Feeding habits of the Pacific Bluefin tuna (Thunnus orientalis) larvae in two nursery grounds based on morphological and metagenomic analyses

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Abstract

The feeding ecology of Pacific Bluefin tuna (PBT: Thunnus orientalis) larvae collected from two nursery grounds, namely the Japan Sea and the Nansei area (western North Pacific), was evaluated based on gut content analyses using morphological and metagenetic techniques. The PBT larvae were collected at the surface layer (≥30 m depth) in 2016 and 2017, and 172 and 114 individuals from the Japan Sea and Nansei area, respectively, were analyzed. A generalized additive model applied revealed that the number of prey in the gut increased with growth, in waters above 24 °C and in subsurface (~30 m depth) waters, during daytime. The total dry weights of prey per gut calculated from the size of copepods and cladocerans also increased during daytime and with growth. Both the morphological and metagenetic analyses indicated that the taxonomic composition of gut contents was influenced by the food selectivity of PBT larvae and by zooplankton (prey) availability in the ambient water. Podonidae were positively selected as PBT larvae prey in both areas, and copepodites and adult Corycaeidae and Pontellidae were positively selected in the Nansei area only. A metagenetic approach indicated Calanidae copepods and soft zooplankton such as appendicularians as important preys in both areas. Other copepods were not positively selected using this approach, but Clausocalanidae and Oithonidae were frequently detected in the Japan Sea. This might be related to the higher abundances of these families in the Japan Sea than in the Nansei area. On the other hand, the cladoceran Penilia avirostris and the copepods Echinostomatidae and Oncaeidae were rarely observed in the guts of PBT larvae although were abundant in the water column. Overall, PBT larvae feed abundantly and grow fast in warm and long-day waters rich in Podonidae, Corycaeidae, Pontellidae, and larval copepods, which contributes to their survival and recruitment in the Japan Sea and Nansei area.

Introduction

Survival during the larval period is a key factor for fish recruitment (Houde, 2008). Some hypotheses, such as the “growth-dependent survival”(Anderson, 1988), “optimal environmental window” (Cury and Roy, 1989), and “match-mismatch” (Cushing, 1990), propose that recruitment variability is driven by variability in prey density, combined with differences in trophodynamics among species. Variability in the abundance of a given species’ preferred prey will in turn impact growth rate, which is directly linked to survival. Rapid growth during the larval period is important for the survival of several fish species (Anderson, 1988) because slow-growing larvae undergo higher predation pressure than fast-growing larvae. This hypothesis applies to Pacific bluefin tuna (Thunnus orientalis: PBT) larvae (Tanaka et al., 2006; Satoh et al., 2013; Watai et al., 2017, 2018; Ishihara et al., 2019).

The trophodynamics of PBT larvae is a key factor controlling growth, similarly to Atlantic bluefin tuna (Thunnus thynnus: ABT) and southern bluefin tuna (Thunnus maccoyii: SBT) (Jenkins et al., 1991; Satoh et al., 2013; Tanaka et al., 2014; Betancor et al., 2019). Prey availability and feeding rate have been shown to affect the larval growth of PBT under natural conditions (Jenkins et al., 1991; Satoh et al., 2013) and also under aquaculture experiments. Under these experiments a change from feeding PBT rotifers to fish larvae drastically accelerated the growth and increased the chance of survival of PBT larvae (Tanaka et al., 2014, 2018). Similarly ABT larvae fed copepods or fish larvae demonstrated more rapid growth than those fed rotifers (Betancor et al., 2019).

Llopiz and Hobday (2015) reviewed the larval feeding habits of bluefin tunas worldwide, and concluded that these larvae prey on specific food items, such as copepods, including the nauplius and copepodite stages, cladocerans, and appendicularians. Landry et al. (2018) also found that bluefin tuna larvae strongly selected cladocerans and poecilostomatoid copepods globally. However, the major gut contents of ABT larvae differ among nursery areas; for example, cladocerans are dominant in the Mediterranean Sea (Catalán et al., 2011) while appendicularians and copepods are dominant in the Strait of Florida and Gulf of Mexico (Llopiz et al., 2010, 2015). Interannual variations in the diet composition of larval ABT have also been reported in the Gulf of Mexico (Tilley et al., 2016) and ontogenetic shifts have been observed (Uotani et al., 1990; Llopiz et al., 2010, 2015; Tilley et al., 2016; Uriarte et al., 2019). Overall, bluefin tunas shift from zooplanktivores to piscivores. Larger larvae consumed larger zooplankton prey (Uotani et al., 1981, 1990; Catalán et al., 2011), and the amounts of appendicularians increased with larval growth of bluefin tunas in the western Atlantic (Llopiz et al., 2015). Larvae ≥6 mm body length (BL) capture fish larvae as prey in the Gulf of Mexico and the Mediterranean Sea (Llopiz et al., 2015; Uriarte et al., 2019), and fish were observed in the guts of SBT at 8 mm BL (Young and Davis, 1990). However, exclusively piscivore PBT larvae have not been reported in the natural marine environment.

Adult PBT spawn in the Nansei area (Ashida et al., 2015), Japan Sea (Okochi et al., 2016), and Kuroshio-Oyashio transition area (Ohshimo et al., 2018b); the latter has only recently been recognized as a possible nursery ground (Tanaka et al., 2020). Although there are only two studies on the feeding habits of PBT larvae, they covered the two nursery grounds of PBT, i.e. the Nansei area in the western Pacific (Uotani et al., 1990) and the Japan Sea (Kodama et al., 2017a). Copepods and cladocerans were the main prey of PBT larvae in both areas (Uotani et al., 1990; Kodama et al., 2017a), but the contribution of cladocerans as prey was one-order higher in the Japan Sea and one-order lower in Nansei area than the contribution of copepods in both areas (Uotani et al., 1990; Kodama et al., 2017a).

It must be pointed out, that the previous two studies on the PBT larval feeding habits (Uotani et al., 1990; Kodama et al., 2017a) varied spatially, temporally and methodologically. The gut contents of the PBT larvae collected in 1980 and 1981 in the Nansei area were only analyzed from a morphological approach (Uotani et al., 1990) and, according to Aoyama et al. (2008), in recent decades, the total zooplankton abundance has decreased, while that of warm-water species increased in the vicinity of Kuroshio, western North Pacific, which is adjacent to the Nansei area. Thus, differences in gut contents would be expected in the Nansei area. Regarding the methodologies used, soft zooplankton, such as appendicularians, Doliolum sp., and Sagittoidae, were only detected as important food sources using metagenetic approaches (Kodama et al., 2017a), and appendicularians, which are important food sources of other bluefin tuna larvae in other locations (Llopiz and Hobday, 2015), were not observed in the guts of PBT using the morphological approach (Uotani et al., 1990; Kodama et al., 2017a).

It is therefore necessary to compare the gut contents of PBT larvae in the two nursery grounds during a similar period using the same approaches in order to understand the feeding habits of PBT and if these have changed in recent years. Documenting differences in feeding habits between the two nursery areas might help explaining the differences in PBT larvae growth rates between two areas (Ishihara et al., 2019), as well as the importance of the water temperature in the Nansei area for fish recruitment (Muhling et al., 2018; Nakayama et al., 2019). Thus, in the present study, PBT larvae were collected both in the Nansei area and Japan Sea during 2016 and 2017 and their gut contents were analyzed using morphological and metagenetic analyses to determine the factors controlling larval diet composition and the relative abundance of each item, as well as diet differences between the two areas.

Section snippets

Field observations and larvae collection

Field operations were conducted in the Nansei area (125–128°E, 25°30′–27°40′N) and Japan Sea (133°27′–135°45′E, 36°04′–37°40′N) in 2016 and 2017 on board the R/V Shunyo-maru of the Japan Fisheries Research and Education Agency (Fig. 1). Operations were conducted during the spawning season in each area: June in the Nansei area and July–August in the Japan Sea (Ashida et al., 2015; Okochi et al., 2016; Ohshimo et al., 2018a). The PBT larvae were collected at the surface by horizontal tow using a

Ocean environment and PBT larvae analyzed in this study

The sea surface temperature in the Japan Sea (median ± interquartile range [IQR]: 26.4 ± 1.16 °C at the sampling sites for diet analyses) was 2 °C lower than in the Nansei area (28.4 ± 0.85 °C), and the difference in temperature between the two areas increased with increasing depth (10, 20, and 30 m; Fig. 3). Total zooplankton density in the Japan Sea (3142 ± 1499 individuals m−3) was three times higher than that in the Nansei area (1018 ± 597 individuals m−3, Fig. 3).

Zooplankton composition

Key factors controlling the feeding habits of PBT larvae

Prey numbers and total DWs in PBT larvae were positively correlated with larval BL. This indicated an ontogenetic shift on the quality of diets at approximately 4.5 mm BL, corresponding to the shift from pre-flexion to post-flexion larva (Miyashita, 2002).

Environmental conditions were also related to the number of prey items in each larva stomach, while they were not related to total DWs. In situ temperature is an important factor for early growth (Ishihara et al., 2019) and for defining the

Conclusions

The present study examined the feeding habits of PBT larvae in two nursery grounds, and showed that foraging success (indicated by stomach contents) was higher in temperatures >24 °C in secondary production waters, and at the subsurface (~30 m depth) with foraging occurring more frequently during the daytime. Spatial differences in the feeding habits of PBT larvae were clearly associated with the available zooplankton taxa in the ambient water. Podonidae were important prey in the Japan Sea, as

CRediT authorship contribution statement

Taketoshi Kodama: Conceptualization, Data curation, Formal analysis, Investigation, Methodology, Resources, Software, Validation, Visualization, Writing - original draft, Writing - review & editing. Junya Hirai: Methodology, Software, Writing - review & editing. Atsushi Tawa: Investigation, Resources, Data curation, Writing - review & editing. Taiki Ishihara: Investigation, Resources, Data curation, Writing - review & editing. Seiji Ohshimo: Data curation, Software, Writing - review & editing,

Declaration of competing interest

We have no conflict of interest.

Acknowledgements

Samples were collected during cruises of RV Shunyo-maru of Japan Fisheries Research and Education Agency, and we thank captain Takayuki Miyazaki, the crew, and many researchers on board. We are grateful to Mr. T. Takahashi, Ms. R. Ishida, and Ms. S. Maeda for their technical assistance. This work was supported by the Fisheries Agency of Japan and Japan Fisheries Research and Education Agency.

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