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. 2026 May 26;109(2):1225–1232. doi: 10.1111/jfb.70508

Temperature determines early‐life success of burbot Lota lota eggs

Pieter Lemmens 1,2,✉, Inne Vught 1, Stien Mertens 1, Daniel De Charleroy 1, Johan Auwerx 2
PMCID: PMC13521713  PMID: 42187085

Abstract

Temperature strongly regulates early‐life development of freshwater fishes, influencing embryogenesis, hatching success and larval survival. Cold‐water species, including burbot Lota lota, are particularly sensitive to warming, yet information on the thermal requirements of their early‐life stages remains limited. We experimentally quantified the effects of incubation temperature on eggs from multiple females of a Western‐European burbot population. Eggs were incubated at five constant temperatures (2, 4, 6, 8, 10°C), and developmental outcomes, including hatching success, abnormal development and incubation time, were recorded. Hatching success was highest at intermediate temperatures (4 and 6°C) and substantially reduced at low (2°C) and high (8 and 10°C) temperatures, with highly elevated mortality and deformities at temperature extremes. Incubation time decreased with increasing temperature, reflecting accelerated development, but higher temperatures reduced developmental stability. Female identity significantly influenced developmental outcomes, and this effect interacted with incubation temperature, indicating that female‐specific responses varied across thermal conditions. These results reveal a narrow thermal window for successful burbot embryogenesis and provide critical information on temperature thresholds for early‐life stages, with direct relevance for habitat assessment, conservation, captive breeding and reintroduction programmes. Populations in temperate European rivers may be particularly sensitive to warming, emphasizing the importance of considering both thermal conditions and temperature‐dependent variation among females when evaluating recruitment potential.

Keywords: burbot, conservation, female effects, hatching success, river warming, temperature

1. INTRODUCTION

Temperature is a fundamental driver of biological processes in freshwater ecosystems, regulating metabolic rates, development and species distributions (Comte et al., 2013; Johnson et al., 2024). Early‐life stages of fish, including eggs, embryos and larvae, are particularly temperature‐sensitive, as water temperature determines developmental rate, success of embryonic development and early survival (Alix et al., 2020; Angilletta, 2004; Lindmark et al., 2022). Even small deviations from optimal temperatures can profoundly impact recruitment and population persistence (Brown et al., 2024; Nunn et al., 2003), especially in cold‐water species (Fullerton et al., 2018; Hari et al., 2006).

Burbot Lota lota is a cold stenothermal freshwater gadid with a Holarctic distribution (Paragamian & Willis 2000; Stapanian & Madenjian, 2013). Despite its broad geographical range, many populations are declining or locally extirpated due to habitat degradation and fragmentation (Bosveld et al., 2015; Stapanian et al., 2010). Eggs are typically laid in winter and early spring in off‐channel or floodplain habitats, where low water temperatures are critical for successful embryogenesis (Müller, 1957; Worthington et al., 2011). Previous studies indicate that burbot eggs are highly thermally sensitive, with survival and hatching success strongly influenced by incubation temperature, although reported optimal temperatures differ among studies (Ashton et al., 2019; Lahnsteiner et al., 2012; Żarski et al., 2010). Information on thermal limits is essential for the effective conservation of burbot, particularly in the light of ongoing warming in river systems (Liu et al., 2020).

In addition to ongoing habitat degradation, pollution, and overexploitation, long‐term warming of rivers has become an increasingly important threat to many freshwater species worldwide (Brown et al., 2024). Warming trends are particularly pronounced in European rivers (0.5–1°C per decade) (European Environment Agency., 2024), increasingly exposing thermally sensitive fishes to suboptimal conditions (Råman Vinnå et al., 2025). Information on the effects of rising temperatures on wild burbot populations is largely lacking, yet many populations are declining or locally extirpated across parts of their natural range (Bosveld et al., 2015; Stapanian et al., 2010). Few observational studies directly associate burbot declines with altered thermal regimes, suggesting that warmer summers may reduce survival, while milder winters can limit reproductive success (Pandakov et al., 2020; Švagždys, 2002). Current conservation and reintroduction programmes largely focus on habitat availability and water quality (Pearce et al., 2025), whereas thermal regimes are rarely considered explicitly. In addition, local adaptation may generate population‐specific thermal optima (Cott et al., 2013). Knowledge of optimal and suboptimal temperatures, and their potential variation within and among populations, is therefore essential to guide effective conservation, captive breeding and reintroduction strategies.

The present study investigates the effects of water temperature on the early‐life stages of burbot Lota lota using a highly standardized laboratory experiment. We incubated individual eggs from multiple burbot females (n = 6) from broodstock originating from a wild Western‐European population at five constant temperatures (2, 4, 6, 8, 10°C), and quantified multiple developmental outcomes to determine temperature ranges associated with successful hatching. This study provides important information to complement conservation, management and reintroduction programmes for endangered burbot populations.

2. METHODS

2.1. Laboratory incubation experiment

Eggs from six burbot females were incubated at five constant temperatures (2, 4, 6, 8 and 10°C) under controlled laboratory settings. Burbot broodstock, originating from wild populations in the river Albe (France) and maintained in outdoor culture ponds for several generations, were induced to naturally spawn in indoor water tanks maintained at 4°C under short photoperiod (8 h light/16 h dark) following procedures described in Vught et al. (2008). Broodstock females were 3–4 years old, 25–30 cm in length and 200–250 g in body mass based on colony records, with fecundity in this stock around 22% of body mass (~6.6 × 105 eggs kg−1). Eggs were collected from the tank bottom after fertilization, rinsed with autoclaved spring water, and individually transferred into 96‐well microplates containing autoclaved spring water using a wide‐mouth pipette. Three plates per female and temperature treatment (temperature×female×plate) were prepared. Plates were kept at 4°C for 24 h prior to incubation in water baths (au bain‐marie) maintained at target temperatures using digitally controlled immersion heaters (IKS Aquastar Temperature Module, IKS ComputerSysteme GmbH), after which unfertilized eggs were removed. Plates assigned to 2, 4 and 6°C were transferred directly, whereas plates assigned to 8 and 10°C were gradually acclimated over 3 h to minimize acute thermal stress. Plate positions within each water bath were randomized across females. Water in the wells was neither replaced nor aerated during egg incubation. Baths were covered with EPS plates to maintain stable temperatures. Transfer of the well‐plates into the water baths marked the formal start of the temperature incubation experiment.

Egg development was regularly monitored under a dissecting stereoscope until 90 days after the start of the experiment. Examination of individual plates was done within a few minutes to avoid warming. Plates incubated at 8 and 10°C were checked daily, those at 4 and 6°C every other day, and those at 2°C every 5 days until the pre‐hatching stage, in order to maintain comparable cumulative thermal exposure (°C*days) across treatments. From then on, all plates were checked daily. At each inspection, eggs were classified as dead, alive, or hatched. Eggs were considered dead (DE) when the embryo appeared partly or completely opaque. Larvae that died during hatching were recorded as dead hatches (DH). Hatchlings were further categorized into (1) normally developed (alive with no visible deformities and normal behaviour, HN), or (2) abnormally developed (alive with malformations or abnormal swimming behaviour, HD).

2.2. Statistical analysis

The effects of incubation temperature, female identity and their interaction on the proportion of eggs in each developmental category (DE, DH, HD, HN) were assessed at the egg level, treating individual eggs as observational units. Unfertilized eggs (UN) were excluded from the statistical analysis. Developmental outcomes were modelled with a generalized linear mixed model (GLMMs) with a binomial error distribution and logit link for each development category separately using the glmmTMB package (Brooks et al., 2017). Temperature and female were included as fixed effects (categorical), and their interaction was explicitly tested. Plate identity nested within temperature and female was included as a random effect to account for non‐independence among eggs from the same plate. Model residuals were checked using the DHARMa package (Hartig, 2024) to assess dispersion, zero‐inflation, uniformity and outliers.

Predicted probabilities for each temperature within each female were estimated using the emmeans package (Lenth & Piaskowski, 2017), and pairwise comparisons between temperatures were conducted with Tukey‐adjusted contrasts on the response scale. Bonferroni correction was applied to ANOVA p‐values across all model terms. Confidence intervals for predicted probabilities and differences were derived from the model. The GLMM accounts for all individual observations and their correlation structure, providing accurate estimates and significance tests. Fertilization rate (proportion of fertilized eggs per plate) was analyzed using a GLMM with female as a random effect, and the significance of female identity was assessed via a likelihood ratio test (LRT) comparing models with and without the female term.

All analyses were performed in R (version 4.5.1).

3. RESULTS

A total of 8640 eggs were incubated and monitored over a period of 90 days. Fertilization rate was overall high, averaging 99% across females and plates (range: 98%–100%), and the random effect of female identity did not significantly contribute to variation (variance = 0.15; LRT χ 2 ≈ 0, df = 3, p = 1). Hatching (HN, HD and DH) was observed at all incubation temperatures, but was low at 8°C and nearly absent at 10°C. Incubation time until first hatching decreased with increasing incubation temperature, occurring after 42 days at 2°C (84°C*days), 30 days at 4°C (120°C*days), 24 days at 6°C (144°C*days), 15 days at 8°C (120°C*days) and 14 days at 10°C (140°C*days).

Incubation temperature had a strong effect on the developmental outcomes of fertilized eggs (Figure 1, Table 1). The percentage of normally developed larvae (HN) was highest at 4°C and 6°C (mean across females and plates, 75% and 74%, respectively), and lowest at 10°C (3%). The percentage of normally developed larvae was still relatively high at 2°C (66%), and was considerably lower at 8°C (19%) (Figure S1). Mortality of eggs (DE) was high at 10°C and 8°C (93% and 47%, respectively), and relatively low at 2, 4 and 6°C (16%–19%) (post‐hoc comparison, p < 0.05).

FIGURE 1.

FIGURE 1

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Proportion of fertilized egg developmental outcomes per plate across temperature treatments (top) and females (right). Colours indicate developmental category [HN (normal hatch) = green, HD (deformed hatch) = light orange, DH (death hatch) = dark orange, DE (death egg) = red].

TABLE 1.

Summary of GLMMs testing the effects of incubation temperature, female identity and their interaction on the proportion of eggs in each developmental category (DE, DH, HD, HN).

Model term Category Chi‐squared df p‐adjusted
Temperature HN 170.244 4 <0.001
HD 24.149 4 0.001
DH 82.033 4 <0.001
DE 92.749 4 <0.001
Female HN 47.273 5 <0.001
HD 123.306 5 <0.001
DH 11.286 5 0.736
DE 34.274 5 <0.001
Temperature × Female HN 159.405 20 <0.001
HD 175.373 20 <0.001
DH 106.903 20 <0.001
DE 176.816 20 <0.001
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Note: For each model term (Temperature, Female, Temperature × Female) and category, the table reports the Chi‐squared statistic (χ 2), degrees of freedom (df), Bonferroni‐corrected p‐value across all model terms, based on a likelihood ratio test (LRT) comparing the full model to a reduced model excluding the term of interest.

Similarly, the percentage of dead hatches (DH) was relatively high at 8°C and 10°C (17% and 10%), and relatively low at 2–6°C (2%–3%). Deformed larvae (HD) were most frequent at 2°C and 8°C (15% and 19%, respectively), intermediate at 6°C (9%), and low at 10°C (6%) and 4°C (5%) (Figure S1). These patterns jointly reflect the proportional nature of hatching outcomes, where increases in one category correspond to decreases in others.

LRTs showed that female identity significantly influenced the proportion of eggs in all developmental categories, irrespective of temperature, while observed significant temperature × female interactions indicate that females also differed in their responses to incubation temperature (Table 1). Females exhibited fairly consistent ranks in the proportion of normally hatched larvae (HN) at 2, 4 and 6°C, near‐zero HN at 10°C, and greater variability at 8°C, where some females still achieved relatively high proportions of normally hatched larvae (Figure S2).

4. DISCUSSION

The present study investigates the effect of incubation temperature on the embryonic development and hatching success of burbot Lota lota eggs from multiple females using a controlled laboratory experiment. Incubation temperature strongly affected both the timing of development and the relative proportions of hatching outcomes. Eggs incubated at 4°C and 6°C produced the highest proportion of normally developed larvae, whereas hatching success was considerably lower at 8°C and almost entirely suppressed at 10°C. At 2°C, egg development was significantly slower, but hatching success remained relatively high. These results confirm that burbot exhibit a relatively narrow thermal window for successful egg development.

Incubation time until first hatching decreased with increasing temperature, reflecting the well‐established temperature dependence of metabolic and developmental rates in ectothermic organisms (Angilletta, 2004; Jarośík et al., 2004; Pettersen et al., 2024). However, accelerated development at higher temperatures was associated with increased egg mortality and higher proportions of abnormal hatching outcomes [abnormally developed larvae (HD) and dead hatches (DH)]. This observation hints towards a trade‐off between developmental rate and developmental stability (Gotthard, 2024). Similar patterns have been reported for other cold‐water and temperate fish species (Melendez & Mueller, 2021; Robinson & Wardrop, 2002). There are multiple potential explanations for these observations. First, increased metabolic demand can compromise organogenesis by exceeding energy reserves provisioned in the egg (Jager et al., 2018; Martin et al., 2020). Second, accelerated developmental processes can disrupt the timing of critical morphogenetic events, resulting in structural abnormalities (Pype et al., 2015). Third, impaired enzymatic function and protein stability may cause cellular damage and developmental delays in specific tissues (Sales et al., 2019; Schnurr et al., 2013). Conversely, the relatively high proportion of deformed larvae observed at 2°C may be linked to prolonged development at lower temperatures, increasing exposure to stressors such as oxidative stress and the accumulation of metabolic byproducts that can interfere with normal cell differentiation and morphogenesis (Zhang et al., 2023). The present study does not allow to pinpoint the exact mechanisms at play.

Hatching success in our study was highest at 4 and 6°C, and declined sharply at 8°C, with almost complete failure at 10°C. Previous studies report lower temperatures for optimal egg survival and hatching, with maximal survival near 2°C and high egg mortality at 5–6°C (Ashton et al., 2019; Lahnsteiner et al., 2012; Żarski et al., 2010). Notably, Lahnsteiner et al. (2012) observed complete hatching failure at 9°C, a pattern closely matching the very low hatching proportion we observed at 10°C. Despite these discrepancies, all studies consistently show strongly reduced hatching at high temperatures and indicate that burbot exhibit a relatively narrow thermal window for successful egg development. Differences in optimal temperature across studies may reflect variation in population‐specific traits (Cott et al., 2013). Burbot are genetically structured into multiple lineages across their Holarctic distribution (Van Houdt et al., 2005), and local adaptation to regional thermal environments may result in population‐specific differences in embryonic thermal tolerance (Lou et al., 2022). The relatively higher optimal temperatures observed in our study may thus reflect the use of broodstock originating from the Albe River (France), near the southern edge of the species' natural European distribution and subject to a maritime climate with mild winters.

While embryonic development in burbot is characterized by a relatively narrow thermal window for successful hatching, larval responses seem to exhibit a wider thermal performance space characterized by a trade‐off between growth and survival, with higher growth at warmer temperatures (20°C) and highest survival at intermediate temperatures (12–15°C) (Barron et al., 2012; Paragamian & Willis 2000; Shiri Harzevili et al., 2004; Wolnicki et al., 2001). Such ontogenetic shift reflects increasing thermal tolerance across early development, from a constrained embryonic stage to a more plastic larval performance phase. These stage‐dependent responses are also relevant in a broader life‐history context, as carry‐over effects in fish may link conditions experienced during embryogenesis to later performance and survival through persistent effects on growth and physiology (Jonsson & Jonsson, 2014; Moore & Martin, 2019).

Female identity significantly influenced developmental outcomes, indicating intrinsic differences among burbot females. These differences may reflect differences in maternal traits between females (e.g., egg size, yolk quantity or composition, maternal age), genetically based variation, or a combination of both (Ashton et al., 2019; Callet et al., 2022; Johnston & Leggett, 2002; Kamler, 2005; Reading et al., 2018). Interestingly, the magnitude of these female‐specific effects varied with incubation temperature. Differences in successful hatching between females were relatively consistent at 2, 4 and 6°C, more pronounced at 8°C, and negligible at 10°C, mirroring the observed female × temperature interaction. Comparable temperature‐dependent female effects have been documented in other fish species (Burt et al., 2011; Green, 2008) and may influence recruitment and population‐level survival under suboptimal or stressful conditions. The observed temperature‐modulated female effects on hatching success potentially enable population persistence under naturally fluctuating and climate‐altered thermal conditions.

The pronounced thermal sensitivity of burbot eggs has important ecological implications. Warming trends in European rivers (European Environment Agency, 2024) can potentially reduce recruitment by exceeding optimal temperatures for embryonic development. Even modest temperature increases beyond the narrow thermal window identified in our study (4–6°C) can substantially increase egg mortality and the proportion of malformed larvae, while accelerated development may also disrupt the timing of hatching relative to prey availability (Johnson et al., 2024). Variation among females adds an additional layer of variability, potentially buffering or amplifying population‐level responses to thermal stress. Populations near their upper thermal limits, or originating from warmer regions, may be particularly vulnerable, whereas variation in temperature response among females could modulate resilience within populations. These patterns are consistent with broader syntheses showing that thermal tolerance is a key determinant of distribution limits and climate‐change vulnerability in freshwater fishes (Souchon & Tissot, 2012), underscoring that conservation planning must explicitly account for species‐specific thermal thresholds alongside water and habitat quality (Radtke & Bernaś, 2025). In this context, habitat features such as deep meanders, off‐channel areas and lateral connectivity to floodplains may provide cooler refuges and buffer populations from warming.

While our study demonstrates clear temperature‐dependent developmental outcomes under controlled laboratory conditions, several limitations apply. Constant incubation temperatures and simplified laboratory settings do not capture the natural thermal variability and environmental complexity experienced by embryos in rivers. Earlier studies indicate that fluctuating thermal regimes and the rate of temperature change during early embryogenesis can influence survival, developmental rate and deformity in fish, although responses are highly species‐ and temperature‐range dependent (Ashton et al., 2021; Blanchard et al., 2025; Kupren et al., 2011; Lim et al., 2017). In burbot specifically, experimental evidence shows that both cyclical and rapidly increasing temperatures during early embryogenesis can elevate deformity and mortality (Ashton et al., 2021). Thermal responses are thus jointly shaped by mean temperature and temporal variability, and extrapolation from constant‐temperature experiments to natural systems should therefore be made with caution. Furthermore, in static systems, temperature may affect embryonic development both directly and indirectly through changes in physicochemical conditions, including dissolved oxygen, pH and metabolite accumulation. These variables were not monitored in the present study, and therefore observed temperature effects may reflect both direct thermal responses and indirect effects mediated through temperature‐dependent changes in water chemistry, which cannot be separated under the present experimental design. In addition, the limited number of females restricts inference on population‐level variability and generalization to natural populations. Finally, our study focused on general thermal effects during early development, but the most sensitive zygote stages may have been partially missed due to the initial 24‐h incubation at 4°C. Future studies incorporating fluctuating thermal regimes, additional females and field‐based validation using high‐resolution winter temperature data are needed to better translate laboratory‐derived thermal thresholds to natural systems and to pinpoint which developmental stages are most vulnerable to warming.

In conclusion, burbot early‐life stages are highly sensitive to temperature, with a narrow thermal window for successful embryogenesis. Female‐specific differences in hatching success interact with temperature, modulating early‐life outcomes and potentially buffering populations under naturally fluctuating and warming conditions, yet populations near their upper thermal limits may remain particularly vulnerable. Our findings emphasize the importance of considering both thermal regimes and inter‐female variability, alongside habitat and water quality, in conservation strategies for cold‐water fishes.

AUTHOR CONTRIBUTIONS

Conceptualisation and development of methods: Pieter Lemmens, Inne Vught, Stien Mertens, Johan Auwerx. Data analysis: Pieter Lemmens, Stien Mertens. Data interpretation: Pieter Lemmens, Inne Vught, Johan Auwerx. Preparation of figures and tables: Pieter Lemmens. Conducting the research and writing: Pieter Lemmens, Inne Vught, Stien Mertens, Johan Auwerx. Funding acquisition: Daniel De Charleroy, Johan Auwerx.

FUNDING INFORMATION

This work was supported financially by the Agency for Nature and Forest (ANB) and the ‘Visserijcommissie’ through long‐term programme funding for the reintroduction of burbot Lota lota in Flanders. SM received funding from the European Biodiversity Partnership Biodivera+ under the Horizon Europe research and innovation programme (grant agreement No. 101052342).

CONFLICT OF INTEREST STATEMENT

The authors declare that they have no conflicts of interest.

Supporting information

Figure S1. Predicted percentages of eggs in the four developmental categories (HN = normal hatch, green; HD = deformed hatch, light orange; DH = death at hatch, dark orange; DE = death at egg stage, red) across temperature treatments. Bars represent predicted proportions from binomial generalized linear mixed models (GLMMs), expressed as percentages, with 95% confidence intervals indicated by error bars. Letters above bars indicate statistically significant differences among temperatures based on Tukey‐adjusted pairwise comparisons of estimated marginal means; bars that do not share a letter are significantly different (p < 0.05).

Figure S2. Female specific responses to each temperature treatment for the four developmental categories [HN (normal hatch) = green, HD (deformed hatch) = light orange, DH (death hatch) = dark orange, DE (death egg) = red]. Bars represent predicted proportions of eggs from binomial generalized linear mixed models (GLMMs), expressed as percentages, with 95% confidence intervals indicated by error bars.

JFB-109-1225-s001.docx (58.5KB, docx)

ACKNOWLEDGEMENTS

We thank Bruno Picavet for technical assistance during the experiment.

DATA AVAILABILITY STATEMENT

The data that support the findings of this study are available from the corresponding author upon reasonable request.

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Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Supplementary Materials

Figure S1. Predicted percentages of eggs in the four developmental categories (HN = normal hatch, green; HD = deformed hatch, light orange; DH = death at hatch, dark orange; DE = death at egg stage, red) across temperature treatments. Bars represent predicted proportions from binomial generalized linear mixed models (GLMMs), expressed as percentages, with 95% confidence intervals indicated by error bars. Letters above bars indicate statistically significant differences among temperatures based on Tukey‐adjusted pairwise comparisons of estimated marginal means; bars that do not share a letter are significantly different (p < 0.05).

Figure S2. Female specific responses to each temperature treatment for the four developmental categories [HN (normal hatch) = green, HD (deformed hatch) = light orange, DH (death hatch) = dark orange, DE (death egg) = red]. Bars represent predicted proportions of eggs from binomial generalized linear mixed models (GLMMs), expressed as percentages, with 95% confidence intervals indicated by error bars.

JFB-109-1225-s001.docx (58.5KB, docx)

Data Availability Statement

The data that support the findings of this study are available from the corresponding author upon reasonable request.

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