Abstract
Lessonia (order Laminariales) is a kelp genus restricted to the temperate southern hemisphere, where species form dense forests from the low intertidal to 25 m depth at wave exposed sites. Lessonia spp. are among the most harvested kelps globally due to their importance in providing raw materials for food, cosmetics, bioactive and biomedical industries. Over-harvesting of natural beds can negatively affect Lessonia populations and the many species that depend on these habitats, including commercially important fish and molluscs, but good harvest management plans reduce these impacts on natural Lessonia stocks. However, the increasing demand for raw materials will likely only be met by aquaculture for which Lessonia shows high potential in pilot scale studies undertaken in Chile, New Zealand, and Australia. In this concise review, we highlight the current knowledge of Lessonia spp. taxonomy and distribution, life history, ecology and ecosystem services, wild harvest, aquaculture, and commercial applications. We discuss future research directions.
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Introduction
Kelps (order Laminariales) form the basis of many coastal temperate marine systems and provide critical ecosystem services to humans (McLachlan 1985; Ramus 1992; Buschmann et al. 2007; Wernberg et al. 2019a, b). For example, Bennett et al. (2015) calculated the value of Australian kelp forest eco-services at AU$10 billion year−1. The genus Lessonia is an important kelp found in cool temperate waters of the southern hemisphere, primarily in the Pacific Ocean (Nelson 2005, 2013; Cho et al. 2006). Like all kelps, Lessonia provides habitat and food for other organisms (Vásquez et al. 2012) and several Lessonia species have economic importance as food and for pharmaceuticals, with wild harvest providing a source of income for many people (Edding et al. 1990; Vásquez et al. 2012; Müller et al. 2019).
Lessonia spp. are among the most harvested seaweeds from natural beds worldwide, which puts pressure on wild populations (FAO 2018; Sernapesca 2020). Although current management plans to reduce the impacts of harvesting exist, the growing demand for Lessonia as a raw material for the alginate industry puts pressure on local populations as do environmental threats such as ocean warming and overgrazing by sea urchins (Vásquez et al. 2012). Several Lessonia species show strong potential in aquaculture which might reduce the ecological impacts of wild harvest (Zuniga-Jara and Soria-Barreto 2018; García-Poza et al. 2020). This concise review presents current knowledge about the genus Lessonia focussing on its taxonomy and distribution, life history, ecological and ecosystem services, wild harvest, aquaculture, and commercial applications. We also identify knowledge gaps for future research.
Taxonomy and distribution
The genus Lessonia was first described by Jean Baptiste Bory de Saint-Vincent in 1825, based on the species Lessonia flavicans which had a type locality in the Falkland Islands (Searles 1978). There are currently 11 recognised species of Lessonia (Asensi and de Reviers 2009; Guiry and Guiry 2022), and their geographic distribution is shown in Fig. 1. Species’ distributions and maximum length are: Lessonia berteroana (intertidal + 1 to -1 m, length < 4 m): Chile (Hay 1987; López-Cristoffanini et al. 2013); Lessonia flavicans (subtidal 2–20 m, length < 4 m): Argentina, Chile, and subantarctic Islands (Falkland Islands/Islas Malvinas) (Searles 1978); Lessonia nigrescens (intertidal + 1 to -1 m, length < 4 m): Chile, Peru, French Polynesia and Antarctica/Subantarctic Islands (Papenfuss 1964; Searles 1978; Santelices 1989; Payri and N'Yeurt 1999; Cho et al. 2006); Lessonia searlesiana (subtidal 1–12 m, length < 3 m): Argentina (Asensi and de Reviers 2009); Lessonia spicata (intertidal + 1 to -1 m, length < 4 m): Chile (Parada et al. 2017; Rosenfeld et al. 2019); Lessonia trabeculata (subtidal 0.5–20 m, length < 2.5 m): Chile (Villouta and Santelices 1986; Hay 1987; Santelices 1989; Vásquez 1993; Cho et al. 2006); Lessonia adamsiae (subtidal 1–22 m, length < 3 m): New Zealand, Snares Islands/Tini Heke (Adams 1994; Zuccarello and Martin 2016); Lessonia brevifolia (subtidal 2–25 m, length < 2.5 m): New Zealand Antipodes Islands, Auckland Islands, Bounty Island, Campbell Island (Papenfuss 1964; Adams 1994; Zuccarello and Martin 2016); Lessonia corrugata (subtidal 1–25 m, length 1–1.5 m): Tasmania (Cho et al. 2006; Scott 2017); Lessonia tholiformis ( subtidal 1-15 m, length < 1 m): New Zealand, Chatham Islands (Cho et al. 2006; Adams 1994); Lessonia variegata (subtidal 1–15 m, length < 1.5 m): north and south islands of New Zealand, and the following off shore islands, Chatham Islands, Auckland Islands, Bounty Island, Campbell Island, Snares Islands/Tini Heke (Papenfuss 1964; Hay 1987; Adams 1994; Nelson 2005; Zuccarello and Martin 2016).
Geographical distribution of the genus Lessonia. Different coloured lines represent species within the genus (Guiry and Guiry 2022)
Life history and morphology
As with all members of the Order Laminariales, Lessonia has a heteromorphic biphasic life cycle (Clayton 1988; Schiel and Foster 2006). The perennial sporophyte (2N) is macroscopic and, depending on species, reaches between 1 and 4 m in length (see above). The sporophyte is attached to the rock substratum by branched haptera that form a holdfast with a conical or ligulate shape. The stipe arises from the holdfast and branches from the base, with each branch bearing a blade (Guiry and Guiry 2022). The blades are simple, flat, ligulate and elongated, broad (L. flavicans, Fig. 2A), narrow (L. trabeculata Fig. 2B) and some species have denticulated margins (e.g. L. variegata Fig. 2C and L. corrugata, Fig. 2D), and the surface can be smooth (e.g. L. berteroana, Fig. 2E and L. spicata, Fig. 2F), rugose (e.g. L. brevifolia and L. corrugata, Fig. 2D) or wavy (e.g. L. adamsiae) (Asensi and de Reviers 2009). The meristem (i.e., growth region) is found at the blade base, and thalli have longitudinal growth and splitting of the blades, resulting in dichotomous branching of the stipe (Asensi and de Reviers 2009; Guiry and Guiry 2022).
The morphology of Lessonia spp. changes with wave exposure, and such morphological plasticity allows it to thrive across a gradient of wave-exposure (Coppin et al. 2020). The blades of L. flavicans and L. vadose at wave-exposed sites in Southern Chile and Argentina are longer, thicker, have a greater number of marginal teeth and a decreased basal blade angle and width compared to wave-sheltered sites (Searles 1978). Moreover, the thalli of L. nigrescens at a wave-exposed site are approximately twice as long as thalli at a sheltered site (45 cm vs. 23 cm) (Searles 1978; Santelices et al. 1980). Interestingly, the occurrence of chimera in Lessonia (detailed below) increases at sites with greater wave energy. For example, L. spicata showed a greater incidence of holdfast fusion at sites exposed to high vs. low water motion (Gonzalez and Santelices 2017). The interaction with grazers may also affect the morphology of Lessonia. For example, in response to grazing, the morphology of L. trabeculata can change from a blade to a “shrub” form that produces a whiplash effect on the rock surface, keeping benthic herbivores away (Vásquez and Buschmann 1997).
Mature Lessonia sporophytes produce large areas of sori on both blade surfaces, where microscopic bi-flagellated zoospores are produced by meiosis (Redmond et al. 2014; Guiry and Guiry 2022). Zoospores (3–6 µm diameter) are released into the water column and dispersed passively by water motion and active swimming using the flagella, which allows for limited locomotion. Zoospores typically settle onto suitable substrata 1–3 days after release (Hay 1987; Edding et al. 1990; Véliz et al. 2006; González et al. 2014; Ruz et al. 2018). Once settled, the zoospores lose their flagella and further adhere to a substratum, where they develop into microscopic haploid female and male gametophytes. There are distinguishable differences in size and morphology of gametophytes (15–90 µm), with the female having larger and more robust cells compared to males (Avila et al. 1985; Hay 1987; Tala et al. 2004; Véliz et al. 2006). Mature female gametophytes produce oogonia, and males develop antheridia in which the gametes are produced. A single egg is extruded from each mature female oogonium, retained on the female gametophyte, and a pheromone is produced that guides the motile sperm released by male gametophytes to the egg for fertilisation (Westermeier et al. 2017; Müller et al. 2019). After fertilisation, the diploid zygote develops into a small juvenile sporophyte. The time it takes to go from zoospore release to a sporophyte varies with species, for example: L. spicata and L. berteroana: 10 – 13 days (González et al. 2014), L. nigrescens: ~ 18 days (Avila et al. 1985) and L. trabeculata ~ 24 days (Mansilla et al. 2014).
Ecology and ecosystem services
Lessonia species form dense forests of up to 20 thalli m−2 from the low intertidal down to ~ 25-m depth (depending on species) at moderate and high wave-exposed sites in the temperate regions of the southern hemisphere (Searles 1978; Santelices and Ojeda 1984; Hay 1987; Steneck et al. 2002; Cho et al. 2006; Gonzalez and Santelices 2017; Mansilla et al. 2020). These forests provide food and habitat for many organisms, including a range of sessile and mobile invertebrates, fishes and seaweed (e. g. Pérez-Matus et al. 2017; Bularz et al. 2022). In Chile, the communities associated with Lessonia forests include > 30 harvested species (e.g., fish, molluscs, crustaceans and sea urchins (Pérez-Matus et al. 2017)) and thus, the ecological health of the Lessonia forests has ecological, social and economic consequences.
Communities of invertebrates within Lessonia forests can differ from those in other habitats close to Lessonia forests (Villegas et al. 2008; Vásquez et al 2012; Bularz et al. 2022). For example, ceramic plates placed for 14 months beneath L. trabeculata had a higher number of taxa and density of organisms compared to plates placed in a nearby barren habitat (Uribe et al. 2015). Similarly, following the removal of the canopy of L. trabeculata in Chile, macroinvertebrate diversity declined although fish and sessile understory diversity did not (Bularz et al. 2022). The reasons for the different communities in Lessonia forests compared to other habitats likely reflects differences in abiotic conditions, habitat structure and species interactions.
Lessonia competes with other seaweed for light and space, and canopy gaps opened by herbivores or disturbance allow the recruitment of other seaweed. For example, there was an increase in the abundance of opportunistic seaweed species such as Codium, Gelidium and Ulva following L. trabeculata removal (Santelices and Ojeda 1984; Bularz et al. 2022), which was likely due to a reduction in competition for light. In Chile, L. nigrescens and Durvillaea antarctica compete for space: at relatively sheltered sites, L. nigrescens appears to be outcompeted by D. antarctica, while at wave-exposed sites, L. nigrescens is dominant as D. antarctica is more susceptible to removal by waves (Santelices et al. 1980). Encrusting crustose coralline algae, primarily Lithothamnion, which dominate in the absence of kelp, inhibit the recruitment of both L. nigrescens and L. spicata due to shedding of the epithelial layer (Parada et al. 2017). Interactions between Lessonia and other seaweed species may also be facilitative. The survival of D. antarctica at wave-exposed sites increases when attached to L. nigrescens holdfasts (Santelices et al. 1980), while the articulated coralline, Corallina officinalis, facilitates the recruitment of L. nigrescens, allowing it to escape from herbivory by the chiton Enoplochiton niger (Camus 1994; Parada et al. 2017).
Grazing also has important effects on Lessonia forests. Sea urchins are ubiquitous in temperate kelp forests, and several species occur in Lessonia forests (Vázquez and Buschmann 1997). In the Chile Sea, urchins such as Tetrapygus niger can overgraze Lessonia and create barren areas largely devoid of macroalgae (Ojeda and Santelices 1984; Vásquez and Buschmann 1997; Perreault et al 2014). The loss of these forests impacts other species that depend on the habitat formed by Lessonia. For example, predation on crabs and urchins is higher outside Lessonia forests than beneath its canopy (Villegas et al. 2008). In addition, squid and elasmobranch attach their eggs to Lessonia stipes, and the whiplash effect of the Lessonia blades deters predators, thereby favouring egg survival (Carrasco and Pérez-Matus 2016; Trujillo et al. 2019). The reduction in whiplash caused by a decline in Lessonia density may also increase grazing by herbivorous fishes (Vasquez and Santelices 1990). Finally, the dispersal of zoospores of L. trabeculata may be facilitated by herbivorous fish. Aplodactylus punctatus consumes L. trabeculata, including reproductive tissue (sorus), and the zoospores remain viable and produce sporophytes at similar levels to that of the undigested sorus after passage through the digestive tract (Ruz et al. 2018). This may have an important role in zoospore dispersal in natural beds, aiding recovery following disturbance. Thus, overall a healthy high-density Lessonia forest plays an essential role in structuring shallow coastal communities due to the habitat they create.
Kelps are highly productive, and kelp forests play an essential role in carbon storage and cycling (Filbee-Dexter and Wernberg 2020; Gao et al. 2021). Carbon dioxide that is fixed through photosynthesis accumulates in the seaweed thallus and, as such, stored for a short time, from months to < 10 years, depending on the life span of the seaweed (Hurd et al. 2022). Seaweed carbon is then released back into the ecosystem as dissolved or particulate organic carbon and enters the coastal food webs (Pessarrodona et al. 2018). In order to understand the role of kelps in carbon cycling, knowledge of primary production rates are essential (Hurd et al. 2022). In Chile, L. nigrescens and L. trabeculata at wave-exposed sites have higher net production rates in spring, which decreases until early autumn, after which it increases again (Tala and Edding 2005). Lessonia trabeculata shows higher production than L. nigrescens per individual, 0.026 g dw day−1 and 0.01 g dw day−1, respectively. However, L. nigrescens beds have a higher thallus density, and thus, the total amount of carbon stored is also higher in those beds 11.46 g C m−2 day−1 for L. nigrescens and 2.46 g C m−2 day−1 for L. trabeculata (Tala and Edding 2007). Wave exposure affects primary production with L. trabelculata forests having double the carbon storage at an exposed site (6.11 t C ha−1) compared to a sheltered site (3.32 t C ha−1) (Aller-Rojas et al. 2020).
Chimeras are genetically heterogeneous individuals formed by the fusion of different genotypes and have been found for several species of red, green and brown seaweeds, including Lessonia ssp. (Rodríguez et al. 2014; Segovia et al. 2015). Chimeras play an important role in seaweed ecology, affecting reproduction, survival and development of seaweed populations (Santelices 2001). Both L. spicata and L. berteroana have frequent chimerism, which are largely intraspecific fusions (González et al. 2014). After the connection is established between holdfasts, the cell walls become thinner and develop plasmodesmata, enhancing communication between cells from different individuals (González et al. 2015). Chimerism may have both costs and benefits for Lessonia populations (González et al. 2014). Intraspecific competition for resources (e.g., light, nutrients), and disease transmission, can increase as the density of individuals increases (Ojeda and Santelices 1984; Rinkevich 2002; Casares and Faugeron 2016). However, these costs can be reduced by environmental conditions. For example, waves enhance both nutrient delivery and irradiance to the blades due to the back-and-forth water movement, supporting higher-density populations (Malm and Kautsky 2004; Oróstica et al. 2014). In northern Chile, more than 60% of L. berteroana individuals were chimeras (Rodríguez et al. 2014). A high density of chimeras reduces the distance between holdfasts, making it difficult for herbivores such as sea urchins to graze in these areas (Segovia et al. 2015). The large phenotypic variation in chimeras also increases the likelihood of Lessonia responding to environmental change due to the increased probability of fertilization between genetically distinct individuals within a densely growing population (González et al. 2014; Segovia et al. 2015). Casares and Faugeron (2016) showed that for L. spicata the formation of chimeras increased reproductive success at the thallus level. Furthermore, the fusion of holdfasts helps Lessonia increase the dissipation and reflection of wave energy arriving on the shore, enhancing survivorship and decreasing coastal erosion, providing an important ecosystem service (Vasquez and Santelices 1984; Komar 1998; Correa et al. 2006). Knowledge about chimeras and how they affect the population is still lacking for many Lessonia species and must be considered when investigating coastal ecosystems where Lessonia is present.
Wild harvest
Lessonia spp. are harvested from the wild in Chile, Argentina, Peru and New Zealand (FAO 2018; Márquez and Vásquez 2020; White and White 2020). Chile is the leading producer of wild-harvested kelp globally and Lessonia species are the most harvested seaweed on the Chilean coast (FAO 2018). There is an annual L. nigrescens and L. trabeculata harvest of 430,000 t and 60,000 t wet weight, respectively (as a comparison, the harvest of Macrocystis pyrifera was 25,000 t), representing 60% of the Chilean national seaweed harvesting in 2020, worth around US$ 110 million (Vasquez and Santelices 1990; Vega et al. 2014; Sernapesca 2014, 2020; Márquez and Vásquez 2020; González-Roca et al. 2021). The harvest of Lessonia in other countries is smaller: Argentina (16 t wet weight), Peru (3,000 t dry weight), and New Zealand (< 1 t wet weight) (Casas et al. 2015; Márquez and Vásquez 2020; White and White 2020).
Commercial landings of Lessonia exports started in northern Chile in the late 1960s. Initially, the harvest was done by collecting drift seaweeds on beaches, where the natural mortality allowed for sustainable collection by fishers (Vásquez et al. 2012; Gouraguine et al. 2021). However, relying on natural processes, such as storms that rip off kelp from the reef, was commercially not sustainable, especially with the increasing demand for beach-cast Lessonia biomass for alginate and abalone food (Camus et al. 1994; Vega et al. 2005; Vásquez et al. 2006). Therefore, in the early 2000s, the brown seaweed fishery became extractive, collecting living Lessonia, Macrocystis and Durvillaea from natural beds to support the increasing international markets with raw material for alginic acid extraction, and seaweed as food for the expanding marine herbivore cultivation industry (e.g., abalone) (Vásquez et al. 2012; Vásquez 2016). At this time, there was a collapse in finfish stocks that caused many fishers to switch to harvesting commercial brown seaweed (González-Roca et al. 2021). Today, harvesting of wild seaweed is an activity that supports thousands of people directly or indirectly throughout South America (Vásquez et al. 2012; Wernberg et al. 2019a, b; Márquez and Vásquez 2020; González-Roca et al. 2021).
In South America, the harvesting of drift L. nigrescens, L. berteroana and L. variegata on the beach or living Lessonia on the shore at low tide is largely done by hand, using low-tech tools such as knives (Vásquez and Westermeier 1993; Vásqueze et al. 2012; González-Roca et al. 2021). Diving operations at depths of more than 10 m require qualified divers and vessels for surface air-supplied diving and equipment to harvest L. trabeculata and L. variegata (Schwarz et al. 2006; Tellier et al. 2011; Gouraguine et al. 2021). Although Lessonia spp. has an extensive distribution throughout South America, harvesting is mainly concentrated at latitudes between 18° and 32° S in the Pacific Ocean (Vásquez 2008; Vásquez et al. 2012; González-Roca et al. 2021). This is due to the dry air and high temperatures from the Atacama Desert providing efficient drying conditions, reducing production costs and making the industry commercially viable (Vásquez 2016).
Harvesting operations disturb Lessonia populations, cause loss of Lessonia biomass, and affect many organisms dependent on Lessonia beds (Wilson et al. 2015; Krumhansl et al. 2017; Lotze et al. 2019; Gouraguine et al. 2021). In Chile, strong negative impacts of harvesting are primarily due to intense and/or prolonged harvesting without the appropriate management (Levitt et al. 2002; González-Roca et al. 2021). Therefore, proper management of kelp harvesting areas is necessary for the sustainable use of this resource. Collapses of some important kelp fisheries have focussed attention on managing kelps forests to ensure harvests (Vea and Ask 2011) and several good examples of well-managed sustainable kelp harvests are known. In Ireland, the government implemented rules in the 1940s to prevent uncontrolled exploitation. Initially, the harvest focused on Saccharina latissima and Laminaria hyperborea and eventually included the brown seaweed Ascophyllum nodosum (Fucales) (Guiry and Morrison 2013). In Canada, a management plan was implemented in 1995 for the harvest of A. nodosum, based on the maximum exploitation rate and seaweed size, and was combined with research and monitoring program to ensure the success of the management plan (Ugarte and Sharp 2001). In Norway, industrial exploitation of Laminaria hyperborea started during the 1960’s where a program based on rotating harvest zones with intervals of five years was implemented. This harvest strategy was based on knowledge of L. hyperborea ecology and ensured the recruitment of juveniles (Vea and Ask 2011).
In Chile, there are three management regimes that determine the allowable harvest: 1. Marine Protected Areas (~ 150,000 km2) where no harvest is allowed, 2. Exclusive Access Areas of territorial user rights for fisheries where, with the government's support, local fishermen manage the harvest, and 3. Open Access Areas with no protection (San et al. 2010; Gouraguine et al. 2021). In the Exclusive Access Area, the harvesting strategy is based on the ecology and life strategy of Lessonia and can be summarized as “how you harvest is more important than how much you harvest” (Vásquez 2008). Management recommendations consist of harvesting kelps with a holdfast larger than 20 cm in diameter, and all kelp must be extracted, with a spacing of 2 m maintained between plants, and the harvesting must be carried out over 8 months between harvests at a particular location. The main advantage of that approach is that the reproductive stock is kept, increasing the substratum for juvenile sporophyte recruitment and reducing the competition per space with adult sporophytes (Vega et al. 2005; Vásquez et al. 2012; Zavala et al. 2015; Vásquez 2016; Westermeier et al. 2016; Campos et al. 2021). The sustainable use of kelp beds is facilitated in protected areas such as highly enforced territorial-user-right areas because they present higher species richness and biomass than open access areas to harvesting (Gelcich et al. 2012; Vásquez et al. 2012; Pérez-Matus et al. 2017; Campos et al. 2021). Good harvest management plans reduce impacts on Lessonia's natural stocks. However, probably only aquaculture will meet the growing demand for raw materials.
Aquaculture
Kelp aquaculture has increased in the last few decades with progress made across the entire production chain, from the nursery to the post-processing of the harvest, as well as the development of new cultivation techniques and the domestication of new species (Le et al. 2022; St-Gelais et al. 2022). Many Lessonia species show potential for cultivation in open water and integrated with fish and mussel farms. However, there is currently no industrial aquaculture of the genus Lessonia (Camus and Buschmann 2017; Stenton-Dozey et al. 2021). Aquaculture of Lessonia spp. will be similar to other members of the order Laminariales, beginning in the laboratory with a ‘nursery phase’ for the microscopic gametophytes (Edding et al. 1990; Edding and Tala 2003; Redmond et al. 2014). The sorus is collected, excised, desiccated then rehydrated to trigger zoospore release. After a couple of weeks, filamentous gametophytes have developed and are kept under a red light as gametophyte stock and used to start sporophyte cultivation (Westermeier et al. 2006; Murúa et al. 2013). Zoospores or gametophytes are seeded onto twine wound around a PVC tube (i.e., “a spool”) and develop into a sporophyte in a few weeks. Zoospores can be seeded directly onto spools by allowing them to settle onto the twine after which they develop into gametophytes and subsequently sporophytes in a nursery. An alternative method is that the zoospores develop into gametophytes in a flask culture. The gametophytes can be vegetatively propagated for extended periods of time (up to decades) under red light. The gametophyte solution can then be sprayed onto spools, and gametophytes then develop into young sporophytes in a nursery (Edding and Tala 2003; Redmond et al. 2014; Visch et al. 2023).
Some species of Lessonia are fertile year-round, such as Chilean L. trabeculata and L. spicata, although they show variation in sorus blade cover over time, with higher cover in autumn and winter, respectively (Tala et al. 2004; Casares and Faugeron 2016). In contrast, for L. adamsiae and L. corrugata, endemic to Snares Island and Tasmania, respectively, sorus formation stops in spring and restarts in the middle of summer (Hay 1987, Nardelli et al. (in prep)). It is possible both species are seasonal anticipators, and the increase in day length is the “trigger” to stop the sorus production (Kain 1989). However, for most Lessonia species, the seasonal reproduction cycles are unknown.
Gametophyte development is regulated by abiotic factors, particularly temperature, light and nutrient supply, which must be optimised for each species (Le et al. 2022). Generally, kelp gametophytes are adapted to the temperatures at which they grow in the environment. However, each kelp life stage has different requirements that must be met for a successful nursery phase. L. corrugata has a narrow thermal optimum for the development of gametophytes at 15.7–17.9 °C, with an upper-temperature threshold of 23 °C, and with no difference in temperature response between female and male gametophytes (Dieck 1993; Paine et al. 2021a, b). Visch et al. (2023) found that temperature and light levels of 12 °C and 60 µmol photons m−2 s−1 are optimal for growth and reducing microscopic contaminants in the early juvenile phase of L. corrugata sporophytes. L. trabeculata has seasonal variation in germination rates, with a higher germination success in cold seasons (autumn and winter) than in spring and summer. The range of temperature tolerance of L. trabeculata gametophytes is comparatively large at 0–25 °C (Dieck 1993; Tala et al. 2004), and similarly, the gametophytes of L. vadosa survive in temperatures close to freezing and up to 21.4 °C (Peters and Breeman 1993). L. nigrescens’s zoospore germination is over 70% at temperatures between 5 – 14 °C, with gametophytes surviving between 1–23 °C (Avila et al. 1985; Dieck 1993). Further, the same species of Lessonia may have different temperature tolerances in different environments. Oppliger et al. (2012) demonstrated that in Chile, L. nigrescens populations from high latitude have less tolerance to high temperatures than populations from lower latitudes. The survival of high latitude gametophytes decreased above 15 °C while low latitude gametophytes had survival greater than 80% up to 20 °C. However, growth was greatest at 20 °C in both populations. Overall, most Lessonia species assessed to date have a broad temperature range (concerning the thermal variation in the temperate zone) for gametophyte survival that would simplify the laboratory management for temperature control.
As for temperature, gametophytes of each Lessonia spp. will have specific light requirements (quantity and duration) that influence their metabolism and growth (Wu 2016; Takahide et al. 2017). Therefore, knowing the light requirements allows for optimising the nursery phase of cultivation. L. nigrescens is found in shallow water (to 1 m depth) and this species develops at relatively high irradiance levels with most 90% of meiospore germination occurring between 75–100 μmol photons m−2 s−1. In addition, the female gametophytes develop more quickly in 100 μmol photons m−2 s−1, compared to lower irradiances, reaching 50 μm in diameter (Avila et al. 1985). In contrast, L. corrugata and L. trabeculata are found between 1–25 m and 0.5–20 m depth, respectively, and are exposed to a more variable regime of solar irradiation. As a result, these species are able to tolerate a wider range of irradiance. For example, L. corrugata female and male gametophytes develop best between 40–100 μmol photons m−2 s−1 while L. trabeculata gametophytes develop best between 10 -70 μmol photons m−2 s−1 (Murúa et al. 2019; Paine et al. 2021a, b). L. flavicans produced ten times more sporophyte biomass at a photoperiod of 18:6 L:D (light: dark) than 6:18 L:D at 25 days of cultivation (Mansilla et al. 2014). Freshwater is another environmental factor that can influence Lessonia growth, either through rainwater or freshwater discharge in semi-enclosed bays. For example, L. flavicans from subantarctic islands showed some tolerance to low salinity, with its growth affected only in cultivation at salinities below 23 PSU (Mansilla et al. 2014).
Water motion is a factor that is well known to affect kelp growth (see above) but has not been studied for the microscopic phases (Veenhof et al. 2021). For L. corrugata, Nardelli et al. (in prep) examined the effect of rotating (15 rpm, ~ 7 cm s−1) the spools in the nursery phase compared to spools that are not-rotated: both had the same exposure to light and water motion was provided via bubbling with air. For rotating spools, the sporophyte blades and holdfasts were larger than non-rotating spools, and when transferred to the sea, the biomass production of rotating spools was ~ 2 times greater. These results show clearly that providing rotational water motion in the nursery phase improves the performance of the at-sea phase for L. corrugata.
In summary, it is necessary to properly identify the specific needs of each species to build a suitable nursery cultivation system, and optimisation of the nursery phase is critical to developing seed stocks that are used to start cultivation in the sea. One potential method of optimizing Lessonia growth in relation to environmental conditions is via selective breeding and cross breeding to generate high-performing kelp cultivars. This has been essential in optimizing production in other kelp species, such as Saccharina latissima and Undaria pinnatifida (Shan and Pang 2021; Mao et al. 2022) and is increasingly being applied in kelp aquaculture (Kim et al. 2017; Goecke et al. 2020).
At-sea cultivation has different challenges than in the nursery, as both depth of cultivation and seasonality influence growth. The first sea cultivation of Lessonia occurred during the 1990s in Chile, with the purpose of reducing the harvesting pressure on natural beds of L. trabeculata (Edding et al. 1990). With the background of many years of ecological and laboratory studies, it was possible to start studies of cultivation in the sea (Ojeda and Santelices 1984; Santelices and Ojeda 1984; Avila et al. 1985; Santelices 1989; Vasquez and Santelices 1990; Venegas et al. 1992). Out-planting methods followed that applied for Saccharina japonica cultivation in Japan, detailed by Kawashima (1984). In Chile, the growth rate of L. trabeculata did not differ between depths of 1 and 6 m (an average of 7.5 mm day−1) but growth increased between spring and late summer and decreased in autumn (Edding and Tala 2003). Westermeier et al. (2006) achieved 0.25 kg fresh weight m−1 after 4 months of cultivation at sea, which is low compared to other kelps such as Saccharina angustissima which can have a yield of up to 3.4 kg fresh weight m−1 after 6 months (Li et al. 2022). The low L. trabeculata production per meter after 4 months at sea, may have been due to the low sporophyte density on growth line (~ 3 ind. m−1, Westermeier et al. 2006). Another farm layout produced ~ 1.8 kg fresh weight m−1 after one year, using seeded vertical dropper lines (Edding and Tala 2003). There is an increasing interest in L. corrugata cultivation in southern Australia (https://www.seaweedsolutions-crc.com/), with ongoing investigations into testing different methods of Lessonia cultivation in the nursery (Paine et al. 2021a, b; Visch et al. 2023) and at-sea, integrating seaweeds with other types of aquacultures such as salmon and mussel production (Paine et al. 2021a, b; Biancacci et al. 2022; Smart et al. 2022). The timing of L. corrugata out-planting affects subsequent growth with better growth performance in spring followed by winter compared to autumn (Nardelli et al. (In prep)). Other kelp species have shown a different response to timing of outplanting. In Norway, Saccharina latissima outplanted in winter performed better than when out-planted in spring (Matsson et al. 2021). In New Zealand, L. variegata has been successfully grown in research-scale cultivation (Stenton-Dozey et al. 2021).
Morphology, such as the shape of blades or holdfasts, may influence the attachment and growth of kelp on lines at sea. For example, the blades of Laminaria digitata are wide in shape, which results in high drag and facilitates detachment, with the holdfasts not being strong enough to keep them attached to the growth line. Consequently, it is not suitable for cultivation in exposed areas (de Bettignies et al. 2013a, b; Kregting et al. 2016). In contrast, S. latissima shows no loss of biomass when grown in moderate flow compared to areas of low flow (Peteiro and Freire 2013). Lessonia species are typically found in regions exposed and moderate exposed to waves and have morphologies that decrease drag and increase flexibility (as discussed earlier), such as long narrow blades and stipes (except L. adamsiae and L. flavicans (Fig. 2A)), also branched holdfast that firmly adhere to the substrate (L. corrugata (Fig. 2D), L. variegata (Fig. 2C)). Most Lessonia have smooth blades except L. corrugata and L. adamsiae for which blades are corrugated. Such surface corrugations on kelp blades are too small to create turbulence and are thought to reduce drag forces at the blade surface by creating spanwise vortices (Hurd 2000; Hurd et al. 2003, 2014; Hurd and Pilditch 2011).
Economic viability is key to start successful industrial cultivation of Lessonia sp. at-scale. Zuniga-Jara and Soria-Barreto (2018) combined data on pilot cultivations and experimental trials with economic viability analysis for commercial scale of Lessonia spp. in Chile. They found that L. trabeculata and L. berteroana met the three prerequisites for commercial cultivation: (1) species’ natural distribution in the area of interest; (2) at-sea cultivation technology; (3) aquaculture interest for the species. L. trabeculata can be cultivated in all seasons except spring, when an increase in biofouling reduces the market value, which makes it impossible to profit from production costs. For example, biofouling decreases the quality of the raw material for application in the alginate polysaccharide (Draget 2016; Zuniga-Jara and Soria-Barreto 2018). The productivity estimate indicates an average of 14 kg m−1 wet weight, reaching 11 t of wet weight weekly of production using four long lines. This study is very helpful in guiding the stakeholders who work to apply basic cultivation knowledge to move from an experimental (few hectares) to a commercial (multiple hectares to km2) scale. The increasing global demand for kelp highlights the need to optimise methods for Lessonia aquaculture as harvesting natural forests will not meet the market needs.
Commercial applications of Lessonia spp.
At least since the fourth century, kelps have been applied as food in Asian countries, and subsequently, consumption and applications, including in the alimentary, cosmetic, food or biomedical industries, have been growing (Koru et al. 2013; González-Roca et al. 2021). Lessonia trabeculata is widely used as a source of food for abalone and sea urchins in Chile (Edding and Tala 2003). Lessonia corrugata has the potential to produce high-quality food when integrated with salmon and mussel farming, being safe for human and animal consumption as it has low concentrations of contaminants such as As, Al, Pb, Cd and Hg but is of high nutritional value for humans considering its high concentrations of minerals such as Na, K, Mg, P, I, Fe, Zn, and Ca (Biancacci et al. 2022). Dried L. nigrescens has a good level of protein (12.8%) and 1.015 kg has a similar amount of protein as 1 kg of eggs (13%) (Fernandez et al. 1973), and higher levels than other brown seaweeds such as Macrocystis pyrifera (10.2%) and D. antarctica (8.2%) (Astorga-España and Mansilla 2014). For L. berteroana, there is a seasonal variation in biochemicals, with higher levels of protein and lipids in autumn (13.5% and 0.9%, respectively) compared to other seasons (Vega and Toledo 2018).
A range of chemicals have been extracted from Lessonia that have human health and agricultural applications. Fucosterol is a triterpene derivative that has been shown in clinical studies to protects human skin against UV damage and reduces metabolic syndromes such as heart disease, stroke and type two diabetes (Hwang et al. 2012; Maeda 2013; Becerra et al. 2015). In low doses (10 µM), fucosterol extracts from L. vadosa also provide antiprotozoal action against leishmania (Becerra et al. 2015). Similarly, fucoidan extracted from L. vadosa showed (in-vitro) anticoagulant activity (Chandía and Matsuhiro 2008) as well as activating the defensive enzymes phenylalanine-ammonia lyase, lipoxygenase and glutathione-S-transferase in plants (Chandía and Matsuhiro 2008). Lessonia flavicans, L. nigrescens, and L. trabeculata extracts provide a mixture of fucans and alginic acid that may be applied in agriculture as a pesticide against harmful fungi in wheat and tobacco (Percival et al. 1983; Chandía et al. 2004, 2005; Matsuhiro and Zambrano 2004). Fucoidan and alginic acid compositions are altered depending on the environmental conditions to which the seaweeds are exposed (water motion, light and temperature) (Martins et al. 2011; Valiente and Mogollón 2013; Harb et al. 2018; Urrea-Victoria et al. 2020). For example, Lessonia from exposed sites produces a high content of polysaccharides compared to sheltered sites, in addition to different gel quality throughout the year (Chandía et al. 2004, 2005; Valiente and Mogollón 2013; Leal et al. 2018; Zou et al. 2019).
Antioxidants are compounds that reduce cellular deterioration under oxidative stress, are beneficial for the human immune system, and have anti-inflammatory properties. Numerous seaweeds have been reported as sources of natural antioxidants (Zimmermann et al. 2005; Hurd et al. 2014; Araújo et al. 2020), including Lessonia. For example, dry tissue and extracts of L. spicata showed high antioxidant activity in aqueous extracts from its holdfast, 100% α-glucosidase inhibitory activity with ~ 170 µg mL−1 and were an effective and safe antihyperglycemic and antitubercular agent for human consumption (Erpel et al. 2021). L. nigrescens methanolic extract (100 µg mL−1) inhibited 99% of Mycobacterium. tuberculosis development, in vitro test (Wächter et al. 2001). Polyphenol extracts from L. trabeculata also showed efficient antioxidant activity with lipase inhibition at doses < 0.25 mg mL−1 (Yuan et al. 2019). Increasingly, Lessonia shows potential for food, cosmetics and many other applications for health and industry.
Future directions
The current 11 species of Lessonia are restricted to the temperate southern hemisphere, forming dense forests on moderate to high wave-exposed shores where they play an essential role in providing food and shelter for many organisms and supporting diverse food webs. There is a considerable published information available on the biology, chemical composition and applications of some species of the genus Lessonia. However, there are knowledge gaps that require further investigation. For example, some studies have shown that beds on wave exposed sites have a greater capacity to store carbon than sheltered sites. This is an important finding and should be studied further to gain a better understanding of the mechanisms that control carbon storage in natural beds. Chimerism in Lessonia, although known to occur in several species, is also a knowledge gap. Understanding how chimerism affects reproduction, development and survivorship would contribute to the understanding of Lessonia ecology but potentially, can also be utilised in Lessonia aquaculture, allowing cultivation at high densities on lines. Lessonia spp. are an important source of raw material with many potential applications for human benefit. Characterization of the Lessonia chemical composition should be studied to meet the market demand. As antioxidants, antifungals, antibacterial agents, and new drugs can be found through bioprospecting of these species.
Management plans introduced in some countries, primarily Chile, show promise in reducing the impact caused by harvesting and maintaining healthy populations. Nonetheless, developing cultivation methods for a Lessonia aquaculture industry is necessary to reduce pressures on natural Lessonia forests. In addition, this activity may generate better quality raw materials due to the selection of seaweed for cultivation and the increase of jobs directly or indirectly linked to seaweed aquaculture. Studies on cultivation techniques, seasonality of reproduction and growth are the main gaps that need to be filled to obtain efficient and sustainable aquaculture.
Data availability
Data sharing not applicable to this article as no datasets were generated or analysed during the current study.
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Acknowledgements
The authors would like to thank Dr. Erasmo Macaya Horta for the photos provided and Dr. Catriona Macleod, Dr. J. Craig Sanderson, Dr. Alecia Bellgrove and Institute for Marine and Antarctic Studies (IMAS) for providing support.
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Open Access funding enabled and organized by CAUL and its Member Institutions This research was funded by the “Seaweed solutions for sustainable aquaculture CRC Project” funded by the Australian government, Institute for Marine and Antarctic Sciences/University of Tasmania, CRCPSIX000144.
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Nardelli, A.E., Visch, W., Wright, J.T. et al. Concise review of genus Lessonia Bory. J Appl Phycol 35, 1485–1498 (2023). https://doi.org/10.1007/s10811-023-02968-3
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DOI: https://doi.org/10.1007/s10811-023-02968-3