The global trade in various seaweeds is being significantly hampered by disease and pest outbreaks. Further, there are no dedicated biosecurity frameworks which specifically consider the potential for trans-boundary movement of seaweed diseases and pests during the trading of seaweeds and their products. This analysis has revealed the similarities, gaps and deficiencies of international and regional biosecurity frameworks related to the top carrageenan-producing countries. Four main challenges to the current biosecurity system have been identified for the carrageenophyte industry: inconsistent terminology for the inclusion of cultivated seaweeds, limited guidance for designating responsibility for the implementation of framework measures, insufficient evidence to develop disease- and pest-specific policies, and limited alignment of biosecurity risks between policies.
Inconsistent terminology for the inclusion of cultivated seaweeds
Of all the identified international biosecurity frameworks, only the International Plant Protection Convention (IPPC) makes reference to ‘aquatic plants’, defining them as ‘Any plant that grows partly or wholly in water, and can be rooted in sediment or free floating on the water surface’ indicating that seaweeds are included under this term (IPPC 2012). Prior to 2012, it was unclear whether seaweeds would fall under the trading sanitary standards of the World Organization for Animal Health (OIE), as the aquatic animal health standard holders, or the IPPC, the plant standard holders. The allocation of seaweeds (macroalgae) to either the plant or animal group is problematic given that algae can be allocated to different kingdoms: Plantae (red and green algae) and Chromista (brown algae), and this is reflected in the commercial naming of seaweed crops (Bolton 2019). As the phylogeny of algae continues to be shaped by advances in molecular biology (Pereira and Neto 2014), the allocation of ‘seaweeds’ to legislation by different standard setting bodies is also uncertain. The carrageenophytes are currently allocated to the kingdom Plantae (Moreira et al. 2000), but genetic interpretation is ongoing. The IPPC scoping study, however (IPPC 2017a), recommended that cultivated ‘aquatic plants’ should be included in their sanitary standards to ‘ensure that aquatic plants, as potential pests and pathways, become subject to, or included in, pest risk analysis whenever relevant, in particular in cases where aquatic plants are intentionally imported for intended uses as plants for planting, e.g. in aquaculture or other aquatic habitats.’ (IPPC 2017a). Current regulation of international biosecurity through the SPS agreement though is clearly divided between two systems related to plants (IPPC) or animals (OIE). The definition of ‘aquatic plants’ implies that the regulation of seaweeds is now under the International Sanitary and Phytosanitary Measures (ISPMs) of the IPPC, but definitive inclusion of all red, brown and green seaweeds (macroalgae) remains unclear. In addition, the risks and uses of important seaweed species are described in the most recent IPPC report on aquatic plants. This report includes species of economic importance, and although it includes 16 seaweed species, no carrageenophyte species are listed, despite equating to 45% of the global production of seaweed. We recommend here that the IPPC makes explicit reference to seaweeds, of specific taxonomy, in future iterations of their regulations. The inclusion of red, green and brown seaweeds into the terminology of IPPC regulations initiates the means by which the most highly traded taxa (e.g. Eucheuma sp. and Kappaphycus spp.) are included in biosecurity legislation focussed on trade of the most common commodities.
Another option to improve the inclusion and consistency of the terminology of seaweeds in policies would be through a concerted effort at international and regional scales to harmonise the current language of seaweed cultivation (e.g. ‘aquatic plants’ vs. ‘algae’ vs. ‘seaweeds’ vs. ‘macroalgae’), a problem which is also observed in the use of terminology for general biosecurity in the aquatic environment (Dahlstrom et al. 2011), invasive species in aquaculture (Hill 2008) and even in specific biosecurity measures of the shrimp industry (Alday-sanz et al. 2018). Another option is for the governing organisations of international biosecurity policies to either update or create new texts which include seaweed specific terminology and to set the standard for its inclusion in future regional and national frameworks. The misalignment of biosecurity language is also reflected in the separation between definitions in the animal and plant standards of OIE and IPPC, where the OIE defines ‘disease’ as all pests or pathogens, and the IPPC defines all ‘pests’ as any pathogenic agent. The ongoing issue of inter-changeable language within the subject of biosecurity (Dahlstrom et al. 2011) will be a challenge to the integration of both seaweed cultivation and biosecurity in international policy.
Limited guidance for designating responsibility for the implementation of framework measures
Without recognition by international organisations who influence the management of the aquaculture industry, the lack of designation of seaweeds to biosecurity frameworks remains unnoticed. Almost all frameworks included seaweed cultivation under the umbrella of general aquaculture, which is of course, a diverse industry. However, frameworks are often tailored to aquatic animal health biosecurity measures which are already internationally regulated through the OIE’s long-standing focus on aquatic animal production sectors (fish, molluscs, crustaceans, amphibians) (OIE 2017). The low level of recognition of the seaweed industry in international aquaculture policy is reflected in the level of global reporting by FAO. The latest ‘State of the World’s Fisheries and Aquaculture’ ‘SOFIA’ report (FAO 2018) provided a summary of the tonnage of aquaculture and capture fisheries production from 1950 to 2015, and yet the tonnage representing global aquaculture excluded any seaweeds or aquatic plants, even though the sector is second only to fin-fish in terms of volume. Although political interest in aquaculture is largely economically driven, as opposed to volumes, more should be done to acknowledge that poor biosecurity in the seaweed industry can impact the trading ability of a country. If the international policy profile of the seaweed industry remains low, then assigning responsibility of the sanitary and phytosanitary to the IPPC, their regional organisations, down to the national authority who should be implementing the measures could continue to appear as a low priority.
Only half of the frameworks identified were binding, mostly through ratification of the text by a member nation, and there was no framework which included any penalties in their approach to implementation. Most of the responsibility for implementation is passed down to national authorities. However, given the lack of clarity on the inclusion of seaweeds in almost all of the frameworks, it is unclear which national authority is responsible for the implementation of the biosecurity measures. As with other sectors in aquaculture, implementation of biosecurity measures is regulated by the national competent authorities which are often those government departments with responsibility for fisheries and/or aquaculture (e.g. Bureau of Fisheries and Aquaculture Resources—BFAR in the Philippines (Jonalyn P. Mateo (pers. comm.) 26/11/2019) and Ministry of Marine Affairs and Fisheries—MMAF in Indonesia (Cicilia S. B. Kambey (pers. comm.) 26/11/2019). Such departments typically regulate the international movement of live aquatic animals using the import risk analysis (IRA) tool of the OIE. Given the widespread occurrence of pests and diseases observed internationally in seaweed aquaculture (Watkiss et al. 2012; Hurtado et al. 2017; Quiaoit et al. 2018), and that seaweed crops have been transplanted internationally to establish new cultivation sites (Loureiro et al. 2015; Hurtado et al. 2017) under the IPPC framework, Pest Risk Assessments (PRA) for the carrageenophyte industry should be initiated by the National Plant Protection Organisation (NPPO) in each producing country (IPPC 2017b), but to date have not been reported (IPPC 2019). Cultivation of seaweeds in most countries is regulated by aquaculture or fishery authorities, and the NPPO is often concerned solely with terrestrial agriculture. A conflict therefore arises, over which authority has the capacity to regulate and has the responsibility to implement the IPPC PRA measures under the framework. The challenge for many seaweed producing countries will be to connect these departments, to allow for active communication and sharing of expertise. Similarly, it will become increasingly important for those nations wishing to trade seaweed products with one another that such equivalent measures are taken. Even after strengthening these lines of communication, a national competent authority can implement SPS measures for ‘plants for planting’ using various approaches (Eschen et al. 2015), and could be designed to be suitable for application in the aquatic environment.
Regional guidelines of the ASEAN region, where selected seaweeds are significantly important commodities, only make reference to the international guidelines of OIE for specific biosecurity measures (ASEAN 2015a, b), predominantly focussing on aquatic animal health or terrestrial crops (i.e. rice and maize). As a result, the recommendations do not align with cultivated seaweeds as ‘plants’ cultivated in an open aquatic environment, and this industry is therefore excluded from national and (as a consequence of a lacking point of reference) international frameworks. The ASEAN Asian Integrated Food Security (AIFS) framework is focused on regional food security, which is exclusive to subsistence crops: rice, maize, soybean, sugar and cassava; therefore, recognition of the seaweed industry and its value to the region is limited. Although ASEAN has published a strategic action plan for cooperation on fisheries (which includes ‘aquaculture’ products), it is unclear whether varieties of seaweeds will be included, if at all, given that any mention of biosecurity is directed to aquatic animal health under the OIE guidelines (ASEAN 2016).
The majority of international and regional scale biosecurity frameworks (79%) for invasive species in the marine environment have been identified as legally binding by Dahlstrom et al. (2011). A lower proportion of frameworks (42%) were found to be legally binding by ratification in this study. Top carrageenophyte-producing countries (which are also low-income or lower-middle income countries as listed by the Development Assistance Committee) can be limited by capacity, resources and economic incentives, therefore, finding it challenging to implement and enforce national policies. For other industries, successful implementation of national policies has required both alignment of policies with the specific biosecurity challenges of the industry and the economic incentive to invest resources in regulation (Chaminade and Padilla Pérez 2014). Science and technology policies in developing countries often imitate objectives or strategies of international frameworks, rather than addressing the specific national challenges (Chaminade and Padilla Pérez 2014). As there is only one international policy which includes seaweed cultivation under the term ‘aquatic plants’, this will then limit the ability for biosecurity measures to be implemented through national legislation. In addition, as incorporation of international frameworks into national legislation is often a complex and expensive process, requiring a certain level of national capacity (Dahlstrom et al. 2011), many seaweed-producing nations will need financial and expert assistance in developing appropriate policies. One seaweed specific framework, although not international policy is a certification initiative by the Aquaculture Stewardship and Marine Stewardship Council, includes elements of biosecurity management. However, certification schemes are often industry focussed, and there remains uncertainty over whether there is any great demand for certified seaweed products by the industry, which is generally considered more sustainable than other sectors of the aquaculture (Porse and Rudolph 2017).
Without an international framework, which specifically includes seaweed cultivation, then the uptake of biosecurity through the trading principle of ‘equivalence’, whereby the receiving nation of a particular seaweed crop for planting will not want to risk trading with a nation which could risk their own national biosecurity, means that, at present, biosecurity is not financially advantageous. This is reflected by the high inclusion rate of economic risks in biosecurity frameworks, as compared with the far fewer references made to ecosystem impacts. Of the top producing countries, carrageenophytes are the third largest exported commodity from Tanzania, behind coffee and cloves (Watkiss et al. 2012), and the largest aquaculture product in the Philippines by volume (Jonalyn P. Mateo (pers. comm.) 26/11/2019). However, when set in the international context, seaweeds comprise one of the lowest unit value sectors of global aquaculture (FAO 2018). Although immediate economic incentives on the global scale, compared with other industries, may be causing poor engagement in the development of policies with the seaweed industry, nations abiding by animal health regulations (e.g. those of the OIE) control for disease in traded animals to protect the wild stocks of those countries from potential incoming pests. In this context, the lack of biosecurity in low-value species being internationally traded to nations, which otherwise control aquatic animal diseases, may pose significant threat to native taxa. Yet, this concept does not appear to be applied to the carrageenophyte industry. Biosecurity approaches in the frameworks also tended to focus on improving response and recovery after the spread of pests, diseases and non-natives, and improving the economic recovery of the whole sector; therefore, management measures are typically directed at traders and buyers and not the farmers, who are losing their household income (Hayashi et al. 2010; Watkiss et al. 2012).
Insufficient evidence to develop specific policies for disease and pests
Only one-third of frameworks used scientific evidence to form the basis of their measures or guidance, which reflects the paucity of literature regarding biosecurity risks in the seaweed industry (Cottier-Cook et al. 2016). Most information for policy development (i.e. reporting disease outbreaks, documenting diseased crops or documenting losses due to diseases or pests) are gathered from stakeholder participation. However, there is a distinct lack of information available on which to assess the main biosecurity risks within the industry. As the information used to design biosecurity management measures in many cases is not specifically based on evidence from the seaweed industry, detection, monitoring and prevention measures are limited in their effectiveness. To develop an effective biosecurity approach on the international scale, there is a requirement for a certain amount and type of knowledge (Bondad-Reantaso et al. 2005). For aquatic animals, this knowledge base is centred on a list of pathogens that are known to cause significant diseases in farmed stocks, have the potential to be transferred by trade in animals and products and do not exist in at least some parts of the range of those traded hosts. The OIE Aquatic Manual and Code series, updated each year, include chapters on specific pathogens, the list of susceptible host species to those agents and ways in which they can be accurately diagnosed, reported and potentially controlled (OIE 2017). Using basic categories, this information would indicate what is the affected crop (better definitions of cultivated species or strains), what the exact disease or pests of this crop are, and where the crop is being grown or traded. In many cases the genetic identity of carrageenophyte crops remains unknown and diseases are yet to be categorised. Even when diseases are known and provided with a broad identity (e.g. ‘ice-ice’ disease), the actual causative agent often remains unknown. In addition, the spatial distribution of cultivated species may also remain unknown. One example of this is exemplified in a national survey of the seaweed industry in the Philippines, which revealed that there were multiple, inter-changeable local names for three species of carrageenophytes being grown across the same regions (Quiaoit et al. 2018). This is also reflected on an international scale in the FAO: ‘State of the World’s Fisheries and Aquaculture’ (SOFIA) report (FAO 2018), where production data in unspecified categories such as ‘Seaweeds nei’ and ‘Algae’ equated to approximately 1 million tonnes in 2016.
Limited alignment of biosecurity risks between policies
Through the analysis of themes in the frameworks, a range of different biosecurity approaches was identified and was interpreted differently, depending on the overall goals of the organisation implementing the framework. For example, the OIE tends to focus on the listing of specific diseases with associated management measures, whereas the IPPC mostly focuses on plants’ pests through the Pest Risk Analysis tool but has no counterpart disease risk analysis tool. This was further reflected in the analysis of included biosecurity risks, where in the case of the CBD protocols, diseases and pests were not specifically included, but the focus was on maintaining biodiversity and reducing the impacts of non-native species through cultivation of native species. Another example was the different meanings of recovery in the case of the response recovery and planning approach. In the IPPC this is aimed at recovery from the physical impact of pests on the environment or crop loss, and for APEC, this was economic recovery after crop loss. This makes vertical integration of approaches difficult to interpret, as all organisations may agree to response and recovery planning in their biosecurity framework but may interpret and implement this differently. Alternatively, an organisation may have more than one framework for biosecurity management, where approaches do not align. For example, the AU-IBAR 10-year aquaculture plan includes pest/pathogen impacts, but the policy reform strategy for fisheries and aquaculture does not specify this impact. Therefore, even in the case where organisations have the specific goal of reducing the impact of pests or pathogens in policy frameworks, the implementation strategy may not be aligned with this goal.
Future policy recommendations
Since identifying the major challenges to biosecurity policy in the carrageenophyte industry, short-term recommendations are given to help improve the use of current biosecurity frameworks, and longer-term recommendations for key organisations are provided in order to improve the integration of cultivated seaweeds into the international policy landscape (Fig. 5).