Progress in Oceanography 206 (2022) 102860

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Progress in Oceanography
journal homepage: www.elsevier.com/locate/pocean

Bottom-up processes drive reproductive success of Japanese anchovy in an
oligotrophic sea: A case study in the central Seto Inland Sea, Japan
Michio Yoneda a, *, Tatsunori Fujita b, c, Masayuki Yamamoto b, Kazuaki Tadokoro d,
Yuji Okazaki d, Masahiro Nakamura a, Masanori Takahashi e, Naoaki Kono e,
Tadashi Matsubara f, Katsuyuki Abo f, Guo Xinyu g, Naoki Yoshie gaFisheries Technology Institute, Japan Fisheries Research and Education Agency, Hakatajima Field Station, Imabari, Japan
Kagawa Prefectural Fisheries Experimental Station, Takamatsu, Japan
Kagawa Prefectural Fisheries Division, Takamatsu, Japand
Fisheries Resources Institute, Japan Fisheries Research and Education Agency, Shiogama Field Station, Shiogama, Japane
Fisheries Resources Institute, Japan Fisheries Research and Education Agency, Hatsukaichi Field Station, Hatsukaichi, Japanf
Fisheries Technology Institute, Japan Fisheries Research and Education Agency, Hatsukaichi Field Station, Hatsukaichi, Japang
Center for Marine Environmental Studies, Ehime University, Matsuyama, Japanbc

A R T I C L E I N F O

A B S T R A C T

Keywords:
Copepods
Elevated temperature
Prey selection
Maternal effectRecruitment dynamics
Seto Inland Sea, Japan

Anthropogenic and/or climate-driven changes in zooplankton dynamics may serve as a bottom-up regulator of
productivity of small pelagic fish. In the central Seto Inland Sea of Japan, the abundance of the recruit fish ofJapanese anchovy (Engraulis japonicus) has markedly declined in the last decade under oligotrophication.
However, the link between the reproductive success of anchovy and environmental variation is largely unclear.
This study explored the potential association between changes in the zooplankton (copepods) community
structure and the reproductive condition of anchovy in this oligotrophic sea using survey data from spring tosummer of 2001–2019. The community structure of copepod species changed markedly in May–July, covering
the main spawning season of anchovy, as decreases in the biomass of several copepods found in cooler water in agiven season (May–June) were observed. Although relationships between chlorophyll a concentrations and thecopepod biomass were unclear, the recent decline of their cooler-water copepods may be attributed to the in­fluences of elevated sea surface temperature and decreasing levels of chlorophyll a. The latter may be associatedwith decreasing nitrogen levels. Among these species, Calanus sinicus and Corycaeus affinis could be important
prey items for anchovy from the analyses of prey selectivity and relationships between the relative condition
factor of females and the copepod biomass. The egg size–temperature relationships of anchovy appeared to be
associated with the relative condition factor of females and survival rates in the early stage of life, suggesting thatfemales with a poor body condition produced smaller eggs in recent years. Maternal food manipulation exper­
iments supported the assumption that larvae born to females fed a restricted food ration exhibited lower star­
vation tolerance and slower growth than born to females provided feed ad libitum. These findings suggest that the
reproductive success of anchovy could be subject to bottom-up trophic drivers mediated by maternal contri­
butions to offspring viability, and this partly explains why the level of anchovy recruitment has rapidly declinedin the last decade.

1. Introduction
Small pelagic fish are key components of marine ecosystems, andsuch populations are often excellent bio-indicators of climate-drivenchanges in marine systems globally (Chavez et al., 2003; Peck et al.,2013, 2021). Because small pelagic fish are susceptible to environmental
cues, environmentally driven natural mortality changes result in
amplified recruitment variability (Houde, 2008; Katara, 2014; Somar­
akis et al., 2019). Because of the tight coupling of small pelagic fish
populations to bottom-up processes, it is important to understand which* Corresponding author at: Fisheries Technology Institute, Japan Fisheries Research and Education Agency, Hakatajima Filed Station, 2780 Kinoura-ko, Hakata,
Imabari, Ehime 794-2305, Japan.
E-mail address: yoneda_michio55@fra.go.jp (M. Yoneda).
https://doi.org/10.1016/j.pocean.2022.102860
Received 14 January 2022; Received in revised form 3 June 2022; Accepted 13 July 2022
Available online 16 July 2022
0079-6611/© 2022 The Authors. Published by Elsevier Ltd. This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/).

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prey are preferred and what number of such prey is needed to cover theenergy requirements of such fish species. Furthermore, as most small
pelagic fish such as anchovy are income breeders, which use concurrent
intake energy to pay for egg production in an ongoing season, therichness of the feeding environment can have important and immediate
consequences on reproductive output (McBride et al., 2015). Explora­
tions of the effects of changes in prey quantity and quality on the
spawning dynamics can be one key process determining the mechanism
by which anthropogenic- and/or climate-driven changes in zooplankton
species composition and their abundance might act as a bottom-up
regulator of fish productivity (Peck et al., 2013).
The Seto Inland Sea is the largest semi-enclosed sea in Japan (Fig. 1a,b) and one of the major fishing grounds for marine fish and shellfish incoastal waters off the Japanese coast. Japanese anchovy (Engraulisjaponicus; hereinafter called anchovy) is a key species for tertiary pro­
ducers in this marine ecosystem, and they primarily utilize copepods as
prey organisms (Yamamoto and Katayama, 2012), among which thegenera Calanus, Paracalanus, Acartia, and Oithona are important con­stituents of the net zooplankton biomass (Uye et al., 1987; Hashimoto
et al., 1997); C. sinicus plays an important role in growth and repro­
duction for planktivorous fish species in these waters (Uye, 2000). The
total annual catch of anchovy peaked in the late 1970 s and 1980 s;
thereafter, as observed for other planktivorous fish species, the catch
rapidly declined in association with decreases in the levels of dissolved
inorganic nitrogen (DIN) and phosphorus (DIP) because of the imple­
mentation of nutrient load reductions to prevent eutrophication(Yamamoto, 2003; Abo and Yamamoto, 2019). Oligotrophication has
become a serious problem throughout the Seto Inland Sea since the2000 s (Abo and Yamamoto, 2019). Decreased DIP content has caused achange in the phytoplankton species composition, thereby altering thefood web structure, suggesting that this might be the major cause of the
reduction of fishery production during the 1980 s and 1990 s (Yama­
moto 2003). In the eastern Seto Inland Sea (Osaka Bay), the decline in

the copepod biomass induced by the decrease of DIN levels and thesubsequent reduction of phytoplankton production resulted indecreased catches of planktivorous fish species, especially sand lance(Ammodytes japonicus) in 1990–2019 (Fujiwara et al., 2022). However,this did not apply to anchovy because the annual catch in the eastern
Seto Inland Sea has gradually increased in the last two decades. In the
Seto Inland Sea, anchovy is considered to comprise a mixed stock ofwidely migratory and sedentary populations (Kono and Takahashi,2019). The former population migrates from the Pacific Ocean to inner
bay areas and vice versa. Ware and Thomson (2005) identified strong
bottom-up trophic linkages among phytoplankton, zooplankton, andcatches of resident fish at the regional and sub-regional scales along thewest coast of North America.
The central Seto Inland Sea (Hiuchi-Nada) is a major spawning
ground of anchovy, and females spawn mainly from spring to summer(Suhara et al., 2013) especially in the eastern waters (Fig. 1b). In thesewaters, anchovy is considered a single stock of sedentary fish, in contrast
to those in the eastern Seto Inland Sea (Fujita et al., 2021; Fujiwara et al.,2022). Boat seine fishermen mainly targeting anchovy larvae and ju­
veniles (recruit fish) operate from June to September in the eastern partsof these waters. The abundance of the recruit fish of anchovy has
dramatically decreased in the last decade despite adequate egg pro­duction (Fig. 1c; Fujita et al., 2021). Fujita et al. (2021) revealed anegative correlation between the abundance of recruit fish and egg
production over a 26-year period (1994–2019). It is assumed thatchanges in survival rates in the early stage of life may be attributable tothe variation of egg quality, as intrinsic (e.g., body size, nutritional
condition) and extrinsic factors (e.g., prey availability, temperature)surrounding the mother that directly and interactively influence egg
quality (Marshall et al., 2008; Green, 2008; Hixon et al., 2014) havesimultaneously changed over this period. However, the bottom-up
linkages through trophic chains in these waters and their reproductive
responses to prey availability have remained unclear.
In this study, we explored the potential association between changes
in the zooplankton (copepods) community structure and the reproduc­tive condition of anchovy under oligotrophication in the central Seto
Inland Sea in 2001–2019 (Fig. 2). The abundance and species compo­
sition of zooplankton communities are regulated by their physical andchemical environment, which could affect fish productivity (Beaugrandet al., 2003; Bouman et al., 2003). Thus, we assumed that changes inprey zooplankton dynamics induced by changes in lower trophic chains
may have bottom-up effects on anchovy reproductive success throughmaternal contributions to larval viability. The gradual warming in
April–June in the last 26 years observed in these waters (Fujita et al.,2021) was also considered. To test our assumption, inter- and intraannual variations of the copepod species composition and biomass inrelation to variations in environmental conditions were first examinedusing data from surveys conducted in spring–summer over the study
period. Second, the reproductive traits and prey selectivity of anchovy inthese waters were examined in relation to environmental conditions.
The recruit fish of anchovy, occupying approximately 88 % of all in­
dividuals, primarily spawned from May to June (Fig. 1c, Fujita et al.,2021). Thus, we focused on variations of the maternal traits of anchovyin May and June. Finally, we performed laboratory experiments to assess
the response of offspring traits to maternal prey and body conditions.
This was performed because the direct effects of prey abundance andnutritional quality on reproduction are more difficult to measure in wild
populations, as the responses of the measured traits of offspring may besuppressed by covariance with bottom-up and top-down effects in theearly stage of life (Green, 2008).

Fig. 1. Map presenting the sampling locations in the central Seto Inland Sea (a,b) and annual variation in the number of recruit fish of Japanese anchovy
hatched from April to August in 2001–2019 [c, bars; modified from Fujita et al.
(2021)]. (b) Four stations for environmental and plankton surveys were
established (closed circles), and eight stations for only zooplankton surveys
were set during the study period (open circles). (c) The ratio of recruit fish bornin May and June is also presented (circle). The ratio was estimated from
dividing the number of recruit fish in May and June by the total number of
recruit fish from April to August.

2. Materials and methods
2.1. Environmental data
The surveys for nutrients and chlorophyll a were conducted in the2

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were collected at 12 stations with a plankton net (NORPAC net or
remodeled NORPAC NET, Rigosha Ltd., Saitama, Japan; mouth diam­
eter: 0.45 m, length: 2 m, mesh opening: 100 µm, fitted with a flow­
meter) towed vertically from 2 m above the sea floor to the surface. Only
data on SST on the days of zooplankton sampling were available. Afterthe net was retrieved, copepods were immediately preserved in 5 %formalin solution. In the laboratory, the preserved zooplankton sample
was split into 2–4 subsamples, from which copepods were counted ineach species and the body length of individuals was measured to thenearest 0.1 mm under a binocular microscope. The carbon content ofeach copepod species was calculated from body length using a regres­sion equation (Liang and Uye, 1996a, b; Uye 1982; Uye et al. 2002).
2.2. Biological data
Anchovy were collected from commercial catches between May andJune in 2001–2019, corresponding to the main hatch dates of recruit fish
(Fig. 1b; Fujita et al., 2021). Specimens were measured to within 0.1 mm
for standard length (SL) and within 0.01 g for body weight and ovarian
weight. Because approximately 80 % of females reach sexual maturity at
80 mm in SL in the Seto Inland Sea (Kono and Takahashi, 2019), only
females with SL ≥ 80 mm were used to examine temporal trends of thematernal body condition. To examine the nutritional body condition of
female anchovy, the relative condition factor (K; Le Cren, 1951) wasused in this study because it is one of the most reliable indicators of thecondition of exploited marine fish (Lloret et al., 2014). K of individual
fish was calculated using the equation K = SW/stSW, where SW is so­matic (ovary-free) body weight and stSW is standardized SW corre­
sponding to the expected SW of an individual of a given SL calculated
from the SW–SL relationship [stSW = exp(− 1.025 + 0.032SL), n = 9574,
p < 0.001, R2 = 0.83]. There was no significant correlation between K
and SL (p = 0.14), indicating that K was independent of SL. K of 1 was abenchmark for the condition of standard fish sampled in this study.
Values of > 1 and < 1 indicated relatively better and worse conditions
compared to standard fish, respectively.
To examine the prey selectivity of adult anchovy, 140 specimens (SL≥ 80 mm) were collected on six dates (June 10 and 24, 2015; May 24,
2016; June 13, 2016; July 1, 2017), corresponding to the dates forzooplankton surveys. After fish sampling, specimens were fixed in 10 %buffered formaldehyde and assessed for SL. Copepods in the formalinfixed stomach were counted for each species under a binocular micro­
scope. The prey selection of anchovy was investigated using the rela­tivized selectivity index (E; Vanderploeg and Scavia, 1979) as follows:
Ei = (Wi − 1/n)/(Wi + 1/n), where n is the number of copepod available∑
and Wi is estimated by (ri/pi)/( (ri/pi)), where ri and pi are the pro­portions of copepod i in the stomach and environment, respectively. E
ranges from − 1 to + 1, with negative values indicating avoidance,
positive values indicating selection, and 0 representing no preference.
The occurrence rate of each copepod species on a given day of sampling
was calculated as the number of specimens for each species divided by
the total number of copepods for all species. In this analysis, C. sinicus,
C. abdominalis, and O. scottodicarloi were excluded because no samples ofthese species were collected on the six sampling dates.
The egg surveys were conducted at 7 stations in the central Seto
Inland Sea (Fujita et al., 2021). The egg samples were preserved onboard
in 5 % buffered formaldehyde. In the laboratory, anchovy eggs were
sorted under a stereoscopic microscope and counted at each station. To
examine inter-annual variation in egg size, both the long and their shortaxes of eggs were measured for all eggs (maximum, 50) collected at eachstation in 2005–2006, 2009–2010, and 2015–2016 using Image-Pro Plusver. 5 (Media Cybernetics, Inc., Bethesda, MD, USA). As anchovy eggs
are ellipsoid, the egg size (mm3) was calculated as follows: V = (long ×
short2 × π)/6 (Yoneda et al., 2014).
The number of recruit fish per egg abundance (RPE) is a good indi­cator of early survival rates in small pelagic fish (Takasuka et al., 2019,2021); thus, these data in May and June of 2001–2019 followed those of

Fig. 2. Conceptual frameworks of the bottom-up trophic linkages from nutri­ents to zooplankton and the influence on anchovy recruitment through repro­
ductive conditions. The abundance of recruit fish of anchovy has declined in thelast decade possibly because of oligotrophication in the central Seto Inland Sea.
It is assumed that changes in prey zooplankton dynamics induced by changes inlower trophic chains may have bottom-up effects on anchovy reproductive
success through maternal effects on larval traits.

central Seto Inland Sea in eastern Hiuchi-nada (Fig. 1a), in which four
stations were established at depths of 21–25 m between April andAugust, covering the spawning season of anchovy, in 2001–2019. The
chlorophyll a concentration was considered a proxy for phytoplankton
biomass in this study. In total, 1400 water samples were obtained from 0m, 20 m and the sea floor to assess the concentrations of nutrients, andthe chlorophyll a density on the surface was measured. Water samples
were filtered using a glass fiber filter (Whatman GF/F, 25 mm), and thenthe concentrations of dissolved inorganic nitrogen (DIN = NH4 + NO2 +NO3), phosphate (PO4), and silicate [Si(OH)2] in approximately 100 mLof the water sample were determined by continuous flow analysis(swAAt or QuAAtro, BL Tech, Tokyo, Japan). The ratios of nitrogen tophosphate (N/P) and silicate (N/Si) were calculated as DIN/PO4 and
DIN/Si(OH)2, respectively. Pigments were extracted from concentrated
phytoplankton cells on glass fiber filter by placing the sample in 5 mL of
90 % acetone for approximately 15 h, and then the concentration ofchlorophyll a was determined by fluorometry (Turner Design Model 10AU, Turner Designs, Inc., CA, USA). Salinity in each station wasmeasured using a conductivity temperature depth profiler. Data on sea
surface temperature (SST) were derived from Fujita et al. (2021).
To examine the temporal variation of prey availability for adultanchovy, surveys for zooplankton abundance were conducted in
May–July from 2001 to 2019. Of these, eight species of copepods(Acartia omorii, Calanus sinicus, Centropages abdominalis, Corycaeus affi­
nis, Microsetella norvegica, Oithona similis, Oncaea scottodicarloi, Para­calanus parvus) were classified as described by Chihara and Murano(1997) to determine the biomass of each species. In total, 5311 samples3

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Fujita et al. (2021).

residuals of the selected models were also examined using the Ljung–Box
test (Ljung and Box, 1978) to ensure that there was no first-order
autocorrelation. The procedures of other environmental analyses arepresented in the Supplementary Materials.
To examine the trends of inter-annual variations in environmental
conditions and the copepod biomass, the variables sampled in May–Julywere visualized as a heatmap using the R package of Superheat (Barterand Yu, 2018). The data were standardized to a mean of 0 and standard
deviation of 1 because comparisons among datasets with different scales
are difficult. To consider the intra-annual variation in SST, the relative
SST was standardized (Supplementary Materials). Hierarchical clus­
tering (dendrogram) based on standardized data was performed to un­derstand the similarity of the inter-annual variability. According to theresults of clustering of copepod biomass variability, the temporal trendof the ratio of the biomass of a given group to the total biomass of all
species was examined using an LMEM including the sampling month as arandom effect.
To examine the potential predator–prey relationships including
chlorophyll a– nutrient, herbivorous and omnivorous copepod–­
chlorophyll a, and carnivorous copepod–herbivorous and omnivorous
copepod, all variables were standardized. The feeding habits of co­
pepods followed Uye and Shimazu (1997) as follows: C. sinicus,
M. norvegica, and P. parvus are herbivorous, whereas A. omorii andO. similis are omnivorous. LMEMs were used to determine which factors
affected the predator concentrations or biomass. The models included
the concentration or biomass of prey as a fixed effect and sampling
month and/or sampling year as a random effect based on the minimum
cAIC. To analyze the chlorophyll a–nutrient relationship, samples werecollected from April to August in 2001–2019, whereas for the analyses ofthe latter two relationships, specimens were collected from May to Julyin 2001–2019. In the copepod analyses, C. abdominalis andO. scottodicarloi were excluded because their frequencies of occurrence
were much lower (<1 %) than those of other copepod species over the
study period. The subsequent statistical procedures were performed aspreviously described.
To determine the temporal trend of the effect of SST on the biomassof copepods, a GAM was applied after the biomass of each species wasstandardized. The data on biomass of copepods were standardized aspreviously explained. The GAM was formulated as follows: incorpo­
rating interactions, Y = a + s(sampling year) + s(SST) + s(sampling
year, SST), where s is the smoothing spline. The subsequent statisticalprocedures were performed as previously explained.

2.3. Experimental data
Anchovy were caught by commercial boat seines in the central Seto
Inland Sea in June 2016, and they were transferred to the Hakatajima
Field Station of the National Research Institute of Fisheries and Envi­ronment of the Inland Sea. Specimens were kept at ambient temperature(range from 12 to 27 ◦ C) under a natural photoperiod over the period,
and daily spawning was observed from May 2017. To examine maternal
effects on larval viability, the body size and age of females as well as
their growth trajectory can affect offspring traits (Green, 2008; Hixonet al., 2014; Burton et al., 2013). To minimize the potential coexisting
effects of her past and current status on larval traits, F1 specimens
hatched from eggs of anchovy collected in the central Seto Inland Sea
were reared artificially under identical environments to examine theeffects of food availability on reproductive traits. Then, F2 specimensborn to F1 females subject to different food rations were compared toassess the effects of maternal food availability on offspring viability.
Detailed experimental procedures are presented in the supplemental
materials. At the Hakatajima Field Station of the National ResearchInstitute of Fisheries and Environment of Inland Sea, all experimental
procedures followed the Animal Welfare Guidelines of the Fisheries
Research and Education Agency, Japan (50322001) and were approvedby the Committee of Animal Welfare of the National Research Instituteof Fisheries and Environment of Inland Sea (no. 2016–4).
To examine the body condition of experimental fish, Ke was usedbecause the SW–SL relationship differs between wild and experimental
fish, as indicated by Lloret et al. (2014). Ke was calculated using thefollowing equation: Ke = SW/stSWe, where stSWe = exp[− 11.83 + 3.14
× ln(SL)] (n = 122, p < 0.001, R2 = 0.88). Egg size (mm3) was calculated
as mentioned previously. Batch fecundity was estimated from specimens
with ovaries containing migratory nucleus oocytes using a gravimetricmethod (Yoneda et al., 2013). The relative batch fecundity was calcu­
lated as follows: relative batch fecundity = batch fecundity/SW. The
relative egg production on the day of the experiment in each tank was
calculated as follows: relative egg production = TE (total number ofeggs) /TEB (mean total number of eggs before experiment), where TE is
the total number of eggs on a given day of the experiment and TEB is themean total number of eggs daily in the last three days before the onset offood manipulation. To analyze the starvation tolerance of larvae, eggs
spawned in each treatment group were collected on two different days
within 26–29 days after the start of the experiment to establish duplicate
tanks. Meanwhile, to assess larval size and growth, eggs were sampled
on three (high food availability) or two (low food availability) different
days. The experiment for comparing larval size and growth was termi­
nated when larvae reached 15 days of age, corresponding to SL of
approximately 8 mm because the abundance of recruit fish in the central
Seto Inland Sea may be dependent on variations in the survival rates oflarvae based on an SL range of 3–8 mm (Zenitani et al., 2007).

2.4.2. Effect of prey availability on the maternal body condition
Classification of the relationship between the prey selectivity of adultanchovy (E) and prey availability in the environment was determinedusing k-means clustering. The best number of clusters in a data set wasdetermined using the R package of NbClust (Charrad et al., 2014), which
provides 30 indices that determine the number of clusters in a data set
and offers the best clustering scheme from different results. Copepods
were classified into several groups based on the highest frequency ofoccurrence of each species in clusters.
The effect of prey availability on the maternal body condition wastested using LMEMs after standardizing copepod biomass and K. The
classification of copepod species was based on the results of the re­lationships between prey selectivity and the occurrence of copepods inthe environment. Moreover, the biomass of C. sinicus was also used inthis analysis because this species is regarded as one of the key secondary
producers linking phytoplankton and higher trophic levels in the Seto
Inland Sea (Uye and Murase, 1997). The models included the biomass ofcopepod species as a fixed effect and sampling year (2001–2019) and/or
month (May and June) as random effects based on the minimum cAIC. In
the residuals of the final models, first-order autocorrelation was tested
using the Ljung–Box test.

2.4. Data analysis
2.4.1. Physical and biological environment
To examine the inter-annual variation of nutrient availability, themonthly average levels of DIN, PO4, and Si(OH)2 at 0 m, 20 m, and thesea floor from April to August in 2001–2019 were analyzed using linear
mixed effects models (LMEMs) with the restricted maximum likelihood
estimation. The monthly average concentration of chlorophyll acollected from 0 m over the study period was also tested using an LMEM.
The models included sampling year as a fixed effect and sampling month(April–August) as a random effect. The significance of fixed effects wastested by Satterthwaite’s degrees of freedom method (Kuznetsova et al.,2017). The model of each factor with and without natural logarithmictransformation was selected on the basis of the minimum conditional
Akaike information criterion (cAIC, Vaida and Blanchard, 2005). The
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2.4.3. Effects of maternal prey availability on body condition and egg size
in wild fish
The temporal trends of K of adult females and RPE and the influenceon the early survival rate (RPE) were analyzed using LMEMs in which
the sampling month (May and June) was a random effect. As RPE
involved data values of zero, a constant value of 0.0001 was added toenable logarithmic transformation. To examine the relationship be­
tween K and RPE the data on K and RPE were standardized, and theprocedures of these analyses were performed as previously explained.
In anchovy, egg size decreases with increasing water temperature(Yoneda et al., 2014). Thus, the relationships between egg size and SST
over a water temperature of 16–24 ◦ C in May–June were comparedamong the sampling periods 2005–2006, 2009–2010, and 2015–2016
using LMEMs. SST and sampling period were fixed effects, and sampling
month was a random effect. Moreover, K of females, RPE, and envi­
ronmental conditions [SST, biomass of all copepods, biomass of two
copepods (C. sinicus and C. affinis)] during the three periods werecompared using LMEMs.

batch fecundity, and relative egg production were tested using LMEMs
in which treatment was a fixed effect and tank or day of experiment wasa random effect. The effect of food availability on relative batchfecundity was tested using an LMEM. The response variable was thenatural logarithm of batch fecundity, treatment was a fixed effect, tank
was a random effect, and logarithm of SW was used as an offset term.
The effects of maternal food availability on larval size and growth rates
were also tested using LMEMs in which maternal food availability (highor low) was a fixed effect and tank was a random effect. The daily
growth rate during exogenous feeding (GR) was calculated as followed:
GR = (SL at age 15 days − estimated SL at first feeding)/12 days. The
estimated SL at first feeding in each treatment was calculated using
LMEMs. All statistical analyses were performed using R version 4.0.3 (RCore Team, 2020).

2.4.4. Effects of maternal prey availability on reproductive traits in captivefish
To examine the effect of maternal food availability on starvation
tolerance of larval fish, a generalised linear mixed-effect model (GLMM)
incorporating binominal response distribution with logit link function
was used. The full models combined maternal food treatment and timeafter hatching as fixed effects and tank as random effects.
The effects of maternal food availability on Ke, egg size, relative

DIN levels from April to August significantly decreased over the 19year study period (p < 0.01, Fig. 3a), whereas PO4 levels increased overthe period (p < 0.001, Fig. 3b). As such, the N/P ratio rapidly decreased
over the study period (p < 0.001, Fig. 3c). Specifically, the estimated N/
P ratio decreased from 10.8 in 2001 to 3.6 in 2019. There was no sig­
nificant temporal trend of Si(OH)2 levels over the study period (p = 0.33,
Fig. 3d), but because of the decrease of DIN, the N/Si ratio significantly
decreased over the study period (p < 0.01, Fig. 3e). The concentrations

3. Results
3.1. Variations of nutrient and chlorophyll a levels

Fig. 3. Temporal trends of concentrations of dis­solved inorganic nitrogen (DIN, a), phosphate (PO4,b), the N/P ratio (c), dissolved silicate [Si(OH)2, d],
the N/Si ratio (e) and chlorophyll a (f) from April toAugust in 2001–2019 in the central Seto Inland Sea.
The average data on nutrients concentrations were
sampled from 0 m, 20 m, and the sea floor at eachstation and the data on chlorophyll a concentrations
were obtained from 0 m. Linear mixed effect models
fitted to the observed data are presented for DIN,
PO4, N/P, and N/Si. Dots indicate 95 % confidence
interval.

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of chlorophyll a on the surface appeared to vary annually (Fig. 3f), butthere was no significant temporal trend over the study period (p =0.212). LMEMs illustrated that the chlorophyll a concentration was
positively correlated with the DIN concentration (p < 0.05, Table S1).
The effects of PO4, Si(OH)2, the N/P ratio, and the N/Si ratio on chlo­rophyll a concentrations were not significant. The concentrations of
DIN, PO4, Si(OH)2, and chlorophyll a appeared to increase as the seasons
progressed, during which SST increased and the range of salinity
widened (Fig. S1). GAMs revealed significant effects of SST and salinity
on the concentrations of DIN and chlorophyll a (Fig. S2, Table S2). The
concentration of DIN gradually increased as SST increased and salinity
decreased. The relationship between the chlorophyll a concentrationand SST exhibited a dome-shaped curve, peaking at approximately
20 ◦ C, whereas the concentration of chlorophyll a rapidly increased assalinity decreased.

Acartia omorii (0.07). <1 % of the average relative biomass was attrib­
utable to Centropages abdominalis and Oncaea scottodicarloi.
Hierarchical clustering of environmental conditions and the copepod
biomass based on standardized data permitted the classification ofvariables into two groups (Fig. 5). Concerning environmental conditions
Si(OH)2, PO4, and SST were categorized into the same group, whereas
DIN, chlorophyll a, and salinity were categorized into another group. In
the former group, the variables appeared to increase in the last decade,whereas those in the latter group tended to decrease. Concerning
copepod species, O. scottodicarloi, C. sinicus, O. similis, and C. affinis werecategorized into the same group (group 1), whereas M. norvegica,
P. parvus, C. abdominalis, and A. omorii were categorized into a separate
group (group 2). The biomass of the former group appeared to decreasein the last decade, whereas that in the second group appeared to increase
in recent years. The ratio of the biomass of group 1 to the total biomassof all copepod species rapidly decreased over the study period (Fig. 6).
The estimated ratio of group 1 was 0.48 in 2001, versus 0.13 in 2019.
GAMs revealed the significant effects of SST and sampling year on
the biomass of six copepod species (Fig. 7, Table S3). A unimodal dis­tribution of biomass was found in A. omorii and C. abdominalis. The
former ranged from 15 to 21 ◦ C in 2013–2016, whereas the latter ranged
from 15 to 19 ◦ C in 2005–2008. In C. sinicus, the biomass was higher atwater temperatures of 15–22 ◦ C in the early 2000 s, but it decreased over
the temperature range after the late 2000 s. In C. affinis and O. similis, the3.2. Variations of copepod communities
Annual and inter-species variations of the biomasses of eightcopepod species from May and July were observed (Fig. 4a). Amongthem, Paracalanus parvus was dominant over the period, and the averagerelative biomass was 0.49 (Fig. 4b). The subdominant species was
Oithona similis (average relative biomass = 0.12), followed by Calanus
sinicus (0.11), Microsetella norvegica (0.10), Corycaeus affinis (0.10), andFig. 4. Temporal trends of the composition of the average biomass (a) and relative biomass (b) of eight copepod species in May–July from 2001 to 2019.
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Fig. 5. Heatmap visualization of the trends of inter-annual variation of environmental conditions (a) and eight copepod species biomasses (b) in May–July from 2001
to 2019. Hierarchical clustering of environmental conditions and copepods based on standardized data permitted classified of the variables into two groups. DIN,
dissolved inorganic nitrogen; PO4, phosphate; Si(OH)2, silicate; SST, sea surface temperature.

biomass peak tended to gradually shift in cooler waters (<20 ◦ C) fromthe early 2000 s to the middle 2010 s. The biomass decreased over thelast 5 years. The biomass of P. parvus had a concave downward temporal
trend from the mid-2000 s to early 2010 s, but unlike the trends for theother five species, the biomass was greater in warmer waters (20–26 ◦ C).
No significant relationship between the biomass of copepods andchlorophyll a levels in May–June was found in A. omorii and C. sinicus,
whereas a negative relationship was observed in M. norvegica, O. similis,
and P. parvus (Table S1).

3.3. Effect of prey availability on the maternal body condition
The data on the relationship between E of adult anchovy (component
1) and the occurrence of copepods in an environment (component 2) fell
into four of five clusters (Fig. S3, Table S4). C. affinis, O. similis, andP. parvus were categorized in different clusters, whereas A. omorii and
M. norvegica were categorized into the same cluster. For the lattercluster, the data were combined in the subsequent analyses. C. affinisand P. parvus displayed higher prey selectivity, whereas A. omorii/
M. norvegica and O. similis exhibited neutral and lower selectivity,
respectively.

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80 h in the low food availability group. There were no significant dif­ferences in SL on the day of hatch and the time of the first feeding be­
tween the maternal food groups (hatching, p = 0.14; first feeding, p =0.51, Fig. 11a, b). Meanwhile, SL at an age of 15 days for larvae derived
from females in the high food availability group was significantly
greater than that of larvae born to females in the low food availability
group (p < 0.05, Fig. 11c). This reflected a significant effect of maternal
food availability on GR (p < 0.05, Fig. 11d). The estimated GR of larvae
from females in the low food availability group was approximately 76 %of that of larvae from females in the high food availability group.
4. Discussion
To the best of our knowledge, this is the first study to demonstrate
the effects of bottom-up processes on the reproductive success of marine
pelagic fish through maternal contributions to offspring viability. Ourfindings indicated that the copepod species composition markedly
changed over the 19-year study period. Among copepod species, thebiomass of several copepods found in the cool-water period of a given
season (May–June), corresponding to the main spawning season andhatch date of recruit fish of anchovy, markedly declined over the last
decade. This recent decrease in biomass appeared to be accompanied byelevated SST and decreasing levels of chlorophyll a. The latter may be inassociation with decreasing nitrogen levels. These bottom-up drivers
appeared to reflect changes of the maternal body condition of anchovy,
subsequently leading to variations of egg and larval traits and eventuallyaffecting recruitment.

Fig. 6. Temporal trend of the ratio of the biomass of group 1 to the total
biomass of all copepod species in May–July of 2001–2019. Group 1 included
Calanus sinicus, Corycaeus affinis, Oithona similis, and Oncaea scottodicarloi. A
linear mixed effect model fitted to the observed data is presented (Ratio = exp[1084.9–142.8 × ln(year)] (year, p < 0.001)). Dots indicate the 95 % confi­
dence interval.

LMEMs revealed no significant effect of the total biomass of all
copepod species on K (Table S1). This finding was replicated forO. similis. There was a negative correlation between K and the biomassesof A. omorii/M. norvegica (Fig. 8a) and P. parvus (Fig. 8d). Conversely,
there was a positive correlation between K and the biomasses of
C. sinicus (Fig. 8b) and C. affinis (Fig. 8c).
3.4. Effects of the maternal body condition on egg size and early survival

4.1. Drivers affecting zooplankton communities

K of female anchovy during the main spawning season significantly
decreased over the 19-year study period (p < 0.001, Fig. 9a, Table S5).
RPE of anchovy in May and June also significantly decreased over the
study period (p < 0.001, Fig. 9b). The effect of K on RPE was significant(p < 0.01), with higher K leading to higher RPE (Fig. 9c).
The effect of the sampling period on the egg size–SST relationshipwas significant (period, p < 0.001, Fig. 10). The estimated egg sizes atstandard SST (20 ◦ C) in 2015–2016 were approximately 96 and 93 % of
those in 2005–2006 and 2009–2010, respectively (Table 1), whereas theestimated egg size at estimated SST in May–June decreased temporally(egg size = 0.250 mm3 in 2005–2006, 0.245 mm3 in 2009–2010, and
0.227 mm3 in 2015–2016) because of the increase of SST over the study
period. K and RPE in 2015–2016 were significantly lower than those in
2005–2006 and 2009–2010.
Estimated RPE in 2015–2016 was approximately 4 % of those in theother two periods. There was no significant difference in the biomass of
all copepods among the three periods, but the biomass of C. sinicus andC. affinis was significantly lower in 2015–2016 than in 2005–2006 and2009–2010.

In this study, temporal changes of the copepod composition in
May–July were observed over the 19-year study period, but using thetrend of the inter-annual variability of the copepod biomass, species
were classified into two groups. C. sinicus, C. affinis, O. similis, andO. scottodicarloi were categorized into the same group, whereas
A. omorii, C. abdominalis, M. norvegica, and P. parvus were categorized
into a second group. The heatmap revealed that the abundance of formergroup appeared to decrease in the last decade, whereas that of the lattergroup appeared to increase. As such, it is noted that the total biomass of
all copepod species appeared to fluctuate over the study period, but theratio of the biomass of the former group dramatically decreased. Our
analyses of the effect of SST on copepod biomass also suggested thateach species appeared to be relatively stenothermal, probably because
there were certain thermal limits on egg production and embryonicdevelopment (Liang and Uye 1996b; Uye, 2000). The biomass peaks of
C. sinicus, C. affinis, and O. similis gradually shifted in cooler water in agiven season (May–June), following decreases in their biomass in thelast decade. Conversely, the biomass of P. parvus, occupying approxi­
mately half of the total biomass of the examined copepods, fluctuatedover the study period, but it appeared to recently increase in warmer
water in that season (mainly July). Concerning M. norvegica, the biomass
and the relative biomass were higher in the last decade. This species is atypical warm-water copepod in the Seto Inland Sea that exhibits higher
egg production in late summer and autumn (Uye et al., 2002). In thecentral Seto Inland Sea, SST in the beginning of May increased gradually
over the 26-year study period. SST increased rapidly from the middle of
May to the beginning of June after 2015 (Fujita et al., 2021). Such in­creases in SST could be one of the factors influencing the shifting
composition and biomass of copepod species in response to the thermal
preference of each species.
There were no positive relationships between the copepod biomass
and chlorophyll a concentration in five herbivorous and omnivorous
copepod species. However, the inter-annual variabilities of environ­mental conditions in May–July indicated that the chlorophyll a levelappeared to be lower in the last decade, during which the concentrationof DIN has decreased in addition to decreases in the N/P and N/Si ratios.

3.5. Effects of maternal prey availability on reproductive traits
Ke in species with high food availability was similar to that at thestart of experiment (p = 0.86) but was significantly lower than that in
species with low food availability (p < 0.01, Fig. S4, Table S6). Egg sizein species with high food availability appeared to be variable [coeffi­
cient of variation (CV) = 11.7 %] compared with the observations in
species with low food availability (CV = 8.8 %, p < 0.05). The relative
batch fecundity did not significantly differ between the two groups (p =0.78). Meanwhile, there was a significant difference in relative egg
production based on maternal food availability (p < 0.001). The averagevalue in the low food availability group over the experiment wasapproximately 40 % of that in the high food availability group.
There were significant effects of the time duration after hatch andmaternal food availability on the survival rate of larvae under starvation(p < 0.001, Table S6); specifically, the estimated times at a survival rateof 50 % were approximately 90 h in the high food availability group and8

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Fig. 7. Temporal trends of the effect of sea surface temperature (SST) on the biomass (mgC/mm3) of six copepod species in May–July from 2001 to 2019. The
standardized biomass was derived from fitted generalized additive models. Pink, white, and light blue indicate high, moderate, and low biomass, respectively, andsolid lines are contour lines.

This is partly because nitrogen may be a restricting factor for phyto­plankton production in these waters, which could largely be influenced
by terrestrial runoff with rainfall events (Supplementary materials). In
these waters, the chlorophyll a concentration remained markedly lower(mean = 1.65 µg/L) over the study period, being much lower than thateven in other parts of the central Seto Inland Sea (Bingo-Nada, Ohara
et al., 2020). In coral reefs in Hawaii, nutrient loading via runoff
generally leads to increases in nutrient concentrations and subsequent
increases in phytoplankton biomass, but the effects persist for only
several days because of high flushing rates (Ringuet and Mackenzie,2005).
Under limited prey availability, temperature-dependent growth andegg production may be hampered, especially in warmer waters, to pri­oritize increasing metabolic demands (Cross et al., 2015; Boersma et al.,2016). In C. sinicus, temperature-dependent egg production can beobserved under satiation feeding (Uye, 1988), but within a certain

temperature range, the size-dependent chlorophyll a concentration
appeared to be a dominating factor regulating egg production in the Seto
Inland Sea (Uye and Murase, 1997; Uye, 2000) and Bohai Sea (Zhang
et al., 2006). Uye and Murase (1997) also suggested that the discrepancy
between the observed and predicted egg production rates of C. sinicus
may have been caused by food limitation in the Seto Inland Sea even in
the 1990 s. The decrease of the biomass of the carnivorous copepod
C. affinis, which was also observed in the cool-water period, may be
attributable to decreases in the availability of prey copepod species.
Meanwhile, P. parvus consumes a variety of prey items such as diatoms
and microprotozoans. P. parvus females have the potential to keep
spawning in waters over a wide temperature range up to 25 ◦ C throughshort-term alternations of generations in the Seto Inland Sea (Liang andUye, 1996b). This appears to be in contrast to the findings in other
copepod species found in cooler water in a given season, including
C. sinicus and O. similis. Accordingly, such bottom-up drivers including
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Fig. 8. Relationship between the relative condition factor (K) of female anchovy and the biomass of copepods during the main spawning season (May–June) from2001 to 2019. Linear mixed effect models fitted to the standardized data are presented. Dots indicate the 95 % confidence interval. (a) Acartia omorii and Microsetella
norvegica, (b) Calanus sinicus, (c) Corycaeus affinis, and (d) Paracalanus parvus.

items might have declined. The increase in SST in May–June in the lasttwo decades (Fujita et al., 2021) may have also facilitated the decreaseof K because of increasing metabolic and energetic demands (Pörtner
and Peck, 2010). Interestingly, there was a positive correlation between
RPE and K of female anchovy over the study period. There was also asignificant difference in egg size at a given temperature among the threedifferent sampling periods accompanied by differences in K and RPE.
Females in 2015–2016 displayed lower K produced smaller eggs at agiven temperature than their counterparts in 2005–2006 and2009–2010. As SST in May–June gradually increased over the period(Fujita et al., 2021), the difference in the estimated egg size at the
average temperature of that season among the three periods increased.
Although there was no significant difference in the biomass of all
copepod species among the three periods, the estimated biomass of
C. sinicus and C. affinis in 2015–2016 was approximately 23 % of that in2005–2006 and 2009–2010. These observations imply that the maternal
body condition and/or ongoing prey availability may affect offspringsurvival in the early stage of life through egg size.

pulsed increases of chlorophyll a concentrations in the warm period
might result in a relatively stable biomass of P. parvus in these waters.
4.2. Bottom-up effect on the reproduction of anchovy
Our findings illustrated that K of female anchovy in May–June was
not significantly influenced by the biomass of all copepod species. This is
likely attributable to the influence of the prey selectivity of adult an­
chovy and inter- and intra-annual variation of the biomass of eachspecies. Cluster analyses suggested that female anchovy prefer toconsume P. parvus and C. affinis, with the former being more abundant
than the latter during the study period. This is consistent with thefindings of a previous study conducted in 1995 (Yamamoto andKatayama, 2012). However, the results for the relationship between K of
female anchovy and copepod biomass revealed a contradiction between
the two species. This is probably attributable to the mismatch in thetiming of the seasonal peak between copepod biomass and K. As previ­
ously mentioned, the biomass of P. parvus increased with increasing SST
over the period of May–July, whereas K of females decreased as theseason progressed [May, K = 1.064 ± 0.002 (n = 4653); June, K = 1.007± 0.001 (n = 5011)]. Anchovy continue to spawn during the prolonged
period (spring–autumn) by quickly transferring energy from ongoing
prey items to eggs (Tanaka et al., 2016). Thus, P. parvus could contributeto successive egg production in anchovy in the warmer-water period of
the spawning season. Meanwhile, the temporal decrease of the C. affinis
biomass was associated with the inter-annual decrease of K in female
anchovy. Conversely, A. omorii, M. norvegica, and O. similis were lessselective prey items for adult anchovy. There was a negative correlation
between K of females and the biomasses of A. omorii and M. norvegica,and no significant correlation was found in O. similis. Specifically,
biomass appeared to increase in former two species the in the last
decade.
The temporal decrease of K in female anchovy in May–June over the
19-year study period was evident, suggesting that the abundance of prey

4.3. Effect of maternal prey availability on offspring traits
Our food manipulation experiment illustrated that a reduction inmaternal food availability resulted in decreases of K and egg size, as
females with high food availability produced significantly larger eggs
than those with low food availability. Meanwhile, there was no signif­
icant difference in relative batch fecundity between the high and low
food availability groups despite the significant difference in relative egg
production between the groups. These observations were consistent
with previous findings using similar food manipulation experiments(Tsuruta and Hirose, 1989; Yoneda et al., 2014).
Although there was a significant difference of egg size between thetwo food availability groups, CV of egg size was larger in the group withhigh food availability, indicating that females under ad libitum feeding
do not always produce larger eggs at a given temperature, as found in a10

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Table 1
Estimated relative condition factor (K), egg size (mm3) at 20 ◦ C, and recruitment
per egg abundance (RPE, 10-3) of anchovy in May–June in three different
sampling periods. Estimated sea surface temperature (SST, ◦ C), the biomass of
all copepods (AC, mgC/m3), and the biomass of Calanus sinicus and Corycaeus
affinis (CC, mgC/m3) over the periods are also presented. Parameters were
estimated using linear mixed effect models.
PeriodEgg size

K

RPE

SST

AC

CC

2005–2006
2009–20102015–2016

0.245*
0.251
0.235***

1.07*
1.08
1.00***

5.86
5.86
0.22***

19.72
20.39
20.47

14.38
13.01
15.03

4.02
4.02
0.92*

*

p < 0.05.
p < 0.001.

***

previous study (Yoneda et al., 2014). There was a significant differencein the duration of survival for starved larvae from females between thehigh and low food availability groups; specifically, larvae hatched fromlarge eggs (from the high maternal food availability group) survived
longer than those hatched from smaller eggs (from the low maternal
food availability group). Meanwhile, there were no significant differ­ences in SL of larvae at hatch and first feeding between the two foodavailability groups, probably because of the use of eggs of similar size.
Rather, larval sizes before the first feeding appeared to correlate withegg size. Thus, the different starvation tolerance of larvae from the twomaternal food availability groups may reflect variation in the endoge­
nous energy of larvae for basal maintenance and behavior after hatch.
These observations are consistent with previous findings in most clu­
peoids (Ganias et al., 2014). Conversely, there was a significant differ­ence in SL of larvae at age 15 days between the food availability groups.
This was caused by a significant difference in GR derived from differ­ences in maternal food availability. These findings imply that both egg
size and ongoing maternal prey availability might affect the growth rateduring the exogenous feeding period, affecting offspring viability under
the paradigms of growth-selective mortality (Meekan and Fortier, 1996;
Takasuka et al., 2004; Robert et al., 2007). However, this is inconsistent
with the findings in haddock (Melanogrammus aeglefinus) that the effectsof egg size on larval traits interact with the effect of prey availability
during the exogenous feeding period. Namely, differences in larval traits
in relation to egg size can be found under low prey availability, but notunder high prey density (Rideout et al., 2005). Further investigation of
the mechanisms of the maternal contribution to larval viability of ma­rine fish is needed.

Fig. 9. Temporal trend of the relative condition factor of female anchovy (a),the recruitment per egg abundance (b, RPE (10− 3)) and relationship between
standardized RPE and standardized relative condition factor (c) for specimens
collected during the main spawning season (May–June) from 2001 to 2019. (b)The relationship between ln(RPE + 0.0001) and sampling year was shown.
Linear mixed effect models fitted to the data are presented. Dots indicate the 95% confidence interval.

4.4. Potential effect on the recruitment variability of anchovy
From the experimental evidence, the larvae at hatch and first feedingin the central Seto Inland Sea in recent years are expected to be smaller
and their starvation tolerance at a given temperature may be lower thanobserved in the 2000 s because the sizes of eggs have decreased inconjunction with decreasing K and increasing SST. Although it remains
unknown whether the growth rates of larvae during exogenous feeding
have changed in response to maternal contributions in the sea, smaller
larvae with lower growth potential would carry a higher mortality riskin the early stage of life (Houde, 2008) even if prey availability remains
constant. Field observations illustrated that the concentration ratios ofcopepod nauplii per larval anchovy in 2015–2019 were much lower
than those in 2002–2005, suggesting a mismatch between food re­quirements and food availability in the early stage of life (Fujita et al.,2021). Lower feeding rates are expected to lead to slower growth, which
increases cumulative mortality in early life stages (Cowan et al., 2000;
Houde, 2008). The reduction of RPE in recent years may therefore
reflect increasing intra-cohort competition for prey in early stages of life
considering hydrodynamic features and potential predators and com­
petitors in these waters (Fujita et al., 2021). It would be difficult todisentangle the causes of decreasing RPE, but the dramatic decrease in

Fig. 10. Relationship between egg size and sea surface temperature (SST)
during the main spawning season (May–June) in 2005–2006, 2009–2010, and2015–2016. Linear mixed effect models fitted to the observed data are pre­sented. n = number of eggs examined. Data are presented as the mean ± SE.

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Fig. 11. Effects of maternal food availability on larval sizes and growth rates in relation to egg size during exogenous feeding. (a) Day of hatch, (b) day of first
feeding (age 3 days), (c) age 15 days, and (d) growth rate. HF = high food availability, LF = low food availability. Data are presented as the mean ± SE.

recruitment abundance in the last decade might be attributable tocoexisting factors induced by changes in the status of maternal andlarval prey availability.

Agency, 2010) to ecosystem-based management (Peck et al., 2013;
Somarakis et al., 2019). Although a sufficient understanding of ecosys­
tems will require a greater focus on environmental surveys, a challenge
for adaptive management is to identify the right balance between
gaining knowledge to improve management in the long term andachieving the best short-term outcome based on current knowledge(Moore and McCarthy, 2010).

5. Conclusions
Our findings revealed dramatic changes in the components of marine
ecosystems ranging from nutrients to zooplankton in the central Seto
Inland Sea, in which oligotrophication and gradual warming during the
spawning season of anchovy have proceeded. Under this situation, thecatch of recruit anchovy (larvae and juveniles) decreased over the study
period (Fujita et al., 2021). This agrees with the expectations in coastal
waters in that compared with offshore regions, it may be more difficult
to identify causal environmental factors behind changes in small pelagic
fish within coastal ecosystems because multiple factors interact between
physical and biological factors to influence the suitability of fish habitats(Peck et al., 2013; 2021). Because of the susceptibility of small pelagic
fish to environmental cues, natural mortality changes result in increased
recruitment variability, making it difficult to conduct fishery manage­
ment for these species (Katara, 2014). In the central Seto Inland Sea, theapproach to ensure sufficient egg production has failed in recent years tosustain a certain number of recruit fish during the ongoing season. Ourfindings demonstrated that bottom-up processes drive the reproductive
success of anchovy. This partly explains why the abundance of anchovy
recruitment has rapidly declined in the last decade despite adequate egg
production. These findings suggest the need to change the strategy fromegg abundance–recruitment proportionality management (Fisheries

Declaration of Competing Interest
The authors declare that they have no known competing financial
interests or personal relationships that could have appeared to influence
the work reported in this paper.
Acknowledgments
We thank the captains and crews of the R. V. YAKURI and staff of the
Kagawa Prefectural Fisheries Experimental Station for their assistancewith sampling and collection of the data. We also thank the staff of theFisheries Resources Institute, Hakatajima Field Station for their assis­
tance with rearing experiments, and editor and anonymous reviewer forconstructive comments on original manuscript. This work was sup­ported by Fisheries Agency of Japan and Japan Fisheries Research and
Education Agency and by Grant-in-Aid for Challenging Research (Pio­neering) (KAKENHI No. 19H05540) from the Japan Society for the
Promotion of Science.
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org/10.1016/j.pocean.2022.102860.
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