Features of metazoan parasites of fish from TW

Parasite communities of fish are driven, in part, by host characteristics such as size, age, trophic level, density, habitat, feeding habits and immunological responses (Timi, Reference Timi2007; Timi et al., Reference Timi, Luque and Poulin2010, Reference Timi, Rossin, Alarcos, Braicovich, Cantatore and Lanfranchi2011), and estuarine fish are not an exception. However, their spatial distributions, particularly those of marine parasites, are mainly determined by temperature–salinity profiles and their association with specific masses of water (Esch and Fernández, Reference Esch and Fernández1993; Cantatore and Timi, Reference Cantatore and Timi2015). In TW, fish inhabit different biotopes with features of marine, freshwater and brackish waters, therefore composing a variety of amphihaline, euryhaline and true estuarine fish assemblages (Ray, Reference Ray2005; Lowe et al., Reference Lowe, Morrison and Taylor2015). Such high variability is mostly determined by the recruitment of species from the sea and/or from rivers, given the relatively small number of truly estuarine fish species (Snigirov et al., Reference Snigirov, Kvach, Goncharov, Sizo and Sylantyev2019). This set of assemblages with differential halotolerance capabilities (Schultz and McCormick, Reference Schultz and McCormick2012) and modes of response to natural and anthropogenic factors are expected to harbour an equivalent variety of parasite assemblages with marine, estuarine and freshwater lineages.

Indeed, and given the ecotonal nature of TW, where gradients dominate the dynamics of biotopes, a high species richness is expected due to an ‘edge effect’ (Odum, Reference Odum1959), defined as the ‘tendency for increased population species richness and density in the junction zone between communities’. This occurs because an ecotone contains representatives of species characteristic of adjacent communities. Indeed, parasite assemblages in ecotonal regions where, for example, convergent masses of water supply their own infective stages, also display ecotonal structure and composition (Lanfranchi et al., Reference Lanfranchi, Braicovich, Cantatore, Alarcos, Luque and Timi2016).

Interesting examples about the effects of environmental features on the composition of parasite assemblages in TW have focused on the influence of hydrological characteristics (Kesting et al., Reference Kesting, Gollasch and Zander1996; Landsberg et al., Reference Landsberg, Blakesley, Reese, McRae and Forstchen1998; Snigirov et al., Reference Snigirov, Kvach, Goncharov, Sizo and Sylantyev2019), mainly of salinity profiles (Zander et al., Reference Zander, Kollra, Antholz, Meyer and Westphal1984; Zander, Reference Zander1998; Blanar et al., Reference Blanar, Marcogliese and Couillard2011; Rashnavadi et al., Reference Rashnavadi, Lymbery, Beatty and Morgan2014), whose gradients determine concomitant variations in parasite burdens depending on the parasite guilds. Indeed, ectoparasites, which are generally monoxenous and live in direct contact with the surrounding water, are more sensitive not only to changes in salinity, but also to other factors, such as temperature and dissolved oxygen, e.g. parasitic copepods are recognized as highly stenohaline (Cavaleiro and Santos, Reference Cavaleiro and Santos2009). On the other hand, heteroxenous parasites depend largely on the availability of other hosts involved in their life cycles (Landsberg et al., Reference Landsberg, Blakesley, Reese, McRae and Forstchen1998). Ectoparasites, in general, as well as trophically transmitted gastrointestinal parasites, face drastic changes in the physical characteristics of habitats when their hosts migrate to estuarine waters. For example, the skate Sympterygia bonapartii harbours parasite communities that are significantly different between estuarine and marine waters after performing reproductive migrations in the Argentine coast when ectoparasites and gastrointestinal helminths are included in the analyses, but no differences are observed when only larval parasites from the body cavity or other tissues are considered (Irigoitia et al., Reference Irigoitia, Incorvaia and Timi2017). These later guilds, represented mostly by long-lived larval helminths, can persist for long periods, generally encysted or encapsulated in fish tissues and body cavities (Braicovich et al., Reference Braicovich, Ieno, Sáez, Despos and Timi2016), and should be able to survive under different conditions when diadromous fish alternate between marine, transitional and freshwater habitats. Thus, for instance, consecutive infections of the ‘sea’ perch Perca fluviatilis with freshwater parasites can take place during seasonal reproductive migrations to lakes (Wierzbicka et al., Reference Wierzbicka, Wierzbicki, Piasecki and Smietana2005).

The freshwater, estuarine or marine origin of fish, and therefore the proportion of each lineage in the host community, are further relevant determinants of the structure of parasite assemblages. A study of 6 estuarine-dependent marine fish species caught in the Mar Chiquita coastal lagoon, Argentina, showed that 5 of them harboured parasite faunas of predominantly marine origin, with only 1 species, the mullet Mugil platanus, with parasite communities dominated by true estuarine parasites (Alarcos and Etchegoin, Reference Alarcos and Etchegoin2010). The authors attributed such differences to the longer residence time of mullets in the coastal lagoon. A broader study, including 22 species of marine, brackish water and freshwater fishes, carried out in the Celestun coastal lagoon, Mexico, also showed the dominance of the marine euryhaline fishes that apparently enter the lagoon already infected with typical marine parasites (Sosa-Medina et al., Reference Sosa-Medina, Vidal-Martinez and Aguirre-Macedo2015). In contrast, in northeastern Bothnian Bay, Baltic Sea, a minor proportion of parasites (8 out of 63) found in 31 sympatric fish species was marine (Valtonen et al., Reference Valtonen, Pulkkinen, Poulin and Julkunen2001). The authors argued that due to ecological factors acting over short time scales, rather than evolutionary ones, marine parasite species are able to utilize both freshwater and marine fish species as intermediate or final hosts, and marine fish can harbour freshwater parasite species. Given the relatively recent origins of the Baltic Sea and Bothnian Bay, the establishment of marine parasites in the bay has probably depended on the immediate presence of suitable intermediate and definitive hosts (Valtonen et al., Reference Valtonen, Pulkkinen, Poulin and Julkunen2001).

Beyond the results of ecological mechanisms, the physical variability of TW is thought to promote evolutionary processes by selecting generalist genotypes to adapt to a wide range of conditions, therefore preadapting them to colonize new habitats (Bamber and Henderson, Reference Bamber and Henderson1988). As an example, living cystacanths of acanthocephalans of the genus Profilicollis, characterized by using marine/estuarine decapod crustaceans as their unique intermediate hosts (Nickol et al., Reference Nickol, Crompton and Searle1999, Reference Nickol, Heard and Smith2002), were found parasitizing the body cavity of a freshwater fish host, Oligosarcus jenynsii, for the first time in the freshwater section of the Mar Chiquita coastal lagoon, Argentina (Levy et al., Reference Levy, Rossin, Braicovich and Timi2020). These findings were interpreted as a possible case of incipient paratenicity for Profilicollis and a colonization event of freshwater habitats, probably promoted by the highly variable conditions typical of estuarine environments.

Thus, in addition to ecological mechanisms, eco-evolutionary mechanisms can be identified as drivers of the composition and structure of fish parasite communities in TW. For instance, in the same coastal lagoon, a euryhaline marine silverside, Odontesthes argentinensis, is commonly reported. It shows substantial genetic differences with conspecifics from adjacent marine coasts, despite no geographic barriers separating them, and is considered an example of a marine to freshwater incipient speciation event (González-Castro et al., Reference González-Castro, Rosso, Delpiani, Mabragaña and Diaz de Astarloa2019). A comparative parasitological study of estuarine and marine samples demonstrated enough qualitative and quantitative differences to be a strong support for the ongoing speciation process proposed for the host in the lagoon (Levy et al., Reference Levy, Canel, Rossin, González-Castro and Timi2021). Beyond a few individual exclusively marine parasites found in estuarine waters and vice versa, some marine parasites seem to have coinvaded the lagoon. Indeed, the nematodes Cucullanus marplatensis and Huffmanela moraveci, both specific to silversides and of marine origin, are commonly reported in marine congeners but not in freshwater ones. Both species are found at high burdens in the estuary, indicating that they have coestablished estuarine populations.

Anthropogenic factors influencing metazoan parasites in TW

In addition to host characteristics and natural abiotic and biotic features of the environment, parasites are influenced by anthropogenic factors, among which climate change, pollution and biological invasion are examined below. Because parasites, similar to free-living organisms, are impacted by habitat modification, they can reveal environmental changes (Hudson et al., Reference Hudson, Dobson and Lafferty2006). The study of parasite community composition and of the variations in time and space of population parameters could provide useful information on anthropogenic alterations affecting parasites themselves, the hosts and/or the ecosystem (Lafferty, Reference Lafferty1997). Parasites may respond to environmental perturbations in different ways (i.e. increasing or decreasing richness and/or abundance) depending on their condition of ecto- or endo-parasites, their direct or indirect life cycle and their host specificity (Marcogliese, Reference Marcogliese2004), and this crucial issue should be considered when using them as sentinels.

Ecological role and impact of metazoan parasites of fish in TW

It is implied in the definition of parasitism that parasites are detrimental to their hosts, showing more or less adverse effects at the individual and population levels (Combes, Reference Combes2001). Parasites may also affect and regulate the community and the ecosystem in which they occur and not necessarily with negative outcomes (Marcogliese, Reference Marcogliese2004; Wood and Johnson, Reference Wood and Johnson2015). The role of parasites at these higher levels of biological organization is difficult to understand and quantify, and perhaps for this reason, it has often been overlooked by ecologists (Marcogliese and Cone, Reference Marcogliese and Cone1997; Bartoli and Boudouresque, Reference Bartoli and Boudouresque2007). Moreover, such roles can vary depending on parasite pathogenicity, the position in the food webs and the condition of generalist or specialist (Hudson, Reference Hudson, Thomas, Renaud and Guegan2005).

Information on the ecosystem effects of parasites, especially on food-web processes and energy flow, is mainly derived from long-term studies in estuaries from southern California (Lafferty and Morris, Reference Lafferty and Morris1996; Lafferty et al., Reference Lafferty, Dobson and Kuris2006a, Reference Lafferty, Hechinger, Shaw, Whitney, Kuris, Collinge and Ray2006b, Reference Lafferty, Allesina, Arim, Briggs, De Leo, Dobson, Dunne, Johnson, Kuris, Marcogliese, Martinez, Memmott, Marquet, McLaughlin, Mordecai, Pascual, Poulin and Thieltges2008; Kuris et al., Reference Kuris, Hechinger, Shaw, Whitney, Aguirre-Macedo, Boch, Dobson, Dunham, Fredensborg, Huspeni, Lorda, Mababa, Mancini, Mora, Pickering, Talhouk, Torchin and Lafferty2008; Lafferty, Reference Lafferty2008). Although parasite biomass often appears negligible, especially when compared with that of free-living organisms, in Carpinteria Salt Marsh, parasites represent a relevant amount of biomass and an important food source (Lafferty, Reference Lafferty2008). Indeed, cumulatively, parasite biomass (i.e. all parasites counted and weighed together) ranges from 6 to 12 kg ha⁻¹ and constitutes one-third of the standing stock of fish biomass and 0.2–1.3% of the free-living animals (Kuris et al., Reference Kuris, Hechinger, Shaw, Whitney, Aguirre-Macedo, Boch, Dobson, Dunham, Fredensborg, Huspeni, Lorda, Mababa, Mancini, Mora, Pickering, Talhouk, Torchin and Lafferty2008). Although parasitic organisms are generally considered only as consumers, they can also be important prey, being ingested with their hosts by their predators or directly eaten as ectoparasites or in free-living stages (Kaplan et al., Reference Kaplan, Rebhal, Lafferty and Kuris2009; Johnson et al., Reference Johnson, Dobson, Lafferty, Marcogliese, Memmott, Orlofske, Poulin and Thieltges2010; Thieltges et al., Reference Thieltges, Amundsen, Hechinger, Johnson, Lafferty, Mouritsen, Preston, Reise, Zander and Poulin2013). For instance, small fish of different species can rely on digenean cercariae for nutrition, partially deviating the energy flow in estuarine ecosystems (Kuris et al., Reference Kuris, Hechinger, Shaw, Whitney, Aguirre-Macedo, Boch, Dobson, Dunham, Fredensborg, Huspeni, Lorda, Mababa, Mancini, Mora, Pickering, Talhouk, Torchin and Lafferty2008; Lafferty, Reference Lafferty2008).

Many heteroxenous parasites, such as cestodes, digeneans and acanthocephalans, having indirect life cycles with 2 or more hosts exploit trophic relationships for transmission, participating in most links of aquatic food webs, particularly those involving fishes, and even dominating them (Lafferty et al., Reference Lafferty, Dobson and Kuris2006a; Lafferty, Reference Lafferty2008). There is growing evidence that parasites are important in food-web topology and improve the nestedness, connectivity and stability of the community (Lafferty, Reference Lafferty2008; Hatcher et al., Reference Hatcher, Dick and Dunn2012). The alteration of predator‒prey interactions is a typical way by which parasites may affect trophic webs. Given the energetic cost of parasitism, infected hosts are often weakened and then more vulnerable to predation. Additionally, behavioural or morphological/physiological alterations imposed by parasites determine an increased susceptibility to the predation of hosts by reducing their ability to avoid predators and/or to escape from them (Thomas et al., Reference Thomas, Cezilly, De Meeüs, Crivelli and Renaud1997). As a result, parasites are facilitated to reach their final host and successfully complete their life cycle, predator species often benefit from enhanced food accessibility, and trophic links are influenced by an increase in predation rates. The manipulative capacity of some parasites to change fish behaviour (e.g. foraging activity, habitat selection, competition, predator‒prey interactions, swimming ability and sexual and mate behaviour) is well documented (Barber et al., Reference Barber, Hoare and Krause2000). There are interesting examples of altered behaviour in TW, with evident ecological consequences, sometimes dramatic ones, especially when fishes serve as intermediate hosts (Lafferty, Reference Lafferty2008). For instance, California killifish Fundulus parvipinnis, the most common fish species in Carpinteria Salt Marsh, shows a very high prevalence and intensity of infection by the trematode Euhaplorchis californiensis, which has birds as final hosts. Infected killifish with encysted larvae in the brain exhibit a conspicuous behaviour that makes them up to 30 times more susceptible to bird catch (Lafferty and Morris, Reference Lafferty and Morris1996). Other examples of altered behaviour in TW fish are available in the literature. The shoaling behaviour in parasitized Fundulus diaphanus is modified, exposing the fish to a higher predation risk by piscivorous birds (Krause and Godin, Reference Krause and Godin1994). Predators may also be facilitated by parasites that damage eyes (Kinne, Reference Kinne1984), obtrude vision (Stumbo and Poulin, Reference Stumbo and Poulin2016) or impair fin mobility in fish hosts, as in the case of Gobius infected by the trematode Cainocreadium labracis (Maillard, Reference Maillard1976). Parasites can increase food and oxygen demand in their fish hosts that, by spending more time close to the water surface or engaged in food acquisition, are consequently easier to prey upon (Curio, Reference Curio and Mehlhorn1988).

In addition to influencing predation rates, other impacts of parasites on their fish hosts have been documented in TW, for example, on sexual selection, with male pipefish avoiding females infected by a trematode (Rosenqvist and Johansson, Reference Rosenqvist and Johansson1995) and on modifications of movement with consequences for population and ecosystem processes such as migration and dispersal (Binning et al., Reference Binning, Shaw and Roche2017). For example, infection with a copepod inhibits the migration to the sea of Gadus merlangus, which remains ‘trapped’ in estuarine waters (Sproston and Hartley, Reference Sproston and Hartley1941). Similarly, the nematode A. crassus, a haematophagous parasite infecting the swim bladder of eel, can limit swimming performance and speed, and some authors argue that this specialist pathogen has contributed to the decline of European eel A. anguilla (Kennedy, Reference Kennedy2007; Palstra et al., Reference Palstra, Heppener, van Ginneken, Szekely and van den Thillart2007). Among the possible population effects of anguillicolosis are the selective capture of infected eels and impairment of the migratory capacity to the Sargasso Sea for spawning and mortality when the infection acts in combination with other environmental stressors (Molnar et al., Reference Molnar, Szekely and Baska1991; Kennedy, Reference Kennedy2007; Palstra et al., Reference Palstra, Heppener, van Ginneken, Szekely and van den Thillart2007). The severity of the impact on eel health depends on the prevalence and intensity of A. crassus, which vary greatly in freshwater and brackish water sites (Dezfuli et al., Reference Dezfuli, Giari, Castaldelli, Lanzoni, Rossi, Lorenzoni and Kennedy2014; Giari et al., Reference Giari, Castaldelli, Gavioli, Lanzoni and Fano2021; Sayyaf Dezfuli et al., Reference Sayyaf Dezfuli, Maestri, Lorenzoni, Carosi, Maynard and Bosi2021) in relation to salinity, which tends to inhibit A. crassus, as it is considered a freshwater parasite (Lefebvre and Crivelli, Reference Lefebvre and Crivelli2012; Giari et al., Reference Giari, Castaldelli, Gavioli, Lanzoni and Fano2021). Thus, an abiotic parameter, along with other factors, could determine the degree of adverse effects of anguillicolosis in different TW and is a promising tool to control the disease (Lefebvre and Crivelli, Reference Lefebvre and Crivelli2012).

Metazoan parasites as bioindicators of environmental health in TW

Parasites can be useful and sensitive indicators of aquatic health (Lafferty, Reference Lafferty2008). There are both advantages and disadvantages in using parasites as health bioindicators in transitional ecosystems. Among the former, some parasites are easier to monitor than their hosts and provide integrated information on the presence, trophic position and abundance of all their hosts over a given period of time (Hechinger and Lafferty, Reference Hechinger and Lafferty2005; Marcogliese, Reference Marcogliese2005). This is especially true for parasites with complex life cycles. Among the disadvantages arises the high degree of temporal variability (both seasonal and interannual) in the parasite levels due to the changes in environmental conditions, which typically and naturally occur in brackish waters (Costa et al., Reference Costa, Marques, Alves, Gamito, Fonseca, Goncalves, Cabral and Costa2012).

There is contrasting evidence on the impact of habitat degradation on aquatic parasites (Sures et al., Reference Sures, Nachev, Selbach and Marcogliese2017). Indeed, stressful conditions tend to reduce heteroxenous endoparasites and have variable effects on monoxenous ectoparasites that could be favoured by a compromised immune response of the hosts or damaged by direct exposure to environmental alterations (Marcogliese, Reference Marcogliese2004). A recent study comparing the community of gill parasites in fishes of 2 estuaries in Brazil showed that parasite species richness and mean abundance of the most prevalent monogeneans are lower where there is significant anthropogenic pressure than that inside a protected area (Falkenberg et al., Reference Falkenberg, Golzio, Pessanha, Patrício, Vendel and Lacerda2019). The relation found between parasitological indices and water quality parameters supports the use of ectoparasites as environmental bioindicators (Falkenberg et al., Reference Falkenberg, Golzio, Pessanha, Patrício, Vendel and Lacerda2019). Cunha et al. (Reference Cunha, Domingues, Cunha and Nunes2021) confirmed monogeneans as sentinels of water quality, but their research in Amazon estuaries indicated a higher parasite abundance in the impacted area than in the reference area. Urbanization, measured through landscape and physicochemical factors, has been proven to influence parasite communities in the estuarine fish Fundulus heteroclitus, with the most significant effects detected in indirect life-cycle parasites (Alfieri and Anderson, Reference Alfieri and Anderson2019). The health of a brackish lagoon in Indonesia has been successfully measured by Palm and Rückert (Reference Palm and Rückert2009), applying a selection of 3 parasitological parameters (i.e. the prevalence of trichodinid ciliates, the ecto/endoparasite ratio and the endoparasite diversity), and this method is suggested to monitor tropical ecosystems characterized by high parasite biodiversity.

The use of fish parasites as bioecological indicators of ecosystem biodiversity and trophic complexity is growing in estuaries and lagoons (Huspeni et al., Reference Huspeni, Hechinger, Lafferty and Bortone2005; Culurgioni et al., Reference Culurgioni, Figus, Cabiddu, De Murtas, Cau and Sabatini2015). The high richness and abundance of helminth parasites, which require several host species and rely on predator‒prey interactions for transmission, are indicative of favourable environmental conditions not only for the parasites themselves but also for all the hosts involved in their life cycles (Culurgioni et al., Reference Culurgioni, Figus, Cabiddu, De Murtas, Cau and Sabatini2015). In the same way, the disappearance or decreased occurrence of a parasite in an ecosystem could suggest a decline in the density of a host due to environmental changes (Giari et al., Reference Giari, Ruehle, Fano, Castaldelli and Poulin2020, Reference Giari, Castaldelli, Gavioli, Lanzoni and Fano2021). A rich parasite community, especially if it includes specialist species, is associated with a diverse and abundant community of hosts; thus, parasites might represent biodiversity indicators in line with the hypothesis that a healthy ecosystem is rich in parasites (Hudson et al., Reference Hudson, Dobson and Lafferty2006; Hatcher et al., Reference Hatcher, Dick and Dunn2012). Helminth larval stages are especially sensitive to abiotic factors (Huspeni et al., Reference Huspeni, Hechinger, Lafferty and Bortone2005) and thus have been proposed to assess the environmental status in brackish systems in combination with standard techniques (Culurgioni et al., Reference Culurgioni, Figus, Cabiddu, De Murtas, Cau and Sabatini2015).

Approximately 50% of global wetland areas have been lost due to anthropogenic impacts, and thus, restoration projects have been developed to recover the health and sustainability of these vulnerable ecosystems (Meli et al., Reference Meli, Rey Benayas, Balvanera and Martínez Ramos2014; Morales-Serna et al., Reference Morales-Serna, Rodríguez-Santiago, Gelabert and Flores-Morales2019). Among other ecological variables (i.e. organic content, water parameters, abundance and diversity of plants and free-living animals) (Zhao et al., Reference Zhao, Bai, Huang, Gu, Lu and Gao2016), parasites might also be candidates to evaluate the efficacy of the restoration processes in TW.

The abundance of trematodes, which is low in degraded estuarine habitats, has been shown to increase following habitat restoration that attracts birds (Lafferty, Reference Lafferty1997). In the Terminos lagoon, one of the most relevant in the Yucatan Peninsula, a parasitological analysis of the fish Poecilia velifera has been performed 5 years after the beginning of a restoration programme (Morales-Serna et al., Reference Morales-Serna, Rodríguez-Santiago, Gelabert and Flores-Morales2019). Because no differences have been found between degraded and conserved sites in terms of parasite community and populations, the diagnostic value of parasites in assessing ecosystem health and progress in restoration appears to be limited in this case (Morales-Serna et al., Reference Morales-Serna, Rodríguez-Santiago, Gelabert and Flores-Morales2019).

In conclusion, can the analysis of parasite fauna be applied as a metric of the status of TW? Some studies say yes (Alfieri and Anderson, Reference Alfieri and Anderson2019; Falkenberg et al., Reference Falkenberg, Golzio, Pessanha, Patrício, Vendel and Lacerda2019), while others say no (Costa et al., Reference Costa, Marques, Alves, Gamito, Fonseca, Goncalves, Cabral and Costa2012; Morales-Serna et al., Reference Morales-Serna, Rodríguez-Santiago, Gelabert and Flores-Morales2019). The main reason for the conflicting responses and the lack of a standardized method is that host–parasite interactions are hardly predictable and not necessarily the same across all ecosystems, but parasites undoubtedly have enormous potential to provide information on environmental health.

TW are still understudied in this aspect and deserve particular attention due to their peculiarities (Falkenberg et al., Reference Falkenberg, Golzio, Pessanha, Patrício, Vendel and Lacerda2019). The open challenge in the use of parasites as bioindicators is selecting the best abiotic variables and the most promising parasite group/species or parasitological parameters that describe the ecological status of a specific transitional environment and its possible changes. This implies a detailed knowledge of the features and functioning of the site, including the parasites present and their life cycles, the biology of hosts and the temporal variations in the parasite level, which should all be taken into account to properly design this kind of study.

Impact of metazoan parasites of fish in TW on human health

Fish occurring in TW may be infected by some parasite species that are potentially harmful to humans and a risk to public health. The high demand for fish as a source of animal proteins, the change in dietary habits with a growing consumption of exotic and raw dishes, and the global trade of foodstuffs have contributed in recent decades to the increase and geographical spread of fish-borne zoonoses. The most relevant among these emerging diseases are anisakidosis, gnathostomiasis and capillariasis caused by nematodes and heterophyiasis caused by trematodes (McCarthy and Moore, Reference McCarthy and Moore2000; Broglia and Kapel, Reference Broglia and Kapel2011). The parasites responsible for the abovementioned diseases use marine, brackish water or freshwater fish as intermediate or transport hosts, and human infection occurs through the consumption of raw or undercooked fish containing larval stages in muscle (filet), body cavity or visceral organs (Broglia and Kapel, Reference Broglia and Kapel2011; Buchmann and Mehrdana, Reference Buchmann and Mehrdana2016; Shamsi, Reference Shamsi2019).

While in the past eating raw or lightly cooked fish was common only in countries with specific traditions (e.g. Japan), cosmopolitan and globalized food habits and the increase in international travel have recently led to a worldwide occurrence of cases of some fish-borne diseases, especially anisakidosis (Buchmann and Mehrdana, Reference Buchmann and Mehrdana2016; Shamsi, Reference Shamsi2019). In addition to Asian dishes, such as sushi and sashimi, which today are highly consumed in Western countries, traditional fish specialities from Europe (salted or smoked herring, marinated anchovies and fermented salmon) and Latin America (‘ceviche’ in Peru, Chile and Mexico and smoked fish in Brazil) may, if not adequately treated, be at risk of transmitting anisakid infection (Laffon-Leal et al., Reference Laffon-Leal, Vidal-Martinez and Arjona-Torres2000; Mercado et al., Reference Mercado, Torres, Munoz and Apt2001; EFSA, 2010).

Reports from TW of the main fish-borne parasites of public health relevance belonging to the genera Anisakis, Pseudoterranova, Contracaecum, Gnathostoma, Capillaria and Heterophyes are listed in Supplementary Table 1 with indication of the fish host and of the locality where they have been found. Members of Anisakis, Pseudoterranova and Contracaecum nematodes, all belonging to the family Anisakidae, show low specificity for their fish hosts and a high adaptability to environmental conditions, allowing the widespread occurrence in teleost populations and a worldwide distribution (Ángeles-Hernández et al., Reference Ángeles-Hernández, Gómez-de Anda, Reyes-Rodríguez, Vega-Sánchez, García-Reyna, Campos-Montiel, Calderón-Apodaca, Salgado-Miranda and Zepeda-Velázquez2020). The complex life cycle involving several hosts is illustrated by Buchmann and Mehrdana (Reference Buchmann and Mehrdana2016) for these 3 genera that contain species of particular clinical importance for human health. Although adults of several species of Contracaecum infect piscivorous birds in any aquatic environment, some congeneric species, together with representatives of most Anisakis and all Pseudoterranova species, are parasites of marine mammals, consequently having marine life cycles (Mattiucci and Nascetti, Reference Mattiucci and Nascetti2008). The presence of these species in estuarine fishes, where they can persist over time, is surely due to fish movements from or to the sea to feed on intermediate hosts or because infected intermediate hosts entered the estuary with tides.

In some geographic areas, the recent recovery of populations of marine mammals serving as final hosts (e.g. seals) seems to be linked to increasing infection levels in fish products (Mehrdana et al., Reference Mehrdana, Bahlool, Skov, Marana, Sindberg, Mundeling, Overgaard, Korbut, Strøm, Kania and Buchmann2014). Anisakid larvae ingested with raw fish by humans invade the alimentary canal and may induce the formation of eosinophilic granulomas, gastrointestinal symptoms and allergic reactions, including anaphylaxis (Broglia and Kapel, Reference Broglia and Kapel2011). Not only live larvae but also dead larvae can elicit allergic responses through parasite heat-resistant molecules, making anisakids particularly insidious and prevalent hidden allergens of public health concern (Audicana et al., Reference Audicana, Ansotegui, Fernandez de Corres and Kennedy2002; Rahmati et al., Reference Rahmati, Kiani, Afshari, Moghaddas, Williams and Shamsi2020). A recent systematic review explored the relationship between fish infection and human allergic anisakiasis and indicated the highest rate of allergic cases in Portugal and Norway (Rahmati et al., Reference Rahmati, Kiani, Afshari, Moghaddas, Williams and Shamsi2020). It is estimated that the number of human anisakid infections is underreported due to frequent misdiagnosis and will increase in the future (Shamsi, Reference Shamsi2019).

Several nematode species of Gnathostoma (including Gnathostoma binucleatum, Gnathostoma spinigerum and Gnathostoma turgidum) could cause disease, although most human cases are due to G. spinigerum being reported in Asia, Thailand and Japan and over the last 30 years also in Latin America from Mexico, Argentina, Peru and Ecuador (Nawa, Reference Nawa1991; Ogata et al., Reference Ogata, Nawa, Akahane, Diaz Camacho, Lamothe-Argumedo and Cruz-Reyes1998). In Mexico, gnathostomiasis represents an emerging public health problem (Rojas-Sánchez et al., Reference Rojas-Sánchez, Lamothe-Argumedo and García-Prieto2014). Gnathostoma parasites move in the body of infected people, causing fever, lack of appetite, nausea, vomiting, diarrhoea, abdominal pain and symptoms associated with their presence under the skin (Shamsi, Reference Shamsi2019). Recently, the possibility of human infections by Echinocephalus misdiagnosed as gnathostomiasis due to its morphological similarity to Gnathostoma has been reported in Australia by the consumption of freshwater fish (Jeremiah et al., Reference Jeremiah, Harangozo and Fuller2011; Shamsi et al., Reference Shamsi, Steller and Zhu2021).

Although human infections are generally assumed to result from eating raw freshwater fish (Ogata et al., Reference Ogata, Nawa, Akahane, Diaz Camacho, Lamothe-Argumedo and Cruz-Reyes1998), saltwater fish are known intermediate hosts in some regions (Waikagul and Diaz Chamacho, Reference Waikagul, Diaz Chamacho and Darwin2007). For example, in some states of Mexico, where human gnathostomiasis is one of the most important public health issues (Alvarez-Guerrero and Alba-Hurtado, Reference Alvarez-Guerrero and Alba-Hurtado2007), estuarine fish are not only commonly reported intermediate hosts for these parasites but also the most consumed and, consequently, the first suspects of being the main sources of human infection (Alvarez-Guerrero and Alba-Hurtado, Reference Alvarez-Guerrero and Alba-Hurtado2007; Díaz Camacho et al., Reference Díaz Camacho, de la Cruz-Otero, Zazueta-Ramos, Bojórquez-Contreras, Sicairos-Félix, Campista-León, Guzmán-Loreto, Delgado-Vargas, León-Règagnon and Nawa2008).

Capillariasis is a food-borne zoonosis recently discovered in the second half of the last century after an epidemic episode resulted in the death of infected people (Cross, Reference Cross1992). This intestinal disease is caused by the nematode Capillaria philippinensis, which is endemic in the Philippines, where the first cases were described, and Thailand but has also widespread to other countries outside Asia (McCarthy and Moore, Reference McCarthy and Moore2000). In the human intestine, female parasites produce embryonated eggs, causing autoinfection and fecal contamination of water (Shamsi, Reference Shamsi2019). The clinical signs are alteration of gastrointestinal functions, diarrhoea and vomiting, which can lead to chronic malabsorption and protein and electrolyte loss, with possible fatal outcomes (Cross, Reference Cross1992). Through experimental infection, several lagoon fish species have been proven to be natural intermediate hosts (Cross and Basaca-Sevilla, Reference Cross and Basaca-Sevilla1991).

Heterophyid trematodes are minute flukes infecting animals and humans. Human heterophyiasis is derived from the consumption of improperly cooked freshwater or brackish water fish, especially mullets and gobies, having metacercariae of the genus Heterophyes encysted in their muscle, and is considered a dangerous endemic disease in Mediterranean countries (Chai, Reference Chai, Motarjemi, Moy and Todd2014; Attia et al., Reference Attia, Elgendy, Abdelsalam, Hassan, Prince, Salaeh and Younis2021). Heterophyes heterophyes is transmitted in lagoons where euryhaline first- (i.e. snails) and second-intermediate hosts (Mugilidae) are abundant, and humans become easily infected after eating raw fish (Taraschewski, Reference Taraschewski1984). Infections occur in Africa (Sudan, Egypt, Tunisia) and are common in the Nile Delta, South Europe (Greece, Italy) and the Middle East (Saudi Arabia, Iran, Iraq, United Arab Emirates, Kuwait, Yemen), with an estimated 30 million people parasitized (Chai, Reference Chai, Motarjemi, Moy and Todd2014; Tandon et al., Reference Tandon, Shylla, Ghatani, Athokpam and Sahu2015). The main symptoms elicited by the trematodes in the small intestine are inflammation, diarrhoea, abdominal pain and weight loss (Chai and Jung, Reference Chai and Jung2017).

Most of the reports of human cases dealt in general with seafood- or freshwater-borne parasitic diseases, while data on fish-borne zoonoses specifically referring to aquatic transitional ecosystems are limited. Thus, it is difficult to quantify the risk deriving from TW compared to coastal and marine waters. Specific projects and studies on risk assessment in TW are needed at the local, national and international levels. However, the analysis of available literature suggests that some fish, such as mugilids, that are typical, widespread and abundant in many TW and may harbour parasites of medical importance could constitute a zoonotic threat (Chai and Jung, Reference Chai and Jung2017). This holds true especially in ill-developed communities where lagoons and estuaries often support important fisheries and aquaculture activities and represent a crucial food source in the absence of tools for control (Harrison, Reference Harrison, Fischer, Krupp, Schneider, Sommer, Carpenter and Niem1995; Froese and Pauly, Reference Froese and Pauly2004; Fajer-Ávila et al., Reference Fajer-Ávila, García-Vásquez, Plascencia-González, Ríos-Sicairos, Parra and Betancourt-Lozano2006). More information about the environmental factors that can influence the parasite prevalence, movements of the fish hosts or their preference for specific zones (more or less saline) determining seasonal trends or the spatial distribution of infection (Rolbiecki and Rokicki, Reference Rolbiecki and Rokicki2002) could help assess and reduce the sanitary risk in TW.

A ‘one-health’ approach integrating medical aspects with consumer, aquatic animal and environmental/ecological aspects is the way to tackle fish-borne parasitic diseases and find potential solutions (Shamsi, Reference Shamsi2019).

Economic impact of metazoan parasites of fish from TW

Brackish waters, especially coastal lagoons, are historically exploited for fish harvesting and production (Cataudella et al., Reference Cataudella, Crosetti and Massa2015). Edible fish of commercial importance harbour numerous parasite species, and some of them could affect fisheries and the market value of fish (Lafferty, Reference Lafferty2008). On the other hand, fishing, especially if intensive, could reduce parasitism, as suggested by the application of mathematical models and the analysis of literature data (Wood et al., Reference Wood, Lafferty and Micheli2010). In contrast, fish farming offers ideal conditions for high pathogen transmission and abundance, especially for parasites with direct life cycles (i.e. Monogenea and Crustacea), and often suffers from significant economic losses due to parasitic outbreaks (Shinn et al., Reference Shinn, Pratoomyot, Bron, Paladini, Brooker and Brooker2015). The economic impact of parasites is more evident for farmers than for fishers (Lafferty et al., Reference Lafferty, Harvell, Conrad, Friedman, Kent, Kuris, Powell, Rondeau and Saksida2015). Therefore, it is not surprising that most of the analyses of the costs associated with parasitic diseases focus on fish farms (Abolofia et al., Reference Abolofia, Asche and Wilen2017; Tavares-Dias and Martins, Reference Tavares-Dias and Martins2017; Peterman and Posadas, Reference Peterman and Posadas2019; Fernández Sánchez et al., Reference Fernández Sánchez, Le Breton, Brun, Vendramin, Spiliopoulos, Furones and Basurco2022; Radwan, Reference Radwan2022). Regardless, in both situations (i.e. activity with wild and farmed fish), the multiple factors that influence infection make it difficult to calculate the economic damage effectively attributable to parasites, and a precise estimation of the costs would require information on morbidity and mortality, which is not always available or known (Shinn et al., Reference Shinn, Pratoomyot, Bron, Paladini, Brooker and Brooker2015; Tavares-Dias and Martins, Reference Tavares-Dias and Martins2017). However, some examples are available, such as losses up to 12–15% in profit margin per tonne of fish caused by ectoparasites (especially monogeneans) in farms, based on the price of Nile tilapia in Mexico (Paredes-Trujillo et al., Reference Paredes-Trujillo, Velázquez-Abunader, Papiol, Rodolfo and Vidal-Martínez2021).

From an economic point of view, parasitic diseases can be detrimental by reducing biological productivity due to increased mortality, slower growth or limited reproduction, with the consequent decrease in potential catch and/or by impairing meat quality, appearance or security with consequent reduction of appeal for consumers, commercial value and marketability (Lafferty et al., Reference Lafferty, Harvell, Conrad, Friedman, Kent, Kuris, Powell, Rondeau and Saksida2015).

Digenetic trematodes have been reported to produce economic losses in aquaculture in terms of reducing fish growth/weight and increasing mortality (Crotti, Reference Crotti2013). Additionally, ectoparasites, such as Monogenea and Crustacea, frequently cause localized epizootics and serious damage to the aquaculture industry (Cone, Reference Cone and Woo1995) and sometimes reduce the production of economically important fish in coastal lagoons (Aladetohun et al., Reference Aladetohun, Sakiti and Babatunde2013). However, ectoparasite occurrence in wild fishes of TW does not necessarily have severe or lethal outcomes, as supported by several examples. In the estuary of Patos lagoon (Brazil), whitemouth croaker, Micropogonias furnieri, harbours 4 parasite species, Gauchergasilus euripedesi (Copepoda), Myzobdella uruguayensis (Hirudinea), Neomacrovalvitrema argentinensis and Neopterinotrematoides avaginata (Monogenea), but the absence of correlation between parasite abundance and host health indices suggests that the found parasite levels are tolerable (Velloso and Pereira, Reference Velloso and Pereira2010). Mullet, Mugil liza, a commercially important fish exploited by fishermen in an estuary system on the northern coast of Rio Grande do Sul (Brazil), was infected by several species of ectoparasites without clinical signs of disease and had the same length–weight relationship as uninfected specimens (Mentz et al., Reference Mentz, Lanner, Fagundes, Sauter and Marques2016). A gill parasitic isopod affecting ~40% of sand smelt Atherina boyeri in 2 Greek lagoons does not constitute a significant threat to fish survival (Leonardos and Trilles, Reference Leonardos and Trilles2003). A study comparing the infection levels in sea bream, Sparus aurata, and sea bass, Dicentrarchus labrax, sampled from 2 different cage farms and from a lagoon in Greece showed a higher prevalence of ectoparasites but lower intensity and pathogenicity in the latter (Vagianou et al., Reference Vagianou, Athanassopoulou, Ragias, Di Cave, Leontides and Golomazou2006). This result was probably linked to the lower fish density and stress level in the lagoon than in the semi-intensive systems.

As seen in the section dedicated to medical impact, Anisakis worms, which infect many marine edible fishes, pose a risk for human health, and their appearance in muscle or viscera can cause rejection by purchasers (Bao et al., Reference Bao, Pierce, Strachan, Pascual, González-Muñoz and Levsen2019). European Union regulations and international guidelines from FAO and WHO require that the fishery production chain monitors and ensures food safety (e.g. performing the visual inspection of fish), but the limits and low efficiency of the control procedures have been pointed out (Levsen and Lunestad, Reference Levsen and Lunestad2010; Llarena-Reino et al., Reference Llarena-Reino, González, Vello, Outeiriño and Pascual2012). The distrust of consumers towards fishery products due to Anisakis, confirmed by a study investigating the opinions of Spanish consumers, may thus negatively impact the seafood business (Bao et al., Reference Bao, Pierce, Strachan, Martínez, Fernández and Theodossiou2018). Additionally, Pseudoterranova decipiens larvae can devalue fish (cod, herring, pollock), causing cosmetic problems to flesh in addition to concern for consumer health (McClelland, Reference McClelland2002).

To our knowledge, only a very few estimates of economic losses due to fish parasites have been carried out at TW sites and are provided by Shinn et al. (Reference Shinn, Pratoomyot, Bron, Paladini, Brooker and Brooker2015), who examined the major marine and brackish aquaculture industries worldwide. For instance, the economic costs of the protozoan Trichodina sp. and the digenean Furnestinia echeneis infections from Bardawil lagoon (Israel) were calculated (see Shinn et al., Reference Shinn, Pratoomyot, Bron, Paladini, Brooker and Brooker2015) according to the mortality data (~40–50% of the stock) of S. aurata fingerlings reported by Paperna et al. (Reference Paperna, Colorni, Gordin and Kissil1977). No economic studies are available for wild populations where the estimate of impact is certainly more difficult and the losses lower than for cultured fish.