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Article

A Physiological Analysis of Desiccation Stress in the Green Tide Species Ulva stenophylloides and Ulva uncialis in the South Pacific

by
Javiera Mutizabal-Aros
1,2,3,4,
Andrés Meynard
1,2,3,4 and
Loretto Contreras-Porcia
1,2,3,4,*
1
Departamento de Ecología y Biodiversidad, Facultad de Ciencias de la Vida, Universidad Andres Bello, Santiago 8370251, Chile
2
Centro de Investigación Marina Quintay (CIMARQ), Facultad de Ciencias de la Vida, Universidad Andres Bello, Quintay 2531015, Chile
3
Instituto Milenio en Socio-Ecología Costera (SECOS), Santiago 8370251, Chile
4
Center of Applied Ecology and Sustainability (CAPES), Santiago 8331150, Chile
*
Author to whom correspondence should be addressed.
J. Mar. Sci. Eng. 2024, 12(11), 1893; https://doi.org/10.3390/jmse12111893
Submission received: 13 September 2024 / Revised: 17 October 2024 / Accepted: 18 October 2024 / Published: 22 October 2024
(This article belongs to the Section Marine Ecology)

Abstract

:
Global green tide blooms of the Ulva genus have been increasing due to human activities, with mass accumulation in Algarrobo Bay, Chile, causing ecological and social issues. In this area, five Ulva species were previously identified, with Ulva stenophylloides dominating across seasons and intertidal zones; Ulva uncialis was the second most abundant, mainly in winter. In this study, we tested the hypothesis that U. stenophylloides is more tolerant to desiccation than U. uncialis, explaining its dominance in the upper intertidal zone. Based on in vitro cultures, we assessed the impact of desiccation stress on weight, blade length, cellular activity, and lipoperoxide levels. In U. uncialis, desiccation treatment caused a decrease in weight; conversely, in U. stenophylloides, both control and desiccation treatments caused a slight decrease in weight. No significant differences (p > 0.05) in blade length or lipoperoxide levels as a function of culture time were detected in the control and desiccation treatment groups for both species. Furthermore, desiccation had no negative effects on the cellular activity of either species. Although the observed weight changes suggest that U. uncialis is more desiccation-tolerant than U. stenophylloides under the experimental conditions, the cellular activity and lipoperoxidation indicate high desiccation tolerance in both species, which partly explains their intertidal dominance.

1. Introduction

Algae living in the upper littoral zone undergo extreme stress due to intense and regular shifts in physicochemical factors with changing tides. These factors include salinity, desiccation, solar irradiance, and temperature [1,2]. Some representatives of the intertidal macroalgae Porphyra (Rhodophyta) and Ulva (Chlorophyta) are among the most desiccation-tolerant species, on the same level as resurrection plants [3,4,5]. Nonetheless, because they inhabit different tidal levels (or bathymetric positions) and a variety of different microhabitats, desiccation stress tolerance is likely to vary among species within these two genera.
In the case of Ulva species, desiccation tolerance probably constitutes an important axis of niche specialization regulating the distribution of members of these species across tidal levels and among intertidal microhabitats. This has been previously demonstrated in seaweed species of the upper, middle, and low intertidal zones regarding, for example, the strong relationship between differential photosynthetic and respiratory performances under desiccation stress and the vertical distribution of these species in the intertidal zone [6,7]. Nonetheless, few studies have been conducted on the relationship between intertidal distribution and stress tolerance physiological mechanisms in Ulva species, except for those focusing on photosynthetic parameters [8], antheraxanthin and zeaxanthin accumulation and protective functions [4], and nitrogen assimilation under desiccation [9]. In fact, it has been previously demonstrated that the more desiccation-tolerant Ulva lactuca, living higher in the intertidal zone, recovered better after a period of constant aerial exposure than the more sensitive mid-intertidal Ulvaria obscura because it maintained its photosynthetic integrity during desiccation [10].
In both desiccation- and salinity-tolerant macroalgal species thriving in the high intertidal zone, it has been demonstrated that a cyclic electron flow mechanism at crucial sites in the photosynthetic apparatus allows them to avoid the photodamage resulting from chronic photoinhibition caused by the accumulation of high ROS levels observed in other more stress-sensitive species [11]. The operation of this PSI-driven cyclic electron flow during severe desiccation (instead of PSII-driven linear electron transport, which is inhibited because of stress) is favored through an increase in amylase activity, starch degradation, and, consequently, NADPH accumulation, providing electrons for PSI [12,13]. Moreover, research on Ulva prolifera has established that NADPH production provides electrons for PSI through starch degradation and allows for the synthesis of excess total RNA, enabling recovery from salt stress [14]. In a similar manner, the intermediate desiccation-tolerant species Ulva compressa has evolved an inner pectin-rich cell wall layer that plasticizes its wall and enables this species to withstand desiccation during emersion and recover after rehydration during the submersion phase of the tidal cycle [15]. Nonetheless, this study also showed that, after a 30 min desiccation period, corresponding to an RWC (relative water content) of 73%, U. compressa displayed a significant decrease in the maximum quantum yield of photosystem II (Fv/Fm) but fully recovered during rehydration. Finally, one of the few studies evaluating antioxidant enzyme capacity in Ulva species under desiccation [16] showed increased peroxidase activity in Ulva lactuca specimens from the high intertidal zone compared with individuals from lower intertidal zones.
Research indicates that different genera or species have various capacities to tolerate desiccation stress, resulting in different degrees of ecological specialization. A study of five macroalgae species on a Chilean rocky shore found that Mazzaella laminaroides and Scytosiphon lomentaria, which are upper mid-littoral and mid-intertidal species, respectively, showed a high antioxidant capacity and were able to fully recover from air-induced desiccation stress, including the recuperation of their cellular structure and a return to basal levels of hydrogen peroxide and oxidized biomolecules [17]. Conversely, the other three species from the mid- and low intertidal zones, including Ulva compressa, were unable to repair the damage caused by the desiccation phase, showing no recovery in photosynthetic efficiency or in the fine structure of the cell, as well as no reduction in the oxidation of their biomolecules [17]. However, it is the capacity of algae to both physiologically cope with and rapidly recover from desiccation stress during emersion/immersion tidal cycles rather than the capacity to retain water that determines their vertical distribution [1,17].
A succession of Ulva species across the seasons was previously verified at several sites in the Yellow Sea during the green tides observed in 2009, with U. compressa being the first to appear, followed by U. flexuosa, U. linza, and, finally, U. prolifera. A clear pattern of succession of Ulva species has also been observed in the green tides that persist almost year-round over the past 20 years at Los Tubos Beach in Algarrobo Bay along the central Chilean coast and in Hiroshima Bay, Japan [18,19,20]. At Los Tubos Beach in Algarrobo Bay, at least five Ulva species were identified through morphological and phylogenetic analyses: Ulva aragoensis, Ulva compressa, Ulva australis, Ulva uncialis, and Ulva stenophylloides [20]. For the species U. aragoensis, U. uncialis, and U. stenophylloides, this was the first registration in Chile. U. stenophylloides has only been previously recorded in Australia, New Zealand, and South Africa. U. uncialis has been previously recorded in Africa, the Indian Ocean Islands, and the Middle East. U. aragoensis is widely distributed [21].
Our previous study at Los Tubos Beach revealed that U. stenophylloides displayed the highest relative coverage year-round and in all intertidal zones. U. uncialis occupied second place in terms of coverage and was more abundant, mostly in the winter season [20]. Because U. stenophylloides dominated in the high intertidal zone across the seasons at Los Tubos Beach, except for in winter when it had a similar but higher coverage than U. uncialis, we initially hypothesized that the former is more desiccation-tolerant than the latter. Few studies have focused specifically on the relationship between intertidal distribution and desiccation stress in species of the genus Ulva. Accordingly, in this study, it was proposed that a differential tolerance to desiccation stress between these two species would explain their distribution in the intertidal zone. Thus, the aim of this work was to evaluate in vitro the influence of desiccation stress on the cellular viability, lipid oxidation (lipoperoxidation), and specific growth rate responses of U. stenophylloides and U. uncialis from Los Tubos Beach in Algarrobo Bay.

2. Materials and Methods

2.1. Seaweed Collection and Environmental Parameter Measurements

U. stenophylloides and U. uncialis adult individuals were collected during the autumn season of 2023 along the rocky intertidal zone at Los Tubos Beach, Algarrobo Bay, Chile (33°21′53.79″ S 71°40′46.30″ W), at a low tide (Figure 1). The air temperature and irradiance were determined along the intertidal zone by using a portable thermometer (HT-822 IR Thermometer, Alphaomega Electronics, Maranata, Spain) and a quantum meter (MQ-200 Apogee Instruments, Logan, UT, USA), respectively.
Seventy-eight individuals of each species were collected and transported to the laboratory in a cooler with frozen ice packs at 5–7 °C. Then, in the laboratory, the samples were cleaned of epiphytes and grazers using a paintbrush and 1 μm filtered seawater.
In previous studies in Algarrobo Bay [20], Ulva stenophylloides were observed to dominate all intertidal zones in all seasons; however, in this case, specimens were collected in the high intertidal zone. Conversely, Ulva uncialis showed the highest coverage in winter, with its coverage being less than 10% in spring and summer, and it was almost absent in autumn. However, this species was mainly observed in the middle and low intertidal zones; thus, in this case, specimens were collected in the middle–low zones.

2.2. Species Identification for Sample Selection

The Ulva samples were examined using an external morphological analysis to classify them at the species level, as per the morphological keys [20]. The matching between the morphological and phylogenetic identification of Ulva species thriving at the same study site was performed in 2022, with no major changes in ecological or climatic conditions across these two years. The morphologies of the species, at least during this specific period and location, did not change significantly. The two dominant species showed unique morphological and microhabitat differences; U. uncialis had thicker, stronger blades than U. stenophylloides, which had softer tissue and less stretch resistance, among other distinct traits.

2.3. Experimental Design

To understand the differential effects of desiccation on the growth rate, lipid peroxidation levels, and cell viability of U. stenophylloides and U. uncialis, two experimental sets (with and without desiccation) were established. Individuals were cultivated in vitro under controlled conditions of light (30–50 µm photon m−2 s−1 irradiance), photoperiod (12:12 light–dark cycle), and temperature (15–17 °C) for 10 days. The control group (non-desiccated algae) was cultivated under constant water immersion, whereas the desiccation group was subjected to a daily 4 h desiccation regime, where the individuals were removed from seawater containers and exposed to air at 18–20 °C and 70–80 µm photon m−2 s−1 irradiance, following the methodology described in [3]. This 4 h desiccation period mimics the daytime low tide that the plants experience in their natural habitat [2,3,5,17].
For the growth rate experiment, 3 experimental units for the control and 3 for the desiccation treatment were established per species, with each experimental unit containing 3 individuals. For the lipid peroxidation levels and cellular viability experiments, 3 experimental units (6.5 L plastic container) for the control and 3 for the desiccation treatment were established per species, with each experimental unit containing 5 individuals or pseudoreplicates. Each experimental unit consisted of a 6.5 L container filled with 3 L (growth rate experiment) or 5 L (lipid peroxidation levels and cellular viability experiments) of 1 μm filtered seawater. During the 10-day culture period, the experiments were maintained under constant aeration and with a daily renewal of 50% of the seawater. Blades about 10–14 cm in length were selected for cultivation, and the initial density per treatment was about 6–11 g L−1 (wet weight) due to high variability among individuals and species.

2.4. Influence of Desiccation on Specific Growth Rate

The weight of the whole individual and the length of the longest blade of each individual in the experimental units were estimated at 2-day intervals. Only the length of the longest blade was considered because the algae of both species had a high number of blades, and due to their cabbage-shaped morphology, the blades had a whorled arrangement. Images of the longest blades were taken daily, with a 20 cm ruler used as a size reference, and the length of each blade was estimated from the tip down to the base, where it met the holdfast, using ImageJ© software version 1.54k [22]. Concerning the weighing method, individuals were removed from the seawater in the experimental units, dried using paper towels, weighed using a Kerner ADB 200-4 (0.0001 g) analytical balance (Balingen, Germany), and returned to their original unit with seawater.

2.5. Influence of Desiccation on Lipid Peroxidation

The lipid peroxidation (or lipoperoxides) concentration, as a means of determining cellular damage, was ascertained at 2-day intervals (during the 10-day experiment) through thiobarbituric acid reactive species (TBARS) using 1 g of fresh algal tissue and the steps described in [23].

2.6. Influence of Desiccation on Cell Viability

After the 10-day culture period, the cell viability of the desiccated and control algae was estimated using an MTT (3-[4,5-dimethylthiazol-2yl]-2,5-diphenyltetrazolium bromide) assay by quantifying the reduction in this reagent to formazan by metabolically active cells (Sigma Aldrich, Burlington, MA, USA). For this purpose, 1 cm2 of the algal blade was cut, and the steps described in [5] from the modified protocol of [24] were followed. More specifically, the algal tissue was submerged in 2 mL of 1.25 mM MTT and 3% NaCl in a 50 mM phosphate buffer (pH 7.4) and maintained for 20 h in the darkness without shaking. Then, 8 mL of 95% ethanol was combined with the mix, and the samples were incubated in boiling water for 20 min to extract the formazan product, which was then measured via spectrophotometry at 570 nm (UV–VIS spectrophotometer RB-10, Dynamica, Salzburg, Austria).

2.7. Data Analyses

Statistical differences between groups and the influence of time on the experimental variables were evaluated using the Kruskal–Wallis or ANOVA test using R Studio Software (Version 2023.12.0+353). Bartlett and Shapiro–Wilk tests were used to check the homogeneity of variance and normality assumptions, respectively. For a variance analysis of the growth rate, repeated-measures ANOVAs testing the effects of time (days) and treatment (desiccation or control) on algal weight and blade length over the 10 days of cultivation were performed for each species—Ulva uncialis and Ulva stenophylloides—independently. For a variance analysis of the treatment group and culture time and their effects on cellular viability (MTT assay) and lipoperoxide concentration, a repeated-measures two-way ANOVA was estimated. Linear regression analyses were also performed between the algal weight (or the length of the longest blade) and culture time (days) in both Ulva species in order to infer the strength of their relationship.

3. Results

3.1. Environmental Parameters at the Sampling Site

The average air temperature was 32 °C in the high intertidal zone, 24 °C in the middle intertidal zone, and 23 °C in the low intertidal zone. Furthermore, the average irradiance was 1383 µm photon m−2 s−1 in the high intertidal zone, 1418 µm photon m−2 s−1 irradiance in the middle zone, and 1050 µm photon m−2 s−1 irradiance in the low intertidal zone.

3.2. Influence of Desiccation on the Average Algal Weight

In terms of U. stenophylloides, the simple linear regressions revealed that both the control (F1,52 = 5.42; p = 0.02383) and desiccation treatment groups (F1,52 = 14.87; p = 0.0003193) displayed a significant decreasing tendency (negatives slopes of −0.1 and −0.2, respectively) and stabilized at a weight of approximately 4 and 3.1 g from day 4 onwards, respectively (Table 1 and Figure 2a). In U. uncialis, it was observed that, from day 4 onwards, the average weight of the desiccation treatment group was always lower than that of the control group, but the variance around the average was greater than that observed in U. stenophylloides (Figure 2b). Nonetheless, as revealed by the linear regression analyses (Table 1), the time evolution of the daily weight gain or loss of U. uncialis in the desiccation treatment group showed a significant decreasing tendency (negative slope of −0.17) (F1,52 = 13.11; p = 0.0006672) (i.e., from 6.9 to 5.2 g), and no weight change over time was observed in the control group (F1,52 = 0.0002951; p = 0.9864) (i.e., around 6.7 g). As revealed by the independent repeated-measures ANOVAs testing the effects of time (days) and treatment (desiccation or control) on algal weight, only treatment was significant in U. uncialis, whereas both treatment and time were significant in U. stenophylloides (Table 2). This study shows that the weight of both algal species was consistently lower under the desiccation than under the control treatment, with U. incialis showing a more distinct pattern than U. stenophylloides.

3.3. Influence of Desiccation on the Average Blade Length

As revealed by the linear regression analysis (Table 3), no significant difference in the response variable blade length as a function of culture time (over the 10 days of culture) was detected in the control and desiccation treatment groups for both Ulva species; nonetheless, the slopes of the control groups were 0.28 and 0.13, reflecting an average increase of 2.55 cm and 1.14 cm in U. uncialis and U. stenophylloides, respectively (Table 3) (Figure 3). On the contrary, the slopes of the desiccation treatment groups were 0.08 and −0.05, reflecting an average slight increase of 0.72 cm and an average decrease of −0.95 cm in U. uncialis and U. stenophylloides, respectively. Moreover, as revealed by the independent (for each species) repeated-measures ANOVAs for the effects of time (days) and treatment (desiccation or control) on blade length, only treatment was significant in both U. stenophylloides and U. uncialis, whereas time and the interaction were not significant (Table 2). It is worth mentioning that a high variance was observed in the blade length data within the groups, especially in U. uncialis.

3.4. Influence of Desiccation on Cellular Viability Based on the MTT Assay

After the 10-day culture period, no significant difference in cellular viability was observed between the desiccation and control groups for both U. stenophylloides (repeated-measures ANOVA, F = 0.411; p = 0.536) (Figure 4a) and U. uncialis (repeated-measures ANOVA, F = 0.271; p = 0.608) (Figure 4b). Nonetheless, in terms of U. stenophylloides, a clear increase in cellular viability as a function of culture time was detected in both the control (F1,52 = 18.85; p = 0.0007997) and desiccation treatment groups (F1,52 = 17.82; p = 0.000999) (Table 4) (Figure 4a), as revealed by the linear regression analysis. On the contrary, in U. uncialis, cellular viability remained relatively constant over the 10-day culture period, fluctuating around an average value (Figure 4b).

3.5. Influence of Desiccation on Lipid Peroxidation Levels

After the 10-day culture period, no significant difference in the lipid peroxidation concentration was observed between the desiccation and control groups for both U. stenophylloides (repeated-measures ANOVA, F = 0.127; p = 0.723) (Figure 5a) and U. uncialis (repeated-measures ANOVA, F = 0.090; p = 0.767) (Figure 5b). As revealed by the linear regression analysis (Table 5), no increase in lipid peroxidation concentration as a function of culture time (over the 10 days of culture) was detected in the control or desiccation treatment groups for both species.

4. Discussion

After 10 days of culture, the average plant weight in the desiccation treatment was lower than that in the control groups for both species. However, no significant differences in the response variable blade length as a function of culture time (over the 10 days of culture) were detected in the control and desiccation treatment for both species. In both treatments, the cellular viability of U. stenophylloides increased over time, while that of U. uncialis remained constant. Moreover, minimal cellular damage in terms of lipoperoxidation was observed in both species, indicating a high tolerance to desiccation stress. The lack of significant differences of these two Ulva species in terms of MTT reduction and lipoperoxidation levels suggests that they both have high metabolic and antioxidant capacities to withstand desiccation stress.
Desiccation during low tidal emersion significantly impacts the photosynthetic rate of intertidal algae, with the severity of the decline depending on the species’ desiccation tolerance [3,4,9,10,25]. Desiccation also leads to various morphological and physiological changes, such as an increased production of reactive oxygen species (ROS), which can cause damage to biological molecules if not properly managed [26]. Certain species, such as the red algae Gracilaria corticata on India’s Veraval Coast and the desiccation-tolerant Pyropia orbicularis on Chile’s central coast, have enzymatic and non-enzymatic mechanisms to counteract desiccation stress [3,7]. These mechanisms are activated during the desiccation and rehydration phases to prevent cellular damage. Conversely, species such as U. compressa and Lessonia spicata, found in mid- and low-intertidal areas, struggle to recover from desiccation damage, showing higher lipoperoxide and carbonyl contents than during hydration [17].
In the present study, we found no significant differences in the MTT reduction and lipid peroxidation levels between the desiccation and control groups; this suggests that both U. stenophylloides and U. uncialis are highly tolerant to desiccation stress. More importantly, this also suggests that, similarly to other macroalgae that survive in the high intertidal zone, these two Ulva species have efficient antioxidant machinery to cope with desiccation, as opposed to low intertidal algae, which are severely damaged under desiccation stress [5,17]. Therefore, they likely have enzymatic and non-enzymatic mechanisms to mitigate the damage from ROS production and the other physiological and morphological changes caused by this stress. In fact, the absence of damage in high desiccation stress-tolerant Pyropia orbicularis was accompanied by a significant increase in the activity of several antioxidant enzymes during the desiccation phase compared with during the hydrated and rehydrated phases [3], which warrants further research in U. stenophylloides and U. uncialis. Thus, further studies are needed regarding antioxidant enzyme activity and the levels of antioxidant metabolites produced under desiccation stress, which may help to confirm the high but differential desiccation tolerances of both Ulva species.
Regarding the poor growth rates of both Ulva species in this research, the first hypothesis is that the filtered seawater used in the experiments may have lacked sufficient nutrients. For example, N and P limitation decreased the growth rate, photosynthetic rate, nitrate reductase activity, and soluble protein content in U. linza [27], and this could explain the limited growth rates of U. uncialis and U. stenophylloides. Indeed, it is highly recommended to supplement the culture medium with standard nutrient salts [28]. Nevertheless, during the 10-day culture period, the experiments were maintained with a daily renewal of 50% of the seawater. Alternatively, the limited growth rate could imply that the acclimation period was insufficient. This is consistent with the fact that plant weight stabilized only on day 4 (Figure 2) and that a sharp increase in MTT reduction was observed from days 2 to 4, especially in U. stenophylloides.
Although we cannot rule out that the effects of desiccation may have been partially masked by those of other stresses, such as nutrient scarcity, both plant weight and blade length showed a trend in lower values in the desiccation than in the control treatment during the culture period for both algae. Stress factors other than desiccation can exacerbate lipid oxidation and decrease MTT reduction in desiccation-sensitive species. However, the two Ulva species showed the contrary, displaying tolerance to oxidative stress, with no lipid oxidation and a consistent or even rising MTT reduction. Additionally, if an unexpected stress factor besides desiccation had an additive harmful effect on growth but not on desiccation tolerance capacity, one can postulate that this hypothesis would explain the poor growth rates of both Ulva species. In this case, this additional and uncontrolled factor may have had a greater effect on the growth rate of U. stenophylloides than on that of U. uncialis. Indeed, the authors of [29] demonstrated that the net photosynthetic rate of U. prolifera increased at a lower salinity; counterintuitively, they found that this was not accompanied by increased growth, as is usually the case in plants. Instead, they suggested that some of the energy produced by the increase in photosynthesis was employed to resist the osmotic pressure caused by the lower salinity. Thus, a similar compensatory mechanism may explain why our experiments showed an inverse trend (or a trade-off) between increased MTT reduction (or cell viability) and a limited growth rate, assuming that an unexpected stress factor besides desiccation had an additive harmful effect, on the fitness of these two Ulva species.
Another factor that could have influenced the poor increase in plant weight and blade length observed in the two Ulva species in our experiments is the initial size of the algae selected, as it has been previously shown in in vitro culture experiments with green tide algae from the Yellow Sea that the specific growth rate gradually decreases with an increase in blade length [30]. Indeed, we lack data that would allow us to determine whether our selection was biased towards adult individuals with extreme maximum intrinsic sizes in the populations of Ulva species from Algarrobo Bay. Therefore, future studies should determine the initial growth rates of U. uncialis and U. stenophylloides by selecting a broader range of initial blade lengths and weights in order to more precisely establish the influence of desiccation stress on growth patterns. Nonetheless, it is worth mentioning that the latter was not possible due to high variability in the weights and sizes of the algal individuals in the field, as well as the logistical and environmental complexities of sampling on the very exposed rocky shores of the coast of Chile. Future studies should be based on the culture of seedlings grown from spores [30]. Additionally, for the same objective, future research on the growth patterns of these two Ulva species from Algarrobo should include sets of experiments comparing algae grown in seawater with and without the addition of a nutrient solution and incorporating the measurement and assessment of growth under a wider array of pH, temperature, and irradiance experimental conditions.
Regarding the distribution of the two examined Ulva species in the intertidal zone and across seasons in Algarrobo Bay, we drew the following conclusions: as shown in previous studies conducted in the Yellow Sea on the molecular identification of the main taxa forming green algal blooms [30], a seasonal succession of several Ulva species occurs in this region. Similarly, in a previous study, we established that U. stenophylloides dominated at Los Tubos Beach in Algarrobo Bay and showed the highest relative cover throughout nearly all seasons and intertidal zones during the 2020–2022 period; the second most abundant Ulva species that also constituted the green blooms in this area was U. uncialis [20]. Nonetheless, this study also demonstrated that, throughout the seasons, the relative coverage of U. stenophylloides was consistently lower in the high intertidal zone than in the medium and low intertidal zones, which is probably also the case for other Ulva species. On the contrary, U. uncialis had the highest abundance in winter and was almost absent in spring and autumn, thus showing a seasonal trend in occurrence; most importantly, U. uncialis did not display significant differences in relative coverage across intertidal zones in winter. Therefore, the high abundance and high desiccation tolerance of both U. stenophylloides and U. uncialis in winter are probably features common to marine organisms that are able to survive in the high intertidal zone, a very harsh environment for non-terrestrial organisms. Consequently, this study suggests that, compared with U. uncialis, U. stenophylloides has a wider tolerance to other abiotic conditions (aside from desiccation stress) that also characterize this environment and are prevalent in other seasons. The experimental laboratory conditions of the present study probably correspond more to the environmental conditions that prevail in the winter season at Los Tubos Beach in Algarrobo Bay, when U. uncialis is highly abundant in the intertidal zone. Therefore, for a better assessment and comparison of the relative desiccation tolerance levels and growth rates of these and other Ulva species, a wider array of experimental conditions should be considered, for example, higher light irradiances and temperatures, which are prevalent during the other seasons.
Besides the dependence on a great capacity to tolerate desiccation stress, the differential distributions of U. stenophylloides and U. uncialis (and other Ulva spp.) in the intertidal zone in Algarrobo Bay and throughout the seasons may also be explained by their segregation along other niche axes, especially by the interaction between their desiccation stress tolerance and physiological tolerance ranges to other abiotic stresses (e.g., temperature and light intensity), nutrient uptake capacities [18,30,31], or plant protection mechanisms against predators. In fact, data on the irradiance, temperature, and relative humidity at Los Tubos Beach in the summer season of 2023 revealed a trend in increasing irradiance and temperature and decreasing relative humidity from the low to high intertidal zones. Another niche component likely explaining the distributional patterns of Ulva species, which has been generally neglected, is their differential capacity to overwinter outside the intertidal habitat; for example, viable and abundant U. prolifera individuals have been found in Yellow Sea sediments, where their somatic cells serve as an overwintering stage capable of regenerating during their spring bloom [32,33]. Here, an important concept is the term “micropropagules”, which is equivalent to “seed banks” in terrestrial ecosystems, corresponding to algal tissue or microscopic stages (generative cells) able to grow and develop into whole plants and survive under harsh conditions in a dormant state, thus playing an important role in the recovery of algal populations [34]. This is particularly important when taking into consideration the fact that Ulva species, such as U. prolifera, possess multiple modes of proliferation [34]. Nonetheless, more recent studies suggest that the micropropagules of U. prolifera are unable to tolerate the high temperatures at the beginning of summer and probably perish due to rapid decomposition and dissipation when beached, therefore not contributing to the seeding of the next year’s bloom. In the case of this species, it has been suggested that their micropropagules overwinter in small numbers in sediments, attaching to the Neopyropia yesoenzis raft in early summer; develop into whole adult plants that subsequently release generative cells; or transform into algal segments that contribute to the micropropagule pool [34]. On the contrary, other micropropagules of high-temperature species, such as U. meridionalis, are able to overwinter in large numbers [35]. This last study also suggests that most micropropagules of Ulva species lay in the surface waters and, in a lower proportion, in sediments near the coast. Therefore, to better characterize the various levels of desiccation tolerance among Ulva species in Algarrobo Bay, future research should consider tolerance ranges to other abiotic stresses and broader spatial scales. In particular, future studies should include other habitats beyond the intertidal zone and, in the sampling design, consider floating algae and micropropagules settled in marine sediments or present in surface waters; additionally, they should study the different intrinsic modes of proliferation of Ulva species.
The distribution of the two examined Ulva species in the intertidal zone and across the seasons in Algarrobo Bay is likely to be strongly correlated with their differential degree of ecological specialization to several abiotic and biotic factors. Contrary to the more generalist U. stenophylloides in Algarrobo Bay, U. prolifera, the main species that causes large-scale green tides along the coasts of Shandong and Jiangsu provinces in China during summer, is probably more adapted and specialized to stress tolerance ranges closer to the maximum limits of certain abiotic variables than any other Ulva species in the Yellow Sea. In fact, U. prolifera has been shown to have better tolerance to high temperatures and light intensities, which prevail during the summer, than the other three Ulva species that flourish during the other seasons and that occur mainly during the early stages of such green algal blooms [30]. This would explain why U. prolifera serves as the dominant species that generally prevails, and that occurs last in the succession of floating rafts (including Pyropia yezoensis aquaculture rafts) and Ulva species that form the green algal blooms in the Yellow Sea. On the contrary, U. compressa, which has an optimal growth temperature of 10 °C [36], was the first to occur (i.e., during winter) in the succession of algae that constituted the green blooms in 2009 in this region. At Los Tubos Beach in Algarrobo Bay, a similar pattern of specialization to a low optimal growth temperature or low irradiance probably occurs in U. uncialis and likely explains its high abundance during winter. This, or the restricted tolerance to other abiotic factors, possibly accounts for why the coverage of U. uncialis was the highest in winter, unlike U. stenophylloides, which occurred throughout all seasons in Algarrobo Bay and is thus probably a generalist species regarding several ecological niche axes.
Finally, the necessity to mitigate the damaging consequences of desiccation and other stresses represents a cost in terms of fitness, and it points to the importance of considering the trade-offs between physiological traits when predicting the organismal response to desiccation stress, growth rates, and/or their distributions on the coast. The authors of [24] found a positive correlation between the cellular viability and specific growth rate of Ulva fasciata, with both increasing towards optimal salinity and decreasing at high or low salinity tolerance extremes. However, our study found no such positive relationship in U. uncialis or U. stenophyloides, indicating that a trade-off exists between stress tolerance to an unexpected stress factor (besides desiccation) and growth; this is probably because nutrient conditions were suboptimal or the acclimation period was insufficient. Indeed, the cellular viability of these species remained high or even improved during the culture period, with no significant increase or difference in the lipid peroxidation concentration between the desiccation and control groups. Thus, despite the poor growth rates after the 10 days of culture, both species maintained high cellular viability and repaired the oxidative damage to their lipids under desiccation stress, indicating a high survival capability under the heterogeneity of abiotic conditions. Therefore, this work suggests that there is probably a fitness trade-off in these two Ulva species, that is, between the ability to counteract desiccation damage and maintain high growth rates under nutrient-limited conditions. This trade-off is species-specific and varies based on factors such as adaptation levels for performance under different nutrient conditions (e.g., in yeasts [37]). For instance, under nutrient-poor conditions, both Ulva species may experience reduced photosynthesis and therefore have less energy for growth [38].
The high MTT reduction levels and low lipoperoxidation in both the control and desiccated algae could be linked to the PSI-driven cyclic electron flow that occurs under stress conditions such as desiccation or salt stress [13], among other alternative metabolic pathways. This process, involving an increase in amylase activity and NADPH accumulation, helps avoid the damage caused by ROS production [13,14]. However, under stress and the concomitant reduction in the photosynthetic rate, some crop plants adapt by inducing alternative metabolic pathways to produce energy; this energy is mainly reallocated to defense and tolerance mechanisms in order to overcome the excessive production of reactive oxygen species (ROS) and the oxidation of biomolecules [14]. In fact, studies on plant mitochondrial responses to salinity and other stresses have revealed adaptative metabolic responses allowing for respiration to generate sufficient energy to cope with stress effects. For example, alternative respiratory pathways and shunts (e.g., the oxidative pentose pathway and the GABA shunt) enable the induction of metabolites in crop plants and Ulva [14,39,40]. Regarding the mechanisms of the latter, we should add the activation of PSI-driven electron flow and its role in preventing damage to the photosynthetic apparatus and even the production of ATP during desiccation, as previously mentioned [11]. Therefore, the main implication of these previous studies and our study in terms of tolerance to desiccation and other stress factors is that Ulva species have an outstanding capacity to thrive in extreme environments, evolve alternative metabolic mechanisms, and cope with stress.

5. Conclusions

The results of this study suggest that both green tide Ulva species from Los Tubos Beach, Algarrobo Bay—U. stenophylloides and U. uncialis—have strong antioxidant capacities and potential mechanisms to tolerate desiccation stress. However, the observed plant weight changes suggest that U. uncialis is more desiccation-tolerant than U. stenophylloides under the experimental conditions; nonetheless, these conditions possibly reflect abiotic conditions more akin to the winter environment than the summer (or spring) environment at Los Tubos Beach. Future research should assess desiccation stress tolerance by including more desiccation-sensitive Ulva species and a wider array of experimental conditions. Future studies should also examine the activity of antioxidant enzymes and the induction of antioxidant metabolites. High variances in algal weight and potentially nutrient-limited culture conditions hindered a more accurate comparison of tolerance capacities between the two species; thus, further research under nutrient-rich conditions and with longer periods of acclimation is required to exclude the potential effects of nutrient limitation on observed growth patterns and ensure adaptation to laboratory conditions. Species such as U. stenophylloides and U. uncialis serve as valuable models for studying alternative respiratory and photosynthetic pathways, as well as the induction of metabolites that enable them to withstand stress and protect their photosynthetic centers in extreme environments such as the high intertidal zone. Moreover, like other studies conducted on green tide Ulva species in the Yellow Sea, further investigation into tolerance limits for various abiotic stresses, nutrient uptake capacities, and their interactions is essential to obtain a better understanding of the spatial and temporal population variability and biology of the green tide Ulva species in Chile. This will help to determine the relative degrees of ecological specialization among these species and enhance the understanding of their ubiquity or restriction in the intertidal zone and microenvironments.

Author Contributions

Conceptualization, L.C.-P. and A.M.; methodology, J.M.-A., L.C.-P. and A.M.; software, J.M.-A. and A.M.; validation, L.C.-P. and A.M.; formal analysis, J.M.-A., L.C.-P. and A.M.; investigation, J.M.-A., L.C.-P. and A.M.; resources, L.C.-P., data curation, J.M.-A., L.C.-P. and A.M.; writing—original draft preparation, J.M.-A., L.C.-P. and A.M.; writing—review and editing, L.C.-P. and A.M.; visualization, J.M.-A., L.C.-P. and A.M.; supervision, L.C.-P. and A.M.; project administration, L.C.-P.; funding acquisition, L.C.-P. All authors have read and agreed to the published version of the manuscript.

Funding

This work was supported by ANID—Millennium Science Initiative Program—ICN2019_015 ICM-ANID and ANID PIA/BASAL FB0002. We thank the anonymous reviewers for their insightful and constructive comments.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

The data presented in this study are available within the article.

Conflicts of Interest

The authors declare no conflicts of interest.

References

  1. Kumar, M.; Kumari, P.; Reddy, C.R.K.; Jha, B. Salinity and desiccation induced oxidative stress acclimation in seaweeds. Adv. Bot. Res. 2014, 71, 91–123. [Google Scholar]
  2. Contreras-Porcia, L.; Meynard, A.; Piña, F.; Kumar, M.; Lovazzano, C.; Núñez, A.; Flores-Molina, M.R. Desiccation stress tolerance in Porphyra and Pyropia species: A latitudinal analysis along the Chilean coast. Plants 2023, 12, 12. [Google Scholar] [CrossRef] [PubMed]
  3. Contreras-Porcia, L.; Thomas, D.; Flores, V.; Correa, J.A. Tolerance to oxidative stress induced by desiccation in Porphyra columbina (Bangiales, Rhodophyta). J. Exp. Bot. 2011, 62, 1815–1829. [Google Scholar] [CrossRef]
  4. Xie, X.; Gao, S.; Gu, W.; Pan, G.; Wang, G. Desiccation induces accumulations of antheraxanthin and zeaxanthin in intertidal macro-alga Ulva pertusa (Chlorophyta). PLoS ONE 2013, 8, e72929. [Google Scholar] [CrossRef]
  5. Guajardo, E.; Correa, J.A.; Contreras-Porcia, L. Role of abscisic acid (ABA) in activating antioxidant tolerance responses to desiccation stress in intertidal seaweed species. Planta 2016, 243, 767–781. [Google Scholar] [CrossRef]
  6. Ji, Y.; Gao, K.; Tanaka, J. Photosynthetic recovery of desiccated intertidal seaweeds after rehydration. Prog. Nat. Sci. 2005, 15, 689–693. [Google Scholar]
  7. Kumar, M.; Gupta, V.; Trivedi, N.; Kumari, P.; Bijo, A.J.; Reddy, C.R.K.; Jha, B. Desiccation induced oxidative stress and its biochemical responses in intertidal red alga Gracilaria corticata (Gracilariales, Rhodophyta). Environ. Exp. Bot. 2011, 72, 194–201. [Google Scholar] [CrossRef]
  8. Papathanasiou, V.; Kariofillidou, G.; Malea, P.; Orfanidis, S. Effects of air exposure on desiccation and photosynthetic performance of Cymodocea nodosa with and without epiphytes and Ulva rigida in comparison, under laboratory conditions. Mar. Environ. Res. 2020, 158, 104948. [Google Scholar] [CrossRef] [PubMed]
  9. Xu, D.; Zhang, X.; Wang, Y.; Fan, X.; Miao, Y.; Ye, N.; Zhuang, Z. Responses of photosynthesis and nitrogen assimilation in the green-tide macroalga Ulva prolifera to desiccation. Mar. Biol. 2016, 163, 9. [Google Scholar] [CrossRef]
  10. Nelson, T.A.; Olson, J.; Imhoff, L.; Nelson, A.V. Aerial exposure and desiccation tolerances are correlated to species composition in “green tides” of the Salish Sea (northeastern Pacific). Bot. Mar. 2010, 53, 103–111. [Google Scholar] [CrossRef]
  11. Gao, S.; Shen, S.; Wang, G.; Niu, J.; Lin, A.; Pan, G. PSI-driven cyclic electron flow allows intertidal macro-algae Ulva sp. (Chlorophyta) to survive in desiccated conditions. Plant Cell Physiol. 2011, 52, 885–893. [Google Scholar] [CrossRef] [PubMed]
  12. Bukhov, N.; Egorova, E.; Carpentier, R. Electron flow to photosystem I from stromal reductants in vivo: The size of the pool of stromal reductants controls the rate of electron donation to both rapidly and slowly reducing photosystem I units. Planta 2002, 215, 812–820. [Google Scholar] [CrossRef]
  13. Gao, S.; Niu, J.; Chen, W.; Wang, G.; Xie, X.; Pan, G.; Gu, W.; Zhu, D. The physiological links of the increased photosystem II activity in moderately desiccated Porphyra haitanensis (Bangiales, Rhodophyta) to the cyclic electron flow during desiccation and re-hydration. Photosynth. Res. 2013, 116, 45–54. [Google Scholar] [CrossRef]
  14. Huan, L.; Xie, X.; Zheng, Z.; Sun, F.; Wu, S.; Li, M.; Gao, S.; Gu, W.; Wang, G. Positive correlation between PSI response and oxidative pentose phosphate pathway activity during salt stress in an intertidal macroalga. Plant Cell Physiol. 2014, 55, 1395–1403. [Google Scholar] [CrossRef] [PubMed]
  15. Holzinger, A.; Herburger, K.; Kaplan, F.; Lewis, L.A. Desiccation tolerance in the chlorophyte green alga Ulva compressa: Does cell wall architecture contribute to ecological success? Planta 2015, 242, 477–492. [Google Scholar] [CrossRef]
  16. Murthy, M.S.; Sharma, C.L.N.S. Peroxidase Activity in Ulva lactuca under Desiccation. Bot. Mar. 1989, 32, 511–513. [Google Scholar] [CrossRef]
  17. Flores-Molina, M.R.; Thomas, D.; Lovazzano, C.; Nuñez, A.; Zapata, J.; Kumar, M.; Correa, J.A.; Contreras-Porcia, L. Desiccation stress in intertidal seaweeds: Effects on morphology, antioxidant responses and photosynthetic performance. Aquat. Bot. 2014, 113, 90–99. [Google Scholar] [CrossRef]
  18. Yoshida, G.; Uchimura, M.; Hiraoka, M. Persistent occurrence of floating Ulva green tide in Hiroshima Bay, Japan: Seasonal succession and growth patterns of Ulva pertusa and Ulva spp. (Chlorophyta, Ulvales). Hydrobiologia 2015, 758, 223–233. [Google Scholar] [CrossRef]
  19. Xia, Z.; Liu, J.; Zhao, S.; Sun, Y.; Cui, Q.; Wu, L.; Gao, S.; Zhang, J.; He, P. Review of the development of the green tide and the process of control in the southern Yellow Sea in 2022. Estuar. Coast. Shelf Sci. 2024, 302, 108772. [Google Scholar] [CrossRef]
  20. Mutizabal-Aros, J.; Ramírez, M.E.; Haye, P.A.; Meynard, A.; Pinilla-Rojas, B.; Núñez, A.; Latorre-Padilla, N.; Search, F.V.; Tapia, F.J.; Saldías, G.S.; et al. Morphological and Molecular Identification of Ulva spp. (Ulvophyceae; Chlorophyta) from Algarrobo Bay, Chile: Understanding the Composition of Green Tides. Plants 2024, 13, 1258. [Google Scholar] [CrossRef]
  21. Guiry, M.D.; Guiry, G.M. AlgaeBase; World-Wide Electronic Publication, National University of Ireland: Galway, Ireland, 2024; Available online: https://www.algaebase.org (accessed on 16 August 2024).
  22. Schneider, C.A.; Rasband, W.S.; Eliceiri, K.W. NIH Image to ImageJ: 25 years of image analysis. Nat. Methods 2012, 9, 671–675. [Google Scholar] [CrossRef]
  23. Caroca-Valencia, S.; Rivas, J.; Araya, M.; Núñez, A.; Piña, F.; Toro-Mellado, F.; Contreras-Porcia, L. Indoor and Outdoor Cultures of Gracilaria chilensis: Determination of Biomass Growth and Molecular Markers for Biomass Quality Evaluation. Plants 2023, 12, 1340. [Google Scholar] [CrossRef] [PubMed]
  24. Chang, W.; Chen, M.; Lee, T. 2, 3, 5-Triphenyltetrazolium reduction in the viability assay of Ulva fasciata (Chlorophyta) in response to salinity stress. Bot. Bull. Acad. Sin. 1999, 40, 207–212. [Google Scholar]
  25. Burritt, D.J.; Larkindale, J.; Hurd, C.L. Antioxidant metabolism in the intertidal red seaweed Stictosiphonia arbuscula following desiccation. Planta 2002, 215, 829–838. [Google Scholar] [CrossRef] [PubMed]
  26. Juan, C.A.; Pérez de la Lastra, J.M.; Plou, F.J.; Pérez-Lebeña, E. The chemistry of reactive oxygen species (ROS) revisited: Outlining their role in biological macromolecules (DNA, lipids and proteins) and induced pathologies. Int. J. Mol. Sci. 2021, 22, 4642. [Google Scholar] [CrossRef]
  27. Gao, G.; Beardall, J.; Bao, M.; Wang, C.; Ren, W.; Xu, J. Ocean acidification and nutrient limitation synergistically reduce growth and photosynthetic performances of a green tide alga Ulva linza. Biogeosciences 2018, 15, 3409–3420. [Google Scholar] [CrossRef]
  28. Sun, J.; Dai, W.; Zhao, S.; Liu, J.; Zhang, J.; Xu, J.; He, P. Response to the CO2 concentrating mechanisms and transcriptional time series analysis of Ulva prolifera under inorganic carbon limitation. Harmful Algae 2024, 139, 102727. [Google Scholar] [CrossRef]
  29. Gao, G.; Zhong, Z.; Zhou, X.; Xu, J. Changes in morphological plasticity of Ulva prolifera under different environmental conditions: A laboratory experiment. Harmful Algae 2016, 59, 51–58. [Google Scholar] [CrossRef]
  30. Cui, J.; Zhang, J.; Huo, Y.; Zhou, L.; Wu, Q.; Chen, L.; Yu, K.; He, P. Adaptability of free-floating green tide algae in the Yellow Sea to variable temperature and light intensity. Mar. Pollut. Bull. 2015, 101, 660–666. [Google Scholar] [CrossRef]
  31. Largo, D.B.; Sembrano, J.; Hiraoka, M.; Ohno, M. Taxonomic and ecological profile of ‘green tide’ species of Ulva (Ulvales, Chlorophyta) in central Philippines. Hydrobiologia 2004, 512, 247–253. [Google Scholar] [CrossRef]
  32. Zhang, X.; Wang, H.; Mao, Y.; Liang, C.; Zhuang, Z.; Wang, Q.; Ye, N. Somatic cells serve as a potential propagule bank of Enteromorpha prolifera forming a green tide in the Yellow Sea, China. J. Appl. Phycol. 2010, 22, 173–180. [Google Scholar] [CrossRef]
  33. Zhang, X.; Xu, D.; Mao, Y.; Li, Y.; Xue, S.; Zou, J.; Lian, W.; Liang, C.; Zhuang, Z.; Wang, Q.; et al. Settlement of vegetative fragments of Ulva prolifera confirmed as an important seed source for succession of a large-scale green tide bloom. Limnol. Oceanogr. 2011, 56, 233–242. [Google Scholar] [CrossRef]
  34. Cao, J.; Liu, J.; Zhao, S.; Tong, Y.; Li, S.; Xia, Z.; Hu, M.; Sun, Y.; Zhang, J.; He, P. Advances in the research on micropropagules and their role in green tide outbreaks in the Southern Yellow Sea. Mar. Pollut. Bull. 2023, 188, 114710. [Google Scholar] [CrossRef]
  35. Xia, Z.; Yang, Y.; Zeng, Y.; Sun, Y.; Cui, Q.; Chen, Z.; Liu, J.; Zhang, J.; He, P. Temporal succession of micropropagules during accumulation and dissipation of green tide algae: A case study in Rudong coast, Jiangsu Province. Mar. Environ. Res. 2024, 202, 106719. [Google Scholar] [CrossRef]
  36. Taylor, R.; Fletcher, R.L.; Raven, J.A. Preliminary studies on the growth of selected ‘green tide’ algae in laboratory culture: Effects of irradiance, temperature, salinity and nutrients on growth rate. Bot. Mar. 2001, 44, 327–336. [Google Scholar] [CrossRef]
  37. Kim, D.; Hwang, C.Y.; Cho, K.H. The fitness trade-off between growth and stress resistance determines the phenotypic landscape. BMC Biol. 2024, 22, 62. [Google Scholar] [CrossRef]
  38. Zou, D.; Gao, K. The photosynthetic and respiratory responses to temperature and nitrogen supply in the marine green macroalga Ulva conglobata (Chlorophyta). Phycologia 2014, 53, 86–94. [Google Scholar] [CrossRef]
  39. Bandehagh, A.; Taylor, N.L. Can alternative metabolic pathways and shunts overcome salinity induced inhibition of central carbon metabolism in crops? Front. Plant Sci. 2020, 11, 1072. [Google Scholar] [CrossRef]
  40. Gupta, V.; Kushwaha, H.R. Metabolic regulatory oscillations in intertidal green seaweed Ulva lactuca against tidal cycles. Sci. Rep. 2017, 7, 16430. [Google Scholar] [CrossRef]
Figure 1. Green tides from Algarrobo Bay, Chile. (a) Green tides in the sandy area, (b) high intertidal zone, (c) middle zone, and (d) low zone.
Figure 1. Green tides from Algarrobo Bay, Chile. (a) Green tides in the sandy area, (b) high intertidal zone, (c) middle zone, and (d) low zone.
Jmse 12 01893 g001
Figure 2. The average daily algal weight (g) ± standard deviation (n = 9) of (a) Ulva stenophylloides and (b) Ulva uncialis under both control and desiccation treatments during the 10-day cultivation period.
Figure 2. The average daily algal weight (g) ± standard deviation (n = 9) of (a) Ulva stenophylloides and (b) Ulva uncialis under both control and desiccation treatments during the 10-day cultivation period.
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Figure 3. The average daily blade length (cm) ± standard deviation (n = 9) of (a) Ulva stenophylloides and (b) Ulva uncialis under both control and desiccation treatments during the 10-day cultivation period.
Figure 3. The average daily blade length (cm) ± standard deviation (n = 9) of (a) Ulva stenophylloides and (b) Ulva uncialis under both control and desiccation treatments during the 10-day cultivation period.
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Figure 4. Average daily cellular activity (MTT) ± standard deviation (n = 3) in (a) Ulva stenophylloides and (b) Ulva uncialis for both control and desiccation treatments during the 10-day cultivation period. FW = fresh tissue.
Figure 4. Average daily cellular activity (MTT) ± standard deviation (n = 3) in (a) Ulva stenophylloides and (b) Ulva uncialis for both control and desiccation treatments during the 10-day cultivation period. FW = fresh tissue.
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Figure 5. Average daily lipid peroxidation levels ± standard deviation (n = 3) in (a) Ulva stenophylloides and (b) Ulva uncialis for both control and desiccation treatments during the 10-day cultivation period. DW = dry weight.
Figure 5. Average daily lipid peroxidation levels ± standard deviation (n = 3) in (a) Ulva stenophylloides and (b) Ulva uncialis for both control and desiccation treatments during the 10-day cultivation period. DW = dry weight.
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Table 1. Regression analysis of the response variable algal weight and the strength of its relationship with time (days) in Ulva uncialis and Ulva stenophylloides over 10 days of cultivation. * indicates significant differences (p < 0.05).
Table 1. Regression analysis of the response variable algal weight and the strength of its relationship with time (days) in Ulva uncialis and Ulva stenophylloides over 10 days of cultivation. * indicates significant differences (p < 0.05).
SpeciesTreatmentResponse VariableR2FProbability (p)Slope
Ulva stenophylloidesControlAlgal weight0.076985.420.02383 *−0.10563
Ulva stenophylloidesDesiccationAlgal weight0.207414.870.0003193 *−0.19892
Ulva uncialisControlAlgal weight−0.019220.00029510.98640.01635
Ulva uncialisDesiccationAlgal weight0.185913.110.0006672 *−0.17054
Table 2. Repeated-measures ANOVAs for the effects of time (days) and treatment (desiccation or control) on the weight and blade length of Ulva uncialis and Ulva stenophylloides over 10 days of cultivation. * and *** indicate significant differences (p < 0.05 and p < 0.001, respectively).
Table 2. Repeated-measures ANOVAs for the effects of time (days) and treatment (desiccation or control) on the weight and blade length of Ulva uncialis and Ulva stenophylloides over 10 days of cultivation. * and *** indicate significant differences (p < 0.05 and p < 0.001, respectively).
Species &
Parameter
Source of VariationdfMSFProbability (p)
Ulva stenophylloides
Algal weight
Time (days)129.21819.6502.31 × 10−5 ***
Treatment17.0484.7400.0317 *
Treatment × Time12.7411.8440.1775
Error1041.487
Ulva uncialis
Algal weight
Time (days)18.9872.5300.11474
Treatment128.8828.1310.00525 *
Treatment × Time19.3382.6290.10797
Error1043.552
Ulva stenophylloides
Blade length
Time (days)11.930.1780.6742
Treatment144.984.1450.0443 *
Treatment × Time110.120.9320.3365
Error10410.85
Ulva uncialis
Blade length
Time (days)141.01.9770.163
Treatment1374.818.0554.69 × 10−5 ***
Treatment × Time112.20.5900.444
Error10420.8
Table 3. Regression analysis of the response variable blade length and the strength of its relationship with time (days) in Ulva uncialis and Ulva stenophylloides over 10 days of cultivation.
Table 3. Regression analysis of the response variable blade length and the strength of its relationship with time (days) in Ulva uncialis and Ulva stenophylloides over 10 days of cultivation.
SpeciesTreatmentResponse VariableR2FProbability (p)Slope
Ulva stenophylloidesControlBlade length−0.00730.61550.4360.1287
Ulva stenophylloidesDesiccationBlade length0.00650.33850.563−0.0505
Ulva uncialisControlBlade length0.00681.36200.2490.2790
Ulva uncialisDesiccationBlade lenght−0.00440.76910.3850.0819
Table 4. Regression analysis of the response variable cellular activity and the strength of its relationship with time (days) in Ulva uncialis and Ulva stenophylloides over 10 days of cultivation. * indicates significant differences (p < 0.05).
Table 4. Regression analysis of the response variable cellular activity and the strength of its relationship with time (days) in Ulva uncialis and Ulva stenophylloides over 10 days of cultivation. * indicates significant differences (p < 0.05).
SpeciesTreatmentResponse VariableR2FProbability (p)Slope
Ulva stenophylloidesControlMTT0.560418.850.0007997 *14.382
Ulva stenophylloidesDesiccationMTT0.545717.820.000999 *13.376
Ulva uncialisControlMTT0.18954.2740.059214.132
Ulva uncialisDesiccationMTT−0.07610.0099280.92210.1781
Table 5. Regression analysis of the response variable lipid peroxidation level and the strength of its relationship with time (days) in Ulva uncialis and Ulva stenophylloides over 10 days of cultivation.
Table 5. Regression analysis of the response variable lipid peroxidation level and the strength of its relationship with time (days) in Ulva uncialis and Ulva stenophylloides over 10 days of cultivation.
EspecieTreatmentResponse VariableR2FProbability (p)Slope
Ulva stenophylloidesControlLipoperoxides−0.070620.076510.7864−4.88 × 10−5
Ulva stenophylloidesDesiccationLipoperoxides0.1473.4130.08757−0.000191
Ulva uncialisControlLipoperoxides−0.043390.4780.5293−6.54 × 10−5
Ulva uncialisDesiccationLipoperoxides0.052491.7750.2056−1.11 × 10−4
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Mutizabal-Aros, J.; Meynard, A.; Contreras-Porcia, L. A Physiological Analysis of Desiccation Stress in the Green Tide Species Ulva stenophylloides and Ulva uncialis in the South Pacific. J. Mar. Sci. Eng. 2024, 12, 1893. https://doi.org/10.3390/jmse12111893

AMA Style

Mutizabal-Aros J, Meynard A, Contreras-Porcia L. A Physiological Analysis of Desiccation Stress in the Green Tide Species Ulva stenophylloides and Ulva uncialis in the South Pacific. Journal of Marine Science and Engineering. 2024; 12(11):1893. https://doi.org/10.3390/jmse12111893

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Mutizabal-Aros, Javiera, Andrés Meynard, and Loretto Contreras-Porcia. 2024. "A Physiological Analysis of Desiccation Stress in the Green Tide Species Ulva stenophylloides and Ulva uncialis in the South Pacific" Journal of Marine Science and Engineering 12, no. 11: 1893. https://doi.org/10.3390/jmse12111893

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