https://orcid.org/0000-0002-2517-2154
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Abstract
Thermotolerance acquisition is an important ecophysiological trait under global warming scenarios because it can allow organisms and populations to adapt, particularly during the most sensitive early stages of a life cycle. Here we used seasonality as a natural scenario to explore whether parental thermal histories can modulate thermotolerance of recruits of a canopy-forming intertidal seaweed (Fucus guiryi) across an ecologically relevant thermal gradient (15–28°C). For this purpose, we harvested embryos from parents after the periods of maximum and minimum accumulated heat exposure (late summer and late winter), and at the onset of summer. During early ontogeny we followed initial embryo size, internal nutrient content, survival, growth and developmental stages as performance metrics to address whether parental acclimation modulates thermal tolerance via provisioning or parental effects. Late winter recruits of F. guiryi exhibited the greatest thermotolerance, showing a broader range of optimal temperatures and higher upper thermal limits for growth and survival, probably associated with better provisioning from parental thalli. Physiological fitness of recruits decreased above 25°C, showing arrested growth, impaired development and dropping survival rates, but functional loss was more abrupt in early summer. Late summer responses confirmed that heat hardening occurs in natural populations, but at the seasonal scale the adaptive significance of this increased thermotolerance is much lower than that induced by winter parental provisioning. Heat-induced thermotolerance occurred from early to late summer due to parental exposure to warming. However, winter provisioning promoted greater thermotolerance acquisition. Exposure to moderate thermal stress at the onset of summer without prior seasonal acclimation resulted in minimum levels of thermal tolerance and loss of offspring fitness. While warmer winters might be neutral or benefit early development, increasing temperatures and poor nutritional conditions at the onset of the summer season may reduce survival and hamper population recruitment.
Highlights
Thermotolerance of Fucus guiryi increased towards the late cold season.
Early summer recruits had the lowest survival under warming.
Seasonal performance of recruits might be driven by parental environment.
Acknowledgements
This research was carried out within the European project BiodivERsA3-MARFOR (Functional Variability and Dynamics of Responses of Marine Forests to Global Change), PCIN-2016-090 (Ministerio de Economía y Competitividad, Spain) and the project PID2020-118045 GB- (Ministerio de Ciencia e Innovación, Spain). ANF was financially supported by Sistema Nacional de Garantía Juvenil y del Programa Operativo de Empleo Juvenil 2014 – 2020 (Contrato personal laboral técnico de apoyo y gestión I+D+i). We thank the Plant Culture unit of SCAI-UMA for providing culture chambers and especially Dr L. Jiménez for her technical assistance. We thank Dr A. Avilés from the Department of Ecology and Geology (UMA) for the nutrient analyses and J.L. Ferres for his help during field samplings. The authors thank C.A. Maggs, G. Pearson and two anonymous reviewers for their helpful contributions to the original manuscript.
Supplementary information
The following supplementary material is accessible via the Supplementary Content tab on the article’s online page at https://doi.org/10.1080/09670262.2022.2081731
Supplementary table S1. Length, surface area, volume and SA:V ratio of embryos of F. guiryi grown at five temperatures (15ºC, 20ºC, 23ºC, 25ºC, 28ºC) and measured at five time points (0, 4, 7, 14, 21 d) in LS and LW experiments.
Supplementary table S2. Two-way Model III ANOVA or Kruskal-Wallis ANOVA (for heteroskedastic data) results for the length, surface area, volume and surface area to volume ratio of embryos F. guiryi grown at five temperatures (15ºC, 20ºC, 23ºC, 25ºC, 28ºC) and measured at five times following embryo fertilization (0, 4, 7, 14, 21 d). Bold font highlights the statistical significance for each factor. Tukey’s HSD post hoc and pair-wise comparisons are detailed in Supplementary table S1.
Supplementary table S3. Two-way repeated measures ANOVA results for the survival and relative growth rates (RGR) of Fucus guiryi embryos grown at five temperatures (15ºC, 20ºC, 23ºC, 25ºC, 28ºC) and measured at four times following embryo fertilization (4, 7, 14, 21 d).
Supplementary table S4. Two-way permutational ANOVA (PERMANOVA) and permutational test of homogeneity of multivariate dispersions (PERMDISP) of the percent composition of embryonic developmental stages of Fucus guiryi from late summer (LS) and late winter (LW) experiments, obtained at five temperature levels (15ºC, 20ºC, 23ºC, 25ºC, 28ºC) and measured at four times (4, 7, 14, 21 d).
Supplementary fig. S1. Photomicrograph of an embryo of F. guiryi, showing the different metrics measured to calculate embryo surface area (SA) and volume (V). 1) Spherical section; 2) Zygote diameter; 3) Embryo length (without rhizoid); 4) Base of the semi cone (big radius); 5) Semi cone tip (small radius). Formulae used in the calculations are indicated.
Supplementary fig. S2. Thermal and nutrient history during the study at the location of parental thalli (Tarifa, Spain). (A) Thermal regime during summer 2018, comparing mean, minimum (Tm) and maximum (TM) temperature in air, sea surface (SST) and in situ temperature. (B). Mean daily sea surface temperature (SST), mean climatological temperature (based on the period 1982–2019) and marine heatwaves (MHW) thresholds at Tarifa (Cádiz, Spain). The region depicted in yellow indicates de occurrence of moderate MHW. (C) Mean monthly nutrient concentrations of nitrate (NO3–), ammonium (NH4+) and phosphate (PO43-) obtained from the IBI-MFC model (CMEMS-Copernicus) for the position 36°00'12.0''N 5°37'01.6''W.
Supplementary fig. S3. Survival curves of embryos of F. guiryi after 3-weeks, at different seasonal experiments. Data for early summer (ES) at 15ºC lied below late winter (LW) data. No curve was obtained for ES as discrete measurements were taken only at control (15ºC) and warming conditions (25ºC). LT50 indicate temperatures at which survival was reduced by 50%. Standard deviation error bars were omitted to gain clarity in the data. Dotted red line indicate a proportion of survival of 0.5.
Supplementary fig. S4. Micrographs of 120 days-old embryos of Fucus guiryi from the late summer experiment. At 20ºC, arrow indicates a dead embryo. At 25ºC, arrows highlight the more irregular shape of embryos and the presence of shorter rhizoids. Embryo length is indicated with blue letters.
Supplementary fig. S5. Non-metric multidimensional scaling (nMDS) ordination plots of the embryonic developmental stages of F. guiryi from two seasons (late summer: LS and late winter: LW), grown at five temperatures, analysed within each measuring time following fertilization. (A) 4 d, (B) 7 d, (C) 14 d, (D) 21 d.
Supplementary data S1. Data sheet with the raw data used in the experiments and for the multivariate analysis of seasonal thermal resilience (PCA) of embryos of Fucus guiryi from physiological control variables.
Supplementary data S2. Supplementary results on embryo morphometry.
Supplementary data S3. Supplementary methods and results to the main text on field environmental variables over the period of study (2018–2019), including detection of threshold thermal values during extreme events.
Author contributions
RSdeP, EB-E, AF-M and MG-S contributed to the conception and design of the study; RSdeP and ANF performed laboratory experiments and statistical analyses; RSdeP organized the database, designed figures and tables and wrote the first and second draft of the manuscript. All authors contributed to manuscript revision, read and approved the submitted and reviewed versions.
Disclosure Statement
No potential conflict of interest was reported by the authors.