Feeding habits of the Pacific Bluefin tuna (Thunnus orientalis) larvae in two nursery grounds based on morphological and metagenomic analyses
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.
References (71)
Plankton production and year-class strength in fish populations - an update of the match mismatch hypothesis
Adv. Mar. Biol.
(1990)- et al.
Intrusions of excess nitrate in the Kuroshio subsurface layer
Continent. Shelf Res.
(2015) - et al.
A global comparative analysis of the feeding dynamics and environmental conditions of larval tunas, mackerels, and billfishes
Deep-Sea Res. II
(2015) - et al.
Long-term change in reproductive condition and evaluation of maternal effects in Pacific bluefin tuna, Thunnus orientalis, in the Sea of Japan
Fish. Res.
(2018) - et al.
Reproductive biology of female Pacific bluefin tuna, Thunnus orientalis, in the Sea of Japan
Fish. Res.
(2016) - et al.
Evidence of density-dependent cannibalism in the diet of wild Atlantic bluefin tuna larvae (Thunnus thynnus) of the Balearic Sea (NW-Mediterranean)
Fish. Res.
(2019) - et al.
A method for studying protistan diversity using massively parallel sequencing of V9 hypervariable regions of small-subunit ribosomal RNA genes
PloS One
(2009) A review of size dependent survival during pre-recruit stages of fishes in relation to recruitment
J. Northwest Atl. Fish. Sci.
(1988)- et al.
Marine biogeochemical response to a rapid warming in the main stream of the Kuroshio in the western North Pacific
Fish. Oceanogr.
(2008) - et al.
Tissue preservation and total DNA extraction form fish stored at ambient temperature using buffers containing high concentration of urea
Fish. Sci.
(1996)
Reproductive condition, batch fecundity, and spawning fraction of large Pacific bluefin tuna Thunnus orientalis landed at Ishigaki Island, Okinawa, Japan
Environ. Biol. Fish.
Evaluation of different feeding protocols for larvae of Atlantic bluefin tuna (Thunnus thynnus L.). Aquaculture
Trimmomatic: a flexible trimmer for Illumina sequence data
Bioinformatics
Time-series metabarcoding analysis of zooplankton diversity of the NW Atlantic continental shelf
ICES J. Mar. Sci.
Trophic ecology of Atlantic bluefin tuna Thunnus thynnus larvae
J. Fish. Biol.
An Illustrated Guide to Marine Plankton in Japan
Optimal environmental window and pelagic fish recruitment success in upwelling areas
Can. J. Fish. Aquat. Sci.
Eukaryotic plankton diversity in the sunlit ocean
Science
UCHIME improves sensitivity and speed of chimera detection
Bioinformatics
Is Oithona the most important copepod in the world's oceans?
J. Plankton Res.
The transition from nauplii to copepodites: susceptibility of developing copepods to fish predators
J. Plankton Res.
A comparison of sampling methods for larvae of medium and large epipelagic fish species during spring SEAMAP ichthyoplankton surveys in the Gulf of Mexico
Limnol Oceanogr. Methods
Molecular-based diet analysis of the early post-larvae of Japanese sardine Sardinops melanostictus and Pacific round herring Etrumeus teres
Mar. Ecol. Prog. Ser.
Emerging from Hjort's shadow
J. Northwest Atl. Fish. Sci.
Accuracy and quality of massively parallel DNA pyrosequencing
Genome Biol.
Differences in larval growth of Pacific bluefin tuna (Thunnus orientalis) between two spawning areas, and an evaluation of the growth-dependent mortality hypothesis
Environ. Biol. Fish.
Density dependence of larval growth of a marine fish, the Southern bluefin tuna, Thunnus maccoyii
Can. J. Fish. Aquat. Sci.
Diet composition and feeding habits of larval Pacific bluefin tuna Thunnus orientalis in the Sea of Japan: integrated morphological and metagenetic analysis
Mar. Ecol. Prog. Ser.
Appendicularians in the southwestern Sea of Japan during the summer: abundance and role as secondary producers
J. Plankton Res.
Presence of high nitrate to phosphate ratio subsurface water in the Tsushima Strait during summer
J. Oceanogr.
Morphology, ecology, classification and specialization of copepods nauplius
Bull. Nansei Natl. Fish. Res. Inst.
Climate sensitivities and uncertainties in food-web pathways supporting larval bluefin tuna in subtropical oligotrophic oceans
ICES J. Mar. Sci.
Feeding dynamics of Atlantic bluefin tuna (Thunnus thynnus) larvae in the Gulf of Mexico
Collect Vol. Sci. Pap. ICCAT
Distinctions in the diets and distributions of larval tunas and the important role of appendicularians
Limnol. Oceanogr.
Cited by (17)
Similarities of distributions and feeding habits between Bullet tuna, Auxis rochei, and Pacific bluefin tuna, Thunnus orientalis, larvae in the southern Sea of Japan
2022, Progress in OceanographyCitation Excerpt :Therefore, we investigated the spatial distributions and feeding habits of BT and PBF larvae in the Sea of Japan and evaluated the species interactions in the tribe Thunnini in this area. Some methods were same with the previous studies (Kodama et al., 2020a; Kodama et al., 2020b), and thus the detailed descriptions were in the supplemental materials. Observations were conducted from 2016 to 2018 in the Sea of Japan during cruises of the R/V Shunyo-maru from the end of July to the beginning of August (Fig. 1).
Abundance and habitats of marine cladocerans in the Sea of Japan over two decades
2021, Progress in OceanographyCitation Excerpt :According to Nip et al. (2003), Podonidae are highly selected as prey because of their dark-pigmented eyes, which contrast considerably with backgrounds, based on the feeding ecology of black seabream (Spondyliosoma cantharus) and Japanese seaperch (Lateolabrax japonicus) in a Chinese coastal region. Hence, marine cladocerans are an essential link between phytoplankton and higher trophic levels in the world ocean (Miyashita et al., 2011), but recent knowledge of distributions and abundance in the Japanese coastal and offshore waters are very limited: they are also the important prey of larval fish in the Japanese coastal and offshore water (Kodama et al., 2017; Kodama et al., 2020a). The Sea of Japan (Japan Sea) is a semi-closed marginal sea in western North Pacific surrounding the Japan archipelago, Korean Peninsula, and Russia (Fig. 1).
Comparative research on ocean top predators by CLIOTOP: Understanding shifts in oceanic biodiversity under climate change
2020, Deep-Sea Research Part II: Topical Studies in OceanographyCladoceran communities in offshore Suruga Bay, Japan: How are they formed?
2023, Journal of Oceanography