The seaweed hydrocolloid industry: 2016 updates,requirements, and outlook

The seaweed hydrocolloid industry, comprising agar, alginate, and carrageenan extracts, continues to grow in the order of 2–3% per year with the Asia-Pacific region increasingly dominating the raw material and manufacturing aspects of the industry. Geographic overviews, also in a historical perspective, of seaweed raw material availability including prices and consumption, manufacturing capacities, and utilizations and sales of extracts is presented. Some current and future industry dynamics, requirements, and changing structures, e.g., Indonesia’s increasingly dominant role within farming of agar and carrageenan-bearing seaweed species, randomly imposing of seaweed harvest restrictions or ban on exports, creation of a global certification standard for seaweed, and supply-demand dynamics for seaweed versus future global population are presented. The industry is increasingly being commoditized and China has become an important and, in many cases, dominant factor within all types of seaweed hydrocolloids and some explanations to this and strategic response by the rest of the industry is also touched upon. Also presented are some areas where the seaweed industry needs help from the scientific community. The main challenge is the ongoing general seaweed deterioration experienced in cultivated species—how are the strains to be improved and revitalized and can cultivation techniques be improved further? There is a general trend towards sustainability and, although seaweed cultivation and harvest can be sustainable, there is interest in the development of greener processes.     

Prospects and challenges for industrial production of seaweed bioactives

Large‐scale seaweed cultivation has been instrumental in globalizing the seaweed industry since the 1950s. The domestication of seaweed cultivars (begun in the 1940s) ended the reliance on natural cycles of raw material availability for some species, with efforts driven by consumer demands that far exceeded the available supplies. Currently, seaweed cultivation is unrivaled in mariculture with 94% of annual seaweed biomass utilized globally being derived from cultivated sources. In the last decade, research has confirmed seaweeds as rich sources of potentially valuable, health‐promoting compounds. Most existing seaweed cultivars and current cultivation techniques have been developed for producing commoditized biomass, and may not necessarily be optimized for the production of valuable bioactive compounds. The future of the seaweed industry will include the development of high value markets for functional foods, cosmeceuticals, nutraceuticals, and pharmaceuticals. Entry into these markets will require a level of standardization, efficacy, and traceability that has not previously been demanded of seaweed products. Both internal concentrations and composition of bioactive compounds can fluctuate seasonally, geographically, bathymetrically, and according to genetic variability even within individual species, especially where life history stages can be important. History shows that successful expansion of seaweed products into new markets requires the cultivation of domesticated seaweed cultivars. Demands of an evolving new industry based upon efficacy and standardization will require the selection of improved cultivars, the domestication of new species, and a refinement of existing cultivation techniques to improve quality control and traceability of products.     

Seaweeds,then and now

An historical overview of meetings of the International Seaweed Symposium is presented. A summary of attempts since 1952 to establish a seaweed industry in British Columbia is given. A brief review of recent developments in the area in relation to a seaweed industry is outlined.     

The First International Seaweed Symposium held in Edinburgh,UK, 1952: applied seaweed science coming of age

Since the first commercial and systematic use of large brown algae for potash in the eighteenth century, chemists have applied their knowledge to benefit the industrial utilization of seaweeds. Towards the end of the nineteenth century, the focus of seaweed chemistry started to shift from the inorganic to the organic content. Trailing the chemists, seaweed botanists also became directly involved in the industrial efforts by surveying and assessing seaweed populations. In the 1930s, a modern seaweed industry emerged, based on seaweed polysaccharides and seaweed meal. Prior to World War II seaweed botanists, chemists and industrialists had no regular, joint international arena.The First International Seaweed Symposium (ISS) was held in Edinburgh, 14–17 July 1952. It was referred to as the follow-up of the limited: “Conference on utilization of seaweeds” which was held in Halifax, Nova Scotia, 1948. A main driving force was the Canadian war effort to extract substitute gelling materials from local seaweeds for use in the foodstuff industry. The conference in Halifax was rooted both in the annual Canadian “Irish Moss meetings” in Ottawa 1944–1947 and in the post-WWII expansion of regional laboratories of the National Research Council of Canada. The First ISS was attended by approximately 160 scientists from 21 countries. The symposium demonstrated the role and secured the position of this new applied, multi-disciplinary seaweed science.     

Seaweed micropropagation techniques and their potentials: an overview

The seaweed industry worldwide uses 7.5–8.0 million tonnes of wet seaweeds annually with a majority of it derived from cultivated farms, as the demand for seaweed based-products exceeds the supply of seaweed raw material from natural stocks. The main advantage of cultivation is that it not only obviates overexploitation of natural populations but also facilitates the selection of germplasm with desired traits. To enhance the economic prospects of seaweed cultivation, varied practices, such as simple and cost effective cultivation methods, use of select germplasm as seed stock coupled with good farm management practices, etc., are adopted. Nevertheless, in vitro cell culture techniques have also been employed as they facilitate development and propagation of genotypes of commercial importance. There are more than 85 species of seaweeds for which tissue culture aspects have been reported. Although the initial aim of these techniques focuses mostly on genetic improvement and clonal propagation of seaweeds for mariculture, recently the scope of these techniques has been extended for use in bioprocess technology for production of high value chemicals of immense importance in the pharmaceutical and nutraceutical sectors. Recently, there has been a phenomenal interest in intensifying seaweed tissue and cell culture research to maximize the add-on value of seaweed resources. This paper deals with the status of seaweed micropropagation techniques and their applications in the context of the marine biotech industry. Further, it also provides an analysis of the problems to be resolved for removing the barriers that are impeding the true realization of potentials offered by these techniques for sustainable development and utilization of seaweed resources.     

Phycological research in the development of the Chinese seaweed industry

The term seaweed industry is employed in a broad sense and includes production both of commercial seaweeds such as Laminaria and Porphyra by phycoculture and of processed seaweed products, such as algin, agar and carrageenan.Before the founding of the People's Republic, China had a very insignificant seaweed industry, producing small quantities of the purple laver Porphyra and the glueweed Gloiopeltis by the primitive rock-cleaning method and the kelps Laminaria and Undaria by the primitive stone-throwing method, both aiming at enhancing the growth of the wild seaweeds. Also, a small quantity of agar was manufactured by the traditional Japanese method of gelling, freezing, thawing and drying the product. The small production was not sufficient to meet the demand of the Chinese people who for ages have appreciated seaweeds and their products for food. Therefore, large quantities of seaweeds and seaweed products had to be imported from various countries, for instance, Eucheuma and Gracilaria from Indonesia and other southeastern Asian countries, Laminaria and agar from Japan, even Porphyra from the USA. Annual Laminaria import from Japan generally amounted to over 10 000 tons and in some years approached 20 000–30 000 tons. Some quantities of the glueweed Gloiopeltis and the vermifuge weed Digenea simplex were exported, mainly to Japan.Since the founding of the People's Republic of China in October, 1949, China has exerted efforts to build up a self-supporting seaweed industry. Now after a lapse of 30-some years, a sizable seaweed industry has been developed. China is now able to produce by phycoculture more than one million tons of fresh seaweeds, including Laminaria, Undaria, Porphyra, Eucheuma, Gracilaria etc. and several thousand tons of seaweed extracts, including algin, agar, carrageenan, mannitol and iodine. At present, China still imports some quantities of seaweeds and seaweed products from various countries but is able to produce sufficient quantities to meet the people's need and even to export some quantities of the seaweeds Laminaria, Undaria and Porphyra and the seaweed products algin and mannitol.At the Tenth International Seaweed Symposium, I presented a paper on the Marine Phycoculture of China, in which I emphasized on the methods of cultivation (Tseng 1981b). Therefore I would like to take this opportunity to supplement the last lecture by presenting a paper on the role of phycological research in the development of China's seaweed industry.     

Is a cooperative approach to seaweed farming effectual? An analysis of the seaweed cluster project (SCP), Malaysia

Seaweed (Kappaphycus spp.) farming has been practised in Malaysia since the late 1970s following government policy incentives (training and farming inputs). However, numerous governance, economic, environmental, technological and sociocultural challenges have limited the industry from achieving its full potential. The Seaweed Cluster Project (SCP) was introduced in 2012 to address some of these challenges. We sought to evaluate the effectiveness of the SCP in delivering its central objectives of increasing seaweed production, optimising the farming area, improving seaweed quality and farming efficiency, raising farmers’ income, and reducing the environmental impact of seaweed farming. Community and industry perceptions of the SCP were obtained from seven communities using a mixed-methods approach based on face-to-face semi-structured interviews, focus group discussions, household surveys, observation and secondary data. Views on the SCP outcomes were generally negative, including low take-up rates by indigenous people, poor stakeholder participation in decision-making, limited acceptance of new technologies, economic vulnerability, a complex marketing system, and low social cohesion of seaweed farming communities. Positive perceptions included recognition that the SCP confers high social status upon a community, reduces operating costs, and facilitates the production of certified seaweed. The SCP’s problems are linked to poor multi-level governance, weak market mechanisms and unintegrated community development. The study concludes with five recommendations to improve the SCP: promote the participation of indigenous people; legalise existing migrant farmers; strengthen local seaweed cooperative organisations; provide entrepreneurship skills to farmers; and fully integrate stakeholders into decision-making.     

Global unbalance in seaweed production,research effort and biotechnology markets

Exploitation of the world's oceans is rapidly growing as evidenced by a booming patent market of marine products including seaweed, a resource that is easily accessible without sophisticated bioprospecting technology and that has a high level of domestication globally. The investment in research effort on seaweed aquaculture has recently been identified to be the main force for the development of a biotechnology market of seaweed-derived products and is a more important driver than the capacity of seaweed production. Here, we examined seaweed patent registrations between 1980 and 2009 to assess the growth rate of seaweed biotechnology, its geographic distribution and the types of applications patented. We compare this growth with scientific investment in seaweed aquaculture and with the market of seaweed production. We found that both the seaweed patenting market and the rate of scientific publications are rapidly growing (11% and 16.8% per year respectively) since 1990. The patent market is highly geographically skewed (95% of all registrations belonging to ten countries and the top two holding 65% of the total) compared to the distribution of scientific output among countries (60% of all scientific publications belonging to ten countries and the top two countries holding a 21%), but more homogeneously distributed than the production market (with a 99.8% belonging to the top ten countries, and a 71% to the top two). Food industry was the dominant application for both the patent registrations (37.7%) and the scientific publications (21%) followed in both cases by agriculture and aquaculture applications. This result is consistent with the seaweed taxa most represented. Kelp, which was the target taxa for 47% of the patent registrations, is a traditional ingredient in Asian food and Gracilaria and Ulva, which were the focus of 15% and 13% of the scientific publications respectively, that are also used in more sophisticated applications such as cosmetics, chemical industry or bioremediation. Our analyses indicate a recent interest of non-seaweed producing countries to play a part in the seaweed patenting market focusing on more sophisticated products, while developing countries still have a limited share in this booming market. We suggest that this trend could be reverted by promoting partnerships for R and D to connect on-going efforts in aquaculture production with the emerging opportunities for new biotech applications of seaweed products.     

Cultivation of red seaweeds: a Latin American perspective

The Latin American seaweed industry plays an important role at a global scale as 17 % of all seaweeds and 37 % of red seaweeds for the phycocolloid industry comes from this region. Increased market demand for algal raw materials has stimulated research and development into new cultivation technologies, particularly in those countries with economically important seaweed industries such as Argentina, Brazil, Chile, México, and Peru. The marine area of Latin America includes almost 59,591 km² of coastline ranging in latitude from 30ºN to 55ºS and encompasses four different oceanic domains: Temperate Northern Pacific, Tropical Eastern Pacific, Temperate South America, and Tropical Atlantic. Commercial cultivation of red seaweed in Latin America has been basically centered in the production of Gracilaria chilensis in Chile. Attempts have been made to establish seaweed commercial cultivation in other countries, going from experimental research-oriented studies to pilot community/enterprise based cultivation trials. Some genera such as Kappaphycus and Eucheuma have been studied in Brazil and Mexico, Gracilaria species in Argentina and Brazil, Gracilariopsis in Peru and Venezuela, and Chondracanthus chamissoi in Peru and Chile. In this short review, we address the Latin America perspective on the status and future progress for the cultivation of red seaweeds and their sustainable commercial development, and discuss on the main common problems. Particular emphasis is given to the needs for comprehensive knowledge necessary for the management and cultivation of some of the most valuable red seaweed resources in Latin America.     

A decade of change in the seaweed hydrocolloids industry

Seaweed hydrocolloid markets continue to grow, but instead of the 3?C5% achieved in the 1980s and 1990s, the growth rate has fallen to 1?C3% per year. This growth has been largely driven by emerging markets in China, Eastern Europe, Brazil, etc. Sales of agar, alginates and carrageenans in the US and Europe are holding up reasonably well in spite of the recession. However, price increases to offset costs in 2008 and 2009 have begun to have a dampening effect on sales, especially in markets where substitution or extension with less expensive ingredients is possible. These higher prices have been driven by higher energy, chemicals and seaweed costs. The higher seaweed costs reflect seaweed shortages, particularly for carrageenan-bearing seaweeds. The Philippines and Indonesia are the dominant producers of the farmed Kappaphycus and Eucheuma species upon which the carrageenan industry depends and both countries are experiencing factors limiting seaweed production. Similar tightening of seaweed supplies are beginning to show up in brown seaweeds used for extracting alginates, and in the red seaweeds for extracting agar. The structure of the industry is also undergoing change. Producers in China are getting stronger, and while they have not yet developed the marketing skills to compete effectively in the developed world markets, they have captured much of their home market. China does not produce the red and brown seaweeds needed for higher end food hydrocolloid production. Stocking their factories with raw material has led to the supply problems. Sales growth continues to suffer from few new product development successes in recent years; although some health care applications are showing some promise, i.e., carrageenan gel capsules and alginate micro-beads.     

Historical context of commercial exploitation of seaweeds in Brazil

Harvested by coastal populations for centuries, seaweeds have played an important role in the economy of a number of countries. In Brazil, they occur along the coastline, but are more diversified and abundant from the northeast to a portion of the southeast coast. Historically, the seaweed industry in Brazil is based on seaweed harvesting of natural beds. This practice continues to this day in a number of coastal communities in Northeastern Brazil. Since the 1960s, species of the genera Gracilaria and Hypnea have been collected in the intertidal zone for extraction of agar and carrageenan. Maximum production was achieved in 1973–1974, a period in which the country exported around 2000 t annually (dry weight) to Japan. Later (1977–1979), there was a sharp drop and annual exports fell to 250 t (dry weight). In 1981, Brazil exported only 150 t of dried seaweed for agar extraction. Between 1990 and 2000, overexploitation, decline in a number of agarophyte populations, poor quality, low price, and lack of a socioeconomic policy led to the almost total disappearance of this industry in Northeastern Brazil. Seaweed harvesting on natural beds is currently in decline, and the population that depended on this resource had to migrate or convert to other economic activities, such as fishing, aquaculture, and underwater tourism. However, the promising results obtained in pilot projects (Gracilaria and Kappaphycus) show that Brazil has significant potential as a seaweed biomass producer.     

Saldanha Bay,South Africa: recovery of Gracilaria verrucosa (Gracilariales,Rhodophyta)

Since World War II the greater Saldanha Bay lagoon system, South Africa, has been an important Gracilaria producer. Two agar factories, built in the 1960's, used Gracilaria from Saldanha Bay as their raw material. In the early 1970's the industry was destroyed as a result of dredging and marine construction operations to establish a harbor in the bay for loading ore. These environmental changes destroyed stocks and prevented the previously significant beachings of the seaweed from occurring. After a few years of no or very low commercial production, the resource slowly started to recover. The size of Gracilaria drifts increased over the following eight years to approximately one-third of the original output. This trend seems to continue. Although the stocks and resultant drifts are unlikely to recover fully to their original quantity, current production is already sufficient to ensure re-establishment of a seaweed industry in Saldanha Bay. This could have considerable socio-economic impact on the area.     

European bioconversion projects and realizations for macroalgal biomass : Saint-Cast-Le-Guildo (France) experiment

Proliferation of macroalgae is a world-wide problem with 50,000 m³ of drift Ulva harvested per year in Brittany and about 1.0 to 1.2 million tons growing in the Venice lagoon. This biomass may be treated by bioconversion (aerobic or anaerobic fermentation) to give useful products (gas, fertilizers or others) and to remove a source of environmental pollution. Such a treatment also may be applied to cultivated or harvested seaweds and to seaweed industry residues.Studies of seaweed methanization showed Laminaria an especially good substrate and Ulva a possible substrate. Research led to a defined way of treating drift algae, encompassing natural hydrolysis and pressing with methanization of the juices.The most advanced full-scale realization for algal biomass utilization is the C.A.T.-Quatre-Vaulx composting plant in Saint-Cast-Le-Guildo (Brittany, France). It produced from seaweed, wood and animal dung a biological quality compost that is competitive with the traditional market products.     

A Global Analysis of the Relationship between Farmed Seaweed Production and Herbivorous Fish Catch

Globally, farmed seaweed production is expanding rapidly in shallow marine habitats. While seaweed farming provides vital income to millions of artisanal farmers, it can negatively impact shallow coral reef and seagrass habitats. However, seaweed farming may also potentially provide food subsidies for herbivorous reef fish such as the Siganidae, a valuable target family, resulting in increased catch. Comparisons of reef fish landings across the central Philippines revealed that the catch of siganids was positively correlated to farmed seaweed production whilst negatively correlated to total reef fish catch over the same period of time. We tested the generality of this pattern by analysing seaweed production, siganid catch, and reef fish catch for six major seaweed-producing countries in the tropics. We hypothesized that increased seaweed production would correspond with increased catch of siganids but not other reef fish species. Analysis of the global data showed a positive correlation between farmed seaweeds and siganids in Southeast Asia (Indonesia, Malaysia, and the Philippines) but not Africa (Tanzania and Zanzibar), or the Western Pacific (Fiji). In Southeast Asia, siganid catch increased disproportionately faster with seaweed production than did reef fish catch. Low continuity, sporadic production and smaller volumes of seaweed farming may explain the differences.     

Unusual distribution of floating seaweeds in the East China Sea in the early spring of 2012

Floating seaweeds play important ecological roles in offshore waters. Recently, large amounts of rafting seaweed have been observed in the East China Sea. In early spring, juveniles of commercially important fish such as yellowtail accompany these seaweed rafts. Because the spatial distributions of seaweed rafts in the spring are poorly understood, research cruises were undertaken to investigate them in 2010, 2011, and 2012. Floating seaweed samples collected from the East China Sea during the three surveys contained only Sargassum horneri. In 2010 and 2011, seaweed rafts were distributed only in the continental shelf and the Kuroshio Front because they had become trapped in the convergence zone of the Kuroshio Front. However, in 2012, seaweed was also distributed in the Kuroshio Current and its outer waters, and massive strandings of seaweed rafts were observed on the northern coast of Taiwan and on Tarama Island in the Ryukyu Archipelago. Environmental data (wind, currents, and sea surface height) were compared among the surveys of 2010, 2011, and 2012. Two factors are speculated to have caused the unusual distribution in 2012. First, a continuous strong north wind produced an Ekman drift current that transported seaweed southwestward to the continental shelf and eventually stranded seaweed rafts on the coast of Taiwan. Second, an anticyclonic eddy covering northeast Taiwan and the Kuroshio Current west of Taiwan generated a geostrophic current that crossed the Kuroshio Current and transported the rafts to the Kuroshio Current and its outer waters. Such unusual seaweed distributions may influence the distribution of fauna accompanying the rafts.     

Production of compost from marine waste: evaluation of the product for use in ecological agriculture

The sea contains large amounts of resources that are sometimes considered as waste. Such material includes the waste generated by the fish-processing industry and seaweed that is washed up on shores. In this study, these waste products were windrow composted, along with pine bark as a source of carbon and aeration. The final mix proportions were 20 % seaweed, 20 % fish waste, and 60 % pine bark (v/v). After 10 weeks, stable, well-structured, hygienic compost, which was rich in organic matter and nutrients and had a low metal content, was obtained. Tests for maturity, hygiene, and phytotoxicity, along with a detailed physical and chemical characterization, showed that this compost can be used as an organic amendment and/or growth substrate for use in ecological agriculture. The only limiting feature was the high salinity, which could easily be lowered prior to composting the material.     

Cultivation and utilisation of red seaweeds in the Western Indian Ocean (WIO) Region

Seaweed farming in the Western Indian Ocean (WIO) Region is carried out in a number of countries, most of them farming Eucheuma denticulatum, Kappaphycus alvarezii and Kappaphycus striatum. These species are farmed mostly in Tanzania with limited production in Madagascar, Mozambique and Kenya; current production (2012) stands at 15,966 t (dry weight) year^?1 of Eucheuma and Kappaphycus, valued at US$ 4.2 million with 95 % of this tonnage coming from Tanzania. Other countries in the region have limited or no seaweed production owing to problems of epiphytes, ice ice and markets. The problem of epiphytes coupled with ice ice that WIO countries are facing causes die-off of Kappaphycus which is the preferred species in foreign markets for its thicker gel, kappa carrageenan (vs. the weaker iota carrageenan from Eucheuma). New efforts are put to curb these problems including moving seaweed farms to deeper waters and cultivation trials of other carrageenophytes as well as agar-producing species, agarophytes. Research work has been initiated to evaluate Gracilaria and Hypnea farming and processing in Tanzania, the Republic of Mauritius and Mayotte. Gracilaria farming is at experimental stages as a biofilter of fishpond effluents and as potential species for the production of agar with growth rates of 1.5–1.9 % day^?1. Hypnea farming is only being initiated in Mauritius and Mayotte at present. Other innovations including value addition by making various seaweed products and encouraging the consumption of seaweed as food at least in Tanzania and Mauritius are increasing further the importance of the seaweed farming and processing industry in the WIO Region.     

Asymmetrical costs of sexual conflict in the seaweed fly, Coelopa frigida

Abstract.  1. Sexual conflict can play an important role in the evolution of animal life-history characteristics, including lifespan. Seaweed flies show an increase in mortality rates when exposed to brown algae. The seaweed stimulates females to oviposit and males to mount females. Females typically respond to male mounts by performing a violent rejection response.
2. Here the contribution of sexual conflict to the increase in mortality seen in the presence of seaweed was determined. The survival of single and mixed sex pairs of flies was followed in the presence and absence of seaweed.
3. The two sexes showed differential survival rates, with females living longer in the absence of seaweed. The presence of seaweed reduced survival in both sexes. In the presence of seaweed, female survival was lower when paired with a male. Over 40% of the reduction in survival in females in the presence of seaweed appears to be attributable to sexual conflict.
4. The presence of a female did not significantly affect male survival. Thus the mortality cost of being in the presence of the opposite sex and seaweed appears highly asymmetric.
5. In the presence of seaweed, female survival was lower when females were paired with small males. Small males exhibit higher levels of harassment of females, thus it is argued that pre-copulatory sexual conflict is the probable cause of the increased mortality cost to females of being in the presence of both males and seaweed.     

183 The Environmental Impacts of Harvesting Beach‐Cast Seaweeds

Until recently the commercial collection of beach‐cast seaweeds in New Zealand was prohibited but the legislation has recently been amended to allow permitting of this activity. This review collates existing information on the role of beach‐cast seaweed in coastal ecosystems to describe the nature and extent of the effects that commercial removals of beach cast seaweed may have on the marine environment. It outlines the amount of beach‐cast seaweed available for harvest in New Zealand and the fate of seaweed when not collected; reviewing current information on the importance of beach‐cast seaweeds and its inhabitants on: feeding and nesting shorebirds, and nutritional contribution of seaweed inhabitants to nearshore coastal ecosystems when seaweed is washed back into the sea It also identifies key research gaps related to any environmental impacts that the removal of beach cast seaweed might have.     

The effect of chronic seaweed subsidies on herbivory: plant-mediated fertilization pathway overshadows lizard-mediated predator pathways

Flows of energy and materials link ecosystems worldwide and have important consequences for the structure of ecological communities. While these resource subsidies typically enter recipient food webs through multiple channels, most previous studies focussed on a single pathway of resource input. We used path analysis to evaluate multiple pathways connecting chronic marine resource inputs (in the form of seaweed deposits) and herbivory in a shoreline terrestrial ecosystem. We found statistical support for a fertilization effect (seaweed increased foliar nitrogen content, leading to greater herbivory) and a lizard numerical response effect (seaweed increased lizard densities, leading to reduced herbivory), but not for a lizard diet-shift effect (seaweed increased the proportion of marine-derived prey in lizard diets, but lizard diet was not strongly associated with herbivory). Greater seaweed abundance was associated with greater herbivory, and the fertilization effect was larger than the combined lizard effects. Thus, the bottom-up, plant-mediated effect of fertilization on herbivory overshadowed the top-down effects of lizard predators. These results, from unmanipulated shoreline plots with persistent differences in chronic seaweed deposition, differ from those of a previous experimental study of the short-term effects of a pulse of seaweed deposition: while the increase in herbivory in response to chronic seaweed deposition was due to the fertilization effect, the short-term increase in herbivory in response to a pulse of seaweed deposition was due to the lizard diet-shift effect. This contrast highlights the importance of the temporal pattern of resource inputs in determining the mechanism of community response to resource subsidies.