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Review

Diversity of Parasitic Animals in Hypersaline Waters: A Review

by
Yuliya Kornyychuk
,
Elena Anufriieva
* and
Nickolai Shadrin
A.O. Kovalevsky Institute of Biology of the Southern Seas of RAS, 2 Nakhimov ave., 299011 Sevastopol, Russia
*
Author to whom correspondence should be addressed.
Diversity 2023, 15(3), 409; https://doi.org/10.3390/d15030409
Submission received: 13 February 2023 / Revised: 6 March 2023 / Accepted: 8 March 2023 / Published: 10 March 2023
(This article belongs to the Special Issue Biodiversity and Ecology Research in Russia: Recent Advances and Future Trends)
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Abstract

:
Hypersaline waters are unique polyextreme habitats, where the salinity limits species richness. There are main patterns of a relationship between salinity and the species richness of free-living aquatic animals, but for parasitic organisms, general regularities have not yet been established. There are quite numerous data on parasites in hypersaline waters worldwide; however, they have not been summarized before. This review tries to fill this gap by summarizing the available data. All parasites, 85 species and forms, found in hypersaline waters belong to five phyla: Platyhelminthes, Nematoda, Acanthocephala, Cnidaria, and Arthropoda. Platyhelminthes are the most diverse phylum with the highest species richness in class Cestoda. Most species were noted in hypersaline waters with a salinity of no more than 100 g·L−1. The total number of parasitic species decreases exponentially with an increase in salinity. The number of free-living animal species inhabiting waters with a salinity from 35 to 210 g·L−1 is approximately 12 times higher than that of parasitic ones in all intervals of this salinity range. Salinity influences parasite richness and composition in two ways—directly and through the availability of hosts. Free-living crustaceans were hosts of most parasite species in hypersaline waters. Artemia spp., the most halotolerant animals, are an intermediate host for 22 species and unidentified forms of parasites.

1. Introduction

Life, including animals, exists in aquatic environments on Earth in a wide range of salinities, from approximately zero to more than 400 g·L−1 [1,2,3]. Salinity is a major environmental factor determining an animal species’ richness in aquatic ecosystems [3,4,5]. Hypersaline waters (salinity > 35 g·L−1) are unique polyextreme habitats, where not only salinity itself limits species richness. Salinity also influences different abiotic parameters making them less comfortable for animal life [3,5]. It worsens oxygen and thermal regimes, increasing the density and viscosity of an environment, which results in a greater energy demand for animal movement, etc.
The main patterns of a relationship between salinity and the species richness of free-living aquatic animals have been established for such unique ecosystems [1,3,6]; in a salinity range from 35 to 400 g·L−1, total species richness monotonically decreases. As for parasitic organisms, such general regularities are not yet established. Salinity, like every other environmental factor, can influence parasites and their composition in two ways: directly and through host organisms. The diversity of hosts, as well as their states, may be more important factors than environmental salinity itself. Parasites are an essential part of every ecosystem [7] and play different roles affecting the fitness of their hosts, manipulating their behavior, regulating host population dynamics, impacting predator–prey interactions, and influencing some ecosystem services such as supporting water bird diversity [8,9,10,11,12,13,14], and, in general, could be used as an indicator of ecosystem health and wellness [15]. Therefore, to better understand the influence of salinity on the whole ecosystem’s structure and functioning, we need to make some generalizations on a parasite richness response to a salinity change.
There are quite numerous data on the findings of parasites in hypersaline waters worldwide; however, they have not been summarized before. The main goal of this review study was to fill this gap by summarizing the available data.

2. Materials and Methods

This review article is based on published data, searched for using various sets of keywords, such as “hypersaline + parasite”, “hyperhaline + parasite”, “hypersaline or hyperhaline + Cestoda”, and “hypersaline or hyperhaline + Trematoda”, using different search engines, such as Scholar Google, ResearchGate, eLibrary, Scopus, Web of Science, and ScienceDirect. In total, more than 75 articles and books comprising original data on parasites inhabiting hypersaline waters were summarized to compile parasite–host annotated checklists, including species (as a preferred taxonomic unit) and unidentified or undescribed “forms”. The locations and the parasite developmental stages are given as stated by the authors.
All parasites found in the hosts permanently inhabiting hypersaline waters (excluding those in widely migrating water birds) were divided into three ecological groups according to the duration of exposure to abiotic impact at the appropriate developmental stages:
-
Group I: Ectoparasites with a direct life cycle; all their life stages are directly affected by the hypersaline environment;
-
Group II: Endoparasitic developmental stages not directly affected by the environment but having younger free-living development stages in the lifeir cycle;
-
Group III: Endoparasitic adults and pre-adults (in definitive hosts) under nondirect abiotic environmental impact (maritae of Trematoda and adults and pre-adults of Cestoda, Nematoda, and Acanthocephala), that have more endoparasitic younger stages than the intermediate host, and were transmitted to definitive hosts via food chains. A definitive host eats an intermediate one.
The taxonomic position of the parasites is given as in [16,17,18,19,20] and the World Register of Marine Species (WORMS).
To analyze the collected data, the authors applied a standard regression analysis [21]. The parameters of the regression were calculated using Equation (1), and the correlation coefficients were calculated in the program MS Excel 2010.

3. Results and Discussion

3.1. Diversity of Parasites Occurring in Hypersaline Waters

All parasite species found in hypersaline waters belong to five phyla: Platyhelminthes, Nematoda, Acanthocephala, Cnidaria, and Arthropoda (Table 1). The total number of parasite species and forms includes 85 parasite species, and Platyhelminthes (flatworms) is the most diverse phylum, with the highest species richness in class Cestoda (Table 1).
All species listed in Table 1 were divided into three ecological groups, the characteristics of which are given above.
Group I
Monogeneans (13 species and unidentified forms) are known from the gills and skin of fish hosts inhabiting three hypersaline water bodies (Table 1). The monogenean fauna in fish inhabiting the hypersaline Bardawil lagoon, where the salinity varies between 38 and 100 g·L−1 [63,64], was lower than that from appropriate fish hosts from Mediterranean waters adjacent to the lagoon with lower salinity [22]. For example, Ancyrocephalus salinus infecting fish species Aphanius dispar and Hemirhamphus far, as well as Lamellodiscus spp., were found on fish Crenidens crenidens in the Mediterranean and Red seas. However, these parasites were not found in those hosts in the lagoon. Nevertheless, the dispersal stages of viviparous monogeneans seem to be resistant to high salinity; living Gyrodactilus salinae were found on its fish host (Aphanius fasciatus) gills under a salinity of 35–65 g·L−1 throughout the year [24].
Crustaceans (five species and forms) were registered on fish in hypersaline waters; all of them are only known from one of the hypersaline lagoons in Western Asia (Table 1).
In group I, parasites are directly affected by the abiotic environment in hypersaline waters at all life stages, and they were presented by Monogenea and Crustacea at a salinity of up to 75 g·L−1 (Table 1). In Monogenea, there are ten species and three forms only identified at the generic level (Table 1). Among them, the greatest species richness is in the family Diplectanidae, genera Diplectanum and Gyrodactylus (Table 1). In parasitic Crustacea, four species and one unidentified form were found (Table 1).
Group II
Twenty-two species and forms of digenetic trematodes are known to infect fishes and only one mollusk species in a hypersaline environment (Table 1).
Metacercaria of unidentified Heterophyidae caused heavy fish infections, especially in grey mullets (up to 100% prevalence with up to 6000 cysts per gram of muscles) [16]. Pygidiopsis genata metacercaria, encysted on the outer wall of the stomach, in the kidney, spleen, liver, muscle, and mesenteries tissues were noted in the cichlid fish Coptodon guineensis inhabiting hypersaline waters in Sebkha Imlili salt flat [27].
Cerithideopsis californica, the Californian hornsnail, is one more mollusk known as a first intermediate host for 17 species and unidentified forms of Trematoda in hypersaline waters (salinity around 60 g·L−1) (Table 1). Water birds appear to be definitive hosts for all of them, and the variety of second intermediate hosts is rather broad (crustaceans, gastropods, pelecypods, and fishes) [28,29,30].
Cestoda cysticercoids, completing their development in aquatic birds, are the most common and diverse parasite taxon (29 species and unidentified forms) in hypersaline water bodies of Europe and Asia (Table 1). Those water bodies provide habitats for feeding and nesting of different water birds, such as flamingos, gulls, and avocets (host species diversity may change due to the birds’ migrations) [31,65]. One of the cestode species, Flamingolepis liguloides (larvae in intermediate host Artemia), is known from water bodies with extremely high salinity above 210 up to 320 g·L−1 (see Table 1), which means cestode eggs can survive even in such extreme conditions.
Myxosporidian spores were found in hypersaline waters and two of their species in grey mullets and Dicentrarchus fishes in the hypersaline Bardawil lagoon (Table 1). In addition to free-living nematodes [66,67], parasitic Nematoda also inhabit a hypersaline environment (Table 1). Acuariidae larvae were noted in anostracan crustacean Artemia from the hypersaline (105–150 g·L−1) Great Salt Lake [31]. In the hypersaline Mar Menor lagoon, Contracaecum sp. larvae were found in the muscles of the European eel Anguilla anguilla [62]. Due to the water and fish exchange between the lagoon and the Mediterranean Sea through natural openings or passages, we can assume that the host fish were infected by nematode larvae in the adjacent regions of the sea.
Group 2 includes more species than group 1. Among them, parthenogenetic generations of four species, one form was identified at the generic level, one at the family, and metacercarii (one Heterophyidae species) belonged to Trematoda (Table 1). Cestoda is a most diverse taxon; its cysticerci of 23 species and 4 were only identified to a genus, as well as plerocercoids of one species were found (Table 1). Myxosporea spores of two species and one only identified to a genus, Nematoda, and two nonidentified species were also noted (Table 1). Parasites of this group were in the endoparasitic developmental stages, which were not directly affected by the environment. However, previous development stages in the life cycle were free living. The highest salinity limits for findings of parasites in this group varied from 51 to 220 g·L−1 (Table 1).
Group III
Two species of Acanthocephala are known from hypersaline waters (Table 1).
The adult Neoechinorhynchus (Neoechinorhynchus) agilis (Rudolphi, 1819) Van Cleave, 1916, was a common parasite in the grey mullet from Lagoon Bardawil, while just eaten cystacanths and preadults were found in the guts of a wide range of fish hosts there, mainly juvenile fish [22]. As N. agilis is known to be strictly specific to Mugilidae, and Mugil cephalus among them [68], we may assume that the worms cannot mature in other fish hosts than Mugilidae. Due to the different Crustacea being intermediate hosts of N. agilis, the fish could not be infected in the lagoon but in adjacent Mediterranean waters [22]. Then, the parasite was mechanically transported in the hypersaline lagoon during host migrations. Thus, these acanthocephalans in their adult or preadult stage can hardly be considered a permanent component of hypersaline ecosystems; the same could be said also for other helminths found in fish of the Bardawil and Mar Menor lagoons [25,26,62].
Adult Acanthogyrus (Acanthosentis) tilapiae that were found parasitized the cichlid fish host, Coptodon guineensis, and most halotolerant among copepods Cletocamtpus retrogressus [1] or high halotolerant Cyprideis torosa (Ostracoda) supposed to be its intermediate hosts [27]. The acanthocephalan likely switched to this fish host from freshwater tilapia when this Sebkha formed [27].
Nine parasite species in group III belonged to Trematoda (maritae of five species and one only identified to a genus), one species to Acanthocephala, one to Cestoda, and two to Nematoda (one identified to a genus). The salinity in the places of their findings varied from 43 to 75 g·L−1 (Table 1). We can assume that a host presence (i.e., fish) is a more important factor than a direct impact of salinity on parasites of this taxon. The upper limit of the water salinity for Acanthocephala and parasitic Crustacea species was 75 g·L−1 and 150 g·L−1 for Nematoda. Among parasitic animals, Cestoda is the most halotolerant, and their larvae are known even from hypersaline lakes with a salinity above 200 g·L−1 (Table 1).
Most species were noted in hypersaline waters with a salinity of no more than 100 g·L−1. The total number of parasitic species decreases exponentially with an increase in the salinity (Figure 1); this relationship can be approximated by the equation (R = 0.959, p = 0.0001):
Y = 131.4e−0.015X,
where Y is the number of species, which have a upper salinity limit of X.
Between the number of free-living animal species and their upper salinity limit, the same relationship was also found before [3,69], which can be described as (R = 0.992, p = 0.0001):
Y = 1212.4e−0.013X,
A comparison of Equations (1) and (2) shows that the exponential coefficients in both equations were very close, 0.015 and 0.013, respectively. Therefore, we may conclude that this monotonic decrease in the species diversity of parasitic animals with an increase in salinity to its value of 210 g·L−1 can be explained, first of all, by a decrease in the number of free-living species, potential hosts for parasites. The number of free-living animal species inhabiting waters with a salinity from 35 to 210 g·L−1 [3] is approximately 12 times higher than that of parasitic ones in all intervals of this salinity range [69]. However, many free-living animal species exist in waters with a salinity higher than 210 g·L−1 [1,3], but the only parasite species, F. liguloides larvae (Cestoda), is known from lakes with a salinity greater than 210 g·L−1. As previously shown, predator animals disappear in ecosystems if the salinity exceeds 100–150 g·L−1 [5,70,71]. This is explained using the balance energy approach [72]; the energy costs for the processes of acclimation to high salinity are so large that the efficiency of using the assimilated energy for growth is significantly reduced. As a result, the production output created by primary consumers is so small that it is not enough to meet the high energy needs of higher-order consumers. In ecosystems, parasites play roles of secondary or tertiary consumers as predators. So, it is highly probable to explain their disappearance in ecosystems in the same way as for free-living predators.
Most parasites that inhabit a hypersaline environment belong to groups II and III (Table 1). They have complex life cycles, i.e., they consistently infect a host of different taxa, and parasitic and free-living stages may alternate. Among different life cycle stages, the endoparasitic ones (larvae, spores, pre-adults, and adults) are the most common component of hypersaline ecosystems consisting of more than 70% of all revealed species and unidentified forms (Table 1). All parasites with direct life cycles in hypersaline waters belong to Monogenea and Copepoda, infecting fish only (see Table 1).
The life cycles of Trematoda, Cestoda, Nematoda, and Acanthocephala are complex and based on ecosystem food chains, but host organisms infected with monogeneans, copepods, and myxosporeans contact directly with the invasive stages of these parasites [73,74]. In the life cycles of these parasitic organisms, there are free-living dispersal stages that are directly affected by abiotic environmental factors and parasitic stages (larvae and mature individuals). For parasitic stages, the interaction with the environment is indirect and mediated by hosts. The “internal” environment of the host organism directly influences endoparasites.
Parasites with complex life cycles infect sequentially individuals of several different intermediate and definitive host species; and the parasitic and free-living stages alternate. Parasites with a direct life cycle have a free-living infective stage releasing from infected hosts and infecting another host specimen of the same species [73,74]. It is essential that actively migrating hosts as fish and birds can carry out parasites acquired elsewhere, and so, they are a transient component in local food webs. Thus, the parasites, carried by them, do not necessarily complete the life cycles within hypersaline waterbodies. More than 30% of the total number of species and unidentified forms of the parasites registered in hypersaline ecosystems are endoparasitic larvae in intermediate hosts permanently inhabiting these extremal biotopes (see Table 1). Adult stages reported from such ecosystems infect, as a rule, water birds and some fishes temporally inhabiting these biotopes (this is especially true concerning water birds).
Parasitic species with complex life cycles prevail in hypersaline ecosystems, but there are also parasites with direct life cycles having a free-living infective stage (Table 1). This cannot suggest self-evident salinity resistance of appropriate free-living parasite life stages. There are data on the real salinity resistance of parasites; for example, digenean Euhaplorchis californiensis cercariae were found to survive and stay active at a salinity of 40 g·L−1 [75]. Experimental data relating to the salinity tolerance of cercariae of Cryptocotyle sp., Levinseniella brachysoma, and Maritrema subdolum are available also [76]. Experiments with Maritrema novaezealandensis cercariae showed that the Trematoda free-living larvae output and survival increased with a salinity growth from 25 to 40 g·L−1, while their infectivity was not affected [77]. The life cycles of some parasitic hydrobionts (so-called autogenic species) could fully complete in a hypersaline water body. For example, in the same hypersaline lagoon (salinity of up to 70–75 g·L−1), the mollusk Pirenella conica was the first intermediate host, and mullets, the definitive host, infected with Heterophyidae metacercariae [22]. In the African salt flat Sebkha Imlili, with a salinity of up to 75 g·L−1, the gastropod Ecrobia ventrosa was the first intermediate host for P. genata, which then infected fish hosts Coptodon guineensis at the metacercarial stage [27].

3.2. Hosts of Parasites

Free-living crustaceans were hosts of most parasite species in hypersaline waters (Figure 2). Artemia spp. are among the most halotolerant animals withstanding a salinity range from 4–5 to 340–360 g·L−1 [78,79]. Among animals, they have the most perfect osmoregulatory mechanism [63] due to the fact that the salinity of internal body solutions varies in a narrow range from 45 to 55 g·L−1 [80,81]. Being the main consumer of phytoplankton in hypersaline waters and reaching a high abundance (up to more than 80 thousand ind. m−3), Artemia spp. play a key role in these ecosystems [71,82,83,84]. So, it is not surprising that Artemia spp. are an intermediate host for 22 species and unidentified forms of parasites (Table 1).
The specific nature of parasites as a biological phenomenon is the duality of their habitat as internal host environment and a host surrounding one [7,9]. The differences in the salinity of Artemia body solutions and water body is a good illustration of this. In this regard, it should probably be remembered that there are two mechanisms of osmoadaptation in free-living animals that are potential hosts of various parasites [4,71]. There are animals–osmoregulators, in which salinity fluctuations in body fluids occur within very narrow limits. At the same time, there are animals–osmoconformers, where the salinity in body fluids is not regulated and corresponds to that in the environment. Among the most halotolerant animal species of one taxon, for example, copepods, there are species in which one or another osmoadaptation mechanism is realized [1,72]. Unfortunately, for the majority of free-living animal species, it has not yet been established which of these two mechanisms is implemented, which makes it impossible to compare the infestation of animals by different parasites with different mechanisms of osmoadaptation. In analyzing the effect of salinity on the distribution of parasites, it is necessary to know the response to the salinity of the parasite and the host. This issue is probably most acute in the case of osmoconformer hosts. There are data on this issue that suggest a smaller range of halotolerance in parasites compared to their hosts [77]. In general, the issue is still not studied in hypersaline habitats.
Artemia spp. can be regarded as key hosts in hypersaline ecosystems [34,35]; for example, in hypersaline waters, avian cestode larvae were found to be extremely rare in another crustacean taxon (Table 1). Flamingolepis liguloides (Cestoda, Hymenolepididae) cysticercoids are the most common parasite of Artemia spp., as this host are a major component in the diet of definitive hosts, such as flamingos and several other water birds [34,35,65,85]. In mollusks inhabiting hypersaline waters, only digenean are known, but rather diverse parasite fauna have been registered in fishes (Figure 2; Table 1).

3.3. Host–Parasite Interactions in Hypersaline Waters

Interactions between parasites and host organisms are usually expected to result in negative effects on infected host individuals. Nevertheless, instead of inducing host mortality, parasites often cause sublethal effects (castration or reduced reproduction, changes in growth rates both in a positive and negative direction, worsening condition, changing filtration or grazing rate, morphological and behavioral traits, etc.) in their hosts [73,84,86]. They also may manipulate their host behavior changing the host food spectrum, diurnal activity, taxes, or altering the host phenotype [34,87,88]. They often decrease food intake and the efficiency of its assimilation [86].
The parasitism of Trematoda parthenogenetic life stages can increase the length of the California horn snail Cerithideopsis californica (Haldeman, 1840), which may live in salinity up to 60 g·L−1, stunting the growth of juvenile snails but to a lesser degree than of adult snails [29]. The Trematoda parthenitae also influence the survival of C. californica, increasing snail mortality rates under hypoxia, especially in conjunction with high water temperature [30]. The parasitism of digenean parthenitae can reduce the reproductive output of a C. californica population, cause differential mortality of parasitized mollusks, and provide a competitive advantage to unparasitized snails [89].
Digenean metacercariae of Heterophyidae in the tissue of fish inhabiting hypersaline lagoons cause so-called “black spot disease” in their fish, second intermediate host [22,27]. Infected fish surround the metacercaria by black pigmented melanin, inducing an immune and antioxidant response in host epithelial mucus and liver [90]. It is worth noting that species belonging to this Trematoda family are often zoonotic and dangerous for birds, mammals, and humans [91].
The invasion of cestode larvae with a relatively low body density increases the time spent by host crustaceans at the water surface [34]. The phytoplankton concentration is higher here, reducing the time spent by Artemia in the lower part of the water column and increasing its diet [34]. In addition, cestode larvae infection can change the phototaxis of their intermediate hosts, Artemia spp. and gammarids; this leads to changes in the vertical distribution of hosts in the water column [88,92]. The most notable feature of Artemia infected with cestode larvae is their red coloration [34,88,92,93,94,95] due to the fact of higher total lipid levels linked to carotenoid pigments [95]. Red-colored infected brine shrimps are better visible to birds eating them several times more efficiently than uncolored ones [96], thus promoting an increase in phytoplankton abundance. The infection of Artemia spp. by cestode larvae Confluaria podicipina lowers host immunity but increases the glycogen, carotenoids, and hemocyanin concentrations in their bodies [34,88]. This can also change host behavior, food and oxygen consumption, and reduce the rate of host reproduction [34,88].
Pleurocerci of cestodes Flamingolepis liguloides and Anomotaenia tringae strongly decrease the feeding rate in Artemia parthenogenetic populations constricting the host gut; nevertheless, F. liguloides do not affect the feeding of Artemia franciscana, possibly due to the lower prevalence in this host [35]. However, Artemia infected by cestode pleurocercoids of Hymenolepididae survive better than uninfected ones, and cestode larvae did not affect the brine shrimp growth rates and its definitive size [95]. The infection of cysticercoids F. liguloides and Wardium stellorae did not affect the host respiration rate of Artemia [97]. F. liguloides larvae parasitism may be not useless for the intermediate host. It made Artemia more resistant to arsenic pollution even under increased temperatures that raised the levels of catalase and glutathione reductase activity, a level of host-protecting antioxidants and hemoglobin [34,93,94,95,98]. Cestode larvae reduced the feeding activity of infected Artemia, leading to a decrease in the intraspecific competition of infected brine shrimps with uninfected conspecific ones for food [31,99]. Infected brine shrimp females are less fertile than uninfected ones [57] or even castrated [50,95].
Ectoparasitic monogeneans on fish, inhabiting hypersaline lakes, were found to be able to damage the gills and skin of fish hosts and, thus, depress their respiration rates and break their osmoregulation; nevertheless, this parasitizing of monogeneans didn’t course fish juvenile mortality [23].
Parasites play important ecosystem roles—regulatory, protective, and stabilizing, as well as redistributing and speed of matter and energy fluxes in ecosystems [7,9,11,89,100,101]. In this, trematodes lead among the parasites due to the fact of free-living dispersal stages in their complex life cycles [8,9,11,100]. Thus, parasite-induced ecosystem effects exist in aquatic ecosystems including hypersaline.
Being the most common effects of parasitism, a reduction of food intake and nutrient efficiency can alter the interaction strength between primary and secondary consumers [102], as well as between secondary and tertiary consumers [103]. The decreased food intake has consequences, such as reduced respiration and movement, growth, and energy storage of infected Artemia, the “key host” of hypersaline ecosystems, which could affect different levels of ecological organization [34,35]. Among those, the decrease in the Artemia population diet results in an increase in phytoplankton abundance [35,71,85]. Reduction of the Artemia diet can slow a mercury flux from the water column to bottom sediments [104]. Lower feeding rates of infected Artemia may benefit uninfected ones by reducing competition for food; this provides a competitive advantage to individuals more resistant to cestode larvae infection [34,35].
The presence of the abovementioned cestode larvae in the hypersaline biocenoses can create a so-called “cascade effect” changing the interaction between different members of communities, as well as whole matter and energy flows through the food webs. Parasites not only mediate the trophic interaction between predators and prey but may also act as one of prey themselves, meaning, first of all, free-living infective stages such as cercariae [8,9,11,100,101] or encysted adolescaria [105]. Probably, the consumption of infective stages may significantly contribute to the diet of predators, and this issue has not been studied yet in hypersaline waters. The parasite-mediated alterations of energy and food flows are largely unknown. Therefore, they are also attractive topics for future studies to develop a deeper understanding of ecosystem functioning in hypersaline environments.

4. Conclusions

Parasites in hypersaline waters of the world are presented consisting of 85 parasite species and unidentified “forms” belonging to five phyla: Nematoda, Acanthocephala, Cnidaria (Myxosporea), Arthropoda (parasitic Copepoda), and Platyhelminthes (Monogenea, Trematoda, Cestoda), which is a most diverse taxon with the highest species richness in class Cestoda parasitizing predominantly Artemia spp.
There exist many potential hosts in hypersaline waters that have not been studied thoroughly concerning their parasites. Hence, the presently known diversity of parasites in hypersaline waters is highly likely to increase with research efforts in the future. Taking into account the important multifaced role of parasites in aquatic ecosystems, including hypersaline ones, scientists should pay more attention to this issue. Future research is necessary on parasite life cycles and the specificity, diets, and osmoadaptations of hosts, as well as the role of birds, including migration, to obtain a better knowledge of the richness and composition of parasites in hypersaline water bodies.

Author Contributions

Conceptualization, N.S. and E.A.; formal analysis, N.S., E.A., and Y.K.; methodology, N.S. and Y.K.; supervision, E.A.; writing—original draft, Y.K. and N.S.; writing—review and editing, N.S., E.A. and Y.K. All authors have read and agreed to the published version of the manuscript.

Funding

The literature search and quantitative data analysis were conducted in the framework of the state assignment of A.O. Kovalevsky Institute of Biology of the Southern Seas of RAS (№ 121041500203-3); the interpretation of the results was conducted in the framework of the state assignment of A.O. Kovalevsky Institute of Biology of the Southern Seas of RAS (№ 121030100028-0).

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Data will be made available upon request.

Conflicts of Interest

The authors declare no conflict of interest.

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Figure 1. The number of parasites species depending on the upper limit of the habitat’s salinity.
Figure 1. The number of parasites species depending on the upper limit of the habitat’s salinity.
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Figure 2. Parasite richness (number of species and unidentified forms) among host taxa in hypersaline waters.
Figure 2. Parasite richness (number of species and unidentified forms) among host taxa in hypersaline waters.
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Table
Table 1. Parasitic animal species found in hypersaline waters around the world.
Table 1. Parasitic animal species found in hypersaline waters around the world.
Parasite/Life StageHostS, g·L−1LocalityReference
Group I *
Phylum PLATHELMINTHES
Class Monogenea
Fam. Calceostomatidae
Parona & Perugia, 1890
Calceostoma calceostoma (Wagener, 1857)		Pisces:
Argyrosomus regius (Asso, 1801)		50–75Bardawil lagoon (Sinai Peninsula), Egypt (Western Asia)[22]
Fam. Diplectanidae
Montichelli, 1903
Diplectanum aculeatum Parona & Perugia, 1889		Umbrina cirrosa (Linnaeus, 1758)
Diplectanum simile Bychowsky, 1957A. regius, U. cirrosa
Diplectanum aequans (Wagener, 1857)Dicentrarchus labrax (Linnaeus, 1758), D. punctatus (Bloch, 1792)
Lamellodiscus echeneis (Wagener, 1857)Sparus aurata Linnaeus, 1758
Pseudorhabdosynochus cf. epinepheli (Yamaguti, 1938) Kritsky & Beverley-Burton, 1986Epinephelus aeneus (Geoffroy Saint-Hilaire, 1817)
Fam. Ancyrocephalidae
Bychowsky, 1937
Ligophorus vanbenedenii (Parona & Perugia, 1890) Euzet & Suriano, 1977		Mugilidae
Fam. Gyrodactylidae
Cobbold, 1864
Gyrodactylus imperialis Mizelle & Kritsky, 1967		Gillichthys mirabilis Cooper, 1864, Oreochromis mossambicus (Peters, 1852)41–45Lake in Salton Sea, California, USA (North America)[23]
Gyrodactylus olsoni Mizelle & Kritsky, 1967G. mirabilis
Gyrodactylus salinae Paladini, Huyse & Shinn, 2011Aphanius fasciatus (Valenciennes, 1821)65Isolated pools in Cervia Saline, the Emilia Romagna region of northern Italy (Europe)[24]
Gyrodactylus n. sp. A.Mugilidae, Aphanius dispar (Rüppell, 1829)50–75Bardawil lagoon (Sinai Peninsula), Egypt (Western Asia)[22]
Fam. Lernaeopodidae
Milne-Edwards, 1840
Naobranchia sp. (as Axine sp.)		Hemiramphus far (Forsskål, 1775)50–75Bardawil lagoon (Sinai Peninsula), Egypt (Western Asia)[22]
Fam. Microcotylidae
Taschenberg, 1879
Microcotyle sp.		Mugilidae
Phylum ARTHROPODA
Class Copepoda
Fam. Caligidae Burmeister, 1835
Caligus apodus (Brian, 1924)		Mugilidae50–75Bardawil lagoon (Sinai Peninsula), Egypt (Western Asia)[22]
Caligus minimus Otto, 1821D. labrax, D. punctatus[22,25]
Caligus tenuis (Beneden, 1852) (as Sciaenophilus tenuis Beneden, 1852)A. regius[22]
Fam. Lernanthropidae
Kabata, 1979
Lernanthropus kroyeri Beneden, 1851		D. labrax, D. punctatus [22,25]
Lernanthropus sp.
Group II. Endopasrasitic nonadult stages
Phylum PLATHELMINTHES
Class Trematoda
Fam. Heterophyidae Leiper, 1909
Heteropyes heterophyes (von Siebold, 1852) Stiles & Hassall, 1900/metacercariae		Pisces:
Chelon ramada (Risso, 1827), Mugil cephalus Linnaeus, 1758, Chelon auratus (Risso, 1810,
Chelon saliens (Risso, 1810), Chelon labrosus (Risso, 1827)		50–75Bardawil lagoon (Sinai Peninsula), Egypt (Western Asia)[25]
Chelon ramada, M. cephalus, Chelon auratus, Mugil sp.[26]
Heteropyes aequalis Loos, 1902/metacercariaeChelon ramada (as Mugil capito)
Stictodora sawakinensis Looss, 1899/metacercariae
Heterophyidae gen. sp./metacercariaeMugilidae,
D. labrax, D. punctatus		50–75Bardawil lagoon (Sinai Peninsula), Egypt (Western Asia)[22]
Pygidiopsis genata Looss, 1907/metacercariaeCoptodon guineensis (Günther, 1862)50–60Sebkha Imlili salt flat, Atlantic Sahara (Africa)[27]
unidentified
digenean metacercariae
Euhaplorchis californiensis Martin, 1950/rediaeMollusca:
Cerithideopsis californica (Haldeman, 1840)		35Carpinteria Salt Marsh, USA (North America)[28]
60Bolinas Lagoon, California, USA (North America)[29,30]
Phocitremoides ovale Martin, 1950/rediae35Carpinteria Salt Marsh, USA (North America)[28]
Pygidiopsoides spindalis Martin, 1951/rediae35Carpinteria Salt Marsh, USA (North America)[29]
Fam. Himasthlidae Odhner, 1910
Acanthoparyphium spinulosum Johnston, 1917/rediae		C. californica35Carpinteria Salt Marsh, USA (North America)[28]
60Bolinas Lagoon, California, USA (North America)[29]
Fam. Cyathocotylidae
Mühling, 1898
Mesostephanus appendiculatoides (Price, 1934) Lutz, 1935/rediae		35Carpinteria Salt Marsh, USA (North America)[28]
Fam. Echinostomatidae
Looss, 1988
Himasthla rhigedana Dietz, 1909/rediae		C. californica60California, USA (North America)[29]
Himasthla sp B./rediae35Carpinteria Salt Marsh, USA (North America)[28]
Echinoparyphium sp./rediaeC. californica60Bolinas Lagoon, California, USA (North America)[29]
Fam. Renicolidae Dollfus, 1939
Renicola buchanani (Martin & Gregory, 1951)		C. californica35Carpinteria Salt Marsh, USA (North America)[28]
Renicola cerithidicola Martin, 197135Carpinteria Salt Marsh, USA (North America)[28]
Renicolidae fam. gen. sp./rediae60California, USA (North America)[29]
Fam. Philophthalmidae
Looss, 1899
Cloacitrema michiganensis McIntosh, 1938		C. californica35Carpinteria Salt Marsh, USA (North America)[28]
Parorchis acanthus (Nicoll, 1906) Nicoll, 1907/rediae60Bolinas Lagoon, California, USA (North America)[29]
Fam. Notocotylidae Lühe, 1909
Catatropis johnstoni Martin, 1956		C. californica35Carpinteria Salt Marsh, USA (North America)[28]
60California, USA (North America)[29]
Fam. Microphallidae Ward, 1901
Probolocoryphe uca (Sarkisian, 1957) Heard & Sikora, 1969		C. californica35Carpinteria Salt Marsh, USA (North America)[28]
Sporosysts with unidentified
xiphidiocercaria		35Carpinteria Salt Marsh, USA (North America)[28]
60Bolinas Lagoon, California, USA (North America)[29]
Class Cestoda
Fam. Dilepididae Fuhrmann, 1907
Fuhrmannolepis averini Spasskii & Yurpalova, 1967/cysticercoids		Crustacea:
Artemia franciscana Kellog, 1906		105–150Great Salt Lake, Utah, USA (North America)[31]
Tebenquiche Lagoon
(Salar de Atacama),
Chile (South America)		[32]
Artemia salina (Linnaeus, 1758),
Phallocryptus spinosa (Milne-Edwards, 1840)		65–70Tengiz Lake, Kazakhstan (Middle Asia)[33]
Anomotaenia tringae (Burt, 1940)/cysticercoidsA. franciscana,
Artemia parthenogenetica Bowen & Sterling, 1978		110–170Salt marshes Odiel and La Tapa, Spain (Europe)[34,35]
A. parthenogenetica110–200Odiel salt marshes, Spain (Europe)[36]
Salterns Nuestra Señora del Rocío, Portuguesas, Portugal (Europe)[37]
A. franciscana Salterns Castro Marim, Las Ánimas, Portugal (Europe)[37]
River Ebro Delta,
La Trinitat coastal saltern complex, Spain (Europe)		[38]
70–160Godolphin lakes,
Unated Arab Emirates (Asia)		[39]
Anomotaenia microphallos (Krabbe, 1869)/cysticercoidsA. parthenogenetica110Odiel and Tinto estuary, Spain (Europe)[36]
Saltern Portuguesas,
Portugal (Europe)		[37]
A. franciscana Saltern Castro Marim, Portugal (Europe)[37]
River Ebro Delta, La Trinitat coastal saltern complex, Spain (Europe)[38]
Anomotaenia sp., probably
A. microphallos/cysticercoids		A. parthenogenetica110–200Odiel salt marshes, Spain (Europe)[36]
Eurycestus avoceti Clark, 1954)/cysticercoidsA. franciscana70–160Godolphin lakes (Dubai)[39]
80Barros Negros Lagoon (Salar de Atacama), Chile (South America)[32]
Salterns Castro Marim, Las Ánimas, Santa Barbara, Portugal (Europe)[37]
Aigues-Mortes saltern, France (Europe)[40]
River Ebro Delta, La Trinitat coastal saltern complex, Spain (Europe)[38]
Artemia sp.133–210salt marshes of Camargue, France (Europe)[32]
A. salina65–80Tengiz lake, Kazakhstan (Middle Asia)[41]
Saltern de Cerrillos, Portugal (Europe)[37]
A. parthenogenetica110Odiel and La Tapa salterns, Spain (Europe)[35]
110–200Odiel Marshes, Huelva Province, SW Spain[36]
Salterns Odiel, Nuestra Señora del Rocío, Portuguesas, Portugal (Europe)[37]
Aigues-Mortes saltern, France (Europe)[40]
86–209Saltern La Tapa, Spain (Europe)[41]
Eurycestus sp./cysticercoidsA. franciscana70Asia (Dubai)[42]
Fam. Hymenolepididae Perrier, 1897
Branchiopodataenia gvozdevi (Maksimova, 1988) Bondarenko & Kontrimavichus, 2004/cysticercoids		A. salina65–80Tengiz Lake, Kazakhstan (Middle Asia)[43]
San Pedro del Pinatar, Spain (Europe)[44]
A. franciscana River Ebro Delta, La Trinitat coastal saltern complex, Spain (Europe)[45]
[38]
A. parthenogenetica Bras del Port, Spain (Europe)[44]
Cloacotaenia megalops (Nitzsch in Creplin, 1829)/cysticercoidsEucypris mareotica (Fischer, 1855)65–80Tengiz Lake, Kazakhstan (Middle Asia)[46]
Diorchis elisae (Skrjabin, 1914) Spassky et Frese, 1961/cysticercoidsE. mareotica65–80Tengiz Lake, Kazakhstan (Middle Asia)[46]
Confluaria podicipina (Szymanski, 1905)/cysticercoidsA. parthenogenetica110–170Odiel and La Tapa salt marshes, Spain (Europe)[34,35]
110–200Odiel salt marsh, Spain (Europe)[36]
Saltern Odiel, Portugal (Europe)[37]
A. franciscana70–160Godolphin lakes (Dubai)[39]
105–150Great Salt Lake, Utah, USA (North America)[31]
Artemia persimilis Piccinelli & Prosdocimi, 196855–86Los Cisnes and Amarga lagoons, Chile (South America)[47]
320Epecuén lagoon, Lagunas Encadenadas del Oeste, Argentina
(South America)		[48]
A. salina65–80Tengiz Lake, Kazakhstan (Middle Asia)[49]
Saltern de Cerrillos, Portugal (Europe)[37]
Fimbriarioides tadornae Maksimova, 1976/cysticercoidsA. salina65–80Tengiz Lake, Kazakhstan (Middle Asia)[50]
A. parthenogenetica110Odiel and Tinto estuary, Spain (Europe)[35]
Saltern Odiel, Portugal (Europe)[37]
Bras del Port, Spain and Aigues-Mortes, France (Europe)[44]
Aigues-Mortes saltern, France (Europe)[40]
A. franciscana River Ebro Delta,
Spain (Europe)		[44]
Aigues-Mortes saltern, France (Europe)[40]
River Ebro Delta, La Trinitat coastal saltern complex, Spain (Europe)[38]
Fimbriarioides ? sp./cysticercoidsA. persimilis55–86Los Cisnes and Amarga lagoons (South America, Chile)[47]
Flamingolepis caroli (Parona, 1887)/cysticercoidsA. salina133–210Salt marshes of Camargue, France (Europe)[51]
Artemia sp.133–210Salt marshes of Camargue, France (Europe)[52]
Flamingolepis dolguschini Gvozdev & Maksimova, 1968/cysticercoidsA. salina65–70Tengiz Lake, Kazakhstan (Middle Asia)[40]
Flamingolepis flamingo (Skrjabin, 1914)/cysticercoidA. franciscana70–160Godolphin lakes (Dubai)[39]
Saltern Castro Marim, Portugal (Europe)[37]
River Ebro Delta, La Trinitat coastal saltern complex, Spain (Europe)[38]
A. parthenogenetica110Odiel and Tinto estuary, SW Spain (Europe)[35]
110–200Odiel Marshes, Spain (Europe)[36]
Salterns Odiel, Nuestra Señora del Rocío, Portuguesas, Portugal (Europe)[37]
Aigues-Mortes saltern, France (Europe)[40]
86–209Saltern La Tapa, Spain (Europe)[45]
A. salina Saltern de Cerrillos, Portugal (Europe)[37]
Artemia sp.133–210Salt marshes of Camargue, France (Europe)[51,52]
Flamingolepis liguloides (Gervais, 1847)/cysticercoidsA. franciscana,
A. parthenogenetica		110–130Odiel and La Tapa salt marshes, Spain (Europe)[34,35]
A. parthenogenetica110–200Odiel Marshes, Spain (Europe)[36]
40–320Çamaltı salt pans, İzmir, Turkey (Asia)[52]
Salterns Odiel, Nuestra Señora del Rocío, Portuguesas, Portugal (Europe)[37]
Aigues-Mortes saltern, France (Europe)[40]
Salt marshes Aigues Mortes, Fangassier, Fos-sur-Mer, Lavalduc, Berre, Hybes-Pesquier, France (Europe)[53]
86–209Saltern La Tapa, Spain (Europe)[47]
Flamingolepis liguloides (Gervais, 1847)/cysticercoidsA. franciscana Saltern Castro Marim, Portugal (Europe)[37]
River Ebro Delta, La Trinitat coastal saltern complex, Spain (Europe)[38]
70–160Godolphin lakes, Dubai (Asia)[39]
Artemia sp.35La Mata lagoon, Bonmati salterns, Spain (Europe)[54]
65–110Su Pallosu pond (south-western Sardinia), Italy (Europe)[55]
133–210Salt marshes of Camargue, France (Europe)[51]
A. salina233–287Chott Marouane and Sebkha Ez-Zemoul lakes, Algeria (North Africa)[56]
Saltern de Cerrillos, Portugal (Europe)[37]
A. salina,
Phallocryptus spinosa (Milne-Edwards, 1840)		65–70Tengiz Lake, Kazakhstan (Middle Asia)[43,57]
Flamingolepis megalorchis (Luhe, 1898)/cysticercoidsE. mareotica65–80Tengiz Lake, Kazakhstan (Middle Asia)[46]
Flamingolepis tengizi Gvozdev et Maksimova, 1968/cysticercoidsE. mareotica65–80Tengiz Lake, Kazakhstan (Middle Asia)[46]
A. salina65–70Tengiz Lake, Kazakhstan (Middle Asia)[49]
Flamingolepis sp. 1/cysticercoidsA. persimilis55–86Los Cisnes lagoon, Chile (South America)[47]
A. franciscana Barros Negros Lagoon (Salar de Atacama), Chile (South America)[32]
Flamingolepis sp. 2/cysticercoidsA. franciscana Chaxas, Tebenquiche and Barros Negros Lagoons (Salar de Atacama), Chile (South America)[32]
Microsomacanthus paramicrosoma (Gasowska, 1931)/cysticercoidsE. mareotica65–80Tengiz Lake, Kazakhstan (Middle Asia)[46]
Parabiglandatrium phoenicopteri Gvosdev et Maksimova, 1968/cysticercoidsE. mareotica65–80Tengiz Lake, Kazakhstan (Middle Asia)[46]
Hymenolepis californicus Young, 1950/cysticercoidsA. franciscana105–150Great Salt Lake, Utah, USA (North America)[31]
A. salina Mono lake and salt pools, California, USA (North America)[58]
Wardium fusa (Krabbe, 1869)/cysticercoidsA. salina65–80Tengiz Lake, Kazakhstan (Middle Asia)[43]
Wardium manubriatum Spassky et Dao, 1963/cysticercoidsPhallocryptus spinosa[49]
Wardium stellorae (Deblock, Biguet & Capron, 1960)/cysticercoidsA. franciscana70–160Godolphin lakes, Dubai (Asia)[39]
River Ebro Delta, La Trinitat coastal saltern complex, Spain (Europe)[38]
A. parthenogenetica110Odiel and Tinto estuary, SW Spain (Europe)[35]
Salterns Nuestra Señora del Rocío, Portuguesas, Portugal (Europe)[37]
Aigues-Mortes saltern, France (Europe)[40]
A. salina65–80Tengiz Lake, Kazakhstan (Middle Asia)[49]
Saltern de Cerrillos, Portugal (Europe)[37]
65–70Tengiz Lake, Kazakhstan (Middle Asia)[40]
Artemia sp.133–210Salt marshes of Camargue, France (Europe)[32]
Wardium sp./cysticercoidsA. franciscana105–150Great Salt Lake, Utah, USA (North America)[31]
A. persimilis55Los Cisnes and Amarga lagoons, Chile (South America)[47]
Hymenolepididae gen. sp/cysticercoidsA. parthenogenetica Saltern Portuguesas, Portugal (Europe)[37]
Fam. Progynotaeniidae Fuhrmann, 1936
Gynandrotaenia stammeri Fuhrmann, 1936/cysticercoids		A. franciscana70–160Godolphin lakes, Dubai (South-Western Asia)[39]
80Barros Negros Lagoon (Salar de Atacama), Chile (South America)[32]
Saltern Castro Marim, Portugal (Europe)[37]
River Ebro Delta, La Trinitat coastal saltern complex, Spain (Europe)[38]
A. parthenogenetica Salterns Nuestra Señora del Rocío, Portuguesas, Portugal (Europe)[37]
110Odiel and Tinto estuary, SW Spain (Europe)[35]
110–200Odiel Marshes, Huelva Province, Spain (Europe)[36]
86–209Saltern La Tapa, Spain (Europe)[45]
Fam. ProgynotaeniidaeFuhrmann, 1936
Gynandrotaenia stammeri Fuhrmann, 1936/cysticercoids		A. salina65–80Tengiz Lake, Kazakhstan (Middle Asia)[50,59,60]
Saltern de Cerrillos, Portugal (Europe)[45,61]
Artemia sp.133–210salt marshes of Camargue, France (Europe)[51,52]
Gynandrotaenia sp./cysticercoidsA. franciscana River Ebro Delta, La Trinitat coastal saltern complex, Spain (Europe)[40]
Scolex pleuronectis larvaeFishes50–75Bardawil lagoon (Sinai Peninsula), Egypt (Western Asia)[26]
Phylum NEMATODA
Class Nematoda insertae sedis
Fam. Acuariidae
Railliet, Henry & Sisoff, 1912
Acuariidae fam. gen. sp./larvae		Crustacea:
A. franciscana		105–150Great Salt Lake, Utah, USA (North America)[31]
Acuariinae fam. gen. sp./larvae Saltern La Tapan, Spain (Europe)[45]
Fam. Anisakidae
Railliet & Henry, 1912
Contracaecum sp./larvae in muscules		Pisces:
Anguilla anguilla (Linnaeus, 1758)		43–47coastal lagoon Mar Menor (Iberian Peninsula), Spain (Europe)[62]
Phylum CNIDARIA
Class Myxozoa
Fam. Myxobolidae Thélohan, 1892
Myxobolus parvus		grey mullets,
Dicentrarchus spp.		50–75Bardawil lagoon (Sinai Peninsula), Egypt (Western Asia)[22]
Fam. Myxidiidae Thélohan, 1892
Myxidium sp.		grey mullets
Group III. Endoparasitic adults
Phylum PLATHELMINTHES
Class Trematoda
Fam. Bucephalidae Poche, 1907
Bucephalus anguillae Spakulova, Macko, Berrilli & Dezfuli, 2002/adults		Pisces:
Anguilla anguilla (Linnaeus, 1758)		43–47Mar Menor lagoon, Spain (Europe)[62]
Fam. Deropristidae Cable & Hunninen, 1942
Deropristis inflata (Molin, 1859) Odhner, 1902/adults
Class Cestoda
Fam. Proteocephalidae La Rue, 1911
Proteocephalidae/larvae		Anguilla anguilla43–46.5Mar Menor lagoon, Spain (Europe)[62]
Phylum NEMATODA
Class Nematoda insertae sedis
Fam. Anguillicolidae Yamaguti, 1935
Anguillicoloides crassus (Kuwahara, Niimi & Itagaki, 1974) Moravec & Taraschewski, 1988/pre-adults and adults		Anguilla anguilla43–47Mar Menor lagoon, Spain (Europe)[62]
Contracaecum sp.
Phylum ACANTHOCEPHALA
Class Eoacanthocephala
Fam. Neoechinorhynchidae Ward, 1917
Neoechinorhynchus agilis (Rudolphi, 1819)/adults		Pisces:
Mugil cephalus		50–75Bardawil lagoon
(Sinai Peninsula), Egypt (Western Asia)		[22]
N. agilis/cystacanths and juvenile adultsSparus aurata Linnaeus, 1758, Dicentrarchus punctatus (Bloch, 1792), Atherina boyeri Risso, 1810, Hemiramphus far (Forsskål, 1775), Argyrosomus regius (Asso, 1801)
Fam. Quadrigyridae Van Cleave, 1920
Acanthogyrus (Acanthosentis) tilapiae (Baylis, 1948) Amin, 1985		Coptodon guineensis (Günther, 1862)50–60Sebkha Imlili salt flat,
Atlantic Sahara (Africa)		[27]
* As provided in Section 2 of this paper.
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Kornyychuk, Y.; Anufriieva, E.; Shadrin, N. Diversity of Parasitic Animals in Hypersaline Waters: A Review. Diversity 2023, 15, 409. https://doi.org/10.3390/d15030409

AMA Style

Kornyychuk Y, Anufriieva E, Shadrin N. Diversity of Parasitic Animals in Hypersaline Waters: A Review. Diversity. 2023; 15(3):409. https://doi.org/10.3390/d15030409

Chicago/Turabian Style

Kornyychuk, Yuliya, Elena Anufriieva, and Nickolai Shadrin. 2023. "Diversity of Parasitic Animals in Hypersaline Waters: A Review" Diversity 15, no. 3: 409. https://doi.org/10.3390/d15030409

APA Style

Kornyychuk, Y., Anufriieva, E., & Shadrin, N. (2023). Diversity of Parasitic Animals in Hypersaline Waters: A Review. Diversity, 15(3), 409. https://doi.org/10.3390/d15030409

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