Aquaculture is one of the fastest growing food producing sectors in the world and is an increasingly important contributor to global food supply and economic growth. Its development is sustained by the correct biological management of the cultured species, the introduction of technological innovations in the production process, the development of new feeds and feeding systems, and the correct prevention and control of diseases (1).

Aquaculture production (fish and shellfish) in the European Union reached 1.2 million tonnes (t) in 2018 and accounted for €3.9 billion in 2020, which represented 1% of world aquaculture production by volume. The EU production is led by Spain (24%), followed by France (21%), Greece (11%), and Italy (10%) (2).

Spanish fish farming has a diversified and internationalized aquaculture sector (Table 1), both in species and production systems, with a total of 73,370 t produced in 2022 (59,123 t of marine fish, 14,122 t of freshwater fish, and 125 t of fish for restocking) (3, 6).

As in other European countries, diseases have impacted the Spanish fish farming sector, affecting the performance and competitiveness of its industry (7, 8). Diseases may cause both a direct impact on the economic performance of a company through increasing losses (mortality, treatments, etc.) and reducing incomes, as well as having an indirect impact by affecting international trade, investments and consumer confidence (9, 10). Thus, national and international aquatic animal health programs are essential to assure the sustainable development of aquaculture, as well as to protect both the industry and the aquatic environment biodiversity of the from the negative impacts of exotic, endemic and emerging disease epizootics (11). However, all too often, a long time elapses from the first observation of an abnormal mortality in the field, to the identification and reporting of the causative agent and, even longer, to the application of appropriate control and risk management measures (12). Therefore, health management, disease surveillance and biosecurity must be part of a strategic and integrated approach that encompasses the policy and regulatory framework for analysing and managing risks to the life and health of people, animals and plants, as well as the associated risks to the environment (11).

Originally, in Europe the Council Directive 91/67/EEC of 28 January 1991 set controls mainly for salmonid (salmon, trout) and bivalve farming. Subsequently, several additional fish species, including some marine species, were listed in the Council Directive 2006/88/EC which enforced the obligation of notifying increases in mortality in aquaculture animals for further investigations. Moreover, EU Member States had to ensure that a risk-based animal health surveillance scheme was applied to all farms and mollusc farming areas, as appropriate for their type of production. Consequently, in Spain, Royal Decree 1614/2008 [implementing Directive 2006/88/CEE; (13)] provided definitions for “emerging disease” and “increase in mortality”. However, these terms can lead to different interpretations by producers and competent authorities, which in Spain are organized by subnational administrations called Autonomous Communities (AC). Nonetheless, Spain was a pioneer in structuring a surveillance system for aquaculture, both for fish farming and bivalve production, based on the risk assessment of the farms and production zones in order to prevent, not only, the occurrence, but also, the spread of the more relevant non-listed aquatic animal diseases. Moreover, the correct diagnostic methodology for use by all Spanish AC was also recommended in a guide (14). Subsequently, Directive 2006/88/CEE has been repealed by Regulation (EU) 2018/1882, which finally considers emergent diseases notifiable, when they fulfil the criteria established in Animal Health Law: AHL Regulation (EU) 2016/429 on transmissible animal diseases. The AHL aims to prevent and control all transmittable diseases in the Union. This transversal AHL enforces health surveillance and risk assessment on the operators to detect the early presence of both notifiable and emergent diseases on a fish farm. It also highlights the importance of implementing biosecurity measures to prevent the introduction of pathogens into farms.

Since disease surveillance focuses mainly on listed (notifiable) diseases both in the European Regulation EU 2020/689 (Annex VI) and at the international level, through the WOAH Aquatic Animal Health Code, the surveillance of those diseases is well-defined. However, countries also have the obligation to report emerging diseases (i.e., a new occurrence of a disease causing a significant impact); for which the indicators for defining such cases are not as well defined. Likewise, the definition of “increased mortality” leaves room for different interpretation by stakeholders, since the European legislation defines this term as “unexplained mortalities significantly above the level of what is considered to be normal for the fish farm or mollusc farming area in question under the prevailing conditions.” Therefore, what is considered as increased mortality should be objectively defined and accepted by the stakeholders responsible for production and health.

Surveillance programs aim to prevent diseases from spreading before they can affect the aquaculture industry. They can also be implemented to contain or eradicate important endemic diseases in the long term. An early detection system is an efficient system for ensuring the rapid recognition of signs that point to a suspected listed disease, or an emerging disease situation, or unexplained mortality in aquatic animals (15).

As aquaculture evolves, growing in volume, economic weight and technological development, it integrates epidemiological methodologies previously applied in terrestrial livestock/animal production systems. This is the case of the tools used for the evaluation of health surveillance systems. For example, the WOAH Tool for the Evaluation of Performance of Veterinary Services (WOAH PVS Tool), designed in 2007 and applied to livestock (16), was adapted in 2013 for aquaculture (WOAH PVS Tool: Aquatic animals) (17). Likewise, SET was designed to provide countries with a comprehensive, oriented and standardized method in order to evaluate animal disease surveillance systems, including zoonoses (18). The basis for SET was the OASIS toolkit (19), to which components of FAO’s Epidemiology and Laboratory Mapping Tools (20) were also added. More recently, a new methodology for the surveillance of diseases of aquatic organisms in developing countries has been proposed by Bondad-Reantaso et al. (9).

Several tools have been developed to help responsible health authorities and experts to evaluate and improve their surveillance programs. This is the case of the Tool for the Evaluation of Performance of Veterinary Services (WOAH PVS Tool), designed by the WOAH (previously OIE) in 2007 for livestock, which was adapted subsequently in 2013 for aquaculture (WOAH PVS Tool: Aquatic). Following a request from member countries in Africa, the FAO’s Animal Production and Health Division (NSAH) developed a surveillance evaluation tool (SET) to provide countries with a comprehensive and standardized way to evaluate animal disease surveillance systems, including zoonoses (18). The basis for the SET was the OASIS toolkit (Outil d’Analyse des Systèmes de Surveillance) from the French agency ANSES [Agence Nationale de Sécurité Sanitaire de l’Alimentation, de l’Environnement et du Travail; (19)] to which components of FAO’s Epidemiology and Laboratory Mapping Tools were added.

SET was developed by FAO in 2017 following a request from projects in African countries for an assessment tool dedicated to animal health surveillance, which could support veterinary services in developing their national surveillance systems. To date, although SET has been used in more than 25 countries in Africa and Asia for a comprehensive assessment of animal health surveillance systems. Although SET tool has not yet been applied in aquaculture, the basic concepts of animal disease surveillance are transferable to aquaculture.

SET originally consisted of a scoring grid that assessed surveillance systems against 90 indicators grouped into 19 categories and 7 major areas (Table 2). Following a thorough document review and interviews with stakeholders at all levels of a specific sector, SET scores are attributed to each indicator in order to provide information concerning the strengths and weaknesses of surveillance in any particular country. These results are then used to develop recommendations and/or a plan to implement specific, measurable and timely actions in order to track diseases better. Governments and development partners have used SET evaluations as a basis for implementing targeted improvement for animal disease surveillance systems at a national level.

Although there are recent studies concerning the health management and biosecurity procedures in marine fish farming in Spain (21), to our knowledge, there are no public studies concerning the performance of aquaculture surveillances system itself. The FAO SET was selected to conduct an assessment on the disease surveillance system of the Spanish fish farming sector. For that purpose, a parallel evaluation of the surveillance systems for the main fish productions of trout (freshwater), and seabream and seabass (marine fish), was conducted.

This current work was implemented as a case study in order to assess the disease surveillance system for fish farming in Spain, using the FAO SET tool (18). SET is an easy, user-friendly tool, based on Excel, where most of the effort focuses on expert opinion discussions in order to score specific indicators. It requires a preliminary in depth understanding of the surveillance framework under analysis at the different levels (e.g., national, subnational, field, laboratory, communication, evaluation), which is achieved through literature and reports compilation and interviews with relevant stakeholders.

SET consists of a Microsoft Excel tool containing 90 indicators (Annex 2) covering all aspects of surveillance, which are grouped into 19 categories and 7 areas (Table 2). Following a thorough document review, as well as interviews with all relevant surveillance stakeholders, evaluators scored each SET indicator based on the realities of the surveillance system assessed. The tool then generated graphical outputs automatically, which allowed for the development of a system-specific action plan for improvement of surveillance. It is worth noting that following the use of SET in this paper, the tool has been updated by increasing the number of indicators to 96, though the tool’s categories and areas remain unchanged.

The SET evaluation consisted of six main phases:

SET was shown to be easily applicable in the evaluation of surveillance in fish farming in this Spanish case study. Out of the 90 indicators in the tool, only that related to “Vector-Borne Diseases” was found not to be appropriate, and it was exchanged for a new indicator concerning “Reservoirs.”

SET is normally used to make a first evaluation with the purpose of proposing an action plan with recommendations and targeted measures to improve corresponding surveillance system. Thereafter, following this first evaluation, it is proposed to conduct follow-up evaluations every 3–5 years in order to assess the progress and improvements of the system studied. In this case, SET was used to compare the surveillance systems of trout versus marine fish (seabass and seabass), thus, providing a novel way to support the structured analysis concerning the benefits and disadvantages of surveillance programs designed for listed diseases (trout farming) versus those based only on the surveillance of abnormal mortalities and emerging diseases. Table 1 shows finfish production in Spain, the correlation between species produced and the listed (notifiable) diseases, according to the European legislation and the WOAH Aquatic Code. Thus, when analysing the correlation of species with a list of notifiable diseases, it was apparent that most of the surveillance efforts only focused on one species (trout), which accounts for less than one sixth of the total finfish production in Spain. In contrast, for seabream and seabass, for which there are no listed diseases, surveillance efforts should be in place in order to focus on the identification of abnormal mortalities and emerging diseases.

SET provided the highest scores for trout surveillance in Laboratory Technical and Laboratory Analytical aspects. This is because the Spanish reference laboratory for fish diseases is only obliged to devote human and technical resources towards diagnosing listed diseases. Another important point is that the surveillance systems are always alert to the possible occurrence of a listed disease. For example, a suspected case of viral haemorrhagic septicaemia (VHS) based on high mortality and compatible clinical signs (which are very similar to signs exhibited by other haemorrhagic diseases, such as enteric redmouth disease, furunculosis, vibriosis, and infectious salmon anaemia; WOAH Aquatic Manual, 2022), is sufficient to open an investigation by competent authorities. The official veterinary services have well-established procedures for performing surveillance on notifiable diseases, such as VHS, for which there are well-defined guidelines related to the definition of suspected cases, as well as early communication procedures, diagnosis and confirmation. However, for marine fish (seabass and seabream), an official case investigation will only be opened if abnormal mortalities are detected. Nevertheless, in this case, except for Murcia Autonomous Community, the indicator of abnormal mortality is not defined, and any sampling is undertaken by the affected farms and the corresponding ADS, as there are no official laboratories for the diagnosis of marine fish diseases, and the official veterinary services do not have well-established procedures for performing surveillance of abnormal mortalities and emerging diseases. It is worth noting though that although Spain benefits from an experienced institutional and private laboratory network, it is not closely connected to the official network and, as such, loses very valuable capacity and information input that is essential for correct management of the health system (24).

Council Directive 2006/88/EC endorsed Member States to approve national measures for limiting the impact of certain relevant diseases in aquaculture and wild aquatic animals not listed in Part II of Annex IV of that Directive. Consequently, the Commission Decision of 15 April 2010 approved national measures and eradication programs regarding certain diseases [i.e., spring viraemia of carp (SVC), bacterial kidney disease (BKD), infectious pancreatic necrosis virus (IPN) and infection with Gyrodactylus salaris (GS)] in Denmark, Finland, Ireland, Sweden, and United Kingdom. However, no measures/eradication programs were approved for any Mediterranean country, despite the growing economic magnitude of the marine fish farming sector and the known impact of certain diseases, such as the case of nodavirus (7, 25, 26).

The two lowest rated categories in SET for both trout and marine fish (seabass and seabream) were “External Communication and Resources” and “Internal Evaluation.” This showed that there was limited and/or inefficient exchange of information on health and disease aspects between the competent authorities and the stakeholders involved (e.g., administration, producers, laboratories, pharmaceutical companies, insurance companies, research centres and universities). In this context, it is very important to value the need for information exchange, as occurs in other countries (27–29) where all cases of disease are reported in a public database, so that any interested stakeholder can consult veterinary inspection reports and mortality farm records. Additionally, competent surveillance authorities and laboratories pass external evaluation exercises, although there is a lack of internal evaluation procedures.

It should be pointed out that most animal production also takes place in inland locations, where animal health surveillance and official veterinary services are well represented. On the other hand, marine fish production takes place in environments (on the coast and off-shore) where, generally, official veterinary services are lacking in both proficiency and a clear legislative framework that can guide their actions. Another observed constraint is that terrestrial animal production units and animal health units are under the same administrative structure, whereas fish farming health and production units are under different administrative structures, both at the national and subnational levels, thus, generating additional burdens for communication and information readiness.

The conclusions and recommendations derived from this study could be of value not only for Spain, but also for fish health authorities and experts that would like to conduct similar assessments of fish disease surveillance systems in other countries. The FAO SET tool has been shown to be very suitable for this purpose, and showed significant higher scores for trout when compared to marine fish (seabass and seabream) surveillance. The main reasons behind this difference seemed to be based on the fact that surveillance for trout is always alert for the possible occurrence of a listed disease (e.g., VHS), whereas surveillance for marine fish (seabass and seabream) should react only after the occurrence of abnormal mortalities, for which standardized methodologies have yet to be implemented.

Therefore, in conclusion, it is recommended that the Spanish marine fish surveillance plan needs to be improved at the national level for seabass and seabream, since marine species have higher production levels and value. In order to assure that the implemented surveillance system meets its objectives, by improving quality and efficiency, it is also recommended to organize periodic re-assessments.

The original contributions presented in the study are included in the article/Supplementary material, further inquiries can be directed to the corresponding author.

The manuscript presents research on animals that do not require ethical approval for their study.

AM: Data curation, Formal analysis, Investigation, Methodology, Writing – original draft, Writing – review & editing. IR-Z: Conceptualization, Methodology, Writing – original draft, Writing – review & editing. GL: Conceptualization, Formal analysis, Methodology, Writing – review & editing. SD: Validation, Writing – review & editing. DF: Supervision, Writing – review & editing. CR: Conceptualization, Supervision, Writing – review & editing. BB: Conceptualization, Formal analysis, Methodology, Writing – original draft, Writing – review & editing.