Knowledge on the Biological and Fisheries Aspects of the Japanese Sardine, Sardinops melanostictus (Schlegel, 1846)

Abstract

Japanese sardine (Sardinops melanostictus) is a significant small pelagic fish and a valuable resource that plays an essential ecological role in the marine ecosystem. It is present in the far Eastern Asian maritime waters, including the Pacific Ocean, Sea of Japan, and the East China Sea. Encircling nets, particularly purse seines, are the most used fishing equipment to catch this species. Their fishing grounds are located entirely in coastal areas. Japanese sardine catches have shown varying trends over the last five decades, with a high frequency of captures occurring in the 1980s before collapsing in the early 1990s. The economic and ecological importance of this species has prompted much research, which provided additional information about their spawning migration, distribution, fisheries, and biology. This research was mostly undertaken in the Sea of Japan and its adjacent waters spanning in the north Pacific Ocean. Despite all this research and the importance of this species in its habitats and in commercial fisheries, there is a lack of a recent review presenting the status of global fisheries and biological information for this species. This paper summarizes and updates information on the global geographical distribution, biological aspects, trends in catches, stock fluctuations and assessment, and management measures of the Japanese sardine population. This paper also summarizes information related to the influence of environmental factors on the occurrence of this species and also identifies information gaps. Further research directions are also discussed in this work, which may help improve the knowledge of Japanese sardine and establish rational management measures for their conservation.

1. Introduction

Small pelagic fish species (SPF) are the largest group of bony fish and represent more than 30% of the total landings of marine fisheries in Japan and the world [1]. Among these SPFs, sardines are the most targeted species due to their nutritional and ecosystem importance. Indeed, according to the Committee on the Status of Endangered Wildlife in Canada [2], these species are an essential source of food for the human population and thus contribute to food security. Furthermore, from an ecosystem point of view, many other fish species such as tuna, amberjack, barracuda, bonito, hake, mackerel, marine mammals (such as sea lions, porpoises, whales), and birds (such as cormorants, gulls, and pelicans) feed on these important small pelagic fish. Due to their short life span and low position in the marine food web, knowledge on the reproductive strategy of these small pelagic species is relevant [1]. Sardines can produce large quantities of pelagic eggs during an extended spawning season. However, environmental factors can sometimes disrupt their reproduction and determine their geographical distribution and biological constraints such as population size and demographic structure [3,4].

Among these sardine species, the exploitation of the Japanese sardine plays an essential role in most Asian countries’ fisheries, especially in Japan, where the exploitation of this species started in the 1950s and continues to the present day. In China, on the other hand, the exploitation of Japanese sardines began in the 1990s and is becoming increasingly important. The Pacific coast of northeast Honshu, Hokkaido, the Sea of Japan and the Korean coasts were the main fishing areas [5], and the catches of Japanese sardines in the Far East has been subject to extraordinary fluctuations [5]. Physiological, ecological, and environmental aspects, such as the distribution, migration, spawning activity, growth and maturation of the Japanese sardine as well as fishing efforts, were the main factors responsible for the enormous fluctuations of this species. Studies have confirmed this assumption about Japanese sardines for several decades [6,7]. The data obtained on Japanese sardine catches indicate several phases of increasing stock abundance over the last 60 years. The first of these phases (1972–1992), was characterized by the intensive fishing of Japanese sardines, especially in Japan and Russia, and the last, relatively recent phase (1992–2018) has been marked by a great deal of exploitation of this small pelagic by the Chinese fishery [8]. The total catch of Japanese sardines was at a low level, around 9200 tons in 1965, but increased in the early 1980s and reached 5,428,922 tons in 1988. This again declined sharply between 1993 and 2007, reaching 1,796,132 and over 200,000 tons, respectively, before being stable at around 100,000 tons per year [8,9] (World Production Statistics (1950–2020)). Due to the worrying fluctuations of this species over the years, research based on the biological and fisheries aspects, including stock assessment and ecosystem management, has increased in recent years, intending to establish management measures for the rational exploitation of this small pelagic species [9].

To this end, several specific research topics on this species have been the subject of scientific publications over the years. However, it is difficult to find a recent study in the scientific literature that updates all the information concerning Japanese sardine, hence the importance of this review, although Yatsu [10] reviewed the population dynamics and management of small pelagics around the Japanese archipelago. Similarly, very relevant research topics on other sardine species have emerged in recent years and strengthened existing knowledge [2,11,12]. Based on the information available in the published literature, this review summarizes information on the population dynamics, reproductive aspects, and catch trends of this species over the last five decades in Asia and Europe. It also presents the stock assessment, stock fluctuations, stock status and management actions undertaken for Japanese sardine. Therefore, the information presented in this paper could allow us to recommend some management measures and future research directions related to the Japanese sardine in its habitats. These future research studies would allow a precise evaluation of the stocks in the aforementioned habitats to establish management actions for the rational exploitation of Japanese sardine.

2. Distribution, Migration, and Recruitment

Many studies have reported the distribution and migratory movements of Japanese sardines in their areas of occurrence using different approaches [5,13,14,15,16,17]. Some of these studies used satellite data from the National Oceanic and Atmospheric Administration (NOAA), satellite images, and water temperature distribution charts to show the movements of Japanese sardines. Other studies used the recruitment-forecasting model, and other studies presented a spatio-temporal analysis using generalized additive models to define the dynamics of this species in Japanese waters. These studies helped us to understand the distribution of Japanese sardines and the main environmental factors (temperature, salinity, fishing effort) that influence their distribution, causing fluctuations in the recruitment and spawning stock biomass of the species in the northwest Pacific.

2.1. Distribution and Migration

The distribution area of Japanese sardine expands when stock levels are high but is limited to coastal waters during periods of low stock levels. Japanese sardines frequent the waters of the Pacific; they are broadly distributed in the northwestern Pacific Ocean, the central Pacific, and the Bering Sea during times of high abundance. Additionally, they are present in the coastal waters of Japan (all coasts) ranging from Okhotsk to the coastal area of southern Kyushu [5,17,18,19,20,21,22,23,24,25,26,27,28,29,30,31,32,33]. Japanese sardine is also present in Chinese waters, in the Japan Sea coast of Korea, and in the Yellow Sea coast of Korea [34,35,36,37]. In the U.S.S.R., they are found in areas as far north as the Gulf of Tartary, Sakhalin, and the eastern coast of the Kamtchatka Peninsula Kronotzki Cape and neighboring localities [8,13]. Figure 1 shows the distribution map of Japanese sardines in waters around the world.

Reproduction and feeding are the most valuable factors determining the migratory movements of marine species. This is the case of Japanese sardine adults and juveniles, which migrate northwards for different ecological reasons in summer and southwards in winter along the Japanese coasts, and the same movement occurs in autumn and winter [14,20,37]. Furthermore, Japanese sardines migrate to breed from December to early May in the southern parts—in bays, in the coastal areas of the open sea, and towards the Tatar Strait and the Sea of Okhotsk off Sakhalin [23]. This species is very dynamic and follows different migratory flows according to its needs and habitation regions. However, several factors influence this dynamism, thus explaining the differences observed in the migration and distribution of this small pelagic fish.

Factors Affecting the Distribution and Migration of Japanese Sardine

The main variables that determine the distribution of this species are climatic conditions (such as temperature), food and reproduction [14,20,27,38,39,40,41,42,43,44,45,46,47,48,49]. The results defined by these authors concerning these aspects are almost the same in all studied areas. The most important factors, which have determined the distribution and migration of this small pelagic fish, are summarized in Table 1.

Figure 1. Distribution of Japanese sardine (Sardinops melanostictus) in the Pacific Ocean indicated in blue, left image (a), and spawning regions and migration patterns by immature (light blue and red arrows) and mature (thick blue and red arrows) Japanese sardines; the light green on the right map shows the spawning grown of this species (b). Images are from [8,50].

Figure 1. Distribution of Japanese sardine (Sardinops melanostictus) in the Pacific Ocean indicated in blue, left image (a), and spawning regions and migration patterns by immature (light blue and red arrows) and mature (thick blue and red arrows) Japanese sardines; the light green on the right map shows the spawning grown of this species (b). Images are from [8,50].

2.2. Mechanisms of Recruitment Variability

With regard to the number of fish surviving to a defined size or age in a given year, recruitment for small pelagic species such as Japanese sardine is generally affected by many environmental parameters such as changes in temperature, prey availability, and the reproduction period. Given the fluctuations, researchers have been interested in the recruitment of this small pelagic species to understand this phenomenon. Many studies have focused on the recruitment of this species and also presented the factors affecting them [1,24,51,52,53,54,55,56,57,58]. An evaluation of these results allows us to conclude that Japanese sardines show recruitment periods with variable fluctuations over the years. The amount of recruitment depends on the distribution area. These fluctuations may be affected by external parameters such as population density (biomass), biological factors, predation, environmental factors (SST, etc.), and sometimes fishing efforts. A correlation exists between larval mortality and environmental variables, which has significant effects on the productivity and recruitment of Japanese sardines [1,15,24,29,33,36,45,48,53,54,57,58,59,60,61,62,63,64,65]. An extensive analysis of the findings of these authors regarding Japanese sardine recruitment shows that environmental and biological factors positively or negatively influence the recruitment of this species according to the area.

Table 1. Factors affecting the distribution and migration of Japanese sardine in their habitats of occurrence.

Factors Affecting Their Distribution and Migration	Areas	Range Degree Celsius (°C)	References
Spawning grounds temperature	northern Pacific coast of Japan.	14–17 °C	[14]
	southern Pacific coast of Japan.	17–19 °C
GSI maturity	Shikanoshima Island,	11 °C	[38]
Spawning grounds temperature	Pacific coast of Japan. Kyushu and Shikoku in Japan, Sanriku coast	11–22 °C	[17,19,20,39]
SST andGSI maturity
Spawning and feeding grounds temperature
Temperature	all reas		[41,42]
Temperature/depth	northern parts of the Pacific	8–20 °C/15–30 m	[43]
Spawning grounds, temperature, salinity, and depth	-	-	[44]
Optimal temperatures for growth	northwest Pacific	16.2 °C	[45]
Spawning grounds temperature and salinity	offshore waters	10–25 °C	[45]
spawning temperature index	western north Pacific	16–17 °C	[46]
Temperature concentration of chlorophyll-a (Chl-a)	western north pacific.	-	[47]
Temperature growth and food density	Kuroshio region to the subarctic Oyashio region	16–17 °C	[45,46,48,63,64]
Habitat temperature	-	0.5–23.8 °C	[27]
GSI maturity	-	11 °C	[49]

Table 1. Factors affecting the distribution and migration of Japanese sardine in their habitats of occurrence.

Factors Affecting Their Distribution and Migration	Areas	Range Degree Celsius (°C)	References
Spawning grounds temperature	northern Pacific coast of Japan.	14–17 °C	[14]
	southern Pacific coast of Japan.	17–19 °C
GSI maturity	Shikanoshima Island,	11 °C	[38]
Spawning grounds temperature	Pacific coast of Japan. Kyushu and Shikoku in Japan, Sanriku coast	11–22 °C	[17,19,20,39]
SST andGSI maturity
Spawning and feeding grounds temperature
Temperature	all reas		[41,42]
Temperature/depth	northern parts of the Pacific	8–20 °C/15–30 m	[43]
Spawning grounds, temperature, salinity, and depth	-	-	[44]
Optimal temperatures for growth	northwest Pacific	16.2 °C	[45]
Spawning grounds temperature and salinity	offshore waters	10–25 °C	[45]
spawning temperature index	western north Pacific	16–17 °C	[46]
Temperature concentration of chlorophyll-a (Chl-a)	western north pacific.	-	[47]
Temperature growth and food density	Kuroshio region to the subarctic Oyashio region	16–17 °C	[45,46,48,63,64]
Habitat temperature	-	0.5–23.8 °C	[27]
GSI maturity	-	11 °C	[49]

2.2.1. Growth-Dependent Recruitment

There have been extensive studies regarding growth-dependent recruitment. The growth rate and recruitment per spawning biomass (RPS) were significant for Japanese sardines [46]. The optimal temperature for the growth rate of juveniles and the reproduction of mature species was around 16 and 17 °C. In Kuroshio-Oyashio, for example, the growth rate of juvenile Japanese sardines controlled by temperature and prey density resulted in positive population recruitment, corroborating with the hypothesis of [66,67]. A low rate of these parameters (temperature and prey density) may lead to the poor growth of juveniles of this sardine type and consequently to a low recruitment of the population size. However, adults’ growth in Japanese sardine is well known to be a negative function of population size [67,68]. The authors of [28,69,70] used linear dynamic models to perform direct tests of the spawning stock biomass and total egg production, and reported a positive effect of the growth rate on the recruitment of Japanese sardine. In the same light, the authors of [63,71,72,73,74] reported positive correlations between early life growth rates and recruitment success in their studies. However, researchers reported a lack of correlation between early-life stage growth rates and recruitment [75,76].

Most studies have shown a real correlation between the growth of juveniles and the recruitment success of this small pelagic. Indeed, the growth rate of Japanese sardine larvae or juveniles can affect the recruitment of its population in a more or less positive way. These age classes are the most vulnerable stages for recruitment. Fishing effort and environmental parameters are the factors that hinder the growth of this species during this critical phase, hence the failure of recruitment. Few studies have shown a negative correlation between these stages and recruitment success. The above factors may be responsible for this negative correlation.

2.2.2. Recruitment of Japanese Sardine and Climate Change

To better understand the correlation between climate change and Japanese sardine recruitment, researchers tested several approaches and environmental parameters, such as maturation ratios, logarithmic recruitment residuals (LNRR) from the simple Ricker model, convergent cross-mapping (CCM) to population dynamics, and SST in potential spawning and feeding areas [54,68,77,78,79,80,81]. Furthermore, authors have observed significant correlations between LNRR and the Monsoon Index (MOI), as well as arctic oscillation (AO) with all the scenarios developed in the Sea of Japan [78]. The combinations between positive MOI and negative AO were positively correlated with the LNRR of Japanese sardine.

Moreover, sea surface temperature (SST) was also an essential factor influencing the recruitment of fish species. Several researchers demonstrated in their research that SST increases primary production, which is favorable to the growth of juveniles of this small pelagic and leads to an increase in population recruitment [54,68,79,80]. Furthermore, these authors demonstrated that the unfavorable global warming condition causes a disadvantage by a population collapse and hence weak recruitment of Japanese sardine. Some studies confirmed that food availability is a potential mediator of climate change effects on fish population dynamics [82,83]. In contrast to these authors, studies showed significant negative correlations between water temperature and the logarithm of recruitment per spawner (LNRPS) in the Kuroshio axis during the winter and early spring [81]. For this author, the water temperature environment affected recruitment through larval survival. In addition to [81], researchers such as the authors of [77] have investigated the relationship between climate change and fluctuations in Japanese sardine populations in the Pacific Ocean. However, the authors of [77] concluded that it was difficult to understand why Japanese sardine stocks increased off Japan during the cold period when recruitment was otherwise positively correlated with temperature.

We can conclude that several environmental factors such as temperature and food availability are favorable to the recruitment of this small pelagic by promoting their growth. This juvenile phase is the best period for the recruitment of this small pelagic. However, the temperature may not be favorable for recruitment in other circumstances. This factor can negatively affect larval survival and therefore lead to low recruitment. Other physical parameters such as fishing effort and low food availability are also unfavorable to the success of Japanese sardine recruitment.

3. Trophic Position, Competition and Predation

To fully understand the trophic position, competition and the predation of Japanese sardines, it is essential to conduct preliminary studies on their feeding habits. For this purpose, studies have been conducted on the stomach contents of Japanese sardines in the Central Sea area of Japan using the fluorometric model 10 method, Turner Designs of [66,84]. Furthermore, the authors of [85] used the strict 99% threshold 18S V9 meta-genetic analysis method to achieve a higher taxonomic resolution of molecular operational taxonomic units (MOTUs). Their study detected the dominant eukaryotic taxa present in the gut contents of Japanese sardines during their principal spawning season in Tosa Bay, Japan.

3.1. Diet Composition

Food is an essential factor in the growth of marine species. This factor increases the survival and growth rate of the different life-history phases of all marine species. Understanding inhabited feeding is essential to understand the biology of certain species for management purposes. In the case of Japanese sardine, several researchers have been interested in the nutritional aspects of this small pelagic. Several authors have conducted studies to determine the diet composition of larval, juvenile, and adult Japanese sardines in several regions. The principal research on this topic is summarized in

Table 2. Main prey’s composition of larval, juvenile and adult stages of Japanese sardine (Sardinops melanostictus).

Japanese Sardine	Main Preys	References
Adults stage	Diatoms, Flagellata, Foraminifera, Radiolaria, Tintinnopsidae and Copepoda (Microsetella, Calanus), Schizopoda, Amphipoda, Decapoda, eggs, larvae of fishes.	[35]
	Zooplankton (Euphausia pacifica, Neocalanus spp. and Calanus sinicus).	[86]
	Plankton.	[87]
	Copepoda, amphipoda, anchovy egg, spherical fish egg diatoms.	[38]
Larval and Juvenile stages	Diatoms and dinoflagellates.	[88]
	Zooplankton (Calanus finmarchicus, Pseudocalanus, elongatus, and Paracalanus parvus.).	[89]
	Paracalanus parvus, Calanus plumchrus, C. finmarchicus, Centropages abdominalis, Schizopoda, Rhizosolenia setigera, Thalassiosira decipiens, T.Clevei and Lauderia annulata.	[90]
	Plankton species as Chaetoceros affinis, C. danicus, Rhizosolenia, alata, R. setigera, Skeletonema costatum and Thalassionema itzschioides.	[91,92]
	Oncaea sp., Microsetella sp., Lamellibranchia larva, Gastropoda larva, microplankton.	[93]
	Microcopepods, nauplius Copepods, diatoms	[88,94]
	diatoms and dinoflagellates, zooplankton, copepod nauplii,
	naupliar copepods, Copepod eggs and nauplii.	[66,95]
	Calanoid copepods, Oithona spp., Oncaea spp. Sapphirina spp. Corycaeus spp., Microsetella spp., Unidentified copepods, Larvaceans, unidentified.
	Protozoa	[96]
	Zooplanktons (copepod, nauplii).	[96,97]
	Eukaryotic, fragile protozoa and gelatinous zooplankton.
	Zooplankton, Copepods, protozoa (Radiolaria and Dinophyta, dinoflagellates), gelatinous zooplankton, chaetognaths, appendicularians, and hydrozoans.	[85]

.

The studies of these different authors have shown that Japanese sardine feeds on phytoplankton, zooplankton, copepods, diatoms, etc. However, according to the results summarized in Table 2, the frequency of prey differed among the studies. The distribution of food in the areas and the environmental variables can be the origin of the distribution of the more or less valuable Japanese sardine prey in the different study areas.

In the feeding habits of Japanese sardines, a big difference was not observed between the diet composition of adult Japanese sardines and that of the larvae and juveniles. All stages of this species feed on phytoplankton and zooplanktons. The only difference noted is that adult Japanese sardines sometimes feed on the eggs of other small pelagic species. This justifies the great difference in prey frequency of Japanese sardines that could be noted between the different regions of the North Pacific where this species is present.

3.2. Trophic Position (TP)

Isotope ratios are measured using analytical instruments known as isotope-ratio mass spectrometers (IRMS). Carbon and nitrogen (δ13C and the δ15N) stable isotope ratios are most often used to explore a wide range of questions surrounding diet (e.g., consumption of animal products or fish; weaning age). Recently, stable isotope ratios of nitrogen (δ15N) and carbon (δ13C) have been frequently used by some researchers to determine the trophic structure of marine species. In the case of small pelagics, few studies have determined the trophic position of Japanese sardines in certain areas. Few works have successfully developed carbon and nitrogen stable isotope distributions (δ13C and the δ15N) of fish and invertebrates and then the additive and scaled models based on nitrogen stable isotope ratios (δ15N) methods [98,99]. These authors found similar results for the trophic level of Japanese sardines in their studies. The research of [98] showed that the trophic position of this species was 3.6 with values of δ13C = −17.0 ± 0.5 for the reference value (−17.5 to −15.8) and δ15N = 10.6 ± 0.8 for the reference value (9.8–12.7). On the other hand, the authors of [99] reported the trophic level of Japanese sardine to be around 3 for δ15N values, ranging from 6.6 to 15.7%. Based on the results of these two studies, we may conclude that the trophic position of Japanese sardine is between 3 and 4 in the south-eastern Izu Peninsula and 3 and 3.4 in the East China Sea and the Sea of Japan.

3.3. Competition and Predation

Japanese sardine and anchovy often compete for plankton [100]. Studies have shown that the food competition differs between species due to differences in nutritional expenditure during the spawning periods [101]. Furthermore, factors such as starvation, prey, transport, egg quality, and maternal effects are the main factors determining competition and predation in Japanese sardines [102]. Concerning predation, amphipods, squids, myctophid fishes, Pacific pomfret (Brama japonica), skipjack tuna (Katsuwonus pelamis), albacore (Thunnus alalunga), blue shark (Prionace glauca), salmon shark, minke whale (Balaenoptera acutorostrata), northern fur seal, and sea birds are the principal predator species, which feed on the larval and adult Japanese sardine [103,104,105,106,107,108,109].

4. Age, Growth and Ageing Methods

4.1. Ageing Methods

The study of the age of marine species is one of the main subjects of interest to researchers to understand population dynamics and specially to assess the stocks of certain species, e.g., that of the of Japanese sardines [69,80,82,110,111,112,113,114,115]. The main methods (direct and indirect methods) developed for these studies to determine the age of this species are the scale readings methods usually used in Japan, the otolith increment methods, and the length-based methods using the von Bertalaffy growth model.

4.2. Age and Growth

Many age-related studies of this species in the Pacific, Sea of Japan, East China Sea, and other areas of its occurrence reported their maximum age to be around 6 to 7 years old (

Table 3. Summary of ecological characteristics of Japanese sardine (Sardinops melanostictus). NB: HSP: high stock period, KOTZ: Kuroshio Oyashio transition zone, LSP: low stock period.

Regions	Longevity	Recruitment Stage	Age at First Maturation, L50	Spawning/Feeding Season	Spawning Area	Major Predators	References
Pacific Ocean	About 7+ years	Generally juveniles, but also larvae	1 year (LSP), 2–3 years (HSP)	November–June, Mainly February–April	Kuroshio coastal area, expands to south of Kyushu in HSP, KOTZ, Oyashio, beyond in the HSP.	Common squid, skipjack tuna, other predatory marine species	[56,117]
Tsushima Current				January–June	Coastal area from Noto Penisula and southern Korea to western Kyushu, expands to East China Sea and southern Kyushu in HSP Kuroshio Current	yellow tail, sea birds and marine mammals	[48,54,78,81,109]
Sea of Japan and East China Sea	About 6+ years		-	-	Sea of Japan and East China Sea		[78]
Tosa Bay, south-western Japan	About 7+ years		-	-	Tosa Bay, south-western Japan		[113]
Pacific coast of Japan northern Japan			2+ years, L50 = 180 mm/Wt ≥ 180 g	February–April	Pacific coast of Japan, Oyashio waters		[118]
Pacific waters around northern Japan	7–9 years		-	-	Pacific waters around northern Japan		[115]
Coastal waters off western Japan	About 7+ years	-	1-year-old L50 = 148 mm (KP), 144 mm (NWK) and 141 mm (SD)	-	Kochi Prefecture (KP), northwestern Kyushu (NWK), and the San-in district (SD)		[119]
Central Pacific and sea of Japan	About 7+ years	-	-	All seasons	North and south sea area around Japan		[19,66]
Sea of Japan	About 7+ years	juveniles, also larvae		during summer	west of Kyushu western part of central and northern areas		[14]

). However, the authors of [115] reported a maximum age of 9 years in the Pacific waters around northern Japan. The length–frequency analysis and otolith readings are generally the most commonly used methods to determine the age and growth of Japanese sardines. Otolith shapes and sizes change with fish growth and the relationship between otolith radius (r: mm) and body length (BL: mm) is mainly linear [111,112,113,114,115,116]. In addition, the authors of [115] indicated a correlation among body growth, recruitment, and age species.

In conclusion, the researchers used several growth methods to determine the age of Japanese sardines. They have made significant progress in defining the longevity of this species in several areas. Most studies have concluded that the maximum age range of Japanese sardine is around seven years, except for [115]. This result of Kawabata on the longevity of this small pelagic is an exception. Several parameters such as sampling and the methodology used in his studies to determine the age of this species may condition this difference. However, the authors who applied these methods concluded that the results were not satisfactory. Therefore, in this review, we propose reassessing the age of this species with adult individuals using the otolith method developed in [115]. Table 3 summarizes the information on studies regarding the age and ecological characteristics of Japanese sardines.

5. Reproductive Aspects

5.1. Reproductive Biology

Many studies showed the variation of the gonadosomatic index of female Japanese sardines in different areas but maximum values were reached when the water temperature was 11 °C [38,39,49,119]. Research such as [120] has shown the relationship between fecundity and egg number in Japanese sardines off southwestern Japan as a function of SST. This result indicated that the lower the SST, the lower the female egg production (less than 30,000 eggs). On the other hand, the higher the SST, the higher the female egg production (over 30,000 eggs). Recently, the research of [49,121] focused on the biology of Japanese sardines to better understand their life history. The authors of [121] studied biology and confirmed an important spawning and nursery area on the South Korean coast, especially Jinhae Bay. Therefore, the management of marine fishery resources in the South Korean Sea must necessarily include the ecological management of Jinhae Bay. Some authors studied the maturation of Japanese sardine male and female gametes [49]. The results found by these researchers showed that four of the eight Hydroxysteroid dehydrogenases (Hsd) 17β genes (hsd 17β 8, hsd 17β 10, hsd 17β 12a, and hsd 17β 12) had higher expression in the ovaries than in the testes. Furthermore, a detailed molecular picture of the ovarian steroidogenic pathway provided a positive basis for understanding the molecular mechanisms in the ovarian physiological process. However, the function of Hsd 17βs in ovarian steroidogenesis is not well established [49]. External factors, such as temperature and diet, and internal factors, such as age and growth, are known to influence gene expression in the brain–pituitary–gonadal (BPG) axis [49,122,123].

5.2. Maturity

In their study, the authors of [118] reported on Japanese sardine maturity at the Pacific coast of Japan. The length at first sexual maturity (L₅₀) of this species was 180 mm, with an average weight higher or equal to 180 g with two years as the corresponding age at sexual maturity for this species in the Pacific coast of Japan. However, Ref. [119] examines the sexual maturation, spawning period, and fecundity by the batch of Japanese sardine. These authors confirmed that the L₅₀ values were 148 mm, 144 mm, and 141 mm successively in Kochi Prefecture (KP), northwestern Kyushu (NWK), and San-in District (SD) for 1-year-olds at the age of first sexual maturity. Regarding the age at first sexual maturity, Ref. [117] reports that Japanese sardines in the Pacific reach their L₅₀ from the age of 1 year old during a low stock period and 2–3 years during a high stock period (Table 3).

A difference between the sizes at first sexual maturity of Japanese sardines was observed by these researchers in different areas. The environmental parameters such as temperature changes were the principal cause of this disparity as it varied between areas.

5.3. Sex Ratio

The sex ratio of Japanese sardine has not been the subject of much research. We have identified two principal studies on this subject in the 1950s and 1990s. One of the studies [124], conducted in the wild, showed that the sex ratio of Japanese sardine is about 1:2 (one male and two females). In contrast, Ref. [125] confirmed that the sex ratio of Japanese sardine in captivity was 1:1 (one male and one female) and that the ratio was definitive regardless of the group density in the captive tank. This result may be because, according to these authors, there is little visual information during nighttime egg-laying. However, for the best control of the biological parameters of the Japanese sardine, we suggest more research to determine the sex ratio of this species in the wild.

6. Fisheries

Japanese sardine is one of the most important commercial fisheries in Japan. This species measures up to 24 cm in standard length, usually 15–20 cm [8]. Reports of a 24.4 cm maximum body length (BL) at the age of nine years for Japanese sardine has been reported [115]. Typically, encircling nets, particularly purse seines, are the main equipment used to catch these small pelagic species [9,126]. In Korea, the purse seine is the main fishing equipment that catches Japanese sardines [127,128]. In Japan, the principal Japanese sardine fishery uses purse seines [129]. The fish are caught mainly at night when they approach the surface to feed. Generally, after harvesting, the fish are submerged in brine and transported to shore [8]. Fishing companies target Japanese sardines for many purposes: as bait, for immediate consumption, for drying, salting, or smoking, and fish meal or oil production. However, the principal use of Japanese sardine is for human consumption. Then again, fishmeal is used as animal feed and sardine oil for many uses as paint, varnish, and linoleum [8].

The exploitation of Japanese sardine is benefits Japan, the Republic of Korea, China, which started to exploit the species in 1990, and Russia [8,9]. Figure 2 clearly shows us an increase in Japanese sardine catches in the 2000s in China greater than that of other countries (Japan, Republic of Korea, and the Russian Federation) from 2013 to 2016. The difference noted in the catches of this species may be explained by the fact that China began to target Japanese sardines in 1990 with important catches from 1997 until 2018 where the annual catches exceed 100,000 tons before slight decreases in 2019 and 2020, While other countries have exploited this species since 1950, Russia started its exploitation of Japanese sardines in 1988. From 2002 to 2017, catches of Japanese sardines were more important in China than those of its Asian neighbors. Unlike China, Japanese sardine catches in Japan and Russia gradually increased in 2019 and 2020 [9], ranging from 451,382 tons in 2018 to 600,010 in 2020 for Japan and 62,887 tons in 2018 to 315,491 tons in 2020 for Russia.

In view of the importance of the total catches of fisheries and Japanese sardine in these regions of the North Pacific, we note that the contribution of this species to the total catch is more or less important according to the regions. According to the total annual catches of fisheries and Japanese sardine obtained by region through FAO and NPFC statistics, this species is more important for Japan than in the other countries. In fact, in Japan, the Japanese sardine catches represent 14.28% of the fisheries’ total catches in Japan in 2020. For Russia and China, in 2020, the catches of this species represented 6.48% and 0.66%, respectively, of the fisheries’ total catches in both countries. In 2018, Japanese sardine represented only 0.38% of the total catches in Korea. Certainly, apart from Japan, the contribution of Japanese sardine in the total catches of the other countries is not very significant, but it deserves special attention because Figure 2 and Figure 3 show us a progressive evolution of the catches of this species in these countries, except in Korea, where there were no catches in 2019 and 2020.

The fishing effort started to increase in 1974 due to the construction of large purse seine fleets [59,129]. According to [109], this high fishing effort was sustainable because the spawning stock biomass (SSB) increased steadily in 1988 when it reached a peak of 5,428,922 tons before landings of the Japanese sardine experienced a drastic drop to 9200 tons in 1965. According to some researchers, several factors are responsible for these fluctuations in Japanese sardine catches. Indeed, the weak recruitment of the Japanese sardine stock or the change of regime of 1988/1989 was associated with negative anomalies of the Pacific decadal oscillation index (PDO) and Monsoon Index (MOI), as well as positive anomalies of the Arctic Oscillation Index (AO) and sea surface temperatures of the southern area of the Kuroshio Extension (KESA-SST), which are all unfavorable to Japanese sardines according to [36,109]. For the population decline after 1988, Ref. [36] attributed the cause to high larval mortality (environmental parameters such as temperature and food availability). However, according to the analysis of Figure 3, the Japanese sardine stock started to increase gradually from 2010 until now due to the high recruitment per spawning stock biomass (RPS) and the reduction in the higher exploitation rate (ER), in other words, the positive outcome of the resource recovery management plans adopted by the managers of Honshu Island [130].

7. Stock Fluctuation and Assessment

Many studies have focused on the population dynamics and stock assessment of Japanese sardines [9,56,131,132,133,134]. These studies used different stock assessment models to assess this small pelagic in various areas. After studying the population dynamic of Japanese sardines, Ref. [9] showed that the catches and biomass are generally variable at the decadal scale with significant replacements of species since the 1900s. The causes of this phenomenon were associated with climate variability, especially regime changes. According to these researchers, the variability of the early survival rate is a principal factor in the population fluctuations of this species.

Other studies showed that the spawning stock biomass was above the B_limit of the Japanese sardine stock in the pacific without Russian catches in 2018 and predicted that stock biomass would increase under the fishing mortality coefficient if recruitment by spawning stock biomass continued [135]. However, the results estimated by the Virtual population analysis (VPA) could be optimistic due to a high exploitation rate (ER) leading to the decline of some stocks of Japanese Sardine in the East China sea because only Japanese catches were taken into account in the VPA analysis [56]. The stock biomass estimate in 2003 was around 130,000 tons [133]. Furthermore, the authors of [134], in 2011–2013, reported that the Japanese sardine stocks was overexploited with U/U_MSY > 1 and B/B_MSY < 0.5. In recent years, the authors of [136] assessed the status of Japanese sardine in the Tsushima Warm Current region of the Northwest Pacific Ocean using the Monte Carlo CMSY approach and the Bayesian state-space implementation of the Schaefer model (BSM) method with the time series of catch and the relevant abundance data (SSB or CPUE). Their results showed that the stock of Japanese sardine was grossly overfished in the year 2017 in this area.

The population size of Japanese sardine is known to fluctuate drastically on interdecadal time scales [14,17]. The fluctuations are related to several factors as species replacement, density effects, and the physical and biological oceanographic environments [52]. Many studies have focused on the fluctuation of the Japanese sardine stock and reported that fluctuations of this species were correlated with population dynamics, as well as environmental and biological factors, such as sea surface temperatures (SST), phytoplankton and zooplankton, climate change, spawning season, location, and fishing activities [48,78,81,136]. For this reason, fisheries must consider the results of these studies for a sustainable harvest and the implementation of conservational measures for this species.

8. Management Measures

As of 2015, IUCN had assessed and assigned conservation status to more than 76,000 species worldwide [8], which listed Japanese sardine as a “Not Evaluated” (NE) species However, some studies affirm that the stock of this species might be slightly overfished [136,137]. As a result, the Japanese sardine stock needs managing before its condition reaches a point of no return. Despite this status, management measures have been in place for Japanese sardines for a long time. Many studies confirmed that the total allowable catch (TAC) was the principal management measure to conserve Japanese sardine stocks [132,133,138,139]. The aim of this approach is to limit the fishing efforts of Japanese sardines, such as the number of vessels, duration or area of fishing operations, etc. Moreover, TAC is efficient for managing overfished stocks in Japan. The current management and maintaining reproduction, reducing uncertainty and risk capacity, protecting selected marine areas, monitoring and indicators were the principal measures of management for Japanese sardine developed by [133] in their research conducted in Japan.

Scientists of Japanese fisheries are currently trying to apply the management strategy evaluation (MSE) framework to evaluate the performance of harvest control rules (HCRs) and management procedures using operating models [139]. The concept of co-management is essential for the management of fisheries in Japan [120], and a socio-ecological approach to the management fisheries would oblige researchers to pay more attention to the interactions between the natural and human components of the ecosystems. This hypothesis confirmed the studied ecosystem approach to fisheries (EAF) [140]. Some authors have shown the balance between the biotic, abiotic, and human components of ecosystems and their interactions using an integrated fisheries approach [140]. The fishery of Japanese sardines around Japanese waters is potentially harvested by Japan, China, North Korea, Russia, South Korea, and Chinese-Taipei. Thus, it is necessary to establish an international framework for stock assessments and management. Responding to this demand, the North Pacific Fisheries Commission (NPFC) formally commenced in 2015, gathering information to conduct sophisticated stock assessments and provide management advice for this species. Recently, the NPFC started implementing some conservation and management measures for Japanese sardines in its jurisdiction of authority [141]. Given the current lack of knowledge of the population structure and insufficient catch statistics of Japanese sardines in the Japan Sea, the East China Sea, and the Yellow Sea, a cooperative fisheries management framework among these countries would be necessary for the proper management of the stocks.

9. Conclusions, Future Research Direction and Recommendations

Throughout this review, we updated information related to the general biology, distribution, aspects of fisheries, stock assessment, stock fluctuation, stock status and management actions for Japanese sardine (Sardinops melanostictus) in the North Pacific regions. The information obtained allowed us to understand the dynamics of this species and its evolution in terms of catches in the North Pacific regions over the last six decades. In addition, this study showed the total percentage of catches of Japanese sardines in relation to the total catches of the main countries that target this species. The evolution of the catches of this species from these countries is becoming more and more important. This study has also shown that there is a lack of information on Japanese sardines, especially with regard to biology, population dynamics and stock assessments in certain regions where the catches of this species are increasing from year to year. More studies are therefore needed in these areas for the rational management of the stocks. From this analysis and previous studies, we therefore, suggest the following recommendations for a more rigorous, effective, and sustainable management approach for the rational exploitation of Japanese sardines:

• Research on the biology, population dynamics and stock assessment in China, Korea, and Russia is significant, necessary and essential for proper management;
• It is essential to carry out a global stock assessment of Japanese sardines using the available data to understand the current state of Japanese sardine and identify effective measures for its sustainable management;
• To reflect further on the natural conditions that hinder the recruitment of the Japanese sardine stocks and to find solutions;
• As a recommendation, the control of the fishing effort and the establishment of TAC in all catch areas is primordial. This measure will help minimize the pressure on the resource;
• It is also imperative to identify and control all areas of reproduction and the periods and put in place strong management measures to protect juveniles, which is the most sensitive period to ensure the recruitment of the stock.