
d-1) following the doubling of the daily food ration
indicates that, as the supply of food increased, the body carbon used
for metabolic turnover decreased. We expect thatK e would continue to decrease if we further
increased the daily food ration. From this perspective, theK e of 0.053 d-1 used
to extrapolate theK es of mesopelagic fish might overestimate the
body carbon release from the mesopelagic fish. However, the consistency
of our model fish-derived respiration rates of mesopelagic fish with
those from the literature (Text S6; Figure S3) indicates that the
uncertainties from the two factors discussed above may offset each
other.
Other factors, such as the simplification of the mean temperature of
seawater in the upper and mesopelagic depths, the use of a
temperature-dependent daily food ration, the exclusion of fish mortality
and reproduction, and the assumption that all mesopelagic fish to be
zooplanktivorous, may also have led to uncertainties in the present
estimation. Further efforts to minimize the negative influences of the
factors discussed above are needed to improve the accuracy of the
estimates of carbon releases from mesopelagic fish in the global open
ocean.
4.4 Implications for the importance of the contribution of
mesopelagic fish to the ocean carbon cycle
By providing the first quantitative estimates of DOC,
CO2, and PC released by mesopelagic fish in the global
open ocean, our results strengthen the argument that mesopelagic fish
may play important roles in the ocean carbon cycle by mediating carbon
export in the ocean. First, our results show that the DOC released by
mesopelagic fish could be an important organic carbon source for
heterotrophic biota in the ocean. Substantial amounts of released DOC,
as well as of CO2 and PC, may be actively transported to
mesopelagic depths through the vertical migration of mesopelagic fish.
The DOC influx to mesopelagic oceans through DVM mesopelagic fish may
narrow the carbon imbalance between the estimated organic carbon
influxes and the measured heterotrophic carbon consumption, which is
significantly higher than the former in mesopelagic oceans (Burd et al.,
2010; Giering et al., 2014; Steinberg et al., 2008).
Second, the PC in the fecal pellets produced by mesopelagic fish could
contribute greatly to carbon export through the biological carbon pump.
As noted above, the amount of PC in fecal pellets (0.35–3.97 Pg C/y)
released by mesopelagic fish is nonnegligible, even substantial. The
contribution of mesopelagic fish to carbon export may be even more
important, if we consider that the sinking rates of fish fecal pellets
are much (even one order of magnitude) greater than those of zooplankton
fecal pellets (Saba & Steinberg, 2012).
5 Conclusions
We propose a carbon release model that divides fish-released carbon into
two parts, i.e., food carbon release and body carbon release (on the
basis of the source: ingested food or the fish body, respectively), and
three forms, DOC, CO2, and PC, which enable the
quantification of the release of carbon by fish. By using14C-labeled living zooplankton to feed a model marine
zooplanktivorous fish, this study provided a detailed methodology for
precisely quantifying the carbon budget and carbon release of marine
fish. By using the carbon release model and parameters derived from the
model fish and the literature, we estimated the DOC,
CO2, and PC released by mesopelagic fish in the global
open ocean. Our results demonstrated that marine zooplanktivorous fish
such as marine medaka can convert substantial fractions of their daily
ingested food carbon (26%–42%)
and
released (/replaced) body carbon (39%–42%) into seawater as DOC.
Mesopelagic fish in the global open ocean were estimated to produce
1.34–15.2, 0.95–10.8, and 0.35–3.97 Pg C/y of DOC,
CO2, and PC, respectively. The conceptual model, the
laboratory experiments with model fish, and the extrapolation to
mesopelagic fish generated a complete solution for estimating the carbon
released by fish, especially by global mesopelagic fish. Our estimation
is undeniably still far from precise, and factors bringing about
uncertainties were discussed. More experimental work is needed to
examine the carbon release parameters of marine zooplanktivorous fish,
and further observations based on multiple methods are suggested to
cover broader areas, especially those at high latitudes, to more
precisely determine the mesopelagic fish biomass and their vertical
migration behaviors at different latitudes. Our study indicates that
mesopelagic fish could be an important source of DOC in the ocean and
play critical roles in the biological pump by producing substantial
amounts of DOC and fast-sinking fecal pellets and by the active export
of DOC, CO2, and PC into deep waters through their diel
vertical migration.
Acknowledgments and Data Statement
We thank Jie Xu, Yehui Tan, and Xingyu Song for their technical supports
for conducting the experiments and measuring the radiocarbon. This work
is supported
by
National
Key Research and Development Project of China (2017YFC0506302), the Key
Special Project for Introduced Talents Team of Southern Marine Science
and Engineering Guangdong Laboratory (Guangzhou) (GML2019ZD0405;
GML2019ZD0402), the National
Natural Science Foundation of China
(41506150),
the Guangdong Basic and Applied Basic Research Foundation
(2015A030310169; 2017A030313217; 2019A1515011645), the Science and
Technology Planning Project of Guangdong Province, China
(2017B030314052).
All the data supporting the conclusions can be obtained from the tables
and figures in the main manuscript and in a related data file in the
repository of ResearchGate
(http://dx.doi.org/
10.13140/RG.2.2.15051.85281).
Author contributions
Q. Liu played a key role in designing and implementing the experiments,
analyzing results and preparing the manuscript. L. Zhou played a key
role in forging the model scenarios,
interpreting
results, preparing the manuscript, and helped the implementation of the
experiments. Y. Wu contributed to the data analysis and paper writing.
X. He contributed to the data analysis and modeling, and paper writing.
N. Gao contributed to implementation of the experiments. Professor L.
Zhang supervised the whole research design, experimental process, data
interpretation, and the manuscript composition
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