Impacts of climate change on the developmental stages of Cystoseira hyblaea (Fucales) and its possible fate under a foreseen warming scenario

In the Mediterranean Sea, marine forests constituted by Cystoseira sensu lato (s.l.) species (Fucales, Phaeophyceae) support highly productive ecosystems, whose decline was ascribed to the interplay of several anthropogenic impacts. Recently, this decline has also been attributed to the increase of seawater temperatures and thermal anomalies, which can alter the reproductive phenology, germling growth and population viability of Cystoseira s.l. species. To manage the conservation of these communities is fundamental to evaluate how current and future foreseen warming scenarios will affect the thermal physiology of different life stages of these species. Moreover, a recognized strategy of management is the identification and protection of contemporary climatic refugia, which may safeguard the persistence of these habitat-forming species. The present research focused on Cystoseira hyblaea Giaccone, which is endemic to the Sicily Channel (Central Mediterranean Sea) and has a narrow distributional range, being only reported in Punta D’Aliga, where it was no longer found, in Cap Bon (Northern Tunisian coast) and in Portopalo di Capo Passero (Sicily, Southern Italy). This species lives in the intertidal and upper sublittoral zone on both semi-exposed and exposed rocky coasts, and its maximum vegetative and reproductive development occurs during winter. Considering the ongoing warming scenario, C. hyblaea could be severely threaten being an intertidal species and due to its cold affinity, the winter reproductive phenology and the restricted distributional range. Therefore, the aim of this study was to assess the thermal tolerance of both embryos and adults of C. hyblaea, in order to evaluate which stage might be the most vulnerable to climate change, and to foresee the possible fate and argue about the future conservation status of this species under a predicted global warming. To perform this research, egg release, zygote settlement, embryo development and adult photosynthetic efficiency were studied, on both early life stages and adults, under five temperature treatments (12, 15, 18, 24, 28 °C) in controlled mesocosms. In particular, ca. 1200 receptacles were cultivated on 6 Petri dishes per temperature treatment. At 0, 20, 44, 92 h after fertilization, 10 random subareas of 2x2 mm were examined in 3 Petri. Chlorophyll a fluorescence of adults was measured at 0, 24, 72, 120 h on 9 fronds in each of the 3 aquaria per treatment. Through the trial, it was observed that the receptacles’ release efficiency did not vary significantly among temperatures. However, the settlement efficiency of C. hyblaea increased from 12 to 18 °C and decreased at 28 °C. Indeed, the extremely low settlement efficiency was at 28 °C, due to the fact that zygotes had undergone lysis because of thermal stress. Regarding the early life stages, embryos showed a complete development only at 12 and 15 °C, while yet at 18 °C mortality increased sharply, being total at 28 °C. In particular, the highest developmental rate was observed at 15 °C (highest percentage of embryos with rhizoids already at 20 h AF), suggesting that this temperature constitutes the thermal optimum for reproduction and development of early developmental stages. On the contrary, adults of C. hyblaea showed a more plastic physiological response and thermal stress did not significantly affect photosynthetic efficiency. The present study demonstrated that adults of C. hyblaea resulted not substantially affected by heat with an expected ability to acclimatise also to elevated temperatures. Contrarily, the early developmental stages resulted strictly stenotherm, requiring a very narrow range of low temperatures for an effective recruitment and development (12-15 °C). Therefore, the recruitment could represent the most vulnerable process to the impacts of climate change in the population dynamics of C. hyblaea. Moreover, the results confirm the cold affinity of this species and suggest that the localities, in which C. hyblaea is confined, are acting as potential climatic refugia. If failure in the recruitment process is reiterated for several years, it will lead to an impoverishment of C. hyblaea populations, ultimately hindering their long-term viability in its current range. Given the fragmented and restricted range and increased frequency of extreme climatic events, C. hyblaea may undergo local extinction. Considering this perspective, the areas in which C. hyblaea manages to survive should receive a higher level of protection. Moreover, this species should be included in the IUCN Red List of Species (IUCN, 2021), being classified as a “Critically endangered” or “Rare”.