Atlantic bluefin tuna spawn early to avoid metabolic meltdown in larvae
Open accessAbstract
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
Cites
Statistics
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 - 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
- Findingreasoning
As summer proceeds (after day 190), the declining Cladocera abundance and increased metabolic costs restrict growth rate.
“As summer proceeds (after day 190), the declining Cladocera abundance and increased metabolic costs restrict growth rate.”
Quote in the paperSubstantial claim - Findingnone given
Larger larvae depend on Cladocera or similar prey larger than nauplii to grow at temperature-limited rates.
“The larger larvae depend on Cladocera or similar prey larger than nauplii to grow at temperature-limited rates (Fig. 2a).”
Quote in the paperSubstantial claim - Findingown data
The minimum viable prey concentration is c. 300 nauplii/m3 near the surface throughout the year.
“From the model, the minimum viable prey concentration is c. 300 nauplii/m 3 near the surface throughout the year”
Quote in the paperSubstantial claim - Findingreasoning
Both the seasonal curve and the absolute value of fitness depend more on the concentration of first feeding prey (nauplii) than on Cladocera.
“Both the seasonal curve and the absolute value of fitness depend more on the concentration of first feeding prey (nauplii) than on Cladocera”
Quote in the paperSubstantial claim - Findingown data
The predicted egg fitness is quite sensitive to supply of nauplii, with the peak appearing c. 20 d later for every 100 nauplii/m3 added.
“The predicted egg fitness is quite sensitive to supply of nauplii, with the peak appearing c. 20 d later for every 100 nauplii/m 3 added (Fig. 3a).”
Quote in the paperSubstantial claim - Findingown data
There is enough food for the larvae during the short time window in June-July.
“Based on measured metabolic needs, growth potential and a mechanistic model of prey encounter rates, we show that there is enough food for the larvae during the short time window in June-July.”
Quote in the paperSubstantial claim - Findingown data
Fitness is three orders of magnitude higher when nauplii concentrations increase from 300 to 500/m3 (at 30 Cladocera/m3).
“By comparison, fitness is three orders of magnitude higher when nauplii concentrations increase from 300 to 500/m 3 (at 30 Cladocera/m 3 ) (Appendix S1: Fig. S3).”
Quote in the paperNot a substantial claim - Findingreasoning
The optimal growth rate occurs before peak temperatures, at a time when food intake supports both the potential growth rate and the metabolic rate.
“The optimal growth rate occurs before peak temperatures, at a time when food intake supports both the potential growth rate and the metabolic rate.”
Quote in the paperSubstantial claim - Findingreasoning
In our model, the first feeding larva is the most temperature-sensitive stage.
“In our model, the first feeding larva is the most temperature-sensitive stage.”
Quote in the paperSubstantial claim - Findingown data
Survival still increases by an order of magnitude if the density is 30 rather than 20 Cladocera/m3.
“but survival still increases by an order of magnitude if the density is 30 rather than 20 Cladocera/ m 3 .”
Quote in the paperNot a substantial claim - Findingown data
The presence of Cladocera increases viability later in the season, when temperatures are high.
“Also, the presence of Cladocera increases viability later in the season, when temperatures are high (Appendix S1: Fig. S3).”
Quote in the paperNot a substantial claim - Findingown data
This prediction does not match the observed breeding time.
“This prediction does not match the observed breeding time (Fig. 3a; no food limitation).”
Quote in the paperSubstantial claim - Premisecitation
Egg developmental time decreases continuously with temperature from 19°C up to 32°C.
“egg developmental time decreases continuously with temperature from 19°C up to 32°C”
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.
- Interpretationreasoning
Food resources modulate how temperature change shifts optimal phenology.
“This means that food resources modulate how temperature change shifts optimal phenology.”
Quote in the paperSubstantial claim - Premisecitation
ABFT hatching success peaks at temperatures c. 25°C.
“ABFT hatching success peaks at temperatures c. 25°C”
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.
- Premisecitation
Larvae grow faster in warmer water (temperature range 22-28°C) if given surplus food.
“larvae grow faster in warmer water (temperature range 22-28°C) if given surplus food (Fig. 1c) (Reglero et al. 2018b).”
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.
- Interpretationreasoning
This may explain why ABFT spawn earlier than predicted with temperature as the only driver of growth.
“This may explain why ABFT spawn earlier than predicted with temperature as the only driver of growth (Reglero et al. 2018b).”
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.
- Interpretationreasoning
At the right temperature, the presence of these prey creates an opportunity in time and space where first feeding tuna larvae can grow.
“At the right temperature, the presence of these prey creates an opportunity in time and space where first feeding tuna larvae can grow.”
Quote in the paperSubstantial claim - Interpretationown data
Phenology can be predicted from fundamental physiological and ecological processes.
“Here, we have modeled the development, growth and survival of individual fish eggs in a seasonal cycle of environmental variables and show that phenology can be predicted from fundamental physiological and ecological processes.”
Quote in the paperSubstantial claim
- May combine two claims. 27
- Classified as probably not a substantial claim. 8
May combine two claims.
PremisecitationSurvival (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.
PremisecitationThe 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 checkedProbably not a substantial claim: may not pass S3 (load-bearing).
PremisecitationSimilar 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.
FindingreasoningHeatwaves, 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 claimMay combine two claims.
FindingreasoningHigh 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 claimMay combine two claims.
Findingown dataThe 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 claimMay combine two claims.
FindingreasoningDuring 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 claimMay combine two claims.
FindingreasoningAn 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 claimMay combine two claims.
FindingreasoningAt 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 claimMay combine two claims.
FindingreasoningAn 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 claimMay combine two claims.
FindingreasoningThese 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 claimMay combine two claims.
FindingreasoningLater 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 claimMay combine two claims.
FindingreasoningAs 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 claimMay combine two claims.
Findingown dataThermal 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 claimMay combine two claims.
FindingreasoningSuch 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 claimMay combine two claims.
Findingown dataFor 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 claimProbably not a substantial claim: may not pass S4 (based).
Findingnone givenIf 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 claimMay combine two claims.
Findingnone givenDevelopment 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 claimMay combine two claims.
FindingreasoningThe 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 claimMay combine two claims.
Findingown dataMetabolic 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 claimMay combine two claims.
Findingown dataThe 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 claimMay combine two claims.
Findingown dataThe 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 claimMay combine two claims.
Findingown dataThe 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 claimProbably not a substantial claim: may not pass S3 (load-bearing).
PremisecitationCladocera 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.
InterpretationreasoningAtlantic 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 claimClassified as probably not a substantial claim.
InterpretationreasoningSeasonal 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 claimClassified as probably not a substantial claim.
InterpretationreasoningThe 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 claimMay combine two claims.
Study design and conductnone givenThe 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 claimProbably not a substantial claim: may not pass S4 (based).
Interpretationnone givenMany 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 claimMay combine two claims.
InterpretationreasoningThe 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 claimMay combine two claims.
InterpretationreasoningThese 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.
PremisecitationThe 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.
InterpretationreasoningABFT 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
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”
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
MinorThe 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.
“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).”
“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).”
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Atlantic bluefin tuna spawn at suboptimal temperatures for their offspring
Reglero, P., Ortega, A., Balbín, R., Abascal, F. J., Medina, A., Blanco, E., de-la-Gándara, F., Álvarez‐Berastegui, D., Hidalgo, M., Rasmuson, L. K., et al. (2018) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2017.1405 · Cited by 67 · see citing works
Self-citationTrophic ecology of Atlantic bluefin tuna <i>Thunnus thynnus</i> larvae
Catalán, I. A., Tejedor, A., Alemany, F., & Reglero, P. (2011) · Journal of Fish Biology · doi:10.1111/j.1095-8649.2011.02960.x · Cited by 64 · see citing works
Self-citationYúfera, M., Ortiz-Delgado, J. B., Hoffman, T., Siguero, I., Urup, B., & Sarasquete, C. (2014) · Aquaculture · doi:10.1016/j.aquaculture.2014.01.031 · Cited by 62 · see citing works
van Denderen, P. D., Gislason, H., van den Heuvel, J., & Andersen, K. H. (2020) · Global Ecology and Biogeography · doi:10.1111/geb.13189 · Cited by 58 · see citing works
Olivar, M., Sabatés, A., Alemany, F., Balbín, R., de Puelles, M. F. D., & Torres, A. (2014) · Journal of Marine Systems · doi:10.1016/j.jmarsys.2013.10.009 · Cited by 49 · see citing works
Davis, T., Lyne, V, & Jenkins, G. (1991) · Marine Ecology Progress Series · doi:10.3354/meps073033 · Cited by 38 · see citing works
Malca, E., Muhling, B., Franks, J., García, A., Tilley, J., Gerard, T., Ingram, W., & Lamkin, J. T. (2017) · Fisheries Research · doi:10.1016/j.fishres.2017.01.019 · Cited by 36 · see citing works
Shima, J., Osenberg, C. W., Alonzo, S. H., et al. (2020) · Ecology · doi:10.1002/ecy.3086 · Cited by 34 · see citing works
Reglero, P., Blanco, E., Alemany, F., Ferrà, C., Álvarez‐Berastegui, D., Ortega, A., de-la-Gándara, F., Aparicio‐González, A., & Folkvord, A. (2018) · Marine Ecology Progress Series · doi:10.3354/meps12516 · Cited by 24 · see citing works
Self-citationLandry, M. R., Beckley, L. E., & Muhling, B. A. (2019) · ICES Journal of Marine Science · doi:10.1093/icesjms/fsy184 · Cited by 24 · see citing works
Retinal adaptations of southern bluefin tuna larvae: Implications for culture
Hilder, P., Battaglene, S., Hart, N., Collin, S., & Cobcroft, J. (2019) · Aquaculture · doi:10.1016/j.aquaculture.2019.04.024 · Cited by 20 · see citing works
Gleiber, M. R., Sponaugle, S., & Cowen, R. K. (2020) · ICES Journal of Marine Science · doi:10.1093/icesjms/fsaa201 · Cited by 15 · see citing works
Atienza, D., Sabatés, A., Isari, S., Saiz, E., & Calbet, A. (2016) · Journal of Marine Systems · doi:10.1016/j.jmarsys.2016.08.003 · Cited by 13 · see citing works
First estimates of metabolic rate in Atlantic bluefin tuna larvae
Blanco, E., Reglero, P., Ortega, A., Folkvord, A., de-la-Gándara, F., Hernández-de-Rojas, A., & Moyano, M. (2020) · Journal of Fish Biology · doi:10.1111/jfb.14473 · Cited by 10 · see citing works
Self-citationFiksen, Ø. (2021) · Zenodo (CERN European Organization for Nuclear Research) · doi:10.5281/zenodo.4693459 · Cited by 1 · see citing works
Self-citationFiksen, Ø. (2021) · Zenodo · doi:10.5281/zenodo.4693460
Self-citationShima, J., Osenberg, C., Alonzo, S., et al. (2020) · doi:10.26686/wgtn.13012961.v1
Flagged first, then by citations
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Almeida, L. Z., Laurel, B. J., Thalmann, H. L., & Miller, J. A. (2024) · Elementa Science of the Anthropocene · doi:10.1525/elementa.2023.00050 · Cited by 27 · see citing works
Vertebrae reveal industrial-era increases in Atlantic bluefin tuna catch-at-size and juvenile growth
Andrews, A. J., Natale, A. D., Addis, P., Piattoni, F., Onar, V., Casasola, D. B., Aniceti, V., Carenti, G., Gómez‐Fernández, V., Garibaldi, F., et al. (2023) · ICES Journal of Marine Science · doi:10.1093/icesjms/fsad013 · Cited by 14 · see citing works
“…b y b i b li o t e c a b i o m ed i c a c en t r a l e un i v e r s i t a d i bo l ogna u s e r on 24 F eb r ua r y 20 23 tigation due to its temperature-driven component (Fiksen and Reglero, 2022) and consequences on the reproductive output of BFT as a multiple-batch spawner (Medina, 2020).”
Persistence of fish populations to longer, more intense, and more frequent mass mortality events
Langangen, Ø., & Durant, J. M. (2024) · Global Change Biology · doi:10.1111/gcb.17251 · Cited by 10 · see citing works
“For example, MHWs have been associated with loss of spawning habitat (Dahlke et al., 2018; Laurel & Rogers, 2020) and reduced egg or larval survival (Fiksen & Reglero, 2022; Laurel & Rogers, 2020; Rogers et al., 2021).”
BackgroundMedina, A., Magro, A., Macías, D., & Varela, J. L. (2022) · Marine Ecology Progress Series · doi:10.3354/meps14129 · Cited by 8 · see citing works
Coldwater, stenothermic fish seem bound to suffer under the spectre of future warming
Roberts, B. J., Chucholl, C., & Brinker, A. (2024) · Journal of Great Lakes Research · doi:10.1016/j.jglr.2024.102351 · Cited by 7 · see citing works
Ottmann, D., Langbehn, T. J., Reglero, P., Álvarez‐Berastegui, D., & Fiksen, Ø. (2023) · Limnology and Oceanography · doi:10.1002/lno.12465 · Cited by 6 · see citing works
“Atlantic blue fi n tuna (hereafter ABFT) is a large pelagic fi sh that spawns in warm oligotrophic waters in both sides of the Atlantic Ocean, in the Gulf of Mexico, Slope Sea, and the Mediterranean Sea (Richardson et al. 2016; Muhling et al. 2017).”
BackgroundMethodInfluentialSelf-citationFive millennia of mitonuclear discordance in Atlantic bluefin tuna identified using ancient DNA
Eriksen, E. F., Andrews, A. J., Nielsen, S. V., Persson, P., Malca, E., Onar, V., Aniceti, V., Piquès, G., Piattoni, F., Fontani, F., et al. (2025) · Heredity · doi:10.1038/s41437-025-00745-1 · Cited by 7 · see citing works
Reglero, P., Tugores, M. P., Titelman, J., Santandreu, M. M., Martin, M., Balbín, R., Álvarez‐Berastegui, D., Torres, A. P., Calcina, N. L., Leyva, L., et al. (2025) · Journal of Plankton Research · doi:10.1093/plankt/fbaf006 · Cited by 6 · see citing works
“Temperature can shift growth rates from positive to negative depending on food availability (Huey and Kingsolver, 2019; Fiksen and Reglero, 2022).”
InfluentialSelf-citationCritical thermal limits of Atlantic bluefin tuna (Thunnus thynnus) larvae
Moyano, M., Blanco, E., Ortega, A., et al. (2026) · Journal of Thermal Biology · doi:10.1016/j.jtherbio.2026.104410 · Cited by 3 · see citing works
Self-citationMoltó, V., Palmer, M., Polin, M., et al. (2024) · Marine Environmental Research · doi:10.1016/j.marenvres.2024.106713 · Cited by 2 · see citing works
Ottmann, D., Reglero, P., Alemany, F., Álvarez‐Berastegui, D., Martín, M., & Fiksen, Ø. (2022) · Limnology and Oceanography Letters · doi:10.1002/lol2.10241 · Cited by 2 · see citing works
“Current studies show that juvenile ALB have not been observed in stomach content of other juvenile or adult scombrids (Fletcher et al. 2013; Sorell et al. 2017; Varela et al. 2019), and juvenile ALB are thought to be too few to cause density-dependent regulation (Arregui et al. 2006; Bakun 2013).”
BackgroundSelf-citationYanagitsuru, Y. R., Mauduit, F., Lundquist, A., et al. (2024) · Conservation Physiology · doi:10.1093/conphys/coae004 · Cited by 2 · see citing works
“…(Dege and Brown, 2003; Grimaldo et al., 2020; Lewis et al., 2020) and food availability (Winder and Jassby, 2011; Lee et al., 2016; Barros et al., 2022; Burris et al., 2022; Fiksen and Reglero, 2022) drive the thermal habitats that organisms occupy in nature (Allen-Ankins and Stoffels, 2017).”
BackgroundThe genome sequence of Atlantic Bluefin Tuna, Thunnus thynnus (Linnaeus, 1758)
Oomen, R. A., Cariani, A., Chavarie, L., Leone, A., Vella, A., Vella, N., Hellström, G., Brodin, T., Sundelöf, A., Blaxter, M., et al. (2025) · Wellcome Open Research · doi:10.12688/wellcomeopenres.23971.1 · Cited by 1 · see citing works
“Recovery may also be affected by climate change, as warmer sea temperatures influence the distribution and abundance of populations (Erauskin-Extramiana et al. , 2019; Fiksen & Reglero, 2022; MacKenzie et al. , 2014; Reglero et al. , 2018).”
Five millennia of mitochondrial introgression in Atlantic bluefin tuna identified using ancient DNAPreprint
Eriksen, E. F., Andrews, A. J., Nielsen, S. V., Persson, P., Malca, E., Onar, V., Aniceti, V., Piquès, G., Piattoni, F., Fontani, F., et al. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.03.24.586294 · Cited by 1 · see citing works
The effect of continuous lighting on the rearing of yellowfin tuna (Thunnus albacares) larvae
Slamet, B., Hutapea, J. H., Gunawan, G., et al. (2023) · IOP Conference Series Earth and Environmental Science · doi:10.1088/1755-1315/1289/1/012020
“Warm temperatures are good for the hatching stage of eggs and absorption of the yolk of tuna larvae, but as the temperature increases it causes difficulties with larval metabolism [4].”
BackgroundCasaucao-Aguilar, A., Mourre, B., Tugores, M. P., Balbín, R., Díaz‐Barroso, L., Hernández‐Carrasco, I., Reglero, P., & Álvarez‐Berastegui, D. (2026) · Frontiers in Marine Science · doi:10.3389/fmars.2026.1705858 · Cited by 1 · see citing works
Self-citationMnich, A., Zavell, M. D., Muhling, B. A., Hernández, C. M., & Cadrin, S. X. (2026) · Integrative and Comparative Biology · doi:10.1093/icb/icag041
Musyl, M. K., McNaughton, L. M., Jia, Y., Humphreys, R. L., & Kramer, R. (2026) · Reviews in Fish Biology and Fisheries · doi:10.1007/s11160-026-10062-3
Matlaga, T. J. H., Burrowes, P. A., Paterson, J. E., & Wood, T. E. (2026) · Journal of Thermal Biology · doi:10.1016/j.jtherbio.2026.104527
Pelagic food web realignment supports resilient larvae of Southern Bluefin Tuna in a warming ocean
Landry, M. R., Laiz-Carrión, R., Malca, E., Swalethorp, R., Décima, M., Quintanilla, J., Borrego-Santos, R., Davies, C., Kranz, S. A., Selph, K., et al. (2026) · Proceedings of the National Academy of Sciences of the United States of America · doi:10.1073/pnas.2601583123
- Authors
- Fiksen, Ø., & Reglero, P.
- Affiliations
- University of Bergen (NO)
- Instituto Español de Oceanografía (ES)
- Corresponding author
- Fiksen, Øyvind
- ORCID
- 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
- Semantic Scholar
- fa594a6d1270cf516f3f3e93ea4163b92fdedf9e
- 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
- hybrid
- doi.org
- Licence
- 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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Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
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