The Brown Seaweeds Fishery in Chile The Brown Seaweeds Fishery in Chile

Chilean fishery of brown algae includes species belonging to the genus Lessonia , Durvillaea , and Macrocystis , which can be found along the coast, ranging latitudes from 18° to 55°S. The exploitation of these seaweeds is done mainly in the Northern coast because the environmental conditions of this region decrease initial production costs. Brown algae are exploited from natural populations and exported to international markets as row material, source of alginates, widely utilized in diverse manufacturing processes and industries. International demand for Chilean kelps has produced sustained increase in harvest during the last decade, reaching more than 390,000 dry tons/year. This chapter approaches the most relevant aspects of the brown seaweed fishery in Chile which covers a wide range of the Southeast Pacific coast, considering the number of commercial species, its abundance and distribution, knowledge achieved on their ecology and biology regarding management, and conservation of these resources, and finally, provides tools for stakeholders and policy makers directed to sustainable management of natural kelp beds occurring in the cold temperate seas.


Introduction
Chile, a narrow and long country with over 4500 km of continental coastline, has an ancient tradition in the use of sea resources. Numerous algae, shellfish, and fish species have been incorporated in the diet and every day habits of his inhabitants, since prehistoric times. The astonishing evidence found at the archaeological site Monte Verde, dated 12,500 years BP and located near Puerto Montt (41°S), provides evidence of Pre-Clovis human settlement in South America, and exhibits ancient use of macroalgae, probably as food and for medicinal purposes [1,2]. The diet of coastal human communities incorporated brown and red algae as significant components along the last 500 years, especially in those coastal populations situated South beyond 30°S [3].
As sources for alginates production, brown algae in Chile are exploited from natural populations and exported to world markets as row and dried commodity for alginates extraction [4,5]. The local national gel industry, as well as invertebrate aquaculture production, utilizes only a minor fraction of the annual harvest [6]. During the last decade, a sustained increase of harvesting has been taking place, because of the international demand for Chilean kelp; production has reached more than 390,000 dry tons associated with an economic return of more than US$ 90 million [5,7]. Chilean brown algae of economic importance belong to genus Lessonia, Durvillaea, and Macrocystis, and they occur throughout the coast from 18° to 55°S [8]. Even this wide distribution range, the exploitation of these resources is done mainly in the Northern region of the country between 18° and 32°S, because environmental conditions, such as remarkable air high temperature and dryness of the coastal desert, which decrease production costs of drying process close to zero and, consequently, the total processing cost before their commercialization [6].
In Chile, the harvest of brown algae is also matter of social relevancy since more than 15,000 people depend more or less directly on the exploitation and collection of this marine resource [9]. As established by local law, only authorized and registered artisanal fisherman are allowed to harvest such kelp [6]; however, enforcement measures and control are difficult to put into effect because of the topography of coastal territory where these natural populations of kelp occur, but also due to their extension and accessibility [10]. From the point of view of their ecological role, kelps have been defined as engineer species in the coastal marine ecosystems; they are key species which participate maintaining and preserving foci of high biological and genetic diversity [11,12]. Also, these species are sensitive to disturbances from both natural and/or anthropogenic origin [13,12].

Species in the fishery
Geographic distribution and occurrence of commercial brown seaweed are associated with high-energy environments in the Southeast Pacific (Figure 1). Lessonia species can be intertidal and subtidal as well; they form belts along exposed rocky coasts ( Figure 1A, B, D); Macrocystis forms shallow kelp beds ranging from intertidal zone to ca. 15 m depth in Northern latitudes ( Figure 1C, G); it is gradually replaced toward Southern areas by Durvillaea (Figure 1F), which dominates the intertidal zone in wave-exposed areas [8]. In South direction and beyond 42°S, Macrocystis is the most abundant and dominant kelp species [15]; Lessonia species have almost continuous distribution along the whole Chilean continental coast; instead, the distribution of Macrocystis is fragmented into populations that form patches in Northern Chile [11,16,13], contrasting with its continuous coastal belts distribution from 42°S toward Cape Horn (55°5 8°S); Macrocystis distribution includes the Chilean Southern fjord zone, surrounding Cape Horn, and ascending in North direction by the Argentinian exposed coast until Chubut area in the Atlantic (41°S). Several elements are combined to determine the observed kelp distri-bution patterns; they result from multifactorial interaction of complex life-history strategies of the involved species with environmental factors, such as spatial and temporal variations in water movement, nutrient availability, light, and temperature [17,16,12]. Chilean kelp species commercially exploited are as follows: Lessonia trabeculata, Lessonia berteroana, Lessonia spicata (members of Lessonia nigrescens complex, for details see [18][19][20]); these are all species having two morphotypes during their natural life cycle, which represent very different ecological roles and requirements, in both environmental and physiological aspects. Large and conspicuous (so, harvestable) sporophytes alternate with microscopic few cell and benthic organisms which are the gametophytes.

Biological and ecological aspects
Studies on the distribution and abundance of Chilean commercial brown seaweed were scarce and locally restricted until the end of 2000 [21-29, 30, 31]. Other than this, the use of noncomparable methodologies in the few studies carried out, which approached biomass stocks information, did not allow extrapolation and inter-annual comparisons of the available total biomass. Similar situation occurred in relation to distribution studies of the involved species, both in temporal and spatial gradients [4]. Harmonization of methods or collection of information, as well as systematization of them, is essential aspects of the population ecology of commercial species, in order to propose adequate regulations and policies that guarantee a sustainable management of these resources.
One of the few extensive and intensive evaluations of biomass distribution of Lessonia trabeculata, Lessonia nigrescens, and Macrocystis pyrifera was done during 2004-2005, for the geographic extension ranging between 26° and 32°S; its main goal was to determine the distribution and abundance of the mentioned species in more than 700 km of coast. During the study, 140 sampling stations were established separated by 4.5 linear km, excluding a priori sandy beaches and soft bottom subtidal areas because they represent inadequate substrates for kelp's spores settlement [6,5]. L. trabeculata was found in rocky subtidal habitats between 0 and 30 m depth in the whole study area. Depending on the extension of the rocky platform into the subtidal zone, local biomass up to 50,000 wet tons was recorded. Estimation of abundance indicated a standing stock of approximately 800,000 wet tons of L. trabeculata in the study area. L. nigrescens was distributed in a continuous pattern along the rocky intertidal zone of the whole study area, with local biomass (sampling station) registered between 50 and 4000 wet tons. Using GIS abundance polygons were constructed which revealed a standing stock of more than 100,000 wet tons of L. nigrescens in the study area [6]. In contrast, Macrocytsis evidenced fragmented distribution within the study area. Local populations were small and estimated biomass fluctuated between 2 and 12 wet tons. The sum of local biomass allowed estimation of a standing stock that did not exceed 200 wet tons for the entire study area at the time [6,5].
Because of Lessonia nigrescens represents more than 70% of total landings of brown Chilean seaweed fishery, several studies have been focused on this species. Studies on genetics, molecular biology, and population ecology show that L. nigrescens is a species complex composed by two cryptic species: Lessonia berteroana and Lessonia spicata [18,42,43]; L. berteroana is distributed from the South of Perú (ca. 15°S) to approximately 30°S, and L. spicata occurs form 30°S toward South [20]. In the last decade, the kelp harvest in Chile has been sustained principally by the Lessonia nigrescens complex, especially in the area known as latitudinal break for biodiversity distribution which location is considered approximately at 30°S [19].
Exploited and unexploited species belonging to Lessonia nigrescens complex form Northern Chile were compared using morphological and demographic parameters such as density, biomass, recruitment, and population structure [5]. These are traits which allow estimation of the effect of harvesting in other natural populations of brown algae [44][45][46][47], and the assessment of the impact of natural disturbances [48,16,13] and other anthropogenic activities on such species [37]. In this context, the morphological and demographic parameters used for evaluate L. nigrescens could be useful as ecological indicators for: (1) to evaluate the consequences of good harvesting practices agreed upon by fisherman, (2) to compare the effect of harvesting in areas with different administration policies, (3) to monitor the sustainability of exploited kelps, and (4) to propose to competent authorities the precautionary and/or recovery adequate measures for sustainable managing of dynamics population of commercially important brown algae.

Collection, harvest, and landings
Largely and until year 2000, the whole brown algae fishery in Chile was based on the collection of natural mortality kelp from coastal populations. A sudden and significant increase of its demand, other than as raw material for alginate source, also as food source for cultivated abalones introduced in Chile in the last 16 years, triggered the harvest of kelp species. Since then, the Chilean brown seaweed fishery becomes an extractive fishery in which converge four main factors: (1) still the international market request for alginic acid source; (2) use for feeding the emergent local farming of several kelp-consuming organisms under controlled conditions; (3) the switch of fishers toward the harvest of commercial brown seaweeds as consequence of the collapse of other benthic fisheries, and (4) the strong impact on local economy produced by the international fluctuation of the price of copper. This metal constitutes the Chilean main resource, representing more than 60% of the internal gross product (PIB, as its acronym in Spanish); it provides direct and/or indirect jobs for thousands of people in the country, being Chile the first copper producer around the world. Local economy is extremely sensitive to fluctuations of international cooper price, and the fall (currently crush) of it provokes significant unemployment, particularly of non-specialized workforce; as one of its primary consequences, unemployed people are forced to migrate to coastal areas where they can develop subsistence economy based on precarious jobs represented by the collection and harvesting of brown seaweeds [9,6].   The significant rise of kelp demand, as commodity source of alginic acid around the world during the last years, explains the increase of kelp extraction. A smaller fraction of this increment is consequence of the yield reduction of kelp used for milling, because of higher humidity contents of lately processed plants if compared with those from previous years [7,50]. From a different perspective, during 1997-1998 when a severe ENSO event occurred, Chilean exports of brown algae showed a considerable peak, probably related to significant mortalities generated by this large scale oceanographic event. The warming of the ocean surface, simultaneously to decreasing of nutrients concentrations, both associated with "El Niño," has strong impact over kelp populations and thousands of dead plants are cast ashore by waves which end collected by fishermen [16,23,60].
Since 2005, the abalone cultivation industry exhibits a remarkable and sustained growth, especially in Northern Chile; this commercial activity consumes close to 4800 tons of fresh alga/ year, mainly Macrocystis; neither the utilization nor the economic yield of this activity is comparable, until date, to demand of Chilean kelp as source for alginate extraction.

Management
Chilean authorities have implemented a management and conservation strategy program for economically important brown algae, considering its economic, social, and ecological importance, and also the significant increase of kelp harvest. The expectative of this program is focused on surveillance of available and harvestable biomass, evaluation of strength of harvesting (Capture per Union Effort-CPUE), and characterization of the productive chain based on these primary producers. As a result of this strategy, carried on since 2010, plus several years of kelp knowledge achieved, recommendations have been established for the management of kelp sustainability. The premise is "how to harvest is more important than how much you harvest" [5]. This program has been implemented in three Chilean conservation tools performed at the country level and which represent three different conservation strategies: (1) marine protected areas (marine park, marine reserve), (2) open-access areas for artisanal fishermen (OAA), where they collect and harvest marine resources, and (3) management areas for exploitation of benthic resources (MAEBR), where organized fisherman have some territorially rights assigned over a sector of the coast. The conservation strategy involved in MAERB is based on co-management (see [50][51][52][53][54][55]).
The main practical recommendations of the program for the sustainability of brown seaweeds are focused on selective harvesting of adult sporophytes and maintenance of a permanent stock of individuals able to reproduce, recruitment facilitation, decrease of grazing by benthic invertebrates, and permitting the sustainability of kelps and the conservation of its associated biodiversity [6,5,56,62]. Considering all aspects mentioned, the following bio-ecological recommendations must be applied to kelp beds subjected to significant, frequent, and intense harvesting: (1) to harvest the whole plant, including the holdfast. According to administration regime (Conservation Strategy) assigned by competent authority to natural populations, the density of both adult plants and juvenile recruitment of Lessonia nigrescens is subjected to temporal variation (Figure 3). In marine protected areas like marine parks or marine reserves (MPA), the annual renewal of kelp populations exhibits a seasonal cycle wherein the natural mortality of adults is compensated by intense juvenile recruitment ( Figure 3A). In MAEBR, the density of adult plants decreases during the maximum harvest period, which is preferably carried on during spring and summer; in these conditions, the annual cycle of kelp renewal is maintained by recruitment of juvenile plants post-harvest ( Figure 3B). In OAA, where the kelp harvest occurs all along the year, adult plants density decreased significantly ( Figure 3C). Thus, constant releasing of substrate by permanent harvesting facilitates sustained juvenile recruitment, which significantly increases the density of recruits throughout the year; this last population renewal process takes places independ-   (Figure 3).
The density of adult plants is greatest in populations inside MPA in contrast to those inside OAA (Figure 3). As previously exposed in MAEBR, the seasonal harvest of Lessonia decreases the density of adults; however, this impact of harvesting is significantly lower than which is observed in OAA (Figure 3). In these open-access areas, the density of adult plants is less because of high harvesting pressure produces contraction of the stock of reproductive plants, and thus negatively affects the kelp renewal. There exists an exception to this pattern observed in OAA constituted by those populations where the difficulty of access to the coastline generates a barrier to permanent harvest. In this case, topography constraints to access generate effects that mimic a sort of natural co-management; in this way, the pattern of size distribution of Lessonia plants in OAA is quite similar to the pattern observed in MAERB [49]. In MPA, Lessonia yield (kg of biomass/m 2 ) is constant throughout an annual cycle and close to 50 kg/m 2 ( Figure 4A). By contrast, the available biomass in MAEBR evidences marked seasonality with an annual cycle of renewal of the kelp post-harvest during spring and summer ( Figure 4B). A similar tendency is observed in OAA, even if with significantly less available biomass which does not surpass 25 kg/ m 2 ( Figure 4C). Available biomass is biggest in MPA populations and lowest in OAA populations. In MAEBR and OAA, the available biomass is 50 and 65% lower, respectively, than stocks in MPA [50]. The available biomass in MAEBR represents the permissible limit for sustainable exploitation of the kelp forests and is evidence of the adequate application of the management plan. On the other hand, the level of available biomass in OAA is an indicator of highly exploited populations, and its management program would help to establish sustainability parameters dealing with a strong harvest pressure [49].  The size structure of Lessonia nigrescens populations, according with the morphological variables suggested [6], varies according to the management and conservation measures applied ( Figure 5). In MPA, 20% of the populations are recruits and 35% are juveniles, and the rest of the population is adults with large-sized plants ( Figure 4A). In MAEBR and OAA, recruits represent 35% of the whole population, while juvenile plants represent 45 and 55%, respectively (Figure 5B, C). In MAEBR, the fraction of adult plants is renewed by the growth of juvenile plants during the annual cycle, while in OAA, strong harvesting pressure facilitates recruitment and colonization of free primary substrate. In MPA, the portion of adult plants available for harvesting is in general, 45% of the population. In MAEBR, the harvestable portion corresponds to 25% of the total available biomass. By contrast, in OAA, the available biomass for commercial harvesting did not exceed 10% of the total plants in the whole Lessonia population studied in Northern Chile [5,49].
After 25 years of observation and assessment of Lessonia populations, after thousands of hours of field monitoring and abundant literature produced, and based on bio-ecological knowledge accomplished, the main concept associated with recommendation for sustainable management of Lessonia nigrescens complex is "how to harvest is more important than how much you harvest" [6]. This resource management practice has been spread among fisherman during the last 15 years and adopted voluntarily as an alternative to the traditional precautionary method, in which the fishing authority imposes a capture quota, arises from the total available biomass [5,49]. However, fulfilling the premise previously mentioned requires good practices on the part of artisanal fishermen, who are the only authorized users to harvest brown algae in Chile. The correct application of the management recommendations of MAEBR seems to be strongly related to the social capital that co-management generates [54], a concept that does not make sense in OAA where harvesting activity is individual and difficult to enforce (see [52][53][54]). The wide latitudinal extension of the littoral zone and several restrictions to it access increase the cost of enforcement and decrease the efficacy of control of the fishing authority [10]. Therefore, as in many other cases if not all of them, the construction of participative awareness is a key factor in the conservation of natural populations of Chilean kelps and the sustainability of this resource [5,49].
As last recommendations, it will be necessary to make significant progress in areas such as: (a) perfection of the capacities of commercial management by using social capital, (b) optimization of control mechanisms and enforcement considering the idiosyncrasy of Chilean artisanal fishermen, (c) improvement of information flow between and among the different actors in the productive chain and the authorities, and (d) establishment of controlled extraction of brown algae by using management plans from territorial perspective.
A participative, adaptive, and multidisciplinary management plan requires ecological indicators that permanently monitor administrative measures agreed upon by the direct users of Lessonia resource. Considering that these ecological indicators need to be validated [55], they can be selected from administrative measures regarding brown algae such as volume harvested, capture per amount of effort, and minimum legal size of capture [50]. Landing of harvested volume is an easy indicator to track and verify but requires an efficient, participative recording system, in real time, allowing the reaching and use of information at the right moment ( Table 1). Capture per amount of effort and minimum legal size are indicators that are comparatively more complex to monitor and enforce, because they depend on the participation of scientific observers and also on the interest of fishermen to generate such records ( Table 1). These indicators are useful tools to assign harvest quotas, establish rotation areas, or to establish extractive or biological bans [49]. Training Table 1. Resource variables proposed to monitor the harvest of Lessonia nigrescens complex.
The effect of harvesting in OAA has been explained by the absence of precautionary management measures in a scenario of high demand for biomass [9,14,44,46]. Thus, management based on the ecosystem approach requires ecological indicators sensitive to harvesting pressure, which allow establishment of decision criteria that are easy to observe, communicate, and measure by both scientific observers and artisanal fishermen [49]. Demographic attributes, such as density of adult plants, biomass per unit of area, recruitment, and size structure all constitute indicators that satisfy these characteristics, are easy to obtain and can be evaluated along spatial and temporal gradients ( Table 2) [49].

Fisheries and Aquaculture in the Modern World
Based on demographic indicators, the rule establishes that the harvest in OAA should begin when the abundance and biomass of a population per unit of area is close to biomass or demographic levels detected in an un-intervened population (e.g., MPA): There is a minimal density of recruits, the portion of adult plants must be above 40% of the total population, and the percentage of remaining adult plants in the area should be enough to generate post-harvest recruitment ( Table 2). Afterward, once the population reaches levels of abundance and biomass per unit of area similar to those found in the population under intense harvesting pressure (e.g., OAA), its sustainability will depend on following elements: (1) stability of recruitment frequency, (2) maintenance of a stock of reproductive individuals, and (3) stability of harvesting frequency. Once these indicators exceed the harvesting period should end and should be followed by a recess period (ban or quotas), until adequate pre-harvest values would be reached ( Table 2). Thus, the installation of a permanent monitoring program of the populations of Lessonia nigrescens complex in OAA and in MAEBR, using demographic indicators, will allow as follows: (a) validation of the application of management plans, (b) detection of the deleterious effects on population dynamics produced by exogenous disturbances in the harvest, (c) respect the necessary period to renew the forest to optimal harvesting levels, and if necessary, (d) determination of extraction quotas by sector, and (e) establishment of extraction bans in a justifiable, participative, and localized way.

Concluding remarks
The landings of brown seaweeds in Chile [61] reach 390,000 wet tons/year being the world's largest landings from natural populations. This fishery is managed under the concept of "good practices," based on biological and ecological knowledge of the species [6,12,14,23,25,32,48,[57][58][59]. Most of the brown macroalgae are known as foundational species of marine ecosystems [12]; they constitute the basis of coastal food webs [14,26,60,62], contribute significantly to the total biomass of the ecosystem [23,32], and are highly connected with all trophic levels [61]; they provide shelter, food, nursery, and breeding areas [23,32,6]. Indiscriminate harvest of a foundational species as L. nigrescens can generate a significant negative impact on the ecosystem with unknown effects. In this context, ecological indicators proposed [49] are tools for stakeholders and policy makers, enabling greater sustainability of exposed rocky shores in cold temperate seas of the world where these kelp of economic importance are key dominant organisms in cover, biomass, and ecological role.