Cited by 22Marine and fisheries researchPhysiological and biochemical adaptationsFish Ecology and Management Studies

Atlantic bluefin tuna spawn early to avoid metabolic meltdown in larvae

Open access
Fiksen, Øyvind, Reglero, Patricia·2022·Ecology

Abstract

Abstract To predict shifts in phenology and distribution of organisms we need to understand how survival through early life stages depends on environmental conditions. Here, we present a mechanistic model of development, feeding and bioenergetics of early life stages in bluefin tuna and predict the optimal time of the year for them to be born. We find that the availability of prey, particularly nauplii, is sufficient for fast growth in tuna larvae while temperature is moderate during midsummer, but not when temperatures increase later in summer. High temperatures benefit egg and yolk-sac stages, but the metabolic needs of feeding larvae are hard to sustain during the warmest periods. Heatwaves, such as the one in 2003, increase larval survival potential, but shorten the viable part of the season for the larvae. Atlantic bluefin tuna is a large, highly migratory marine top predator that spawns while temperatures are rising, but before the heat leads to a metabolic meltdown in larvae. This means that food resources modulate how temperature change shifts optimal phenology.

AI snapshot

Written from the paper’s full text.

TL;DR

A mechanistic individual-based model of Atlantic bluefin tuna early life stages predicts that spawning peaks in June/July because larvae must grow before summer warming makes feeding-larva metabolism unsustainable. Food availability, especially nauplii, modulates how temperature shifts optimal spawning phenology.

Key findings

  • The model predicts a peak in egg fitness in June/July, at about day 190, matching observed spawning dates in the Balearic Sea; later-born larvae face a “metabolic meltdown” when high temperatures and declining Cladocera mean ingestion supports metabolism but not growth.
  • Predicted egg fitness is sensitive to first-feeding prey: the fitness peak appears c. 20 d later for every 100 nauplii/m³ added, and the minimum viable prey concentration is c. 300 nauplii/m³ near the surface.
  • Metabolic meltdown occurs at 22, 25, and 28°C if ingestion is 30%, 60%, and 90% of body mass per day, respectively.
  • The 2003 Mediterranean heatwave increased fitness by one order of magnitude for eggs spawned on days 170–190 compared with the cold year 2004, but metabolic meltdown occurred earlier; fitness was three orders of magnitude higher when nauplii increased from 300 to 500/m³ at 30 Cladocera/m³.

Methods

  • The authors built a mechanistic individual-based model following a tuna egg from birth to post-flexion metamorphosis at c. 7.5 mm body length, including temperature-dependent hatching, development, metabolism, visual acuity, day–night light cycles, gut dynamics, prey detection, and seasonal prey fields; the model is coded in Python 3.7.
  • Field data came from ABFT larvae sampled in spring and summer from 2001 to 2017 in the Balearic Sea, with sea surface temperatures from NOAA CoastWatch/NASA and zooplankton prey densities mainly from long-term monitoring near Mallorca and annual surveys.
  • Fitness was defined as accrued survival probability from spawning day through hatching, growth, feeding, and survival, with predation mortality assumed around 0.6/day in early life stages; sensitivity was tested at 300–600 nauplii/m³.

Limitations

  • The paper states that the prey abundance at which food becomes limiting depends on larvae building intermittent energy stores during no-food periods, that energetic costs of activity and swimming are not explicitly represented, and that metabolism and ingestion are assumed independent although ingestion, specific dynamic action, and assimilation efficiency may interact.
  • The paper states that the predicted fitness benefit of the 2003 heatwave assumes prey populations do not decline.
  • Evident from the text: yolk-sac duration and routine metabolic rate were measured only at 25°C and 26°C, with Q10 = 2 assumed for both; Cladocera capture probability is assumed to increase linearly with larval growth; and field validation is limited to the Balearic Sea.

Model-written summary. Check it against the paper before relying on it.

Integrity signals

Registry

Crossref · 10.1002/ecy.3568

Cites

36 of 36 references verified0 citation errors · 0 not checkable

Statistics

Nothing to recompute.

Claims the paper makes

7 of 17 cited sources checked · 4 supported · 0 flagged · accuracy not yet measured

  • Premisecitation

    As ABFT larvae grow larger, they select for larger zooplankton, particularly Cladocera.

    “as they grow larger, they select for larger zooplankton (Catalan et al. 2011, Landry andBeckley 2019), particularly Cladocera”
    Quote in the paperSubstantial claim1 of 2 sources checked
    • cites Catalan et al. 2011 source
    • cites Landry and Beckley 2019 source

      The ‘Feeding preferences of larval BFT’ section (page unavailable) reports that ABFT larvae selectively feed on cladocerans, and that the smallest BFT larvae feed mostly on copepod nauplii. It does not establish that growing ABFT larvae increasingly select larger zooplankton, particularly cladocerans; it notes that many larvae instead switch to fish prey after reaching about 10 mm. (LLM, conf=0.84)

      Experimental — accuracy not yet measured
  • Premisecitation

    ABFT larvae first feed on the early stages of copepods (nauplii) near the surface.

    “Their larvae first feed on the early stages of copepods (nauplii) near the surface”
    Quote in the paperSubstantial claim1 of 2 sources checked
    • cites Catalan et al. 2011 source
    • cites Landry and Beckley 2019 source
  • Premisecitation

    First feeding tuna larvae depend on production of copepod nauplii and Cladocera, which are tightly linked to the microbial food web.

    “The first feeding tuna larvae depend on production of copepod nauplii and Cladocera, which are tightly linked to the microbial food web (Landry et al. 2019).”
    Quote in the paperSubstantial claim1 of 1 sources checked
    • cites Landry et al. 2019 source

      The Feeding preferences of larval BFT section (page unavailable) says the smallest larvae prey mostly on copepod nauplii and that cladocerans contribute disproportionately to larval diets, but it does not establish that first-feeding larvae depend on both. The Introduction and Plankton food webs supporting larval BFT section (pages unavailable) describe the prey’s trophic pathways as alternate and poorly understood, not tightly linked to the microbial food web. (LLM, conf=0.88)

      Experimental — accuracy not yet measured
  • Premisecitation

    Malca et al. (2017) measured the growth rate of surviving bluefin tuna larvae, based on otolith readings from a survey in the spawning area.

    “Malca et al. (2017) measured the growth rate of surviving bluefin tuna larvae, based on otolith readings from a survey in the spawning area (Appendix S1: Fig. S4).”
    Quote in the paperSubstantial claim1 of 1 sources checked
    • cites Malca et al. (2017) source
  • Findingreasoning

    A 'metabolic meltdown' in which energy needs to fuel metabolism exceed ingestion as temperature increases occurs for larvae born later in the season.

    “A 'metabolic meltdown'in which energy needs to fuel metabolism exceed ingestion as temperature increase (sensu Huey and Kingsolver 2019)occurs for larvae born later in the season (Fig. 2c).”
    Quote in the paperSubstantial claim
  • May combine two claims. 27
  • Classified as probably not a substantial claim. 8
  • May combine two claims.

    Premisecitation

    Survival (egg fitness) ultimately depends on predation mortality, which may be in the order of 0.6/day in early life stages of tuna.

    “survival (egg fitness) ultimately depends on predation mortality, which may be in the order of 0.6/day in early life stages of tuna (Davis and Lyne 1991)”
    Quote in the paperSubstantial claim1 of 1 sources checked
    • cites Davis and Lyne 1991 source

      The Advection-diffusion-mortality modelling section estimates instantaneous mortality of 7–8-day-old southern bluefin tuna larvae at 0.66 per day, close to the claimed order of magnitude. It does not establish that this mortality was due to predation; it says starvation may also have contributed. The estimate concerns larvae, not egg survival or egg fitness. Page numbers are unavailable in our copy. (LLM, conf=0.88)

      Experimental — accuracy not yet measured
  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Premisecitation

    The temperature-food ration dependence is a logical and well known response in fishes, and recently also seen in a tropical larval tuna, but often ignored in predictions of thermal performance, phenology and spatial distributions.

    “The temperature-food ration dependence is a logical and well known response in fishes (Brett 1979), and recently also seen in a tropical larval tuna (Gleiber et al. 2020), but often ignored in predictions of thermal performance, phenology and spatial distributions.”
    Quote in the paperNot a substantial claim1 of 2 sources checked
    • cites Brett 1979 source
    • cites Gleiber et al. 2020 source
  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    Similar conditions occur in the Gulf of Mexico, another main spawning area for ABFT.

    “Similar conditions occur in the Gulf of Mexico, another main spawning area for ABFT (Landry et al. 2019).”
    Quote in the paperNot a substantial claim1 of 1 sources checked
    • cites Landry et al. 2019 source
  • May combine two claims.

    Findingreasoning

    Heatwaves, such as the one in 2003, increase larval survival potential, but shorten the viable part of the season for the larvae.

    “Heatwaves, such as the one in 2003, increase larval survival potential, but shorten the viable part of the season for the larvae.”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Findingreasoning

    High temperatures benefit egg and yolk-sac stages, but the metabolic needs of feeding larvae are hard to sustain during the warmest periods.

    “High temperatures benefit egg and yolk-sac stages, but the metabolic needs of feeding larvae are hard to sustain during the warmest periods.”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Findingown data

    The availability of prey, particularly nauplii, is sufficient for fast growth in tuna larvae while temperature is moderate during midsummer, but not when temperatures increase later in summer.

    “We find that the availability of prey, particularly nauplii, is sufficient for fast growth in tuna larvae while temperature is moderate during midsummer, but not when temperatures increase later in summer.”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Findingreasoning

    During the heatwave in 2003, the predicted metabolic meltdown for tuna larvae occurred early, lowering the optimal temperature, and shifted optimal time of birth 2-4 weeks earlier in the season compared with cooler years.

    “During the heatwave in 2003, the predicted metabolic meltdown for tuna larvae occurred early, lowering the optimal temperature, and shifted optimal time of birth 2-4 weeks earlier in the season compared with cooler years.”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Findingreasoning

    An egg spawned at day 180 grows faster through the egg and first feeding phase, but slower as it approaches the post-flexion stage.

    “An egg spawned at day 180 grows faster through the egg and first feeding phase, but slower as it approaches the post-flexion stage.”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Findingreasoning

    At birthday 200, the temperature is high while Cladocera abundance plunges, and food intake does not support growth of larger larvae, leading to a metabolic meltdown where ingestion rates support metabolic needs, but not growth.

    “At birthday 200, the temperature is high while Cladocera abundance plunges, and food intake does not support growth of larger larvae, leading to a metabolic meltdown where ingestion rates support metabolic needs, but not growth (Fig. 2c).”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Findingreasoning

    An egg spawned at day 160 encounters a good food supply as a larva relative to its energetic needs, but also low temperatures and growth rates while they are small and vulnerable to predation.

    “An egg spawned at day 160 encounters a good food supply as a larva relative to its energetic needs, but also low temperatures and growth rates while they are small and vulnerable to predation.”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Findingreasoning

    These mechanisms create a peak in egg fitness in June/July (at about day 190) for this seasonal pattern in prey supply and temperature, and matches the actual spawning dates quite well.

    “In summary, these mechanisms create a peak in egg fitness in June/July (at about day 190) for this seasonal pattern in prey supply and temperature, and matches the actual spawning dates quite well.”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Findingreasoning

    Later in the season, temperatures increase and food intake cannot cover larval metabolic needs, and late offspring face a metabolic meltdown in which no energy is available for growth.

    “Later in the season, temperatures increase and food intake cannot cover larval metabolic needs, and late offspring face a metabolic meltdown (sensu Huey and Kingsolver 2019) in which no energy is available for growth.”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Findingreasoning

    As food supply increases, the optimal breeding time is progressively later in the season as potential for larval growth is higher under warmer temperatures.

    “As food supply increases, the optimal breeding time is progressively later in the season as potential for larval growth is higher under warmer temperatures.”
    Quote in the paperNot a substantial claim
  • May combine two claims.

    Findingown data

    Thermal tolerance in terms of hatching success is quite wide in ABFT embryos, and our model shows how food limitation can narrow the viable thermal range of feeding stages.

    “In contrast, thermal tolerance in terms of hatching success is quite wide in ABFT embryos, and our model shows how food limitation can narrow the viable thermal range of feeding stages.”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Findingreasoning

    Such interannual temperature variation affects egg fitness differently, depending on the level of food limitation: more food increases the threshold for metabolic meltdown, and then warmer water is beneficial to ABFT larvae.

    “Such interannual temperature variation affects egg fitness differently, depending on the level of food limitation: more food increases the threshold for metabolic meltdown, and then warmer water is beneficial to ABFT larvae.”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Findingown data

    For eggs in the main spawning period (days 170-190), the 2003 heatwave increased fitness by one order of magnitude compared with the cold 2004, while metabolic meltdown occurs earlier.

    “For eggs in the main spawning period (days 170-190), the 2003 heatwave increased fitness by one order of magnitude compared with the cold 2004, while metabolic meltdown occurs earlier (Fig. 3b).”
    Quote in the paperSubstantial claim
  • Probably not a substantial claim: may not pass S4 (based).

    Findingnone given

    If eggs and larvae grow according to their temperature potential, with no limits from darkness, digestion, or food, then relative egg fitness follows the temperature cycle.

    “If eggs and larvae grow according to their temperature potential, with no limits from darkness, digestion, or food, then relative egg fitness follows the temperature cycle.”
    Quote in the paperNot a substantial claim
  • May combine two claims.

    Findingnone given

    Development of eggs and yolk-sac larvae are faster if temperature increases, but the first feeding larva needs abundant food supplies to grow fast.

    “Development of eggs and yolk-sac larvae are faster if temperature increases, but the first feeding larva needs abundant food supplies to grow fast.”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Findingreasoning

    The more food limited is the larval growth, the earlier is the egg fitness peak, as ingestion needed for growth increases with high temperatures later in season.

    “The more food limited is the larval growth, the earlier is the egg fitness peak, as ingestion needed for growth increases with high temperatures later in season (Fig. 3a).”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Findingown data

    Metabolic meltdown occurs at 22, 25 and 28°C if ingestion is 30%, 60% and 90% of body mass per day, respectively.

    “Metabolic meltdown occurs at 22, 25 and 28°C if ingestion is 30%, 60% and 90% of body mass per day, respectively (Appendix S1: Fig. S5).”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Findingown data

    The model matches this growth rate at c. 500 nauplii/m3, while the predicted peak in egg fitness remains within the observed spawning period.

    “The model matches this growth rate at c. 500 nauplii/m 3 (Appendix S1: Fig. S4), while the predicted peak in egg fitness remains within the observed spawning period (Appendix S1: Fig. S3).”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Findingown data

    The seasonal peak in egg fitness does not depend on the peak in Cladocera and is present even if both prey types are kept constant over time.

    “The seasonal peak in egg fitness does not depend on the peak in Cladocera and is present even if both prey types are kept constant over time”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Findingown data

    The seasonal peak in Cladocera suggests a classical match-mismatch driven phenology in ABFT, but the seasonally stable abundance of nauplii was more decisive for predicted phenology and growth of first feeding larvae in the model.

    “The seasonal peak in Cladocera suggests a classical match-mismatch driven phenology in ABFT, but the seasonally stable abundance of nauplii was more decisive for predicted phenology and growth of first feeding larvae in the model.”
    Quote in the paperSubstantial claim
  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    Cladocera have a peak of abundance in the summer.

    “particularly Cladocera, which have a peak of abundance in the summer (Atienza et al. 2016).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Atienza et al. 2016 source
  • May combine two claims.

    Interpretationreasoning

    Atlantic bluefin tuna spawn while temperatures are rising, but before the heat leads to a metabolic meltdown in larvae.

    “Atlantic bluefin tuna is a large, highly migratory marine top predator that spawns while temperatures are rising, but before the heat leads to a metabolic meltdown in larvae.”
    Quote in the paperSubstantial claim
  • Classified as probably not a substantial claim.

    Interpretationreasoning

    Seasonal cycles in prey availability and temperature interact to determine optimal spawning phenology.

    “Therefore, seasonal cycles in prey availability and temperature interact to determine optimal spawning phenology.”
    Quote in the paperSubstantial claim
  • Classified as probably not a substantial claim.

    Interpretationreasoning

    The mechanistic model allows us to identify windows in spatial and temporal cycles of temperature and resources between which animals can migrate to ease physiological stress, reproduce or increase growth rates.

    “The mechanistic model allows us to identify windows in spatial and temporal cycles of temperature and resources between which animals can migrate to ease physiological stress, reproduce or increase growth rates.”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Study design and conductnone given

    The model does predict in situ larval growth with realistic prey abundances, and the predictions of spawning time compare well with observations.

    “Despite these limitations, the model does predict in situ larval growth with realistic prey abundances, and the predictions of spawning time compare well with observations.”
    Quote in the paperSubstantial claim
  • Probably not a substantial claim: may not pass S4 (based).

    Interpretationnone given

    Many tuna species spawn in the warm oligotrophic open ocean, where metabolic meltdown is a constant risk for the early life stages.

    “Many tuna species spawn in the warm oligotrophic open ocean, where metabolic meltdown is a constant risk for the early life stages.”
    Quote in the paperNot a substantial claim
  • May combine two claims.

    Interpretationreasoning

    The tolerance measured for larvae fed ad libitum may not reflect ecologically relevant temperature tolerance under food limitation and can be an overestimate for natural conditions.

    “However, the tolerance measured for larvae fed ad libitum may not reflect ecologically relevant temperature tolerance under food limitation and can be an overestimate for natural conditions.”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Interpretationreasoning

    These larvae appear to grow near the temperature maximum estimated by Reglero et al. (2018b), indicating these survivors were not limited by their food supply.

    “These larvae appear to grow near the temperature maximum estimated by Reglero et al. (2018b), indicating these survivors were not limited by their food supply.”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Reglero et al. (2018b)

      Couldn’t be matched to a paper in Crossref, so it can’t be checked.

  • May combine two claims.

    Premisecitation

    The Cladocera species in ABFT spawning areas are heat tolerant, and increased in abundance during the 2003 heatwave.

    “The Cladocera species in ABFT spawning areas are heat tolerant, and increased in abundance during the 2003 heatwave (Atienza et al. 2016).”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Atienza et al. 2016 source
  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Interpretationreasoning

    ABFT abundance increased after 2003, and the heatwave may have contributed to this.

    “ABFT abundance increased after 2003, and the heatwave may have contributed to this.”
    Quote in the paperNot a substantial claim
33 of 33
  • The paper relies on this without support.

    Larvae do not find food in darkness and the gut empties during the night.

    “The larvae do not find food in darkness and therefore the gut empties during the night.”
  • The authors state this as an assumption.

    Capture probability of Cladocera increases linearly from 0 to 1 as larvae grow from first feeding to metamorphosis.

    “we assume a linear increase from 0 to 1 in capture probability of Cladocera as larvae grow from first feeding to metamorphosis.”
  • The authors state this as an assumption.

    Metabolism and ingestion are independent.

    “metabolism and ingestion have been assumed to be independent”
  • The authors state this as an assumption.

    Prey populations do not decline during the 2003 heatwave.

    “The predicted fitness benefit of the 2003 heatwave assumes that prey populations do not decline”
  • The paper relies on this without support.

    ABFT larvae only thrive in water above 20°C, making zooplankton associated with the deep chlorophyll maximum below the thermocline inaccessible.

    “The larvae only thrive in water above 20°C, which means that zooplankton associated with the deep chlorophyll maximum below the thermocline are inaccessible”
5 of 5

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

Each contradiction between two passages listed here was confirmed by an independent check.

  • Conflicting descriptions of metabolic meltdown

    Minor

    The paper defines metabolic meltdown as metabolism exceeding ingestion, but describes the day-200 meltdown as a state in which ingestion supports metabolism, though not growth.

1 of 1

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Authors
Fiksen, Ø., & Reglero, P.
Affiliations
  • University of Bergen (NO)
  • Instituto Español de Oceanografía (ES)
Corresponding author
Fiksen, Øyvind
Venue
Ecology
Publisher
Wiley
Published
2021-11-11
Volume
103
Issue
1
Pages
e03568-e03568
ISSN
  • 0012-9658 (ISSN-L)
  • 1939-9170
OpenAlex
W3207830576
Cited by
22
References
35
Citations by year
2026: 6 · 2025: 3 · 2024: 6 · 2023: 4 · 2022: 2 · 2021: 1
FWCI
1.31
Type
journal article
Language
en
Open access
Locations
  • Ecology (publishedVersion, cc-by-nc)
  • PubMed (publishedVersion)
  • DIGITAL.CSIC (Spanish National Research Council (CSIC)) (submittedVersion, cc-by-nc-nd)
  • Zenodo (CERN European Organization for Nuclear Research) (submittedVersion, cc-by)
  • NORA - Norwegian Open Research Archives (submittedVersion, cc-by-nc)
Funders
Horizon 2020 Framework Programme (773713 (PANDORA))
Topics
  • Physical Sciences › Environmental Science › Global and Planetary Change › Marine and fisheries research
  • Physical Sciences › Environmental Science › Ecology › Physiological and biochemical adaptations
  • Physical Sciences › Environmental Science › Nature and Landscape Conservation › Fish Ecology and Management Studies
Keywords
Thunnus thynnus, spawning timing, larval development, bioenergetics, heat waves, early life stages, larval survival, climate change, mechanistic model, 2003 European heatwave
MeSH terms
Animals, Atlantic Ocean, Energy Metabolism, Larva, Seasons, Temperature, Tuna

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