- 1Atmosphere and Ocean Research Institute, The University of Tokyo, Chiba, Japan
- 2College of Bioresource Science, Nihon University, Fujisawa, Kanagawa, Japan
- 3Fisheries Resources Institute, Japan Fisheries Research and Education Agency, Yokohama, Kanagawa, Japan
- 4Department of Fisheries, School of Marine Science and Technology, Tokai University, Shizuoka, Japan
- 5Field Science Education and Research Center, Kyoto University, Kyoto, Japan
- 6Osaka Aquarium Kaiyukan, Osaka, Japan
- 7Marine Biological Section, University of Copenhagen, Helsingør, Denmark
- 8Graduate School of Frontier Sciences, The University of Tokyo, Chiba, Japan
Pacific bluefin tuna (Thynnus orientalis; PBT) can maintain their body temperature above ambient water (i.e., thermal excess) through high heat production and heat retention. The endothermic ability develops at 20–40 cm fork length (
1 Introduction
Animal body temperature is determined by internal heat production and heat exchange with the external environment (Schmidt-Nielsen, 1997; Butler et al., 2021). Each species possesses an optimal body temperature range and employs various strategies to maintain body temperature within this range (Butler et al., 2021). Based on their thermoregulation strategies, animals are classified as either endotherm or ectotherm. Endotherms sustain body temperatures above the surrounding environment through elevated metabolic heat production (Schmidt-Nielsen, 1997; Butler et al., 2021). In contrast, ectotherms do not retain their body temperature with their heat production; instead, they primarily rely on external heat sources, exploiting environmental thermal gradients to regulate body temperatures (Angilletta, 2009; Butler et al., 2021). Most fish are ectotherms: this is because the aquatic habitat is a challenging environment to maintain body temperature due to the high heat capacity of water, and the metabolic heat they produce is further lost through the gills and the skin. Nevertheless, among fish, a few species can maintain their body temperatures above ambient water, known as endothermic fish (Bernal et al., 2012; Wegner et al., 2015; Bernal et al., 2017). The endothermic ability is restricted to specific tissues/organs; therefore, it is referred to as “regional endothermy” to distinguish it from the “endothermy” observed in mammals and birds (Carey and Teal, 1969; Carey et al., 1971).
Tunas (tribe Thunnini) are notable examples of endothermic fish and have long been explored for their ability to maintain body temperatures (Kishinouye, 1923). Tuna species achieve their endothermic ability through both high heat production and retention capacity, and exhibit unique morphological traits associated with them. They possess a unique vascular arrangement around specific tissues/organs (e.g., red muscle, liver), where arteries and veins alternate (Kishinouye, 1923; Carey et al., 1971; Dickson and Graham, 2004). The vascular pattern, referred to as rete mirabile, functions as the counter-current heat exchangers to retain metabolic heat, and heat from venous blood returning to the heart is passed to arterial blood, thereby reducing heat loss at the gills.
Tuna species also exhibit high metabolic rates, generally measured by oxygen consumption rate (
Pacific bluefin tuna and other bluefin tuna species, including Atlantic bluefin tuna (Thunnus thynnus) and southern bluefin tuna (Thynnus maccoyii), have well developed retia mirabilia among tuna species, and the adults generally show high heat retention capacity exceeding 10°C of thermal excess (

Figure 1. (A) Map of the western North Pacific Ocean, showing the study area (shaded area). Schematic of near-surface currents around Japan: Kuroshio Current, Kuroshio Extension, and Oyashio Current (gray arrows) (B) Enlarged map of the study area. The white triangle represents the release location of tagged Pacific bluefin tuna juveniles. The yellow-filled circle indicate the location of the Iburi Center, Osaka Kaiyukan Marine Biological Research Institute.
It has long been known that PBT juveniles with a fork length of 30 cm or more exhibit a thermal excess of 3°C–4°C post-capture compared to the ambient water (Funakoshi et al., 1985), indicating that PBT of this size and larger already have developed the endothermic ability. The long-term measurements of
The mechanistic basis of thermal excess enhancement has mainly been attributed to the heat retention capacity, the development of retia mirabilia, because PBT develop the vascular structure rapidly during the juvenile stage (Funakoshi et al., 1985; Malik et al., 2020). Moreover, a biologging study has also shown that the heat retention capacity considerably improves with growth, while that of the heat-production rate decreases after >45 cm
Recent technological advancements have enabled the miniaturization of biologging devices and the in situ measurement of body temperature in small-sized tuna (<30 cm
2 Material and methods
2.1 Analysis of biologging data
2.1.1 Summary of analyzed data and electronic devices
In this study, we analyzed time-series temperature data of body (

Table 1. Information on the individuals used for heat-budget model analysis. Fish size is expressed in fork length. The parentheses in size range analysis column indicate size estimated from growth rate due to the lack of size information at recapture.
Over the 4-year tagging survey, a total of 3,281 PBT juveniles were captured by trawling in the coastal area of Tosa Bay (2012–2015: n = 1,044, 1,725, 236, 276), and 2,518 fish were released with dart tags (2012–2015: n = 923, 1,147, 201, 247). Of the dart-tagged fish, 321 fish were surgically implanted with an archival tag (LAT2910; Lotek Wireless Inc. Ontario, Canada) into their peritoneal cavity and released from the coastal area (2012–2015: n = 75, 62, 77, 107). In total, 307 fish were recaptured off Tosa Bay, its adjacent waters, and in California, United States (2012–2015: n = 128, 60, 45, 74). Of these, 93 were archival-tagged individuals (2012–2015: n = 23, 8, 23, 39), but for about half of the fish, the archival tags themselves were not recovered, or the data were not retrieved due to the tag malfunction. As a result, 41 fish were used for the heat-budget model in our previous study (Kitagawa et al., 2022). In this study, we selected nine individuals with more than 2 months of time-series data for analysis (Table 1), excluding 32 individuals with shorter data records, because this study aimed to evaluate the development of endothermic capacity from the 20 to >40 cm size range.
The archival tags consisted of a body (
The tagging procedure was described in detail in previous studies (Furukawa et al., 2017; Fujioka et al., 2018). Briefly, a scalpel was used to make a 1 cm incision along the body approximately 0.5 cm from the midline and 1–2 cm anterior to the anus, through which the archival tag was inserted into the peritoneal cavity. At the tagging timing, the straight fork length of each fish (
2.1.2 Time-series data analysis
Igor Pro Ver 8.1 (WaveMetrics Inc., Portland, OR, United States) and its add-on package of Ethographer (Sakamoto et al., 2009) were used to analyze the
2.1.3 Heat-budget model (HBM)
To analyze body temperature dynamics in juvenile PBT, we employed a heat-budget model to estimate changes in the whole-body heat-transfer coefficient (
where,
In our previous study (Kitagawa et al., 2022), we assumed that the ambient water temperature at a given time,
The parameters were estimated for each day using maximum likelihood method. We used the “lm” function in R [v.4.3.1, R Core Team (2023)] to estimate the parameters for models with different values of
2.1.4 Allometry of HBM parameters
To clarify the development of the heat-production rate in PBT, the heat-production rate was compared to body mass. The relationship between body mass (
where,
2.1.5 Body size estimation of the tagged PBT
To estimate the scaling exponent of the heat-production rate, the body mass of PBT juveniles on each day was estimated based on a calculation in a previous study (Kitagawa et al., 2022). Briefly, the estimation was conducted through two processes: (1) estimating the fork length on each day using the growth rate, and (2) estimating the body mass from the estimated fork length. The growth rate of PBT’s fork length is rapid and linear in 0-age fish, for example, at 0.45
2.2 Metabolic rate measurement
2.2.1 Fish collection and maintenance
Swimming respirometry was conducted at the Iburi Center (IC) of Osaka Kaiyukan Marine Biological Research Institute (Figure 1B) from August 9 to 26, 2022, and from August 15 to 9 September 2023. Juvenile Pacific bluefin tuna, ranging from 16.6 to 28.2 cm in fork length, were captured by hook-and-line trolling over a period of 2–3 days (August 11–13, 2022, August 18–19, 2023) off the waters of Tosa Bay, Japan. The captured fish were transported to IC on the final day of fishing each year. Upon arrival, the fish were transferred from the transport tank to 5-ton holding tanks (diameter 2.6 m, depth 0.94 m) with a custom-made dip-net, where the lower part was made of vinyl sheet and thus filled with water during fish handling. A total of 97 fish (2022:
2.2.2 Swimming respirometry
A Steffensen-type swim tunnel respirometer (SW10210, Loligo Systems, Viborg, Denmark) situated at the IC was used to measure the oxygen consumption rate (
The fish were transferred from the holding tank to the swim tunnel using a nylon sling. The fish were first given 0.5–3 h to acclimate to the swim tunnel at a water speed of 45–60
After each 15 min period, the water flow was increased by an additional 0.3
The oxygen consumption rate (
where
2.2.3 Scaling of metabolic rate
In this study, the standard metabolic rate (SMR) was determined to calculate the scaling exponent of a metabolic trait. The SMR is defined as the metabolic rate when swimming speed is zero, and for tunas, it is typically derived from the relationship between metabolic rate and swimming speed, known as the “swimming curve” (Dewar and Graham, 1994; Sepulveda and Dickson, 2000). Previous studies have reported a linear relationship between metabolic rate and swimming speed in tunas, and this study also identified a similar linear relationship (Dewar and Graham, 1994; Sepulveda and Dickson, 2000). Consequently, a linear model was employed for the estimation, where the oxygen consumption rate at a given speed (
where
The minimum swimming speed (
2.2.4 Calculating red muscle and ventricle masses
Metabolic heat produced through aerobic metabolism in red muscles (RM) is a major source of body temperature, and the ventricle is closely related to aerobic capacity (Graham and Dickson, 2001). To evaluate the development of red muscle and ventricle in the early juvenile stage, a portion of PBT juveniles captured for swimming respirometry were measured for the masses of red muscle (
Twenty-one fish (mean ± s.d. fork length: 20.6 ± 3.2 cm, body mass: 142.4 ± 80.6 g) were used to quantify total red muscle mass (
The ventricular masses (
3 Results
3.1 Heat-production rate
Time-series data of the

Figure 2. Example of time-series data of electronically tagged Pacific bluefin tuna (ID 2012-0932). The vertical dashed lines depict the estimated fork length at the time. (A) Body temperature (
For the fish, the heat-production rate (

Figure 3. Relationship between the response time-lag (Lag
The heat-production rate (

Figure 4. Changing relationship of
3.2 Relationship between the development of heat-production rate and endothermic ability
In the case of
where the
In this equation, the relationship between

Figure 5. The effects of heat-production rate (
The HBM parameters estimated for each day were plotted on a log-log graph, revealing that the thermal excess increased as
3.3 Swimming respirometry
The oxygen consumption rate was linearly correlated with the swim speed (Figure 6A) (Equation 5). The minimum swim speed was evaluated for six fish (mean ± s.d. fork length: 23.0 ± 3.5 cm, body mass: 193 ± 90 g) by decreasing the flow speed. The average speed was

Figure 6. (A) Relationship between the swim speed (
The mean (±s.d.) value of mass-specific

Table 2. Summarized information on fish body size and measurements of physiological traits. Each physiological trait is represented as a value relative to body mass. Mean ± s.d., and min-max range (in parentheses) are presented.

Table 3. Scaling exponents for physiological traits. Each row represents a physiological trait and its corresponding scaling exponent values, including absolute values and values relative to body mass (or mass-specific, ms). Scaling exponent values with a
3.4 Development of red muscle and ventricular masses
Total red muscle mass was evaluated using the fish’s cross-sectional area [

Figure 7. Scaling relationships between body mass (g) and (A) red muscle mass (g; scaling exponent: 1.12), (B) ventricular mass (g; scaling exponent: 1.15), (C) relative red muscle mass (%), and (D) relative ventricular mass (%; scaling exponent: 0.15). Each point represents an individual, with the solid black lines indicating the linear regression fits, and the shaded areas representing the 95% confidence intervals.
The relative value of red muscle mass to body mass ranged 3.77%–10.69% (mean ± s.d.: 6.07% ± 1.79%) (Table 2; Figure 7C), but the scaling exponent of the relative red muscle mass was not significantly larger than 0 (
4 Discussion
Endothermic fish, such as tuna and lamnid sharks, can maintain the temperatures of certain tissues/organs higher than the surrounding water, if in cold water, by retaining high levels of heat production. In the early juvenile stage, a strong correlation has been observed between red muscle mass and thermal excess (Dickson et al., 2000; Kubo et al., 2008), suggesting that heat production plays an important role in thermal excess. However, thermal excess is influenced not only by heat production, but also by heat retention capacity. Since the development of the rete mirabile occurs around the same time as the red muscle (Funakoshi et al., 1985; Malik et al., 2020), the ontogenetic pattern of heat production capacity and the extent to which heat production specifically contributes to thermal excess remain insufficiently understood compared to the heat retention capacity. Therefore, in this study, we aimed to explore the ontogenetic pattern of heat production capacity and to discuss the extent to which heat production contributes to the thermal excess between the inside and outside of the body. The thermal excess of juvenile PBT increased with growth as shown in our previous study [Figure 2; Kitagawa et al. (2022)]. By estimating parameters using a heat-budget model, we found that heat production is maintained at a high level in the early juvenile stage. Through comparison of the parameters of the heat-budget model, we found that a high heat-production rate is important for the early formation of thermal excess. To reinforce the mechanistic basis for highly maintained heat production in early juveniles, scaling exponents were estimated for physiological and/or morphological traits related to aerobic metabolic capacity, such as metabolic rate, red muscle mass, and ventricular mass.
4.1 Ontogenetic patterns of heat production in PBT
The heat production rate (
4.2 Contribution of juvenile-specific high heat production into endothermic ability in juvenile PBT
We aimed to discuss the extent to which heat production contributes to the rise in thermal excess by comparing parameters estimated using a heat-budget model (Figure 5). The heat-budget model estimates parameters for heat production and heat retention capacity, denoted as
Figure 5B also provides insights into the challenges small-sized fish face in maintaining thermal excess. For example, the plots of
4.3 Mechanistic basis of juvenile-specific high heat production
To examine the juvenile-stage-specific development of aerobic capacity, metabolic rate, red muscle mass, and ventricular mass, we measured and evaluated their scaling exponents (Table 3). The mass-specific
In the early juvenile stage (15–35 cm
For red muscle, it has been reported that the scaling exponent for PBT 20–60 cm
4.4 Ecological implications of high metabolic rate
Although high heat production should be associated with high energetic costs, the ontogenetic pattern of
A recent study has provided ecological insights into the high scaling exponents of metabolic rate during the early life stages of fish (Norin, 2022). The relationship between metabolic rate and growth rate has long been recognized (Altringham and Block, 1997; Sogard, 1997), with species or individuals exhibiting higher metabolic rates often showing faster growth rates, provided they meet their dietary demands (Auer et al., 2015a; 2015b; 2015c). Since mortality rates are highest during the early life stages of fish, rapid growth is believed to enhance survival rate (Sogard, 1997; Norin, 2022). Therefore, the study hypothesized that the ontogenetic scaling of the metabolic rate in fish is a result of selective pressures associated with high mortality in early life stages (Norin, 2022). The eco-physiological features of PBT juveniles are considered to coincide with this concept.
4.5 Conclusions and perspectives
It has been known that tunas begin to exhibit higher body temperature than ambient water at fork lengths of 20–40 cm, but the development of heat production capacity and its contribution to the difference between body and water temperature at this stage has not been fully understood. By examining multiple traits related to heat-producing capacity in PBT juveniles, this study provides new insights into the ontogenetic patterns of heat production capacity and its physiological basis underlying the development of endothermic ability in PBT juveniles. Our findings demonstrate that the juvenile-specific high heat-production rate is critical during the early stages of endothermic development. The observed high heat-production rates during this stage contrast with the subsequent decline as the fish grow larger. This study elucidates the ontogenetic development of metabolic heat production in juvenile PBT and its role in the acquisition of endothermic capability.
However, although the results of the present study implied a developmental shift in the physiological state, further studies are needed to explore internal changes, particularly energetic dynamics through ontogeny, in natural environments. Pioneering studies have proposed the measurement of heart rate in bluefin tunas (Clark et al., 2008; Clark et al., 2010), and recent technological advances in data loggers enable the measurement of long-term heart rate in bluefin tuna (Rouyer et al., 2023). It is hoped that an increasing number of physiological traits measured using biologging techniques will clarify the developmental process from exothermic to endothermic attributes in tuna species.
Data availability statement
The original contributions presented in the study are included in the article/supplementary material, further inquiries can be directed to the corresponding author.
Ethics statement
The animal study was approved by Animal Ethics Committee of the University of Tokyo. The study was conducted in accordance with the local legislation and institutional requirements.
Author contributions
TA: Conceptualization, Data curation, Formal Analysis, Funding acquisition, Investigation, Methodology, Project administration, Software, Validation, Visualization, Writing – original draft, Writing – review and editing. MF: Conceptualization, Data curation, Funding acquisition, Investigation, Methodology, Software, Validation, Writing – original draft, Writing – review and editing. KF: Writing – review and editing, Funding acquisition, Resources, Supervision. TN: Writing – review and editing, Investigation, Methodology, Supervision. HI: Writing – review and editing, Investigation, Resources. YK: Writing – review and editing, Resources. HF: Resources, Writing – review and editing. MS: Writing – review and editing, Methodology, Supervision. JS: Writing – review and editing, Methodology, Supervision. TK: Writing – review and editing, Conceptualization, Funding acquisition, Project administration, Resources, Supervision.
Funding
The author(s) declare that financial support was received for the research and/or publication of this article. This study was financially supported by the Research and Assessment Program for Fisheries Resources, the Fisheries Agency of Japan, the Japan Society for the Promotion of Science (JSPS) [grant number 23K14004], the Core Research for Evolutional Science and Technology (CREST) program of the Japan Science and Technology (JST) Agency [grant number JPMJCR23P2 to ST], and a Sasakawa Scientific Research Grant from the Japan Science Society [grant number 2023-4027].
Acknowledgments
We extend our sincere gratitude to the fishermen who supported the collection of specimens for this study. This research was supported by the Cooperative Program [number JURCAOSKAV23-49] of Atmosphere and Ocean Research Institute, the University of Tokyo. We are also deeply grateful to the staff of the Osaka Aquarium Kaiyukan, Iburi Center, for their invaluable assistance in rearing Pacific bluefin tuna. Additionally, we would like to thank Taiyo Komatsubara from Nihon University for his significant contribution to the quantification of red muscle. Their support and collaboration were crucial to the success of this research.
Conflict of interest
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
Generative AI statement
The author(s) declare that Generative AI was used in the creation of this manuscript. During the preparation of this study, we used Trinka AI and ChatGPT to correct grammar.
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Keywords: biologging, heat-budget model, metabolic rate, respirometry, red muscle development
Citation: Abe TK, Fuke M, Fujioka K, Noda T, Irino H, Kitadani Y, Fukuda H, Svendsen MBS, Steffensen JF and Kitagawa T (2025) Juvenile-specific high heat production contributes to the initial step of endothermic development in Pacific bluefin tuna. Front. Physiol. 16:1512043. doi: 10.3389/fphys.2025.1512043
Received: 16 October 2024; Accepted: 06 May 2025;
Published: 29 May 2025.
Edited by:
Christel Lefrancois, UMR7266 Littoral, Environnement et Sociétés (LIENSs), FranceReviewed by:
Lene H. Petersen, Texas A&M University at Galveston, United StatesAnthony (Tony) John Hickey, The University of Auckland, New Zealand
Copyright © 2025 Abe, Fuke, Fujioka, Noda, Irino, Kitadani, Fukuda, Svendsen, Steffensen and Kitagawa. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
*Correspondence: Takaaki K. Abe, dC5hYmUuaHBhQGdtYWlsLmNvbQ==