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Differential effects of pollution on adult and recruits of a canopy-forming alga: implications for population viability under low pollutant levels


Marine macroalgal forests are highly productive and iconic ecosystems, which are seriously threatened by number of factors such as habitat destruction, overgrazing, ocean warming, and pollution. The effect of chronic, but low levels of pollutants on the long-term survival of the canopy-forming algae is not well understood. Here we test the effects of low concentrations (found in good quality water-bodies) of nitrates, heavy metals copper (Cu) and lead (Pb), and herbicides (glyphosate) on both adults and recruits of Carpodesmia crinita, a Mediterranean canopy forming macroalga. We show that although adult biomass, height and photosynthetic yield remain almost unaffected in all the assays, low Cu levels of 30 µg/L completely suppress adult fertility. In addition, all the assays have a strong and negative impact on the survival and growth of recruits; in particular, glyphosate concentrations above 1 µg/L almost totally inhibit their survival. These results suggest that the long-term viability of C. crinita may be severely compromised by low pollutant levels that are not affecting adult specimens. Our results provide important data for a better understanding of the present-day threats to marine canopy-forming macroalgae and for the design of future management actions aimed at preserving macroalgal forests.


Anthropogenic pressures are affecting biological and ecological ecosystems worldwide. Changes in species phenology and geographical distribution, as well as abrupt habitat shifts are well documented1,2,3,4,5. Macroalgal forests formed by species of the orders Fucales and Laminariales are structurally and functionally complex ecosystems6,7,8,9,10,11. These highly productive and iconic ecosystems are declining in some areas due to the accumulation of anthropogenic impacts, such as those related to intensive land use, pollution, warming or invasive species12,13,14,15,16,17,18,19,20,21,22. The loss of macroalgal forests also implies a loss or impoverishment of ecosystem services such as nutrient cycling, food production, nursery habitat provision, erosion reduction, and control of water quality13. Globally, deterioration of these complex habitats is often associated with a replacement of canopy-forming algae by ephemeral and structurally simpler macroalgae, affecting the status and functioning of these ecosystems13,23.

Marine ecosystem shifts can be gradual and can take long periods of time to become evident24,25,26 hiding the possible causes that provoke their declines. Progressive decline of macroalgal forests can be the result of several subtle and chronic causes over the canopy-forming algae, but with drastic consequences in the long term14. There is a current lack of knowledge on the subtle anthropogenic stressors affecting the permanence of macroalgal forests, which might be behind the local declines of these ecosystems. However, policy and management initiatives that seek to conserve or recover lost habitats, require the capacity to anticipate and suppress the mechanisms that drive such losses27.

Several species of the order Fucales, which are amongst the most important canopy-forming brown algae in shallow temperate rocky bottoms28,29, have experienced severe declines in the North-Western Mediterranean due, amongst other causes, to pollution and eutrophication26,30,31,32,33,34,35,36,37 that began in the 1970s and increased steadily until the 1990s38,39. At the same time, biocides used in antifouling paints, for recreational boats, containing toxic compounds gained popularity in the 1970s40. It was not until the implementation of the EU Water Framework Directive (2008/56/EC) that the amount of pollution steadily decreased in EU Mediterranean countries due to the construction of water treatment plants35,41.

Some studies provide unequivocal evidences that pollution drastically affects the persistence of fucoid forests in the Mediterranean42,43 and it has been proved that these forests can come back, if restored, once the pollution levels have decreased and pollutants are not critical for fucoid survival44. However, we still need to understand the effects of pollutants at all the different macroalgae life stages. Organisms in early stages of development may have different requirements and environmental needs to those in adult stages. In fact, recruits may be more sensitive to stressors than adults, as it has already been reported for several species of Fucus, which in their early stages showed higher mortality, ultrastructural changes and growth retardation compared to adults when exposed to heavy metals45,46,47,48. The number and growth rate of recruits is related to the number of successful adult individuals49, which means that sublethal effects of pollutants on recruits may be affecting the long-term viability of populations. Thus, ascertaining the lethal and sublethal effects of pollution in both adults and recruits will help to provide a full understanding of population replenishment and persistence in specific environmental conditions.

Although it is difficult to disentangle the effects on the species and habitats of the different pollutants that are being thrown in Mediterranean coastal waters, here we have selected three different kinds of pollutants that by themselves are known to affect macroalgae: nitrates as a proxy for nutrient pollution36,42,43, copper (Cu) and lead (Pb) as representatives of pollution by heavy metals44, and glyphosate as a persistent organic pollutant that is one of the most widely used herbicides50 although is not generally considered in most marine monitoring programs51.

This study aims to evaluate the effects of low pollutant concentrations (nitrates, Cu, Pb and glyphosate) currently reported in non-contaminated areas of the northwestern Mediterranean Sea (i.e., continuous low/moderate concentrations of pollutants) on populations of adult and juvenile of Carpodesmia crinita (Duby) Orellana and Sansón (syn. Cystoseira crinita Duby)52, a canopy-forming alga that makes important shallow water macroalgal forests all across the Mediterranean53. Adult survival, growth, fertility and photosynthetic activity, as well as recruit density and size, were monitored from June to December 2018 under different pollution conditions. The aim was to gather information on the subtle and non-visible threats affecting the marine canopy-forming macroalgae from the northwestern Mediterranean. Such information is essential for establishing successful conservation action to preserve and restore marine forests.

Materials and methods

Target species and collection

Carpodesmia crinita (Duby) Orellana and Sansón (syn. Cystoseira crinita Duby)52 is a Mediterranean endemic species that can create dense populations in shallow and sheltered rocky shores (mainly between 0 and 1 m depth)18,53,54,55,56. In recent decades, C. crinita has experienced severe declines and even local extinctions in different areas of Spain, France, Italy, Croatia, Montenegro and Greece31,33,34,57,58,59,60,61. Although several stressors have been attributed to its demise, only Sales et al. (2011) have reported pollution as being a factor in the decline of populations of C. crinita and other Fucales in a Mediterranean bay.

For our study, Carpodesmia crinita samples were collected by a snorkeler in June 2018 from a unique population in the Natura 2000 site of Castell-Cap Roig, Cala Estreta (41°86′62.1″N, 3°17′50.7″E). Specimens, similar in shape, length and phenological state, were carefully removed from the rock while preserving their attaching disc to ensure survival during the experiment and transported immediately to the Laboratory for Experimentation with Living Organisms (LEOV) located in the Center for Advanced Studies (CEAB-CSIC) in Blanes, Spain. Once in the laboratory, epiphytes and sediment were carefully removed and specimens were placed in aquaria with ambient seawater at 18 °C and natural light levels for a one week acclimatization period.


Six specific treatments were applied as follows: 4 µM nitrate (nutrients); 30 µg/L copper; (heavy metal), 10 µg/L lead (heavy metal); and three different concentrations of glyphosate (herbicide), at 0.5 µg/L, 1 µg/L and 10 µg/L. The water in the tanks was renewed once a week to maintain the selected concentrations throughout the experiment. These particular concentrations were selected because they are frequently found in Mediterranean coastal waters. Although nitrate concentrations in open Mediterranean Sea waters range from 0.03 to 4.59 µM62, the average annual concentrations in coastal areas close to the sampling site are usually below 1 µM42,43,54. Nevertheless, slightly polluted areas can reach values close to 10 µM36,43. The concentrations of heavy metals used in Cu and Pb treatments were just above the thresholds used by the European Union to categorize a water mass as being of good environmental quality (< 25 µg/L for Cu and < 7.2 µg/L for Pb; Directive 2008/105/CE). Glyphosate has been detected at concentrations around 1 µg/L in unpolluted coastal waters51,63,64.

Experimental set up

After acclimatization, adult individuals of C. crinita were placed in each of the six treatments and a control (with filtered and sterilized ambient seawater), using four replicate 20 L tanks per treatment (Fig. 1). One adult individual and three large (approx. 100 cm2) flat stones, with even surfaces, were placed in each tank following methodology previously described to obtain recruits in experimental tanks65. The stones, located at the bottom of the tanks, provided adequate substrata for the settlement of zygotes, which came from fertile adult specimens located in the same tank. Recruits were visible to the naked eye after 1 month. The seawater was continuously aerated by air pumps (Hailea ACO-5504), maintained at a constant temperature of 18 °C (Hailea Chiller HC 500 A) in a natural light regime and with a constant flow of natural seawater (pump Jet NJ 3000) in a closed-water circuit, being completely replaced once a week.

Figure 1

Experimental setup. Four replicate tanks (20 L) were used for each treatment (control without pollutant, 4 µM nitrate, 30 µg/L copper, 10 µg/L lead, and glyphosate at 0.5 µg/L, 1 µg/L and 10 µg/L). In each tank, one adult individual of Carpodesmia crinita and three stones (to provide substrata for the settlement of the zygotes) were placed. All tanks were maintained at 18 °C for 6 months, continuously aerated by air pumps, with a natural light regime and with a constant flow of natural seawater in a closed circuit.


The effects of the different pollutants on C. crinita was evaluated by measuring several variables both in adults and recruits. Biomass, total height and effective quantum yield (Fv/Fm) of photosystem II (PSII) were measured monthly in adult specimens.

Changes in wet weight and height were measured for each specimen at each sampling time. Specimens were dried with absorbent paper before being weighed in mg. The height of each adult individual was determined by measuring the length (in mm) of the longest perennial axis using a ruler. Weight and height rates (WRt and HRt) were estimated as the change in weight and height at a given time (Wt and Ht) relative to the initial measures (initial weight Wi and initial height Hi) as:

$${\text{WR}}_{{\text{t}}} = \left( {{\text{W}}_{{\text{t}}} {-}{\text{W}}_{{\text{i}}} } \right)/{\text{W}}_{{\text{i}}} \;{\text{and}}\;{\text{HR}}_{{\text{t}}} = \left( {{\text{H}}_{{\text{t}}} - {\text{H}}_{{\text{i}}} } \right)/{\text{H}}_{{\text{i}}} .$$

Effective quantum yield was used as an indicator of PSII performance to assess photosynthetic efficiency. Macroalgal fronds were incubated in the dark for 15 min after which Fv/Fm measurements were estimated by applying a saturation pulse using a Pulse Amplitude Modulated Fluorometry (Diving-PAM Underwater Fluorometer, Waltz, Germany) with an absorption coefficient of the leaves of 0.65, a measuring light intensity (meas-int) of 10 and an out-gain of 10 for the electronic signal gain (amplification factor). Measuring Fv/Fm following a period of dark adaptation is a common technique for measuring stress in plants66.

A fecundity level (FL) was assigned by categorizing individuals from 0 to 4 at the beginning and at the end of the experiment: 0 (sterile individuals), 1 (less than 25% of terminal branches fertile), 2 (between 25 and 50% of terminal branches fertile), 3 (between 51 and 75% of terminal branches fertile) and 4 (more than 76% of terminal branches fertile). A fecundity index (FI) was calculated for each specimen as follows: FI = FLf – FLi , where FLi is the initial fertility level and FLf is the final fertility level.

For recruits, we only took density and mean height measures at months 3 and 6 to avoid any harm to the recruits from manipulation. The stones harboring the recruits were taken out of the water and the mean density was measured by counting the number of recruits per cm2 (N = 30 random samples per treatment) under the binocular microscope at 10x. The mean height of the recruits was obtained by measuring individual lengths (N = 60, random samples per treatment) under the binocular microscope using an ocular micrometer.

Statistical analyses

Changes in wet weight, and height, photosynthetic efficiency, and fecundity index for adults and density and height for recruits, were selected as response variables. Different models were fitted to analyze the effect of the pollutants on each variable. Wet weight and height variation in adults, computed as a percentage of the initial state, were analyzed using Linear Models with Random Effects (LMER). Treatment (pollutants, plus the control; 7 levels) was used as a fixed factor, while specimen identity and time (6 levels) were used as random factors, in order to account for the lack of independence between observations repeated at different times. Generalized Linear Mixed Models (GLMM), with a quasi-Poisson error distribution and a logit link function were used to test the effects of pollutants on the Effective Quantum Yield, with treatment as a fixed factor and specimen identity and time as random. LMER and GLMM models incorporate random effects and therefore can cope with repeated measures over time67. Finally, the fecundity index was analyzed by means of a Linear Model (LM), with treatment as a fixed factor.

A Generalized Linear Model (GLM) with a Poisson error distribution and a logit link function, with pollutants (7 levels) and time (2 levels) as fixed factors, were used to test the effects of pollutants on recruit density. The recruit’ height data were transformed (natural log) and analyzed using a LM, with pollutants and time, once again, as fixed factors.

For all the fitted models, we applied a Type II Wald χ2 test to determine the effect of the fixed factors. For those models in which the effect of the fixed factors was significant, a pairwise post hoc Tukey’s Test was applied to test for differences between the different levels of the factors. All analyses were performed by statistical software R (R Development Core Team, 2014). Models were fitted using the functions “glmer”, “lmer”, “lm” and “glmmPQL” from the lme4 package68 and MASS package69. The Wald χ2 test was performed using the “ANOVA” function from the car package70. For multiple comparisons, we applied the Tukey test using the “lsmeans” function from the lsmeans package71.


Adult responses

Change in wet weight (ww) over time for each treatment of C. crinita is shown in Fig. 2. Wet weight was similar among treatments (χ26 = 7.792, p = 0.253; supplementary Table S1) and while weight reduction always ranged from 25 to 65% by the end of the experiment, the rate of reduction depended on the treatment. Although specimens subjected to nitrate treatment initially increased in weight, they sharply decreased its weight after the 4th month, finally reducing its weight by 40% at the end of the experiment.

Figure 2

Mean wet weight variation of adult individuals of Carpodesmia crinita under control and the different pollutant conditions over a period of 6 months. Weight variation is given in parts per unit. Vertical bars represent standard errors.

Similarly, height was more or less constant throughout the experiment for all treatments except for lead, where specimens reduced a 39% initial height after 6 months (Tukey test, p < 0.05 for Pb and control, Cu and nitrate treatments; supplementary Table S1 Fig. 3).

Figure 3

Mean height variation of adult individuals of Carpodesmia crinita under control conditions and the different pollutant treatments for 6 months. Height variation is given in parts per unit. Vertical bars represent standard errors.

Mean effective quantum yield (Fv/Fm) values did not differ significantly among treatments (χ26 = 3.305, p = 0.770; supplementary Table S1; Fig. 4). The main quantum yield values were in the range of, approximately, 0.6 to 0.8 which is considered an optimal range for brown algae72,73,74,75.

Figure 4

Mean photosynthetic yield (Fv/Fm) of adult individuals of Carpodesmia crinita under control conditions and the different pollutant treatments for 6 months. Vertical bars represent standard errors.

Fecundity level (FL) of adult C. crinita specimens at the beginning of the experiment for all treatments was similar, ranging from 1.5 to 2.5 (F6,21 = 0.733, p = 0.915). However, by the end of the experiment, the fecundity index had changed significantly among treatments (F6 ,21 = 3.087, p < 0.05; supplementary Table S2; Fig. 5). Although there were no differences among the fecundity level of individuals from control, nitrate, Pb, and glyphosates treatments all the specimens from the copper treatment (independent of their initial fecundity level) were sterile (Tukey test, p < 0.05 for Cu and glyphosate 0.5 µg/L, and Cu and nitrate).

Figure 5

Mean variation of fecundity index of adult individuals of Carpodesmia crinita under control conditions and the different pollutant conditions treatments, 6 months after the beginning of the experiment. Vertical bars represent standard errors.

Recruit responses

Recruit density was significantly higher in the control tanks than in the tanks with pollutants at both measuring times, with 104.6 (± 10.36) and 82.5 (± 9.837) mean individuals/cm2 (± SE), at month 3 and month 6, respectively (Figs. 6 and 7a–c). The lowest recruit density was found in glyphosate treatments of 1 µg/L and 10 µg/L (ca. 1.5 individuals/cm2 at both month 3 and month 6; Tukey test, p < 0.001). However, all the other treatments (Cu, Pb, NO3- and 0.5 µg/L glyphosate) also produced lower recruit densities than that of the control treatment, with values at month 6 ranging from 4.733 (± 0.716) to 30.3 (± 3.823) individuals/cm2; (Tukey tests, p < 0.0001). The differences in recruit densities among treatments were already evident in month 3, and the same trend was observed at month 6 (χ26 = 7785.9, p < 0.001; supplementary Table S2; Figs. 6 and 7a–c).

Figure 6

Mean recruit density (number of recruits) of Carpodesmia crinita under control conditions and the different pollutant treatments at 3 months and 6 months after the beginning of the experiment. Vertical bars represent standard errors. Horizontal lines (ab and c) indicate significant differences between treatments.

Figure 7

Top: Example of stones with recruits at month 3: (a) control, (b) nitrate and (c) glyphosate 0.5 µg/L. The horizontal scale bars represent 1 cm. Bottom: Recruits of Carpodesmia crinita at month 3 under different treatments: (d) control, (e) nitrate and (f) glyphosate 0.5 µg/L. Scale bars represent 0.5 mm.

Recruits in the control tanks grew to the largest sizes, reaching a mean of 1.468 (± 0.034) mm at months 6 (Tukey tests, p < 0.0001 for all comparisons). Recruits treated with Cu, Pb and 0.5 µg/L glyphosate were around four times smaller than the recruits in the control tanks after six months, whereas those under nitrate and 1 and 10 µg/L glyphosate were around eight times smaller. The marked differences in the mean size of recruits under different treatments became evident after 3 months and remained constant until the end of the experiment (F6,819 = 178.37, p < 0.001; supplementary Table S2; Figs. 7d–f and 8).

Figure 8

Mean height of recruits of Carpodesmia crinita under control conditions and the different pollutant treatments at months 3 (black dots) and 6 (empty dots) after the beginning of the experiment. Vertical bars represent standard errors. Horizontal lines indicate the significant differences between treatments.


Research into the specific responses of macroalgae to pollutants currently focuses mainly on their capacity to accumulate heavy metals and their use as bioindicators44,76,77,78. Moreover, most studies tend to deal with concentrations that are only found in highly polluted sites, such as areas where domestic, agricultural or industrial sewage discharge occur into coastal waters50,64,79,80,81. This meaning that the effects of toxic compounds are only known for very large concentrations, in places where macroalgal forests have already disappeared.

We have shown, in this study, how subtle pollutant concentrations over a period of six months may have no visible effects on adult populations of macroalgae, but can seriously compromise their mid-term and long-term viability by reducing the fertility of the adults and the survival of recruits. A number of studies have already shown that high levels of eutrophication36,43,82, heavy metals44,83 and pesticides50,64 result in reduction in adult survival, growth and photosynthetic capacity for many species of Fucales, and that this can lead to forests of these species being replaced by simplified systems. However, low to moderate levels of pollution rarely result in an immediate deforestation of fucoid assemblages43,84 since fucoids seem to be able to resist a certain degree of pollution. In fact, fucoids can survive in areas with pollution levels two to three times higher than those found at “unpolluted” reference sites43,44 which demonstrates that these macroalgae can resist a constant weak pollution source to a certain extent12,84,85. However, our results indicate that the lack of observed detrimental effects on adult individuals in well-established populations may well be concealing the real ecological effect – at the population level – of these low concentrations of pollutants.

Based on our results, growth (as changes in weight and height) and the effective yield of C. crinita adults seem not to be drastically affected by low but continuous (6 months) pollutant levels. Although most experimental studies on the effects of pollutants on brown algae are short-term experiments, the effects of heavy metals on its growth capacity appear to be species-specific83. Some Fucus species reduce their growth when exposed to concentrations ranging from 12–50 µg/L of Cu for 10 days and they stop their growth at higher concentration (300 µg/L of Cu)83. On the other hand, Sargassum cymosum did not change their growth compared to the control treatment when exposed to 10 to 50 µM of Pb for 7 days86. Regarding to the effective yield brown algae (Ascophyllum nodosum and Fucus vesiculosus) were not affected when exposed to Cu levels of 10 µg/L of Cu for 14 days87, neither Sargassum cymosum under Pb exposition (< 50 µM for 7 days)86. However, huge glyphosate levels (882.5 µg/L for 6 days) negatively affect chlorophyll absorbance of Fucus virsoides50.

We observed a market reduction in survival and growth of recruits at nitrate levels that do not affect adults (Figs. 6 and 8). It has previously been reported that physiological nutrient uptake and saturation mechanisms differ for recruits and adults: a moderate enrichment of nitrates can be beneficial for the growth and development of many adult kelp and fucoid species88,89,90,91,92, which accumulate nitrogen intracellularly with non-saturating nutrient uptake kinetics93,94, whereas nutrient uptake saturation occurred in recruits95. Such physiological differences might be linked to the higher sensibility of recruits to moderate/high nitrate concentrations.

Similarly, studies have shown the capacity of some adult brown algae to resist moderate heavy metal pollution, especially from copper44,48,96, but we have shown that even low copper concentrations seriously affect the fertility of adults from the species C. crinita, as well as the settlement and growth of recruits. The reasons for the copper impacts are unknown, but macroalgae may respond either by reducing the creation of reproductive structures, which suggests a trade-off between reproduction, growth and survival97, or by inhibiting the cell wall formation in zygotes during egg fertilization, thus preventing their normal development46. Furthermore, copper also can disrupt zygote germination and reduction in growth and normal development of juveniles of Fucales45,46,98 and gametophyte development on kelps99,100.

Glyphosate toxicity on marine environments has often been disregarded due to its apparent rapid microbial degradation101 and strong absorption by soils and sediments that potentially limit runoff in surface waters102. However, recent works show that moderate levels of glyphosate do exist in marine environments51 and that its strong capacity to bind with organic matter may help protect it from degradation103. The scarce studies dealing with the impacts of glyphosate on marine macroalgae are based only on adult stages and show that high concentrations can strongly affect growth, chlorophyll content and photosynthetic yield50,64,104,105. However, at lower concentrations of less than 1 µg/L, commonly found in coastal waters51,64, glyphosate did not show any impact on the adults50,104. Our experiments confirmed this as there were no signs of impairment on adult specimens of C. crinita at glyphosate concentrations of 1 µg/L. Nevertheless, at this concentration, and even at the lower concentration of 0.5 µg/L, we did observe reduced recruitment and increased mortality of recruits. As is the case with terrestrial plants, the toxicity of glyphosate on aquatic photosynthetic macrophytes depends on its ability to inhibit an enzyme implicated in the synthesis of the aromatic amino acids essential for protein synthesis106,107 as well as its ability to increase shikimic acid, which is related to a decline in carbon fixation intermediates108.

The levels of water pollution were probably not high enough to drive rapid extinctions of algal forests, but in the light of our experiments, we suggest that this pollution probably affected the settlement and growth of new individuals. Since recruitment plays an essential role in ensuring the stability of macroalgal populations, impacts on their recruits could have triggered a gradual decline and even local extinctions of many fucoid populations.

With the implementation of the EU Water Framework Directive (2008/56/EC), water quality has significantly improved in many EU countries35,41, but this has not led to a recovery of canopy-forming macroalgal populations35. Many water bodies classed as having a “good environmental status” still display chronic but moderate/low levels of pollution109,110,111 which, by preventing the recruitment of new individuals as our results suggest, may explain the fact that natural populations of fucoids are not recovering. This situation is probably not restricted to the Mediterranean Sea, as most marine coastal environments are now polluted to some extent, but we contend that it can be included among the several plausible causes triggering the decline in canopy-forming macroalgae23. We must also bear in mind, other factors such as overgrazing, invasive species or increasing temperatures, which may also be significantly involved in the decline of macroalgal populations112. Finally, since many areas are subjected to cumulative impacts112,113, future experiments that address the cumulative effects of two or more of these stressors will help to elucidate the dynamics of the decline in macroalgae forests. This knowledge needs to be incorporated into future conservation and restoration management in order to ensure the preservation of canopy-forming macroalgal populations and their associated biodiversity and ecosystem services.

Currently we are witnessing a general decrease of fucoid forests in the Mediterranean Sea26,30,31,32,33,34,59 which seem not to be able to recover35 unless some recovery management actions are implemented65,114,115. Thus, the future of Mediterranean fucoid forests must go hand in hand of a sustained decrease in all kind of pollutants in seawater (nutrients, heavy metals and persistent organic pollutants) and management actions oriented to facilitate the recovery of the populations.

Data availability

The datasets analyzed during the current study are available from the corresponding author on reasonable request.


  1. 1.

    Scheffer, M., Carpenter, S., Foley, J. A., Folke, C. & Walker, B. Catastrophic shifts in ecosystems. Nature 413, 591–596 (2001).

    ADS  CAS  Article  PubMed  Google Scholar 

  2. 2.

    Jackson, J. B. C. et al. Historical overfishing and the recent collapse of coastal ecosystems. Science 293, 629–637 (2001).

    CAS  Article  PubMed  Google Scholar 

  3. 3.

    Hughes, T. P. et al. Climate change, human impacts, and the resilience of coral reefs. Science 301, 929–933 (2003).

    ADS  CAS  Article  PubMed  Google Scholar 

  4. 4.

    Schiel, D. R., Steinbeck, J. R. & Foster, M. S. Ten years of induced ocean warming causes comprehensive changes in marine benthic communities. Ecology 85, 1833–1839 (2014).

    Article  Google Scholar 

  5. 5.

    Filbee-Dexter, K. & Scheibling, R. E. Sea urchin barrens as alternative stable states of collapsed kelp ecosystems. Mar. Ecol. Prog. Ser. 495, 1–25 (2014).

    ADS  Article  Google Scholar 

  6. 6.

    Dayton, P. K. et al. Patch dynamics and stability of some California kelp communities. Ecol. Monogr. 54, 253–289 (1984).

    Article  Google Scholar 

  7. 7.

    Dayton, P. K., Tegner, M. J., Parnell, P. E. & Edwards, P. B. Temporal and spatial patterns of disturbance and recovery in a kelp forest community. Ecol. Monogr. 62, 421–445 (1992).

    Article  Google Scholar 

  8. 8.

    Ballesteros, E. et al. Deep-water stands of Cystoseira zosteroides C. Agardh (Fucales, Ochrophyta) in the Northwestern Mediterranean: Insights into assemblage structure and population dynamics. Estuar. Coast. Shelf Sci. 82, 477–484 (2009).

    ADS  Article  Google Scholar 

  9. 9.

    Reed, D. C. & Foster, M. S. The effects of canopy shadings on algal recruitment and growth in a giant kelp forest. Ecology 65, 937–948 (1984).

    Article  Google Scholar 

  10. 10.

    Gianni, F. et al. Conservation and restoration of marine forests in the Mediterranean Sea and the potential role of Marine Protected Areas. Adv. Oceanogr. Limnol. 4, 83–101 (2013).

    Article  Google Scholar 

  11. 11.

    Wernberg, T. & Filbee-Dexter, K. Missing the marine forest for the trees. Mar. Ecol. Prog. Ser. 612, 209–215 (2019).

    ADS  Article  Google Scholar 

  12. 12.

    Steneck, R. S. et al. Kelp forest ecosystems: biodiversity, stability, resilience and future. Environ. Conserv. 29, 436–459 (2002).

    Article  Google Scholar 

  13. 13.

    Airoldi, L. & Beck, M. Loss, status and trends for coastal marine habitats of Europe. In Oceanography and Marine Biology: An Annual Review (eds. Gibson, R. N., Atkinson, R. J. A. & Gordon, D. M.) vol. 45 345–405 (Taylor & Francis, Milton Park, 2007).

    Google Scholar 

  14. 14.

    Krumhansl, K. A. et al. Global patterns of kelp forest change over the past half-century. Proc. Natl. Acad. Sci. 113, 13785–13790 (2016).

    CAS  Article  PubMed  Google Scholar 

  15. 15.

    Connell, S. et al. Recovering a lost baseline: missing kelp forests from a metropolitan coast. Mar. Ecol. Prog. Ser. 360, 63–72 (2008).

    ADS  Article  Google Scholar 

  16. 16.

    Gorman, D., Russell, B. D. & Connell, S. D. Land-to-sea connectivity: linking human-derived terrestrial subsidies to subtidal habitat change on open rocky coasts. Ecol. Appl. 19, 1114–1126 (2009).

    Article  PubMed  Google Scholar 

  17. 17.

    Ling, S. D., Johnson, C. R., Frusher, S. D. & Ridgway, K. R. Overfishing reduces resilience of kelp beds to climate-driven catastrophic phase shift. Proc. Natl. Acad. Sci. 106, 22341–22345 (2009).

    ADS  CAS  Article  PubMed  Google Scholar 

  18. 18.

    Sales, M. & Ballesteros, E. Long-term comparison of algal assemblages dominated by Cystoseira crinita (Fucales, Heterokontophyta) from Cap Corse (Corsica, North Western Mediterranean). Eur. J. Phycol. 45, 404–412 (2010).

    Article  Google Scholar 

  19. 19.

    Vergés, A. et al. The tropicalization of temperate marine ecosystems: climate-mediated changes in herbivory and community phase shifts. Proc. R. Soc. B Biol. Sci. 281, 20140846 (2014).

    Article  Google Scholar 

  20. 20.

    Vergés, A. et al. Long-term empirical evidence of ocean warming leading to tropicalization of fish communities, increased herbivory, and loss of kelp. Proc. Natl. Acad. Sci. U. S. A. 113, 13791–13796 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. 21.

    Wernberg, T. et al. Climate-driven regime shift of a temperate marine ecosystem. Science 353, 169–172 (2016).

    ADS  CAS  Article  PubMed  Google Scholar 

  22. 22.

    Capdevila, P. et al. Warming impacts on early life stages increase the vulnerability and delay the population recovery of a long-lived habitat-forming macroalga. J. Ecol. 107, 1129–1140 (2019).

    Article  Google Scholar 

  23. 23.

    Filbee-Dexter, K. & Wernberg, T. Rise of turfs: a new battlefront for globally declining kelp forests. Bioscience 68, 64–76 (2018).

    Article  Google Scholar 

  24. 24.

    Sagarin, R. D., Barry, J. P., Gilman, S. E. & Baxter, C. H. Climate-related change in an intertidal community over short and long time scales. Ecol. Monogr. 69, 465–490 (1999).

    Article  Google Scholar 

  25. 25.

    Eriksson, B. K., Johansson, G. & Snoeijs, P. Long-term changes in the macroalgal vegetation of the inner Gullmar fjord Swedish Skagerrak coast. J. Phycol. 38, 284–296 (2002).

    Article  Google Scholar 

  26. 26.

    Thibaut, T., Blanfuné, A., Boudouresque, C. F. & Verlaque, M. Decline and local extinction of Fucales in French Riviera: the harbinger of future extinctions?. Mediterr. Mar. Sci. 16, 206 (2015).

    Article  Google Scholar 

  27. 27.

    Brown, C. J., Saunders, M. I., Possingham, H. P. & Richardson, A. J. Interactions between global and local stressors of ecosystems determine management effectiveness in cumulative impact mapping. Divers. Distrib. 20, 538–546 (2014).

    Article  Google Scholar 

  28. 28.

    Feldmann, J. Recherches sur la végétation marine de la Méditerranée. La côte des Albères. Rev. Algol. (Université de Paris, 1937).

  29. 29.

    Giaccone, G. Écologie et chorologie des Cystoseira de Méditerranée. Rapp. Comm. int. Mer Médit 22, 49–50 (1973).

    Google Scholar 

  30. 30.

    Cormaci, M. & Furnari, G. Changes of the benthic algal flora of the Tremiti Islands (southern Adriatic) Italy. In Sixteenth International Seaweed Symposium vols 398–399 75–79 (Springer, Netherlands, 1999).

  31. 31.

    Thibaut, T., Pinedo, S., Torras, X. & Ballesteros, E. Long-term decline of the populations of Fucales (Cystoseira spp. and Sargassum spp.) in the Albères coast (France, North-western Mediterranean). Mar. Pollut. Bull. 50, 1472–1489 (2005).

    CAS  Article  PubMed  Google Scholar 

  32. 32.

    Thibaut, T., Blanfuné, A., Verlaque, M., Boudouresque, C.-F. & Ruitton, S. The Sargassum conundrum: very rare, threatened or locally extinct in the NW Mediterranean and still lacking protection. Hydrobiologia 781, 3–23 (2016).

    Article  Google Scholar 

  33. 33.

    Blanfuné, A., Boudouresque, C. F., Verlaque, M. & Thibaut, T. The fate of Cystoseira crinita, a forest-forming Fucale (Phaeophyceae, Stramenopiles), in France (North Western Mediterranean Sea). Estuar. Coast. Shelf Sci. 181, 196–208 (2016).

    ADS  Article  Google Scholar 

  34. 34.

    Mariani, S. et al. Past and present of Fucales from shallow and sheltered shores in Catalonia. Reg. Stud. Mar. Sci. 32, 100824 (2019).

    Article  Google Scholar 

  35. 35.

    Pinedo, S., Zabala, M. & Ballesteros, E. Long-term changes in sublittoral macroalgal assemblages related to water quality improvement. Bot. Mar. 56, 461–469 (2013).

    Article  Google Scholar 

  36. 36.

    Munda, I. M. Changes and degradation of seaweed stands in the Northern Adriatic. Hydrobiologia 260–261, 239–253 (1993).

    Article  Google Scholar 

  37. 37.

    Munda, I. M. Impact of pollution on benthic marine algae in the Northern Adriatic. Int. J. Environ. Stud. 43, 185–199 (1993).

    CAS  Article  Google Scholar 

  38. 38.

    Béthoux, J. P. et al. Nutrients in the Mediterranean Sea, mass balance and statistical analysis of concentrations with respect to environmental change. Mar. Chem. 63, 155–169 (1998).

    Article  Google Scholar 

  39. 39.

    Palanques, A., Sánchez-Cabeza, J. A., Masqué, P. & Leon, L. Historical record of heavy metals in a highly contaminated Mediterranean deposit: the Besos prodelta. Mar. Chem. 61, 209–217 (1998).

    CAS  Article  Google Scholar 

  40. 40.

    Terlizzi, A., Fraschetti, S., Gianguzza, P., Faimali, M. & Boero, F. Environmental impact of antifouling technologies: state of the art and perspectives. Aquat. Conserv. Mar. Freshw. Ecosyst. 11, 311–317 (2001).

    Article  Google Scholar 

  41. 41.

    Bokn, T. L., Moy, F. E. & Walday, M. Improvement of the shallow water communities following reductions of industrial outlets and sewage discharge in the Hvaler estuary Norway. Hydrobiologia 326–327, 297–304 (1996).

    Article  Google Scholar 

  42. 42.

    Pinedo, S., Arévalo, R. & Ballesteros, E. Seasonal dynamics of upper sublittoral assemblages on Mediterranean rocky shores along a eutrophication gradient. Estuar. Coast. Shelf Sci. 161, 93–101 (2015).

    CAS  Article  Google Scholar 

  43. 43.

    Arévalo, R., Pinedo, S. & Ballesteros, E. Changes in the composition and structure of Mediterranean rocky-shore communities following a gradient of nutrient enrichment: descriptive study and test of proposed methods to assess water quality regarding macroalgae. Mar. Pollut. Bull. 55, 104–113 (2007).

    Article  CAS  PubMed  Google Scholar 

  44. 44.

    Sales, M., Cebrian, E., Tomas, F. & Ballesteros, E. Pollution impacts and recovery potential in three species of the genus Cystoseira (Fucales, Heterokontophyta). Estuar. Coast. Shelf Sci. 92, 347–357 (2011).

    ADS  CAS  Article  Google Scholar 

  45. 45.

    Andersson, S. & Kautsky, L. Copper effects on reproductive stages of Baltic Sea Fucus vesiculosus. Mar. Biol. 125, 171–176 (1996).

    CAS  Article  Google Scholar 

  46. 46.

    Bond, P. et al. Arrested development in Fucus spiralis (Phaeophyceae) germlings exposed to copper. Eur. J. Phycol. 34, 513–521 (1999).

    Article  Google Scholar 

  47. 47.

    Nielsen, S. L., Nielsen, H. D. & Pedersen, M. F. Juvenile life stages of the brown alga Fucus serratus L. are more sensitive to combined stress from high copper concentration and temperature than adults. Mar. Biol. 161, 1895–1904 (2014).

    CAS  Article  Google Scholar 

  48. 48.

    Nielsen, H. D. & Nielsen, S. L. Adaptation to high light irradiances enhances the photosynthetic Cu2+ resistance in Cu2+ tolerant and non-tolerant populations of the brown macroalgae Fucus serratus. Mar. Pollut. Bull. 60, 710–717 (2010).

    CAS  Article  PubMed  Google Scholar 

  49. 49.

    Capdevila, P., Hereu, B., Riera, J. L. & Linares, C. Unravelling the natural dynamics and resilience patterns of underwater Mediterranean forests: insights from the demography of the brown alga Cystoseira zosteroides. J. Ecol. 104, 1799–1808 (2016).

    Article  Google Scholar 

  50. 50.

    Falace, A. et al. Effects of a glyphosate-based herbicide on Fucus virsoides (Fucales, Ochrophyta) photosynthetic efficiency. Environ. Pollut. 243, 912–918 (2018).

    CAS  Article  PubMed  Google Scholar 

  51. 51.

    Mercurio, P., Flores, F., Mueller, J. F., Carter, S. & Negri, A. P. Glyphosate persistence in seawater. Mar. Pollut. Bull. 85, 385–390 (2014).

    CAS  Article  PubMed  Google Scholar 

  52. 52.

    Orellana, S., Hernández, M. & Sansón, M. Diversity of Cystoseira sensu lato (Fucales, Phaeophyceae) in the eastern Atlantic and Mediterranean based on morphological and DNA evidence, including Carpodesmia gen. emend. and Treptacantha gen. emend. Eur. J. Phycol. 54, 447–465 (2019).

    CAS  Article  Google Scholar 

  53. 53.

    Sales, M. & Ballesteros, E. Seasonal dynamics and annual production of Cystoseira crinita (Fucales: Ochrophyta)-dominated assemblages from the northwestern Mediterranean. Sci. Mar. 76, 391–401 (2012).

    Article  Google Scholar 

  54. 54.

    Ballesteros, E. Els vegetals i la zonació litoral: espècies, comunitats i factors que influeixen en la seva distribució. Arx. Secc. Ciències IEC 101, 1–616 (1992).

    Google Scholar 

  55. 55.

    Ballesteros, E. Flora Phycologica Iberica. Vol. 1. Fucales. Gómez-Garreta, A. (ed.). Sci. Mar. 66, 187–188 (2002).

    Article  Google Scholar 

  56. 56.

    Sales, M. & Ballesteros, E. Shallow Cystoseira (Fucales: Ochrophyta) assemblages thriving in sheltered areas from Menorca (NW Mediterranean): relationships with environmental factors and anthropogenic pressures. Estuar. Coast. Shelf Sci. 84, 476–482 (2009).

    ADS  CAS  Article  Google Scholar 

  57. 57.

    Munda, I. The effects of organic pollution on the distribution of fucoid algae from the Istrian coast (vicinity of Rovinj). Acta Adriat. 23, 329–337 (1982).

    Google Scholar 

  58. 58.

    Montesanto, B. & Panayotidis, P. The Cystoseira spp. Communities from the Aegean Sea (NE Mediterranean). Mediterr. Mar. Sci. 2, 57 (2001).

    Article  Google Scholar 

  59. 59.

    Bianchi, C. N., Corsini-Foka, M., Morri, C. & Zenetos, A. Thirty years after: dramatic change in the coastal marine ecosystems of Kos Island (Greece), 1981–2013. Mediterr. Mar. Sci. 15, 482–497 (2014).

    Article  Google Scholar 

  60. 60.

    Mačić, V. & Antolić, B. Distribution of rare Cystoseira species along the Montenegro coast (South-Eastern Adriatic sea). Period. Biol. 117, 441–447 (2015).

    Article  Google Scholar 

  61. 61.

    Iveša, L., Djakovac, T. & Devescovi, M. Long-term fluctuations in Cystoseira populations along the west Istrian Coast (Croatia) related to eutrophication patterns in the northern Adriatic Sea. Mar. Pollut. Bull. 106, 162–173 (2016).

    Article  CAS  PubMed  Google Scholar 

  62. 62.

    Ignatiades, L., Gotsis-Skretas, O., Pagou, K. & Krasakopoulou, E. Diversification of phytoplankton community structure and related parameters along a large-scale longitudinal east-west transect of the Mediterranean Sea. J. Plankton Res. 31, 411–428 (2009).

    Article  Google Scholar 

  63. 63.

    Burgeot, T. et al. Oyster summer mortality risks associated with environmental stress. In Summer Mortality of Pacific Oyster Crassostrea gigas. The Morest Project. (eds. Samain, J. F. & McCombie, H.) 107–151 (EditionsQu. Versailles, 2008).

  64. 64.

    Kittle, R. P. & McDermid, K. J. Glyphosate herbicide toxicity to native Hawaiian macroalgal and seagrass species. J. Appl. Phycol. 28, 2597–2604 (2016).

    CAS  Article  Google Scholar 

  65. 65.

    Verdura, J., Sales, M., Ballesteros, E., Cefalì, M. E. & Cebrian, E. Restoration of a canopy-forming alga based on recruitment enhancement: methods and long-term success assessment. Front. Plant Sci. 9, 1832 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  66. 66.

    Murchie, E. H. & Lawson, T. Chlorophyll fluorescence analysis: a guide to good practice and understanding some new applications. J. Exp. Bot. 64, 3983–3998 (2013).

    CAS  Article  PubMed  Google Scholar 

  67. 67.

    Pinheiro, J. C. & Bates, D. M. Linear Mixed-Effects Models: Basic Concepts and Examples. In Mixed-Effects Models in Sand S-PLUS. Statistics and Computing. (eds. Pinheiro, J. C. & Bates, D. M.) 3–56 (Springer, New York, 2000).

  68. 68.

    Bates, D., Mächler, M., Bolker, B. & Walker, S. Fitting linear mixed-effects models using lme4. J. Stat. Softw. 67, 1–48 (2015).

    Article  Google Scholar 

  69. 69.

    Venables, W. N. & Ripley, B. D. Modern applied statistics with S. (2002).

  70. 70.

    Fox, J. & Weisberg, S. An R Companion to Applied Regression. (SAGE Pubblications, Inc., 2019).

  71. 71.

    Lenth, R. V. Least-squares means: the R package lsmeans. J. Stat. Softw. 69, 1–33 (2016).

    Article  Google Scholar 

  72. 72.

    Abdala-Díaz, R. T., Cabello-Pasini, A., Pérez-Rodríguez, E., Álvarez, R. M. C. & Figueroa, F. L. Daily and seasonal variations of optimum quantum yield and phenolic compounds in Cystoseira tamariscifolia (Phaeophyta). Mar. Biol. 148, 459–465 (2006).

    Article  CAS  Google Scholar 

  73. 73.

    Yu, Y. Q. et al. Diurnal changes of photosynthetic quantum yield in the intertidal macroalga Sargassum thunbergii under simulated tidal emersion conditions. J. Sea Res. 80, 50–57 (2013).

    ADS  Article  Google Scholar 

  74. 74.

    Gévaert, F. et al. Laminaria saccharina photosynthesis measured in situ: photoinhibition and xanthophyll cycle during a tidal cycle. Mar. Ecol. Prog. Ser. 247, 43–50 (2003).

    ADS  Article  Google Scholar 

  75. 75.

    Huppertz, K., Hanelt, D. & Nultsch, W. Photoinhibition of photosynthesis in the marine brown algae Fucus serratus as studied in field experiments. Mar. Ecol. Prog. Ser. 66, 175–182 (1990).

    ADS  Article  Google Scholar 

  76. 76.

    Davis, T. A. et al. A review of the biochemistry of heavy metal biosorption by brown algae. Water Res. 26, 265–275 (2011).

    ADS  Google Scholar 

  77. 77.

    Evans, L. K. & Edwards, M. S. Bioaccumulation of copper and zinc by the giant kelp Macrocystis pyrifera. Algae 26, 265–275 (2011).

    CAS  Article  Google Scholar 

  78. 78.

    Pan, Y. et al. Screening of seaweeds in the East China Sea as potential bio-monitors of heavy metals. Environ. Sci. Pollut. Res. 25, 16640–16651 (2018).

    CAS  Article  Google Scholar 

  79. 79.

    Hopkin, R. & Kain, J. M. The effects of some pollutants on the survival, growth and respiration of Laminaria hyperborea. Estuar. Coast. Mar. Sci. 7, 531–553 (1978).

    ADS  CAS  Article  Google Scholar 

  80. 80.

    Marsden, A. D., DeWreede, R. E. & Levings, C. D. Survivorship and growth of Fucus gardneri after transplant to an acid mine drainage-polluted area. Mar. Pollut. Bull. 46, 65–73 (2003).

    Article  PubMed  Google Scholar 

  81. 81.

    Pellegrini, M. et al. Interactions between the toxicity of the heavy metals cadmium, copper, zinc in combinations and the detoxifying role of calcium in the brown alga Cystoseira barbata. J. Appl. Phycol. 5, 351–361 (1993).

    CAS  Article  Google Scholar 

  82. 82.

    Mangialajo, L., Chiantore, M. & Cattaneo-Vietti, R. Loss of fucoid algae along a gradient of urbanisation, and structure of benthic assemblages. Mar. Ecol. Prog. Ser. 358, 63–74 (2008).

    ADS  Article  Google Scholar 

  83. 83.

    Strömgren, T. The effect of dissolved copper on the increase in length of four species of intertidal fucoid algae. Mar. Environ. Res. 3, 5–13 (1980).

    Article  Google Scholar 

  84. 84.

    Rodríguez-Prieto, C. & Polo, L. Effects of sewage pollution in the structure and dynamics of the community of Cystoseira mediterranea (Fucales, Phaeophyceae). Sci. Mar. 60, 253–263 (1996).

    Google Scholar 

  85. 85.

    Boudouresque, C. F., Marcot-Coqueugniot, J. & Nédélec, H. The phytobentos of a Mediterranean Harbour, Port Vendres. In Proceedings of the International Seaweed Symposium 229–234 (1981).

  86. 86.

    Costa, G. B. et al. Effects of copper and lead exposure on the ecophysiology of the brown seaweed Sargassum cymosum. Protoplasma 253, 111–125 (2016).

    CAS  Article  PubMed  Google Scholar 

  87. 87.

    Baumann, H. A., Morrison, L. & Stengel, D. B. Metal accumulation and toxicity measured by PAM-Chlorophyll fluorescence in seven species of marine macroalgae. Ecotoxicol. Environ. Saf. 72, 1063–1075 (2009).

    CAS  Article  PubMed  Google Scholar 

  88. 88.

    Topinka, J. A. & Robbins, J. V. Effects of nitrate and ammonium enrichment on growth and nitrogen physiology in Fucus spiralis. Limnol. Oceanogr. 21, 659–664 (1976).

    ADS  CAS  Article  Google Scholar 

  89. 89.

    Chapman, A. R. O. & Craigie, J. S. Seasonal growth in Laminaria longicruris: relations with dissolved inorganic nutrients and internal reserves of nitrogen. Mar. Biol. 40, 197–205 (1977).

    CAS  Article  Google Scholar 

  90. 90.

    Gerard, V. A. In situ rates of nitrate uptake by giant kelp, Macrocystis pyrifera (L.) C. Agardh: tissue differences, environmental effects, and predictions of nitrogen-limited growth. J. Exp. Mar. Biol. Ecol. 62, 211–224 (1982).

    CAS  Article  Google Scholar 

  91. 91.

    Buschmann, A. H. et al. Ecophysiological plasticity of annual populations of giant kelp (Macrocystis pyrifera) in a seasonally variable coastal environment in the Northern Patagonian Inner Seas of Southern Chile. J. Appl. Phycol. 26, 837–847 (2014).

    Article  Google Scholar 

  92. 92.

    Braga, A. D. C. & Yoneshigue-Valentin, Y. Growth of Laminaria abyssalis (Phaeophyta) at different nitrate concentrations. Phycologia 33, 271–274 (1994).

    Article  Google Scholar 

  93. 93.

    Wallentinus, I. Comparisons of nutrient uptake rates for Baltic macroalgae with different thallus morphologies. Mar. Biol. 80, 215–225 (1984).

    CAS  Article  Google Scholar 

  94. 94.

    Gordillo, F. J. L., Dring, M. J. & Savidge, G. Nitrate and phosphate uptake characteristics of three species of brown algae cultured at low salinity. Mar. Ecol. Prog. Ser. 234, 111–118 (2002).

    ADS  CAS  Article  Google Scholar 

  95. 95.

    Thomas, T. E., Harrison, P. J. & Taylor, E. B. Nitrogen uptake and growth of the germlings and mature thalli of Fucus distichus. Mar. Biol. 84, 267–274 (1985).

    Article  Google Scholar 

  96. 96.

    Nielsen, H. D., Brownlee, C., Coelho, S. M. & Brown, M. T. Inter-population differences in inherited copper tolerance involve photosynthetic adaptation and exclusion mechanisms in Fucus serratus. New Phytol. 160, 157–165 (2003).

    CAS  Article  Google Scholar 

  97. 97.

    Guillemin, M. L., Valenzuela, P., Gaitán-Espitia, J. D. & Destombe, C. Evidence of reproductive cost in the triphasic life history of the red alga Gracilaria chilensis (Graciliarales, Rhodophyta). J. Appl. Phycol. 26, 569–575 (2014).

    CAS  Article  Google Scholar 

  98. 98.

    Scanlan, C. M. & Wilkinson, M. The use of seaweeds in biocide toxicity testing. Part 1. The sensitivity of different stages in the life-history of Fucus, and of other algae, to certain biocides. Mar. Environ. Res. 21, 11–29 (1987).

    CAS  Article  Google Scholar 

  99. 99.

    Garman, G. D., Pillai, M. C. & Cherr, G. N. Inhibition of cellular events during early algal gametophyte development: effects of select metals and an aqueous petroleum waste. Aquat. Toxicol. 28, 127–144 (1994).

    CAS  Article  Google Scholar 

  100. 100.

    Chung, I. K. & Brinkhuis, B. H. Copper effects in early stages of the kelp Laminaria saccharina. Mar. Pollut. Bull. 17, 213–218 (1986).

    CAS  Article  Google Scholar 

  101. 101.

    Giesy, J. P., Dobson, S. & Solomon, K. R. Ecotoxicological Risk Assessment for Roundup® Herbicide. Rev. Environ. Contam. Toxicol. 167, 35–120 (2000).

    CAS  Google Scholar 

  102. 102.

    Pérez, G. L., Solange Vera, M. & Miranda, L. A. Nitrate and phosphate uptake characteristics of three species of brown algae cultured at low salinity. In Herbicides and Environment (ed. Kortekamp, A.) 343–368 (InTech, 2011).

  103. 103.

    Solomon, K. R. & Thompson, D. G. Ecological risk assessment for aquatic organisms from over-water uses of glyphosate. J. Toxicol. Environ. Heal. Part B Crit. Rev. 6, 289–324 (2003).

  104. 104.

    Cedergreen, N. & Streibig, J. C. The toxicity of herbicides to non-target aquatic plants and algae: assessment of predictive factors and hazard. Pest Manag. Sci. 61, 1152–1160 (2005).

    CAS  Article  PubMed  Google Scholar 

  105. 105.

    Pang, T., Liu, J., Liu, Q., Zhang, L. & Lin, W. Impacts of glyphosate on photosynthetic behaviors in Kappaphycus alvarezii and Neosiphonia savatieri detected by JIP-test. J. Appl. Phycol. 24, 467–473 (2012).

    CAS  Article  Google Scholar 

  106. 106.

    Franz, J. E., Mao, M. K. & Sikorinski, J. A. Glyphosate, a unique global herbicide. Weed Technol. 12, 564–565 (1998).

    Article  Google Scholar 

  107. 107.

    Siehl, D. L. Inhibitors of EPSP synthase, glutamine synthetase and histidine synthesis. In Herbicide Activity:Toxicology, Biochemistry and Molecular Biology (eds. Roe, R. M., Burton, J. D. & Kuhr, R. J.) 37–67 (1997).

  108. 108.

    Duke, S. O., Baerson, S. R. & Rimando, A. M. Glyphosate. In Encyclopedia of Agrochemicals (John Wiley & Sons, Inc., 2003).

  109. 109.

    Billen, G. et al. Nitrogen flows from European regional watersheds to coastal marine waters. Eur. Nitrogen Assess. 271–297 (2011).

  110. 110.

    Giani, M. et al. Recent changes in the marine ecosystems of the northern Adriatic Sea. Estuar. Coast. Shelf Sci. 115, 63–74 (2012).

    ADS  Article  Google Scholar 

  111. 111.

    EEA. Nutrients in transitional, coastal and marine waters (CSI 021). (2015).

  112. 112.

    Strain, E. M. A., Thomson, R. J., Micheli, F., Mancuso, F. P. & Airoldi, L. Identifying the interacting roles of stressors in driving the global loss of canopy-forming to mat-forming algae in marine ecosystems. Glob. Change Biol. 20, 3300–3312 (2014).

    ADS  Article  Google Scholar 

  113. 113.

    Halpern, B. S. et al. A global map of human impact on marine ecosystems. Science 319, 948–952 (2008).

    ADS  CAS  Article  PubMed  Google Scholar 

  114. 114.

    Verdura, J., Sales, M., Ballesteros, E., Cefalí, M. E. VI Jornades de Medi Ambient de les Illes Balears. In Programa de seguiment científic de l’Estació d’Investigació “Jaume Ferrer”: recuperació d’una població de Cystoseira barbata desapareguda a Cala Teulera (Port de Maó) (ed. Pons, G. X., del Valle, L., Vicens, D., Pinya, S., McMinn, M., Pomar, F.) 180–183 (Societat d'Història Natural de les Balears. Maó, Spain, 2018).

  115. 115.

    Falace, A., Kaleb, S., De La Fuente, G., Asnaghi, V. & Chiantore, M. Ex situ cultivation protocol for Cystoseira amentacea var. stricta (Fucales, Phaeophyceae) from a restoration perspective. PLoS ONE 13, e0193011 (2018).

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We would like to thank Jorge Santamaría for his valuable help during the experiments and Sílvia Terradas and Paula Mura for technical support. This project has received funding from the Horizon 2020 EU Research and Innovation Program (MERCES; No. 689518) the European Union’s EMFF program, AFRIMED (EASME/EMFF/2017/ and the Spanish Ministry Project ANIMA (CGL2016-76341-R, MINECO/FEDER, UE). SC, JV, AV and EC are members of the Catalan Government’s consolidated research group 2017 SGR 1521 MedRecover.

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S.C., J.V. and E.C. conceived the ideas and designed methodology. S.C., J.V. collected samples in the field and performed pollution experiments in aquaria. S.C., J.V. and E.C. analyzed the data. S.C. and E.C. led the writing of the manuscript. S.C., J.V., A.V., E.B. and E.C. contributed significantly to the draft of the paper and gave final approval for publication.

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Correspondence to Sònia de Caralt or Emma Cebrian.

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de Caralt, S., Verdura, J., Vergés, A. et al. Differential effects of pollution on adult and recruits of a canopy-forming alga: implications for population viability under low pollutant levels. Sci Rep 10, 17825 (2020).

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