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Epidemiological surveillance of wildlife consists of monitoring the health status and risk factors in these animal populations (Toma et al., 2010). Improved knowledge allows measures to be taken to face major issues such as the preservation of biodiversity, the conservation of vulnerable species, the maintenance of the economy associated with domestic animals and the protection of public health. It is thus recognised that wildlife epidemiosurveillance needs to be better integrated into the One Health approach (Karesh and Cook, 2005; Buttke and Wild, 2014; Cunningham et al., 2017; Sleeman et al., 2017), which involves an integrated view of public, animal and environmental health. Many species of terrestrial wildlife are indeed responsible for zoonosis. For example, Eurasian badgers (Meles meles) in the United Kingdom and Ireland and wild boars (Sus scrofa) in Spain, are reservoirs of Mycobacterium bovis, which are involved in the transmission of Bovine tuberculosis to cattle (Réveillaud et al., 2018). Another example of pathogen’s transmission between wildlife and domestical animals is the canine distemper virus in the lion (Panthera leo) population of the Serengeti National Park in Tanzania. This virus is similar to the one circulating in domestic dogs (Canis lupus familiaris) and the contacts between these two species make it possible to transmit the virus between them (Cleaveland et al., 2000; Viana et al., 2015). In addition, terrestrial wildlife is very present in the cities and could also be responsible for the transmission of zoonosis. Rodents such as the Norway rat (Rattus norvegicus) are known to be intermediate hosts of alveolar echinococcosis and since 1996, the red fox (Vulpes vulpes) has been described as one of the definitive hosts of this parasite. These species present in our cities are therefore likely to transmit this parasitosis to humans through their faeces (Bresson-Hadni et al., 2004; Vuitton et al., 2010).

Unlike terrestrial wildlife, the interactions between the health of marine mammals and human or domestic animal health may seem less obvious, given the more limited contact with marine mammals (Crespo and Hall, 2001). Moreover, difficulties are met to conduct the monitoring on marine wildlife, as access to these animals is difficult because of their habitat and their behavior (i.e., cryptic species, highly mobile species, diving behavior). Nevertheless, marine mammals should be considered as sentinel species not only for the health of the oceans but also of humans’ health (Bossart, 2011). Thus, the monitoring of strandings represents a valuable source of data to inform conservation management (IJsseldijk et al., 2020b). In addition to the spatiotemporal mortality trends and the cause of death, necropsies and complementary analysis carried out on stranded animals allows to understand the circulation of pathogens (bacteria, viruses, parasites and fungi) in these animal populations (e.g. Stokholm et al., 2021) which can constitute a conservation or public health issue (Ossiboff et al., 2021). In addition to detecting pathogens that would cause the death of the animal, it is possible to identify pathogens carried by an animal without being responsible for the death, or to detect antibodies, which would provide evidence that the targeted agent is circulating in the population (Bodewes et al., 2015; Measures and Fouchier, 2021). Laboratory analysis can also detect phenomena such as antibiotic resistance in isolated bacteria which is of public health interest (e.g. Gross et al., 2022). As with terrestrial wildlife, determining the causes of mortality and monitoring the health status of marine mammals ultimately makes it possible to identify the main threats to these animals and to respond to a public health issue, particularly with the early detection of zoonotic agents (Kuiken et al., 2005).

Therefore, many coastal countries in Europe and around the world have set up systems to record strandings and carry out post-mortem examinations of carcasses, thus taking advantage of these strandings to improve scientific knowledge (Perrin and Geraci, 2009). In Europe, some of these networks are effective for health surveillance and carry out necropsies with additional analysis for diagnostic purposes, such as in Germany (Institute of Wildlife and Marine Research of the University of Hanover), in Netherlands (Faculty of Veterinary Medecine, Department of Biomolecular Health Sciences, Division of Pathology, Utrecht University), in Great Britain (UK Cetacean Stranding Investigation Programme and ZSL Institute of Zoology), in Belgium (Faculty of Veterinary Medicine in Liège), in Italy (National Reference Center for Diagnostic Activities on Stranded Marine Mammals) and in Spain (University of Valencia, University of Las Palmas de Gran Canaria). These efforts have led to numerous publications that make it possible to assess the health status of populations at least on a regional scale (e.g. Prenger-Berninghoff et al., 2008; Arbelo et al., 2013; Mahfouz et al., 2014; van de Velde et al., 2016; Kershaw et al., 2017; Pintore et al., 2018; Coombs et al., 2019; Kapetanou et al., 2020; Numberger et al., 2021; Audino et al., 2022). Routine analysis are also carried out, but apart from a few main pathogens known in marine mammals, they often differ from one country to another (Guillerit, 2017). This is why standardisation of analysis between countries would allow the results obtained to be inferred at the population level of these widely distributed mobile species. This is all the more important as there are other considerations to be taken into account when conducting health monitoring of marine mammals. They are protected species covered by numerous regional and international directives and conventions. At the international level, these are mainly the Convention on the Conservation of Migratory Species of Wild Animals (CMS, Bonn Convention) and the Convention on the Conservation of European Wildlife and Natural Habitats (Bern Convention). In the North East Atlantic, the OSPAR (Oslo-Paris) convention and ASCOBANS (Agreement on the Conservation of Small Cetaceans of the Baltic, North East Atlantic, Irish and North Seas) both cover the conservation of marine mammals. These species are also regulated in French law through the decree of the 1^st of July 2011 in application of the CITES Convention (Washington Convention) and Directive 92/43/EEC (European Directive known as the Habitats-Fauna-Flora Directive). Furthermore, at European level, the 2008/56/EC Marine Strategy Framework Directive (MSFD) published on the 25^th of June 2008 and transposed in France in a series of regulations concerning the marine environment, requires knowledge of the health status of marine mammal populations to be improved.

The French National Stranding Network (NSN) is coordinated by the Pelagis observatory in La Rochelle (Support and Research Unit, UAR 3462 La Rochelle University - French National Center for Scientific Research), appointed by the Ministry of Ecology to monitor the status of marine mammal populations and support the implementation of public conservation policies relating to these species. The monitoring of strandings makes it possible to meet the requirements linked to the regulated status of these species. For example, among the descriptors defined by MSFD and used to define Good Ecological Status (GES), marine mammals are involved in descriptor D1 “Biodiversity” and descriptor D8 “Contaminants” with the following expectations: (1) monitoring of coastal cetacean populations, (2) monitoring of seal populations, (3) monitoring of marine mammals at sea, (4) monitoring of marine mammal strandings, (5) monitoring of interactions with human activities, (6) monitoring of chemical contaminants in cetaceans. Thus, the monitoring of strandings is an integral part of this monitoring.

The NSN was created in 1972 as a natural science network. Since its beginnings, the network has relied on the participation of volunteers (correspondents), but over time it has become partially professional, with some correspondents such as field agents of the French Biodiversity Agency (Office Français de la Biodiversité - OFB) for whom this activity is part of their missions. The network has evolved from a descriptive activity of stranded animals to the detection of the main causes of mortality through the examination and necropsy of some selected carcasses and the study of the ecology of species through various samples and data analysis. From this point of view, this network is particularly functional and generates approximatively twenty publications per year in the field of ecology (e.g. Spitz et al., 2014; Peltier et al., 2021; Chouvelon et al., 2022; Méndez-Fernandez et al., 2022; Rouby et al., 2022). Certain zoonotic pathogens (Brucella sp. and Erysipelothrix rhusiopathiae) and epizootic agents (morbillivirus and avian influenza virus) are only investigated if macroscopic lesions are suggestive of infection by these pathogens. In this global context, Pelagis has developed a strategy to better monitor the health of marine mammals based on stranded marine mammals. To this end, it is necessary to develop the network and strengthen the system for monitoring the health of marine mammals in order (1) to harmonise the methods used to diagnose and identify the causes of mortality with greater accuracy (2) to improve the understanding of the main threats to marine mammals, particularly emblematic or critical species (because of their rarity or the associated conservation issue) as well as strandings associated with phenomena of interest (e.g. unusual mortality events); (3) to improve the ability to analyse data through epidemiological models (4) to allow the acquisition of knowledge on the circulation of pathogens in these populations and their impact on animal and public health in case of zoonosis; (5) to allow the early and easy detection of peak mortality and other monitored factors; and finally, (6) to allow the early detection of major (re-)emerging, exotic or zoonotic diseases. Thus, this strategy falls within the field of eco-epidemiology while integrating the “One Health” approach.

The French stranding network provides a case study: the conceptual framework will be confronted with reality, considering the objectives, structure, functioning and tools of the NSN, which will need to evolve further to better meet the requirements of the strategy. The limits and needs will be identified as well as the long-term prospects. The objective is to present the strategy developed at the French level (metropolitan and overseas) in order to integrate it into a future strategy shared at the European level to standardise practices and especially complementary analysis, necessary for a better evaluation of the health status of these mobile marine species.

The health monitoring of marine mammals as presented here is an ambitious project requiring as many stranding data as possible. Pelagis’ first ambition was to improve its means of expertise in order to conclude with more precision and certainty on the causes of mortality. The development of these means was the opportunity to reinforce the global health monitoring of marine mammal populations. This strategy will allow to improve the knowledge of the health status of these species subjected to numerous pressures by following the evolution in time and space of diseases associated with conservation and public health issues while ensuring the early detection of emerging and/or zoonotic diseases of importance. It will also allow a better assessment of the consequences of anthropic activities on these animal populations and on the environment.

The high number of strandings in metropolitan France, combined with logistical, financial and human resources, imply that the highest level of examinations cannot be implemented on every stranded marine mammal. Thus, a strategy with different surveillance modalities has been established, allowing us to choose the individuals on which the most in-depth investigations will be carried out, while representing at best the stranded marine mammal population. The strategy, based on four surveillance modalities which are general event-based surveillance, programmed surveillance, specific event-based surveillance and syndromic surveillance should imply many evolutions. Among these, the main ones are the dissemination of expertise means and their appropriation by the network actors, the ability to meet the sampling plan and the appropriation of the P3 sampling protocol within the framework of the programmed surveillance and the integration of standardised data (standardized samples and analysis), which imply a significant reorganisation of the database structure.

The systematic performance of standardized analyses within the framework of the PS will make it possible to carry out descriptive epidemiology by identifying the health problems of populations and by measuring them in time and space. In addition to being able to infer the results obtained to a reference population, the laboratory analyses that complete the necropsy allow the cause of death to be investigated with greater precision.

Various criteria were considered in order to define the reference population for the sampling plan to conduct the PS. Emblematic Species already included in the strategy for monitoring contaminants in cetaceans (bottlenose dolphin for the 3 metropolitan seaboards, common dolphin for the Atlantic coast, harbour porpoise for the English Channel coast and stripped dolphin for the Mediterranean coast) on the French coast established by Pelagis within the framework of the MSFD were considered as a priority (Méndez-Fernandez et al., 2019). Moreover, to date, very few studies have been conducted on the pathogens circulating in marine mammal populations in France, not allowing species to be targeted according to their health vulnerability, with the exception of the striped dolphin, which has been the victim of mass mortalities caused by morbillivirus on several occasions in regional waters (Dhermain et al., 1995; Keck et al., 2010; Van Bressem et al., 2014) and harbour seals which have been victims of Avian Influenza in the North Sea (Bodewes et al., 2015). These two species were therefore also considered as a priority. The lack of general data at this stage has therefore led to the selection of the most frequently encountered stranded marine mammal species as reference populations in the first instance, while ensuring that the previously mentioned priority species are included. This will allow us to obtain initial data on the circulation of pathogens in these populations as well as on their health impact, and to subsequently make more specific choices concerning the marine mammal species and pathogens monitored. It is expected that after a period of one or two years, other strategic choices will be made. For example, instead of conducting the PS on a representative sample of the entire stranded population, the priority could be shifted to emblematic species. However, the distribution of logistical means and expertise on the territory did not allow to make this choice at this stage: for example, to be interested in the striped dolphins in the same way as the common dolphins would imply making a very important logistical effort in the Mediterranean coast. Thus, according to the current sampling plan, some species-seaboard pairs are under-represented, or even unrepresented when they constitute less than 0.5%. It will therefore be difficult or impossible to obtain valid data for these species, such as the long-finned pilot whale, which will be only marginally represented in the plan. The same applies to the maritime frontage. With less than ten animals in the sampling plan for the Mediterranean the information obtained will be very limited. It is also important to remember that current knowledge does not allow us to estimate the representativeness of the living marine mammal population based on strandings, which also implies a major limitation. Furthermore, the sampling plan is confronted with major sampling biases that must be considered when analyzing the various data obtained. Indeed, a series of non-standardised filters related to detectability, reporting, access to carcasses, DCC, human and logistical response capacities make these biases unavoidable and must therefore be considered when analyzing and interpreting the data.

Morevover, as these are mobile species that should be considered on a basin or regional scale, collaborations with neighbouring countries where strandings of animals from the same populations as those occurring on our coasts will be necessary. Although necropsy and common sampling protocols have already been proposed on a European scale, the situation is different for routine analysis (IJsseldijk et al., 2020a). Thus, a minimum of common routine analysis should be considered in order to obtain more global and representative data of these animal populations and to ensure large-scale health surveillance in a One Health context. The agreements of ASCOBANS and ACCOBAMS as well as the ICES and OSPAR working groups and the European Cetacean Society should be the framework for discussions and exchanges on practices with other European countries in order to harmonise not only necropsies and tissue sampling (Jauniaux et al., 2019; IJsseldijk et al., 2020a) but also the complementary analysis carried out by the laboratories as initiated at the pathology workshop of the European Cetacean Society in 1991 (Kuiken and García Hartmann, 1991).

The choices concerning standardised routine analysis within the framework of P3 and therefore of programmed surveillance were made according to several criteria: the improvement of knowledge and the interests for conservation and public health in relation to the financial cost and technical and logistical feasibility (easy access to laboratory techniques).The post mortem investigation and tissue sampling protocol already established under the auspices of ASCOBANS (Agreement on the Conservation of Small Cetaceans of the Baltic, North East Atlantic, Irish and North Seas) and ACCOBAMS (Accord sur la Conservation des Cétacés de la Mer Noire, de la Méditerranée et de la zone Atlantique adjacente) (IJsseldijk et al., 2020a), has guided our choices as well as the most frequently analysis performed in foreign European networks (Prenger-Berninghoff et al., 2008; van de Velde et al., 2016; Kershaw et al., 2017; Sonne et al., 2020; Stokholm et al., 2023). Investigations for morbilliviruses, influenza viruses and Brucella sp. will be sought for their known impact on marine mammal populations for the first two and for their zoonotic character for the last two. Morbilliviruses have indeed been the cause of mass mortalities on several occasions in regional waters, in the Mediterranean and in the North and Baltic Seas (Dhermain et al., 1995; Rijks et al., 2008; Keck et al., 2010; Duignan et al., 2014; Van Bressem et al., 2014). For influenza, a mass mortality event has also occurred in the North Sea (Bodewes et al., 2015). Furthermore, the risk for public health is not negligible as the high reassortment potential of this virus means that it could become more virulent and pathogenic, both for marine mammals and humans (Anthony et al., 2012; Fereidouni et al., 2016; Van den Brand et al., 2016). Similarly, brucellosis of marine origin, in addition to affecting reproduction, has repeatedly caused infections in humans and is most likely under-diagnosed (Brew et al., 1999; Jouffroy, 2020). Moreover, herpesviruses will be investigated as various studies have shown that these viruses circulate widely in marine mammal populations and that the clinical pictures, although variable, can lead to death (Duignan et al., 2018). Finally, mycotic agents will be looked for in their entirety as they are considered a major emerging cause of mortality in both humans and marine mammals (Reidarson et al., 2018). Other pathogens for which the risks are less known or for which massive mortality events have occurred but in distant waters have not been retained at this stage. They will nevertheless be the subject of reflection by a working group on the prioritisation of health hazards in marine mammals and may at any time be included in the P3 protocol or in the case of SES. In addition, future collaboration with neighbouring countries may identify other risks to be monitored.

The results of analysis carried out on carcasses, although they are of DCC 1 or 2, should be interpreted with caution, particularly for bacteriological analysis, due to possible post-mortem contamination (Palmiere et al., 2016). Also, it should always be considered that pathogen testing on carcasses allows us to know if the animal was infected at the time of death but not if the animal was infected earlier and then cured. Therefore, it does not give an overall picture of the circulation in the population. For this, it would be desirable to obtain seroprevalences as it has been carried out for avian influenza in seals (Bodewes et al., 2015; Measures and Fouchier, 2021).

Epidemiological vigilance will be ensured by the different modalities, in particular for cases managed with specific event-based surveillance. The example of the major avian influenza outbreak in Europe in 2022 (Adlhoch et al., 2022) reminds us of the importance of detecting potential outbreaks in marine mammal populations. Epidemiological vigilance will be constrained by certain limitations such as the DCC of the carcass, which will have a strong impact on the ability to obtain quality information. The identification of cases subject to specific event-based surveillance based on spontaneous reporting by correspondents implies that they are well informed and that case definitions are simple, sensitive and specific enough. In addition, case management under SES requires the availability of network correspondents trained in the level of examination and sampling protocol required for the case but also the involvement of laboratories performing the defined analysis. Although the volume of animals covered by this surveillance modality can be estimated, it is important to note that it is impossible to know precisely the number, nature and location of data that will be collected.

Beyond the defined strategy, ad hoc surveys may be carried out to answer specific questions from research projects or to respond to questions related to the epidemiological context, as could have been done by looking at the susceptibility of marine mammals to SARS-CoV-2 in marine mammals during the epidemic that Europe experienced, as it has been done in Italian waters for example (Audino et al., 2021).

Many aspects of the strategy are based on data obtained over the last five years for which all the information is already available (2016 to 2020). This arbitrary choice of a relatively short period was made to consider population shifts and changes in the environment (environmental parameters, fishing practices, construction of offshore parks…) and to try to be as close as possible to what might happen in the coming year. The time windows of the MSFD could possibly be used as early as 2025 (beginning of the third MSFD cycle) in order to harmonise the strategies.

Generally speaking, the strategy for strengthening health surveillance developed by Pelagis provides a framework that allows all the actors in the NSN to be informed of the approach followed and to understand its ins and outs. Thus, the effort of training (a 3 days initial training is required to incorporate the NSN, and retraining every five years at least, concurrently with the evolution of protocols) and informing correspondents is essential to guarantee their support and investment in the project and to limit operator bias harmonising practices. It is also important to continue to train new correspondents at the various levels, as the more numerous they are, the greater the number of animals evaluated.

The overall cost of this strategy, implemented in January 2023, is significant mainly due to the laboratory analysis carried out within the framework of the PS, which are added to the logistical costs of managing strandings. The discussions that will be conducted by the working group on the prioritisation of health hazards should make it possible to reach a compromise between the benefits of these analysis and the associated cost in the next two years.

Although there are many constraints to strengthening health monitoring, the structure of the NSN is very similar to that of an epidemiological surveillance network, which makes it a major strength. Moreover, the network has already proven its capacity to detect almost all strandings and to collect data on a large scale in space and time.

Similarly, health monitoring should focus on live marine mammals too. This mainly concerns pinnipeds, including those entering care centres before being released, but also live cetacean strandings. Finally, marine mammal populations in French overseas waters that face different problems to those in metropolitan France should also be subject to health monitoring.

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

The main work was carried out by SW under the guidance of FC, and with the main support of EM. All authors contributed to the article and approved the submitted version.