Nomenclature

Scientific name

The currently accepted scientific name is Pelvetia canaliculata (Linnaeus) Decaisne & Thuret 1845 but the species was previously known (basionym) as Fucus canaliculatus Linnaeus 1767 (Guiry and Guiry 2021).

Nomenclatural synonyms

The following homotypic synonyms (i.e. corresponding to the same type) are listed by Guiry and Guiry (2021):

  • Fucus canaliculatus Linnaeus 1767

  • Halidrys canaliculata (Linnaeus) Stackhouse 1809

  • Fucodium canaliculatum (Linnaeus) J. Agardh 1848

  • Ascophyllum canaliculatum (Linnaeus) Kuntze 1891

  • Ascophylla canaliculata (Linnaeus) Kuntze 1891

In addition, the species has several heterotypic synonyms including Fucus excisus Linnaeus 1753, Pelvetia canaliculata f. radicans Foslie 1894, Pelvetia canaliculata var. libera S.M. Baker 1912, or Pelvetia canaliculata var. acutilobata Lami 1939.

Vernacular names

Pelvetia canaliculata is known as Cow Tang or Channelled Wrack (Dickinson 1963; Lyons 2000) in English; its common name in Gaeilge / Irish is Dúlamán (Lyons 2000; Guiry and Guiry 2021), and it is referred to as Botelho-bravo in Portuguese (Pereira 2015, 2016).

Taxonomy and genetic data

Pelvetia canaliculata (Linnaeus) Decaisne & Thuret is a common brown macroalga (Phylum Ochrophyta, Class Phaeophyceae), belonging to the Fucaceae within the order Fucales (Silberfeld et al. 2014; Guiry and Guiry 2021). Pelvetia canaliculata is the only species within the monotypic genus Pelvetia. Other species previously reported in this group (i.e. Pelvetia babingtonii, P. compressa, P. siliquosa, and P. limitata) have been reclassified within the genus Silvetia by Serrão et al. (1999), and are therefore not included in this review. Based on the internal transcribed spacers (ITS-1, ITS-2 and 5.8S sequences) of nrDNA, Serrão et al. (1999) demonstrated differences in the nucleic acid sequence, as well as in the structure of the oogonia. Using phylogenetic markers, Cánovas et al. (2011) showed that the diversification of the Fucaceae occurred around 19.5–7.0 million years (Ma) old. Divergence of the lineage leading to P. canaliculata was estimated at 16.4–5.4 Ma and could have taken place during opening of the Bering Strait in the latest Miocene. Pelvetia canaliculata is closely related to Ascophyllum nodosum, Pelvetiopsis limitata, Hesperophycus californicus and Fucus spp., a group of species commonly named ‘fucoids’. Fucoids dominate North-East Atlantic temperate intertidal rocky shores, forming distinct distributional zones which are determined by abiotic and biological constraints (Schonbeck and Norton 1980; Serrão et al. 1999; Silberfeld et al. 2014).

Although there is no complete genome reported for P. canaliculata (NCBI database, https://www.ncbi.nlm.nih.gov/ searched 21 January 2022), some molecular analyses have been conducted, based mainly on ribosomal RNA-genes, cytochrome oxidase (cox1, cox3), photosystem II proteins (psbA, psaA), ATP synthase subunits (atp9, atpB), NADH dehydrogenase (nad1, nad4), ribulose-1,5-bisphosphate carboxylase large subunit (rbcL) and small subunit (rbcS) genes.

Morphology and anatomy

External morphology

The mature thalli of P. canaliculata typically reach a length of 10–15 cm, with dichotomously dividing branches. The young thalli are greenish-yellow, turning brown with age, forming dense tufts of linear and leathery fronds from 0.5 to 1 cm in width, without a midrib or air bladders (Fig. 1). The common name ‘channelled wrack’ refers to its distinct inwardly curled branches, folded like a narrow canal/channel which retains moisture, or even water, at least initially during emersion. Desiccated thalli have a characteristic black and crispy appearance, and moisture can be quickly absorbed from air at high humidity or during periods of rainfall permitting survival during long periods of emersion between tidal cycles. Thalli are fixed to rocky substrata by a small basal disc having the shape of a truncated cone-shaped disc, 4–6 mm wide and 3–5 mm high (Almaraz et al. 1995). During the reproductive season in summer, yellow-orange receptacles of 1–2 cm long are visible at the terminal of the branches (Subrahmanyan 1957). They form swollen irregularly shaped depressions, containing numerous conceptacles that are visible as dots (Fig. 1C, D; and Sect. “Life cycle, reproduction and development”).

Fig. 1
figure 1

Illustration of Pelvetia canaliculata, Co. Galway, Ireland. (A) Adult thalli on the upper shore, absent from rockpools; B) Expansion of the mat-forming juveniles surrounding adult individuals; C) Sporelings, 1–20 mm long, on rocky substratum; D) Fertile thalli displaying channelled structure and bearing reproductive structures; E) Receptacles with flask cavities corresponding to the conceptacles

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Anatomy and cytology

Similar to other fucaceaen species, P. canaliculata has a parenchymatous structure, formed by three different tissue types, i.e. the meristoderm, the cortex and the medulla (Almaraz et al. 1995). The meristoderm is monostratified and consists of rectangular epidermal cells (6–28 µm long / 17–39 µm wide), whereas the cortex consists of a few layers of rounded cells (7–28 µm long / 7–31 µm wide). The medulla consists of circular cells (diameter 15–50 µm in the central part of the thallus), arranged around large intracellular spaces. Growth occurs at the apex, where a larger cell is surrounded by smaller cells, constituting the pro-meristem. In contrast to the apex, basal cells of the attachment disc are distributed in a disorderly fashion, forming a compact structure without differentiated layers. The meristoderm cells are larger at this point (Almaraz et al. 1995). Within receptacles, conceptacles consist of cavities with walls formed by several layers of flattened cells. Paraphyses are branched filaments formed by rectangular cells, developed from conceptacle walls (Subrahmanyan 1957).

The thallus of P. canaliculata is entirely covered by a mucilaginous layer mainly composed of sulphated polysaccharides, while alginic acid is the main constituent of the cell wall (see Sect. “Carbohydrates” for more details on polysaccharide composition) (Evans et al. 1973). Within epidermal cells, chloroplasts and nuclei are generally located in the basal part of the cells. Numerous Golgi bodies (ca. 0.5–1 µm long) are situated around the nucleus, and many vesicles are found near the surface of epidermal cells (Evans 1968; Evans et al. 1973). Electron microscopy revealed that P. canaliculata, similar to A. nodosum, contains no pyrenoids (Evans 1968). The chloroplasts have transverse lamellated thylakoids that are U-shaped at certain points (Fig. 2).

Fig. 2
figure 2

Micrograph (632 × 45,000) of a chloroplast of Pelvetia canaliculata from Evans (1968) with permission from © John Wiley & Sons, Inc., indicating the absence of a pyrenoid. The U-shape of the thylakoids (arrowed) is characteristic of the species

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Distribution and ecology

Geographical distribution and global change impact

Pelvetia canaliculata is a common species on sheltered to moderately-exposed rocky shores in the North-East Atlantic, distributed from the Arctic Ocean and Norwegian Sea to the Atlantic coasts of the Iberian peninsula, including the North Sea and the English Channel. The species is abundant in Iceland, Norway, Netherlands, Great Britain, Ireland, as well as in France, Portugal and Spain (Fig. 3).

Fig. 3
figure 3

Geographical distribution of Pelvetia canaliculata, adapted with permission from Springer Nature Customer Service Centre GmbH: [Springer] [Seaweed Phylogeography] by Neiva et al. (2016), © 2016; and according to distribution data of AlgaeBase (Guiry and Guiry 2021)

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Based on mitochondrial DNA and species distribution models, Neiva et al. (2016) investigated the geographical history of Pelvetia. They suggest that the species experienced a substantial post-glacial latitudinal range shift (models having revealed possible habitats in southern Morocco), and that populations at its southern limit could be at risk from climate change. Contrastingly, the projections of other models suggested that the distribution of P. canaliculata (and A. nodosum) is related to non-climatic drivers such as wave exposure and substratum availability (Martinez et al. 2012). A local extinction has been reported from Berlengas Island off central Portugal, which may be related to sea surface temperature (SST) warming (Neiva et al. 2016). Moreover, by comparing the fucoid assemblages in northern Spain (Asturias) between 1977 and 2007, Lamela-Silvarrey et al. (2012) noted a decrease in biomass and primary net production of P. canaliculata. This could be the result of a higher grazing pressure, shortened growth periods, inter-annual fluctuations or early evidence of climate change impacts, emphasizing the need to map and monitor seaweed populations. The application of emerging technologies, such as unoccupied aerial vehicle (UAV)-mounted hyperspectral remote sensing, may allow the accurate mapping of canopy-forming species including P. canaliculata and thus aid effective and sustainable management (Rossiter et al. 2020).

Local horizontal and vertical distribution

Pelvetia canaliculata occupies the extreme upper regions within the intertidal zone above mean high water neap (MHWN). It can be exposed to atmospheric conditions for several days, experiencing large and extreme variations in temperature and irradiance, in addition to osmotic and nutrient stress (Haas and Hill 1933; Schonbeck and Norton 1980; Pfetzing et al. 2000). Its distribution ranges from the lower limit of the spray zone (supralittoral zone) often dominated by lichens (e.g., Hydropunctaria maura – formerly Verrucaria maura), to the upper limit of the intertidal canopy, sometimes overlapping with Fucus spiralis. Depending on shore topography, it forms a distinct and characteristic band on North-East Atlantic shores, which can extend across several meters (Cotton 1912; Schonbeck and Norton 1980). Its vertical zonation implies a high resistance to prolonged emersion and resultant desiccation. Its slow growth rate, intolerance to prolonged submergence, a relatively high light requirement and a high sensitivity to grazers are factors considered to contribute to the extreme vertical distribution of Pelvetia (Schonbeck and Norton 1980).

Environmental factors

Desiccation

Pelvetia canaliculata is highly tolerant to extreme and prolonged water loss, surviving several consecutive days between spring tides in an emersed state (up to 90% of time; Fish and Fish 1989). Dring and Brown (1982) demonstrated that P. canaliculata (and F. spiralis) could tolerate water loss of 80 to 90% and regained complete photosynthetic capacity within 2 h, while Fucus serratus and Laminaria digitata could not tolerate a water loss exceeding 60 and 55%, respectively. Pfetzing et al. (2000) showed that P. canaliculata recovered fully even when algae were emersed for up to 7 days at 10˚C. Contrastingly, recovery at 25˚C was complete after emersion for 4 days, but not for 8 days, indicating that tolerance was temperature-dependent. Meanwhile, % dry matter and drought-tolerance of P. canaliculata (assessed in experimental desiccation treatments) also exhibited seasonal variation (Schonbeck and Norton 1979b).

Unlike most other brown macroalgae, P. canaliculata is unable to tolerate prolonged submersion and requires regular emersion periods (De Oliveira and Fletcher 1977; Rugg and Norton 1987). In contrast to low-intertidal F. serratus which grew well when submerged for 11 h in culture, P. canaliculata performed better when submersed for only 1–2 h; when submerged for 11 h, signs of necrosis occurred (Schonbeck and Norton 1979a). More recently, Kim et al. (2011) also reported that P. canaliculata germlings exhibited better growth under periodic exposure than continuous submergence and were less sensitive to emersion than F. spiralis germlings. This intolerance to prolonged submersion also may explain its consistent absence from rockpools (Fig. 1A).

Temperature

Based on its geographic distribution in the North-East Atlantic from Norway to Portugal (see Sect. “Geographical distribution and global change impact”), P. canaliculata experiences, and apparently tolerates, a wide range in both water and atmospheric temperatures. Its high-shore position superimposes additional diurnal and tide-imposed temperature fluctuations, with exposure to low or high temperatures (which can be below 0˚C or exceeding 30˚C depending on location and time of the year) during emersion. According to Strömgren (1977), experimental short exposure to high temperature (> 20˚C) has a positive effect on growth rate; however, prolonged exposure to water temperatures above 30–35˚C induced growth cessation. It is likely that the reported tolerance to extreme temperatures depends on whether thalli were emersed or submersed. Also, culture experiments suggested that the optimum growth temperature and the response of P. canaliculata to temperature fluctuation depended on season (Pfetzing et al. 2000). The degree of short-term growth responses was strongly positively correlated with temperature in winter, and less pronounced in summer: maximum growth occurred between 10 and 20˚C in algae collected in February, but at 20–23˚C for samples collected in June and April (Pfetzing et al. 2000). In situ studies suggest that extreme temperatures can cause damage (bleaching and deaths of individuals) as observed during the exceptionally hot weather in summer 1983 on the Isle of Man (Hawkins and Hartnoll 1985). Regarding effects of temperature on biochemical composition, Pfetzing et al. (2000) demonstrated an increase in both volemitol and mannitol content when algae were grown at elevated temperatures under controlled conditions.

Light

Exposure to light is suggested to be a factor controlling the distribution of P. canaliculata. Compared to mid-intertidal or lower shore species, P. canaliculata experiences longer emersion periods, thus receiving higher dosages of photosynthetically active radiation (PAR) which implies a greater requirement for light tolerance and photoprotection. Harker et al. (1999) compared the responses of P. canaliculata and Saccharina latissima (previously Laminaria saccharina) to saturating light: an increase in non-photochemical quenching of fluorescence (NPQ) and de-epoxidation ratio (DR) of the xanthophyll cycle was observed in both species. However P. canaliculata appeared more tolerant to light stress as it exhibited a two-fold higher NPQ, and this was correlated with a DR of 0.65 (compared to 0.5 in S. latissima). Comparing hydrated and desiccated thalli, the same authors also reported that DR was higher in P. canaliculata than in S. latissima at the same level of desiccation. After prolonged emersion, the efficiency of de-epoxidation and thus the xanthophyll cycle in P. canaliculata decreased gradually, suggesting a decline in photoprotection capacity over time (Harker et al. 1999). Hupel et al. (2011) showed that UV treatments (i.e. PAR, PAR + UV-A or PAR + UV-B for 21 days) had no effect on chlorophyll content, and that there were no effects on phenolic content or antioxidant capacity after UV-B exposure.

Carotenoid composition is likely to be responsible for the high photoprotective capacities of P. canaliculata (Harker et al. 1999; Hupel et al. 2011). Indeed, the xanthophyll cycle pool size (i.e. sum of violaxanthin, antheraxanthin and zeaxanthin) was higher in P. canaliculata than in S. latissima, and the ability to accumulate zeaxanthin was three times that of S. latissima (Harker et. al 1999). By isolating the two subunits of the light-harvesting complexes (LHC) from P. canaliculata, De Martino et al. (1997) showed a heterogeneity in xanthophyll distribution that could indicate a specific photoprotective role for one of the two sub-units. While the more acidic fraction contained chlorophyll-a, chlorophyll-c and fucoxanthin, the less acidic fraction had a more complex pigment composition, i.e. similar levels of chlorophyll-a but additionally pigments from the xanthophyll cycle. In addition to adjusting its xanthophyll cycle, P. canaliculata can acclimate quickly to high light through its phenolic composition as suggested by Connan et al. (2007) who demonstrated a trend to diurnal alternations in the phenolic pool. Similarly, Kirke et al. (2019) reported a seasonal shift in phlorotannin isomerization, likely to be caused by combined effects of light, temperature and dehydration, which also was reflected in bioactivity profiles.

In culture, embryos of Pelvetia could survive for only 90 days in darkness, in contrast to those of F. spiralis which survived for more than 120 days (De Oliveira and Fletcher 1977). Light may thus also be a contributing factor to inter-specific competition (see Sect. “Associated species and species interactions”) with shading by Fucus spp. canopies limiting the recruitment and ultimate distribution of P. canaliculata (Schonbeck and Norton 1980).

Wave exposure

The distribution of P. canaliculata seems to be negatively affected by wave exposure, as suggested by its absence, or relatively reduced density, at the most exposed sites (Subrahmanyan 1960; Dunstone et al. 1979; Burrows et al. 2008). In such sites, thalli also tend to be smaller and bushier as the number of dichotomies increases with wave exposure (Dunstone et al. 1979). Subrahmanyan (1960) found that P. canaliculata settled more easily and grew faster on rough and sheltered substrata; impacts of high wave exposure on germling settlement may thus ultimately limit its distribution.

Nutrient and CO2 availability

Nutrients accumulated by macroalgae (i.e. including inorganic forms of nitrogen, phosphate, carbon) are generally supplied by surrounding seawater during submersion. Additionally, in intertidal species, carbon can also be assimilated directly from air during emersion whilst algae are sufficiently hydrated for photosynthesis to take place (Maberly and Madsen 1990). High activity of carbonic anhydrase, an enzyme which plays an important role in CO2 conversion, was observed in Pelvetia (Giordano and Maberly 1989). Photosynthetic activity and productivity of intertidal algae including P. canaliculata are thus likely to benefit from current increases in atmospheric carbon (Ní Longphuirt et al. 2013).

As nutrient availability is dependent on tidal cycle and shore level, P. canaliculata potentially experiences severe nutrient deficiency during prolonged periods of emersion as it is located in the extreme upper intertidal zone. The low phosphate uptake rates reported for both Pelvetia and A. nodosum suggest a low nutrient requirement, regardless of season (compared to Fucus spp. for which uptake rate slightly decreased in summer; Hurd and Dring 1990). However, Pelvetia accumulated six times more phosphate than A. nodosum within 1 h, which may be related to the respective shore positions of the two species (Hurd and Dring 1990). Studying the phosphate uptake of several fucoid species, Hurd and Dring (1990) demonstrated that P. canaliculata and Fucus spp. exhibited a transient uptake pattern, i.e. an initial high absorption (resulting from previous phosphate limitation, ~ 1 h), followed by a zero-uptake phase (~ 1 h), and, finally, a stabilization of uptake rate at an intermediate level.

The nutrient requirement of Pelvetia also appears to depend on season and immersion time, with growth being reduced under nutrient shortage (Schonbeck and Norton 1979a, b). When exposed to nutrient limitation in the laboratory, winter-collected individuals grew faster when submersed for longer periods, while immersion time had no effect on the growth rate of thalli collected in summer, possibly as they were already acclimated to low nutrient levels (Schonbeck and Norton 1979a,b).

Salinity

Pelvetia canaliculata appears to be more abundant in sites with reduced seawater salinity (Dunstone et al. 1979), although it can withstand severe osmotic stress as implied by its location within the upper intertidal zone. Here, osmotic stress arises from water loss and evaporation during prolonged periods of emersion, and low salinity conditions during dilution by freshwater inflow or rain, which implies a high physiological acclimation potential of P. canaliculata. The species has a high cation-exchange capacity that may be involved in osmotic regulation; it accumulates high amounts of mannitol (in addition to volemitol), a known osmolyte present in many brown macroalgae (Reed et al. 1985) (see Sect. “Carbohydrates” and “Animal feed”). Interestingly, in sheltered salt marshes, P. canaliculata occurs in two morphological forms: the common P. canaliculata and P. canaliculata var. libera. The latter is distinguished by its distinct thallus shape (curling of the younger parts of the thallus), its colour (darker) and by the fact that it is unattached (Baker 1912). In addition, reproduction is mostly, if not entirely, vegetative.

Associated species and species interactions

As P. canaliculata inhabits the upper most zone on temperate rocky shores, it is typically only accompanied by few other macroscopic species. Its distribution may be intermixed with maritime lichens (such as Lichina and Hydropunctaria/Verrucaria species), Littorina spp. and barnacles (Chthamalus montagui, Chthamalus stellatus or Semibalanus balanoides), as well as Catenella casepitosa and Hildenbrandia rubra (Rhodophyta). Depending on niche availability, small patches of F. spiralis or F. ceranoides may be associated with P. canaliculata. The marsh form P. canaliculata var. libera sometimes co-occurs with the red alga Bostrychia scorpioides (Haas and Hill 1933). Intolerant to extended submersion, P. canaliculata is absent from rockpools which are commonly occupied by Ulva intestinalis (Chlorophyta) at this high shore level, although small patches of U. intestinalis may be present in damp patches or underneath mature P. canaliculata. Evidence from the North Wales coast suggests that the associated epifaunal community is limited but commonly includes amphipods, Littorina saxatilis, Littorina obtusa, Apohyale prevostii (previously Hyale nilssoni) or Acarines sp., with species abundance influenced by thallus size and abiotic conditions such as wave exposure (Dunstone et al. 1979).

The extreme vertical distribution of P. canaliculata reduces competition with Fucus spiralis, a species less tolerant to desiccation which grows faster, and which is typically positioned just below the Pelvetia zone. Pelvetia zygotes failed to reach macroscopic size in the presence of F. spiralis but when this species was removed experimentally, Pelvetia distribution extended to lower levels before recolonization by F. spiralis (Schonbeck and Norton 1980; Hawkins and Hartnoll 1985). Also, Kim et al. (2011) reported reduced growth of Pelvetia germlings when mixed with F. spiralis germlings in cultures, emphasizing a potential inter-specific competition.

Pelvetia lives in symbiotic association with several fungi (Sutherland 1915), especially with the obligate Mycophycias ascophylli (basionym Stigmidium ascophylli (Cotton) Aptroot 2006), an endophytic ascomycete also encountered in Ascophyllun nodosum (Smith and Ramsbottom 1915; Kingham and Evans 1986; for a recent review, see Garbary et al. 2017). Using enzyme immunoassay systems, mycotoxins such as diacetoxyscirpenol, PR-toxin, mycophenolic acid, deoxynivalenol, and cyclopiazonic acid (> 1000 ng g−1) were detected in Pelvetia thalli from the Kandalaksha Gulf (Russia), produced by the association with micromycetes (Burkin et al. 2021). Mature receptacles of P. canaliculata can also be infected by M. ascophylli where mycelia cross the intercellular spaces of the cortical region, leading to a decrease in the number of receptacles (Subrahmanyan 1957). In addition to fungi, a strain of the bacterium Streptomyces cyaneofuscatus M-27 was isolated from the inner part of Pelvetia receptacles, and more isolates were detected in summer due to the seasonal reproduction of the alga. Some chemical compounds produced by this bacterial strain were identified as belonging to anthracycline family, exhibiting antitumor and antifungal activities (Braña et al. 2015). Proteobacteria and Actinobacteria are the predominant cultivable bacterial endophytes associated with P. canaliculata, mostly Pseudoalteromonas, Rhodococcus, and Bacillus (19, 16, and 13%, respectively) (Tourneroche et al. 2019). Future metagenomics approaches of seaweed microbiomes will undoubtedly reveal further insights into seaweed-bacteria physical and chemical interactions (Egan et al. 2013).

Life history

Life cycle, reproduction and development

Pelvetia canaliculata is a perennial species with a reproductive period from January to November, followed by growth and development of juveniles between August and December. Receptacles develop at the tip of the fronds, typically beginning to emerge in January although at this time they are difficult to differentiate from vegetative parts and reach maturity in summer (Subrahmanyan 1957) (see Fig. 1D in Sect. “External morphology”). The life cycle is dominated by the diploid phase: when haploid gametes are fertilized, they form a diploid zygote which develops into a mature (diploid) individual (Fig. 4). Similar to other Fucales, P. canaliculata has monoecious thalli: receptacles contain hermaphrodite conceptacles that produce both male (i.e. antherozoids (also called “spermatozoids”) within antheridia) and female (i.e. oosphere/egg within oogonia) gametes on the same individual (Fig. 4) (Manton et al. 1953; Hardy and Moss 1979). Sexual maturity is reached after at least two years, while the life expectancy is about 4 to 5 years.

Fig. 4
figure 4

A Life cycle of Pelvetia canaliculata (drawing of the fertile individual, adapted from William H. Harvey, Phycologia Britannica, plate CCXXIX, 1846–1851), with conceptacle and details A1 and A2, adapted from Subrahmanyan (1957). Illustrations of (B) Oogonium almost mature containing two oospheres and (C) Zygote (Hardy and Moss 1979, © International Phycological Society, http://intphycsociety.org, reprinted with permission of Taylor & Francis Ltd, http://www.tandfonline.com on behalf of International Phycological Society, http://intphycsociety.org)

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Compared to other species of Fucales, the first division of the initial development of the conceptacle of P. canaliculata is longitudinal (Subrahmanyan 1957). The cells in conceptacle can be differentiated by their prominent nucleus and dense cytoplasm. The uppermost cells of the lining tissue of the conceptacle elongate to then form oogonia (i.e. female reproductive structure) and many paraphyses (i.e. sterile filaments that can be branched or unbranched). Antheridia (i.e. male reproductive structure producing spermatozoids) develop subsequently on paraphyses (see Subrahmanyan (1957) for a more detailed description of conceptacle development in comparison with that of other Fucales). Once conceptacles are mature, gametes are released in the surrounding seawater from August to September (Moss 1974). Although smaller, the proboscis-bearing spermatozoids are similar to those of Fucus (Fig. 4C), with 64 spermatozoids produced by each antheridium (Manton et al. 1953; Subrahmanyan 1957). The eggs resulting from the external fertilization are protected in the thallus groove until the development of the zygotes, which is controlled by light and temperature (Moss 1974). Pelvetia zygotes germinate more quickly than Fucus zygotes, i.e. after 9–12 h compared to 13–17 h, respectively (Kropf 1989).

Pelvetia has the particularity to produce two spherical oospheres (or ‘eggs’) in an oogonium which undergoes multiple cell divisions (Subrahmanyan 1957; Evans 1968; Moss and Hardy 1979) (see Fig. 4B). Each oogonium is surrounded by three distinct layers, i.e. the exochiton, the mesochiton and the endochiton. The pair of oospheres is released from a mature oogonium after the exochiton rupture. The remaining mesochiton, which is about 8 µm thick, may protect eggs from desiccation (Moss 1974) or could participate to the subsequent attachment of the zygote to the substratum prior to rhizoid development (Hardy and Moss 1979). Consisting of two transparent fibrous layers composed of both alginates and fucoidans (Moss 1974), the presence of the mesochiton around both oospheres, which persists for a long time compared to Fucus spp., can affect antherozoid penetration. This may result in differential stages of development of the two zygotes from of the same pair (Hardy and Moss 1979). Moss (1974) showed that spermatozoids penetrate the oospheres in the equatorial zone of the mesochiton.

Compared to other fucalean species, in P. canaliculata the initiation of rhizoids from the zygote can be delayed by several days after egg release: in cultures, rhizoids were generally visible 13 to 17 days after fertilization, emerging through the mesochiton layer (Moss 1974; Hardy and Moss 1979). The cytoplasmic calcium (Ca2+) plays an important role in rhizoid growth and zygote development (Kropf 1989). Ca2+ gradients contribute to zygote polarity / axis orientation, in addition to other factors such as light orientation. The resulting axis determines where the first rhizoid will emerge. Latest updates on polarity induction in Pelvetia were reviewed by Kropf (1997).

Algal growth and population structure

Pelvetia canaliculata is a slow-growing species, increasing in length by 1.8 to 4.8 cm per year, based on removal experiments from the Isle of Man (Subrahmanyan, 1960). As a result, the species is not suitable for cultivation, limiting its potential for valorization. Life expectancy is thought to be 4–5 years, although there are only limited data on population structure (e.g. age composition, size class distribution, sex ratio, density). Thallus density appears to be negatively correlated with size (Dunstone et al. 1979), and distribution is dependent on hydrodynamic conditions (see Sect. “Wave exposure”). A decrease in dry weight (DW) of Pelvetia was observed in July–August, coupled with a decrease in mannitol content (Black 1949).

Chemical composition

Several studies have reported on the chemical composition of P. canaliculata, specifically focusing on the high content of carbohydrates, alginic acid and mannitol (Black 1949; Black et al. 1952; Sousa et al. 2021) (Table 1).

Table 1 Examples of chemical composition of Pelvetia canaliculata reported in the literature. These data do not take into consideration spatio-temporal variations resulting from both adjustment to environmental conditions and adaptive features, as presented in more detail in Sect. “Inorganic constituents” and “Organic constituents”
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Water content

Maehre et al. (2014) estimated the water content of P. canaliculata to be 615.6 g kg−1 fresh weight. However, such data are difficult to interpret in isolation as water content is strongly dependent on time of collection / season and environmental conditions (e.g. tidal cycle, relative humidity, wind speed, solar radiation and temperature impact the desiccation rate), and on the technique used to assess moisture. As an example, during tidal emersion, Pelvetia displayed a water loss of 68% in 8.5 h in March, compared to 63% in 9.25 h in July, with most water lost within the three first hours (Isaac 1933). In situ, individual thalli of Pelvetia can lose 60% in weight after 8.75 h of air-exposure, compared to 47.75% when covered by other individuals (Isaac 1933). Previous comparative observations on the salt marsh form P. canalicuata var. libera and the common form occurring on rocky shores suggested that surrounding vegetation strongly affected evaporation (De Oliveira and Fletcher 1977). There was a linear relationship between water content and photosynthesis and respiration for both forms but, under natural conditions, surrounding humidity regimes affected retention of photosynthetic activity (De Oliveira and Fletcher 1977).

Inorganic constituents

Ash, mineral and metal content

The reported ash content of P. canaliculata, representative of the total amount of minerals, ranges from 200 to 220 g kg−1, which is equivalent to 15 to 25% DW (Table 1). Black (1949) demonstrated that the observed seasonal variation in ash content of P. canaliculata corresponded to that of mannitol, reaching a minimum in September. Tayyab et al. (2016) observed a higher ash content in spring (219 g kg−1) than in autumn (210 g kg−1), and ash represented 199 and 174 g kg−1 dry matter of P. canaliculata from Bodø (Norway) in spring and autumn, respectively (de la Moneda et al. 2019). A more detailed overview of the specific mineral composition of P. canaliculata (and other macroalgal species) is presented in Biancarosa et al. (2018) and Maehre et al. (2014). Pelvetia can accumulate heavy metals and, for example, contained the highest level of mercury among 21 species of red, brown and green macroalgae studied, with 0.04–0.05 mg kg−1 DW (Maehre et al. 2014; Biancarosa et al. 2018). Compared to other brown macroalgae, P. canaliculata also contained high levels of copper (Cu) and iron (Fe), with 2.6–3.9 and 130–300 mg kg−1 DW, respectively. By contrast, Pelvetia contained relatively small amounts of phosphorus (P), calcium (Ca), and potassium (K), representing respectively 0.70, 14, and 17 g kg−1 DW (Biancarosa et al. 2018). When collected from clean, near-pristine waters in Ireland, Pelvetia and F. spiralis possessed a lower zinc concentration (~ 20 mg kg−1) than other macroalgae, possibly related to their upper shore position (Stengel et al. 2004). In comparison, Pelvetia from a polluted estuary in mid-western Ireland contained up to 400 mg Zn kg−1 DW (O’Leary and Breen (1997), demonstrating the importance of biomass origin when reporting and interpreting such data.

Inorganic nitrogen

Nitrogen (N), in the forms of nitrate, nitrite or ammonium, is one of the main elements required by seaweeds for growth. Typically, N content in brown macroalgae is lower than in red or green species and follows fluctuations in ambient water. As an example, the N content of P. canaliculata collected Norway represented 16.3 and 6.88 g kg−1 DW in spring and autumn, respectively (de la Moneda et al. 2019), following seasonal nutrient availability in seawater. Early studies by Haas and Hill (1933) suggested that total N represented 2.19% DW in P. canaliculata, compared to 1.02% in the marsh form P. canaliculata f. libera. The same authors highlighted the absence of ammonia (NH3) in P. canaliculata exposed to the air, in contrast to submersed specimens, as well as a decrease in the amino nitrogen relative to amide nitrogen.

Organic constituents

Carbohydrates

Sulphated polysaccharides

Alginates (or alginic acid) and sulphated polysaccharides are the major carbohydrates found in brown seaweeds, where they are, together with proteins and cellulose, the primary components of cell walls (Kloareg et al. 1986). Fucans and fucoidans are the most abundant sulphated polysaccharides and can be synthesized by all cell types in Pelvetia as observed by using a labelling with 35SO4 followed by autoradiography (Evans et al. 1973). They are structurally and compositionally highly diverse, being composed of l-fucose in addition to other sugar monomers in different proportions. Sulfated fucans may be polymerized as neutral polysaccharides and subsequently modified by sulfotransferases and sulfatases, i.e. enzyme activities that, on the basis of molecular evidence, involve a common ancestral pathway shared between animals and brown algae (Michel et al. 2010; Popper et al. 2011). Fucoidans have been reported to contain d-xylose, as well as d-mannose and d-galactose residues potentially acting as branching sites in Pelvetia (Painter 1983). To elucidate fucoidans structure, Descamps et al. (2006) identified a fucoidan-degrading activity from a Flavobacteriaceae isolated from P. canaliculata. The authors showed that fucoidans are degraded in tetrasaccharide and a hexasaccharide units that are themselves composed of disaccharide repeat units.

Pelvetia canaliculata has a high content of sulfated fucoidans, which represent 40% DW of its isolated cell walls (Kloareg 1986), while alginic acid represent 15% DW (Black 1949). Sulfated fucans are highly hygroscopic and assist with the regulation of water potential in the vicinity of cell membranes in species that frequently experience immersion (Evans et al. 1973; Mabeau and Kloareg 1987). However, although sulfated polysaccharides may be an adaptation to highly ionic environments through structural or osmotic functions, they are composed of sulfur which is limiting in non-marine environments and a high requirement for it in terrestrial habitats may confer a disadvantage (Michel et al. 2010).

Fucans composition of extracts is highly dependent on the extraction procedure used. In this regard, Black et al. (1952) obtained optimum extraction with 0.17 N hydrochloric acid, pH 2.0–2.5, 70˚C for 1 h, followed by fractional precipitation with alcohol, and purification with formaldehyde, resulting in a 63% fucoidan yield containing 41% fucose. Similarly, while the fucans from Pelvetia extracted by alkali were rich in fucose and sulphate, fucans extracted by solubilization in Triton X-100 had a higher amount of uronic acid and xylose (Mabeau et al. 1990). More recently, Deniaud-Bouet et al. (2014) showed that the fucan content from Pelvetia was increased approximatively tenfold when enzymatically extracted with alginate lyase followed by protease, compared to sequential extraction with water containing 0.1% Na2SO5, 1 M NaCl containing 0.1% Na2SO5 and 4 M NaCl containing 0.1% Na2SO5.

Moreover, sulphated fucans are thought to be bound to cellulose. Among brown algae, Pelvetia has the lowest cellulose content, which constitutes just 0.6% of the dry weight of the cell walls, resulting in a relatively low stiffness, compared to Laminaria hyperborea stipes that are rigid and contain up to 10% cellulose (Black 1950). In addition, cell walls contain alginates, i.e. hydrophilic polymers of β-d-mannuronic acid and α-l-guluronic acid. Alginates impact seaweed mechanical strength and flexibility with greater stiffness being associated with lower mannuronic acid to guluronic (M:G) ratios (Indergaard and SkjAk-Braek 1987). In Pelvetia, the M:G ratio has been shown to vary with age; younger, more supple tissues had a ratio 2–4 times higher than old tissue (Haug et al. 1974).

Mannitol and volemitol

Synthesized from fructose-6-phosphate, mannitol is a multi-functional compound being involved in photosynthesis, osmotic regulation and antioxidant activity. It can accumulate and be present in high concentrations in brown algae, representing 5–9% DW of Pelvetia and up to 34.34% DW in L. hyperborea (Black 1949; Graiff et al. 2016). In the marsh form P. canaliculata f. libera, mannitol is masked by the presence of mannitan, an anhydride of mannitol (Haas and Hill 1933). From samples collected in Scotland, Black (1949) reported a minimum in mannitol content in January–February, coinciding with minimal photosynthetic activity, and dry weight. By contrast, two peaks of mannitol were observed in P. canaliculata, i.e. in May and September, which could be linked to the reproductive cycle (see Sect. “Life cycle, reproduction and development”). Drew (1969) highlighted a hexose-mannose conversion pathway in this species, as well as in Ascophyllum. Indeed, P. canaliculata showed the ability to convert exogenously supplied 14C-mannose to mannitol, in addition to convert rapidly 14C-glucose to 14C-mannitol.

In addition to mannitol which constitutes a major part of storage carbohydrates in Phaeophyceae, Pelvetia has the capacity to synthesize the heptitol volemitol in high concentrations. The accumulation of volemitol was found to correlate with photosynthetic activity (Drew 1969; Kremer 1973; Reed et al. 1985; Pfetzing et al. 2000). Mono- and di-β-glucosides of mannitol and volemitol has also been isolated from Pelvetia (Lindberg and Paju 1954). The accumulation of volemitol is specific to the alga, and is not directly synthetized by the fungal endosymbiont Mycophycias ascophylli (previously Mycosphaerella pelvetia) (Kremer 1973). Following cultivation experiments, Pfetzing et al. (2000) reported an accumulation of mannitol and volemitol during submersion and exposure to elevated temperatures, while concentrations decreased under prolonged emersion at 25˚C. This suggests that both sugar alcohols could be involved in response to thermal or desiccation stress. In addition, volemitol could play a role in osmoregulation (Reed et al. 1985), although Kremer (1976) observed little content variations under reduced salinity. For identification, the 13C NMR spectra of mannitol and volemitol extracted by EtOH 70% or distilled water contain 3 and 7 peaks respectively, i.e. at 72.35, 70.78, and 64.79 ppm; and at 74.35, 72.95, 72.23, 71.09, 71.00, 64.76, and 63.53 ppm respectively (Pfetzing et al. 2000). The synthesis of volemitol is the result of the reduction of fructose-6-phosphate by a NADH-linked dehydrogenase (Kremer 1977). Kremer (1977) proposed the following biosynthesis pathway: sedoheptulose-7-phosphate volemitol-1-phosphate volemitol. As volemitol is a major product of photosynthesis, it is strongly 14C-labeled after short-term photosynthesis in \(\mathrm H^{14}\mathrm{CO}_3^-\) (Kremer 1977).

Other Carbohydrates

Pelvetia canaliculata contains traces of laminarin (i.e. between 0.03 and 3.5% DW), a common carbon storage polysaccharide usually encountered in brown algae whose seasonal variations in concentration follow those of mannitol (Black 1949) (Table 1). Three types of laminarin have been identified in P. canaliculata by liquid chromatography-mass spectrometry (LC–MS), with molar mass of 3200, 3600 and 3900 Da (Graiff et al. 2016). Kropf et al. (1993) suggested a link between the Pelvetia cell wall and development including rhizoid polarity in developing embryos. This was further illuminated when Hervé et al. (2016) reported the occurrence of Arabinogalactan proteins (AGPs) in brown algal cell walls, including those of Pelvetia. Hervé et al. (2016) showed that AGPS controlled polarity in the development of Fucus embryos. AGPs are relatively well characterized from land plants where they are known to be involved in cell–cell communication and development (Pereira et al. 2021). Among algae, they had previously been reported from freshwater green algae including Micrasterias, Penium and Chara (Domozych et al. 2009, 2014) and the green seaweeds Ulva and Codium (Estevez et al. 2009; Přerovská et al. 2021). Although brown algae last shared a common ancestor with green algae and land plants 1600 Million Years Ago (Yoon et al. 2004), AGPs may share similar functions in the two groups; namely in reproduction and development.

Protein content and amino acids

Compared to other macroalgal species, protein content of P. canaliculata is reportedly low and varies seasonally between 1 and 8% DW (Table 1). Across several species of brown, red and green macroalgae from Norway, Tayyab et al. (2016) noted the lowest crude protein content in P. canaliculata, representing 105 and 75 g kg−1 DW in March and October, respectively. In comparison, Alaria esculenta (Phaeophyceae) and Porphyra sp. (Rhodophyta) contained 158 and 372 g kg−1 DW in spring, respectively (Tayyab et al. 2016). Based on total amino acid residues, Maehre et al. (2014) calculated a protein content of 57.2 g kg−1 DW in Pelvetia from Norway in May. The maximal crude protein content (determined in March) coincided with maximum inorganic nitrate content in seawater; while the minimum occurred in September–October following reproduction (Black 1949).

The amino acid (AA) composition of Pelvetia and other macroalgae collected in Norway was studied by Maehre et al. (2014). Glutamic and aspartic acids were the predominant AA (representing 15.0, 5.9 and 5.5 g kg−1 DW, respectively), followed by alanine, leucine and glycine. By contrast, levels of cysteine, histidine, methionine and tyrosine were low (< 1.5 g kg−1 DW). Additionally, ɣ-aminobutyric acid betaine, glycinebetaine and laminine are reported from P. canaliculata (Blunden et al. 1985), as well as an octapeptide of glutamic acid (Haas and Hill 1931). Recently Badmus et al. (2019) demonstrated the effect of drying treatments on the levels of nutritionally important compounds: considering P. canaliculata, freeze-drying and oven-drying at 40˚C retained highest levels of protein, amino acids, and phenolic contents, while microwave-drying was more suitable for some other compounds.

Lipids and fatty acids

Lipid content of P. canaliculata is reportedly relatively high compared to other macroalgal species, with levels of 37 or 58 g kg−1 DW, depending on extraction method (ether or dichloromethane/methanol, respectively), compared, e.g., to 13 and 15 g kg−1 DW in A. esculenta (Maehre et al. 2014). Sousa et al. (2021) determined the lipid content of Pelvetia as 5% DW. Liem and Laur (1976) analyzed the content, composition and distribution of polar lipids of P. canaliculata: thalli contained 16 polar lipids, representing 50–58% of total lipids, and contents were higher in vegetative than reproductive thallus parts. The same authors also demonstrated a high level of glycosyl esters diglycerides (DEG) located in the photosynthetic apparatus, with the predominance of phosphate and sulfate monoesters (Liem and Laur 1976). A predominance of sulfolipids over phospholipids has also been reported and, comparatively, Pelvetia was richer in phosphatidyl-choline than F. serratus and F. vesiculosus (Liem and Laur 1974). Numerous aliphatic alcohol sulphates (AAS) were subsequently shown to be free in the cell protoplasm (Liem and Laur 1976).

The detailed fatty acid profile of P. canaliculata has been reported by Schmid et al. (2014), who also demonstrated a distinct seasonal trend in both levels and profiles. Total fatty acid (TFA) content of P. canaliculata from Ireland represented 6.4% DW and 2.9% DW in June 2012 and November 2011, respectively. A reduction in monounsaturated fatty acids (MUFA) in November (c. 28.6% TFA, mainly oleic acid (C18:1w9)) was correlated with an increase in polyunsaturated fatty acids (PUFA) (c. 40.3% TFA, mainly arachidonic acid (20:4w6)) and saturated fatty acids (SFA) (c. 31.1% TFA, mainly myristic (C14:0) and palmitic (C16:0) acids). A contrasting profile was observed in samples collected in October along the northern coast of Norway, where the sum of MUFA represented the largest proportion of fatty acids, i.e. 42% of TFA, compared to 34 and 21% of TFA for PUFA and SFA respectively (Biancarosa et al. 2018). In these latter populations, dominant fatty acids were also oleic, arachidonic, linoleic (C18:2w6), palmitic and myristic acids, representing 17.37, 6.32, 4.99, 2.70 and 2.50 mg g−1 DW respectively (Biancarosa et al. 2018). The ratio of omega-6/omega-3 fatty acids reached only 0.3 in P. canaliculata from Norway, compared to 1.8 in P. canaliculata from Ireland, also collected in winter. Such regional and seasonal variations in fatty acid profiles highlight the strong environmental and geographical influences that likely contribute to the adaptive plasticity of this high-shore species.

Pigments

As a member of the Phaeophyceae, major pigments in Pelvetia canaliculata, are chlorophyll-a (chl-a) and -c (chl-c), β‐carotene (β‐car) and fucoxanthin (Stengel et al. 2011). In addition, high levels of pigments involved in xanthophyll cycle, i.e. violaxanthin, antheraxanthin and zeaxanthin, have been identified in Pelvetia, as well as low levels of pheophytin-a (De Martino et al. 1997; Harker et al. 1999; Fernández-Marín et al. 2011a; Hupel et al. 2011). Sousa et al. (2021) measured 602 mg kg−1 DW of pheophytin-a, and 236 mg kg−1 DW of β‐carotene in P. canaliculata collected in June 2019 in Portugal, both pigments being involved in photoprotection.

Environmental conditions greatly affect algal pigment composition, especially for upper shore species such as Pelvetia, when exposed to fluctuating light and temperature, and desiccation. Based on a cultivation experiment applying artificial exposure to PAR + UVA radiation, Hupel et al. (2011) showed that chl-a, chl-c and carotenoids (i.e. xanthophyll + β -car) contributed to 65%, 15% and 15% of the total pigment pool, respectively. Following PAR + UV-B exposure, chlorophyll/carotenoids ratio changed to 70% chl-a, 10% chl-c and 20% carotenoids, representing 0.38, 0.04 and 0.11 mg g−1 DW, respectively.

In situ, Martins et al. (2021) reported up to 60% higher chlorophyll and carotenoid contents in P. canaliculata when collected at low tide, with the xanthophyll cycle constituting an important photoprotective mechanisms in this species (De Martino et al. 1997; Harker et al. 1999) (see “Light”). Moreover, a de-epoxidation of the xanthophyll cycle (i.e. transformation of violaxanthin into zeaxanthin) has also been observed in Pelvetia dehydrated in darkness, concomitantly with a decrease in photosynthetic activity (Fernández-Marín et al. 2011a). While de-epoxidation is normally observed under excess light conditions, it could act as a defensive mechanism enhancing tolerance to desiccation and resulting oxidative stress, counteracting the production of reactive oxygen species ROS. Also, de-epoxidation could be reversed by rehydration, associated with the recovery of the initial Fv/Fm (Fernández-Marín et al. 2011a). The same authors showed that other factors such as immersion, anoxia or high temperature could induce de-epoxidation in the dark. Results suggest that de-epoxidation and accumulation of zeaxanthin is due to the inhibition of zeaxanthin-epoxidase activity under stress (Fernández-Marín et al. 2011b). The mechanisms responsible of the xanthophyll de-epoxidation in darkness has been recently reviewed by Fernández-Marín et al. (2021).

Other Constituents

Phenolic compounds

Total extractable polyphenol content is relatively high in P. canaliculata compared to other brown, red or green macroalgae, as demonstrated by de la Moneda et al. (2019). However, phenolic contents are highly fluctuating as they constitute a diverse and complex compound pool involved in multiple stress responses and, thus, vary across sites and seasons (Kirke et al. 2019). A positive correlation between phenol level in P. canaliculata and measured air-temperature has been demonstrated (Connan et al. 2007). Also, phenolic content varied with light exposure, decreasing from 8.92 to 6.99 mg g−1 DW when exposed to PAR-A radiation (21 days) and from 7.27 to 5.82 mg g−1 DW under PAR-B radiation (Hupel et al. 2011), with no difference observed between PAR and UV treatments.

Phenolic contents of 40.4 g kg−1 DW in autumn and 26.9 g kg−1 DW in spring, have been reported (de la Moneda et al. (2019). Total phenol content (TPC) in P. canaliculata from Brittany (France) in March represented 3% DW, compared to 6 and 4% in A. nodosum and Bifurcaria bifurcata (Phaeophyceae), respectively (Connan et al. 2007). From a methanolic extract Sousa et al. (2021) reported a content of 5.5 mg gallic acid equivalents (GAE) g−1 DW in P. canaliculata collected from Portugal in June, compared to 4.0 mg GAE g−1 DW in samples collected in Ireland in spring (O’Sullivan et al. 2011).

In addition to variations induced by environmental conditions to which the material is exposed before collection, the TPC levels reported in the literature highly depend on extraction processes applied across different studies, particularly as phenols are bound to sulfated polysaccharides and proteins in the cell wall (Deniaud-Bouët et al. 2014). Deniaud-Bouet et al. (2014) showed that phenols represented 2% of extract when enzymatically extracted with alginate lyase following by protease, compared to 31% with sequential extraction with water containing 0.1% Na2SO5, and 1 M NaCl containing 0.1% Na2SO5. Similarly, using 50% ethanol, Garcia-Vaquero et al. (2021) tested different extraction methods (i.e. ultrasound-assisted extraction (UAE), microwave-assisted extraction (MAE), ultrasound–microwave-assisted extraction (UMAE), hydrothermal-assisted extraction (HAE) and high-pressure-assisted extraction (HPAE)). Highest phenolic yields from P. canaliculata were obtained by UAE, i.e. TPC of 250.6 ± 6.0 mg GAE g−1, total phlorotannin content of 203.9 ± 4.9 mg phloroglucinol equivalents g−1, total flavonoid content of 122.6 ± 3.4 mg quercetin equivalents g−1 and total tannin content of 79.5 ± 4.6 mg catechin equivalents g−1. Similarly, highest antioxidant activities were achieved by UAE, i.e. 95 mM Trolox equivalents g−1 for DPPH and 80 mM Trolox equivalents/g for FRAP activities (i.e. Ferric Reducing Antioxidant Power). The FRAP activity was reduced when other methods were used.

Regarding polyphenol composition, using UPLC-MS, Tierney et al. (2014) and Kirke et al. (2019) reported the predominance of large phlorotannins (i.e. degree of polymerization consisting predominantly of 6–14 phloroglucinol units (PGU), corresponding to m/z 745–1738) in P. canaliculata. Seasonal variations can slightly affect the degree of polymerization, increasing the relative abundance of phlorotannins between 9 and 14 PGUs up to 82% (Kirke et al. (2019). To cleave the permethylated phlorotannins of P. canaliculata, polyhydroxy phenols or biphenyls can be obtained by semi-preparative isolation using sodium in liquid ammonia (Glombitza and Klapperich 1985). A portion of phlorotannins is cell wall-bound and in Pelvetia, this proportion is maximal in the receptacles, where phlorotannins may perform a protective role; by contrast, in Fucus the highest proportion of cell wall-bound phlorotannins occurs in the stipe (Birkemeyer et al. 2020).

Vitamins

Vitamin composition of P. canaliculata reported by Biancarosa et al. (2018) suggests that the species is potentially a valuable source of α-, β-, γ-, and δ-tocopherol, representing 93, 18, 20 and 123 mg kg−1 DW, respectively. These levels are higher than in other brown algae, except for F. spiralis and A. nodosum which contained higher levels of δ-tocopherol, with 144 and 194 mg kg−1 DW, respectively (Biancarosa et al. 2018).

Valorization

Human food

Having been used as a sustenance during the Irish Great Famine of 1845–1847, today P. canaliculata is sold in different dried forms, or as a seasoning mix. It is usually cooked, in small quantities, with traditional vegetables, or used as a multi-vitamin/mineral food supplement and can be dried and sprinkled over food (Green 2014; Mæhre et al. 2014; Pereira and Correia 2015; Pereira 2016).

Animal feed

Pelvetia canaliculata has been traditionally used to feed livestock animals. Recently, Molina-Alcaide et al. (2017) analyzed nutrient and total polyphenol content in several macroalgae, in addition to gas production kinetics, methane emission and in vitro rumen fermentation, aiming to evaluate the potential use of seaweeds as feed for ruminants. Their results suggest that, of seven species examined, P. canaliculata biomass had the lowest degradability. The effective degradability of Pelvetia was on average 444 g kg−1 dry matter (DM), and thus lower than that of A. esculenta and L. digitata. Also, Tayyab et al. (2016) estimated the degradability of Pelvetia as 290 g kg−1 DM, compared to 925 and 913 g kg−1 DM in L. digitata and P. palmata, respectively. The crude protein (CP) degradation was also the lowest in Pelvetia (322 g kg−1 CP). The average gas production rate (AGPR) of P. canaliculata was 1.38 mL h−1, compared to 4.95 mL h−1 in Palmaria palmata (de la Moneda et al. 2019). Similar unfavourable results were obtained based on chemical composition and 24 h in vitro rumen fermentation of eight species collected in Norway (de la Moneda et al. 2019). The low degradability of P. canaliculata, coupled with the low protein content, does not render it a suitable candidate for feeding dairy ruminants.

Bioremediation

The high bioremediation potential of brown algal biomass has received attention, specifically for the removal of toxic metals which cause harmful effects in the marine environment and on human health (Hackbarth et al. 2014; Bulgariu and Bulgariu 2020). Pelvetia biomass acts as a natural cation exchanger with documented good biosorption capacities for copper (Cu2+), zinc (Zn2+), lead (Pb2+), nickel (Ni2+), barium (Ba2+) and chromium (Cr3+) ions, with uptake being dependent on pH. For example, P. canaliculata treated with NaCl had a maximal nickel biosorption capacity of 100 mg g−1 at pH 4.0 (Bhatnagar et al. 2012). Maximum chromium uptake from aqueous solutions was ~ 0.6 mmol g−1 at pH 4.0 (Vilar et al. 2012), while the maximum uptake capacities for the hexavalent chromium were 1.8 and 2.3 mmol g−1 for the raw and protonated P. canaliculata, respectively (Hackbarth et al. 2016). Maximum uptake capacity for Pb2+ at pH 4.0 and Cd2+ at pH 4.5 were 1.25 mmol g−1 (2.5 mEq g−1; 259 mg g−1) and 1.25 mmol g−1 (2.5 mEq g−1; 140 mg g−1), respectively (Hackbarth et al. 2014). Similarly, Pelvetia presented a high capacity for the removal of barium, i.e. 69% compared to 56% and 31% in Sargassum cymosum and Gracilaria birdiae, respectively (Fontão et al. 2020). The maximal uptake capacity for copper or zinc ions (i.e. ~ 2.4 mEq g−1) was also achieved at pH 4.0 when all binding sites were occupied, whereas uptake capacity was reduced at low pH (Girardi et al. 2014). Costa et al. (2010) have suggested that there was competition between H+ and metal ions for the same binding sites, responsible for a decrease in uptake capacity for Pb2+ at lower pH. Moreover, Na-loaded P. canaliculata was a good natural cation exchanger for multi-metal systems (e.g. Na+/H+/Cd2+, Na+/H+/Pb2+, Na+/H+/Cu2+, Na+/H+/Zn2+ and Na+/H+/ Cd2+/Pb2+/Cu2+/Zn2+), as demonstrated by Hackbarth et al. (2015). These authors point out that there could nevertheless be competitive uptake between Pb and Cu ions. The high biosorption capacity of Pelvetia appears to be associated with a high amount of carboxylic and sulfonic groups present in the biomass surface which bind metals (Vilar et al. 2012; Girardi et al. 2014; Hackbarth et al. 2014; Fontão et al. 2020). In this regard, Hackbarth et al. (2014) demonstrate a higher uptake capacity for Pb than for Cu ions, due to a higher affinity of lead ions for sulfonic groups.

The presence of metals or other pollutants in the water, reportedly, adversely affects Pelvetia growth. Short-term exposure to Cd (> 400 µg L−1) or Pb (> 45 µg L−1) induced a significantly higher growth of Pelvetia collected from Norway, while the addition of Hg (> 5 µg L−1) had a negative effect on growth (resulting in a 50% reduction in growth rate when exposed to ~ 100 µg L−1 for 10 days in culture) (Strömgren 1980). More drastically, the Wreck of the Amoco Cadiz in March 1978 along Brittany coasts (France) caused a progressive decline in the previously dense cover of Pelvetia, which took a year and a half before showing first evidence of recolonization (Floc’h and Diouris 1980).

Biological and nutraceutical activities

Antioxidant activity

Several studies have reported high levels of bioactive capacities of extracts from P. canaliculata biomass; these have mostly been attributed to phenolic and polysaccharide contents. Pelvetia extracts notably display a strong antioxidant activity, possibility related to compounds accumulated due to the multiple stresses it experiences at its natural position in the extreme upper intertidal. For example, Connan et al. (2007) demonstrated that the antioxidant capacity (evaluated by DPPH assay) of P. canaliculata generally paralleled phenol contents. Similarly, Sousa et al. (2021) reported that FRAP antioxidant activity was closely related to the total phenolic content. Additionally, lyophilized Pelvetia, when supplemented as a source of biological compounds, could increase the antioxidant activity of sunflower oil sixfold, improving its stability and maintaining its nutritional properties. Also, a link between the degree of phlorotannin polymerization / isomerization and antioxidant activity has been established, with a higher degree of structural complexity potentially leading to lower activity (Kirke et al. 2019). As a result, the established natural variation in phenolic profiles may thus affect reported bioactivity levels.

Extraction solvent and methodology can also influence detected activity; for example, after extraction with ethanol–chloroform–water and phase separation, Hupel et al. (2011) demonstrated that the aqueous phase, analyzed by DPPH, exhibited a high antioxidant activity (i.e. EC50 at 0.04–0.06 g L−1), which was twice as active as the crude extract (i.e. EC50 at 0.06—0.19 g L−1), and four times more active than an ethanolic extract (i.e. EC50 at 0.25—0.38 g L−1). Methanolic extracts of Pelvetia also exhibited a FRAP activity of 71.5 µM ascorbic acid equivalents (AAEq) g−1 DW, which was lower than reported activity of F. vesiculosus extracts (i.e. 109.8 AAEq g−1 DW) but higher than those of L. hyperborea (i.e. 25.6 AAEq g−1 DW) (O’Sullivan et al. 2011). Through a β-carotene bleaching assay, the latter authors also showed that Pelvetia extracts reduced bleaching by 53.9%, compared to 76.3% and 71.2% for A. nodosum and F. vesiculosus extracts, respectively.

Other bioactivities

Polysaccharides from P. canaliculata have revealed interesting anticoagulant activity (Colliec et al. 1991). After hydrolysis and gel filtration, Colliec et al. (1994) obtained a highly purified fucoidan fraction exhibiting anticoagulant activity coupled to a low viscosity. This low molecular weight fraction had a high content of fucose units and ester sulphate groups, with reduced levels of uronic acids and proteins, compared to the crude fucoidan. Methanolic extracts of P. canaliculata then significantly increased glutathione (GSH) activity in Caco-2 cells and had a superoxide dismutase (SOD) protective effect (O’Sullivan et al. 2011). Pelvetia canaliculata also contains polyphenols that act as inhibitors of the digestive enzymes α-amylase, lipase and trypsin, and could be incorporated in human ‘health foods’ and/or be used in the treatment of diabetes (Barwell et al. 1989). It should be noted that some activities reported for ‘Pelvetia’ could be linked to its symbiosis with fungi or bacteria (see Sect. “Associated species and species interactions”). For example, Lemos et al. (1985) isolated 55 bacterial strains from P. canaliculata from Spain, including four antibiotic-producing strains. Other compounds of interest purified and characterized from P. canaliculata include two iodoperoxidase enzymes (PcI and PcII) with vanadium dependent activity, with potential in diverse pharmaceutical and industrial applications (Almeida et al. 2000).

Bioenergy production

According to recent investigations, Pelvetia has some theoretical potential for biogas (methane) production, although biomass supply is limited and not likely sustainable as the species cannot be cultivated. Biomass pretreatment and conversion methods remain to be optimized, but methane yield could be improved by using a mechanical pretreatment, e.g. a Hollander beater normally used in the paper industry (Rodriguez et al. 2018). Applying this, methane production could be increased by 74% when beating for 1 h, however 50 min appeared to be optimal considering the cost associated to the pretreatment. Based on a new approach coupling a fuzzy logic model to particle swarm optimizer, Nassef et al. (2021) recently confirmed a positive effect of long beating time on the methane yield from P. canaliculata, as well as low feedstock to inoculum ratios.

Current industrial products

Although little valorized so far, some limited but diverse P. canaliculata extracts, ingredients and products have been developed by the cosmetics sector. Notably, several extracts with antioxidant and anti-aging activities are already commercialized for incorporation in face cream or emulsions. This includes the liquid PelvetianeⓇ extract from the company SOCRI (Italy), and the isoflavone-rich P. canaliculata extract produced by Ziaja which is used, in combination with a Porphyra umbilicalis extract, in a marine active firming cream. Both extracts are derived from algae sourced in Brittany (France). An ingredient containing polysaccharides with similar properties, Ambre oceane™ SPE, has also been developed by Seppic (France) who also produce a hair application (XYLISHINE) incorporating Pelvetia polysaccharides due to their moisturizing properties.