Sturgeon Parasites: A Review of Their Diversity and Distribution

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Introduction
Sturgeons are members of the Acipenseriformes order, which is over 200 million years old and comprises twenty-seven species and two families, the Acipenseridae and Poyodontidae [1].The species has a long life cycle and is native to the Northern Hemisphere [2,3].The natural habitats of sturgeons are the freshwaters of Europe, Asia and North America.The species inhabit inland water, bays, estuaries, and the coastal regions of seas and oceans.Although most sturgeon species migrate and spawn in freshwater, they also spend a significant amount of their life cycle in brackish water.The Caspian basin accounted for up to 90% of caught sturgeon, but as many fisheries have collapsed, many individual species or populations are now endangered.Two such examples are the Huso and Acipenser genera, with a total of 17 species [4], the most well-known of which are Acipenser ruthenus, Acipenser stellatus, Acipenser gueldenstaedti, Acipenser oxyrhynchus, Huso huso, Acipenser persicus, Acipenser sturio, and Acipenser naccarii.Sturgeon species differ significantly from other fish species not solely because of their anatomy, but also because of their longevity and behavior.The Danube is a well-known habitat for sturgeon populations, although in recent years only four species were found [5] out of the six previously known [6].Such decreases in sturgeon populations are mainly due to dams, pollution, and overfishing [7,8].With the effective wild population decreasing, the sturgeon parasitic infestations are becoming more important and, like in many other fish species, they are becoming more prominent as aquaculture is expanding [9].
Sturgeons are host to many parasites, such as protozoans, trematodes, nematodes, monogeneans, helminths, and argulidaes [10].These parasites are among the most significant factors responsible for weight loss, impotence, strange behaviour, deformed gills, and epithelial lesions [11], ultimately resulting in the diminishing of wild stocks or in financial losses in the case of fish farming.In addition, external parasites have the potential to spread bacteria, viruses, and other pathogens, resulting in a boost of secondary fungal, bacterial, and viral infections [12,13].Sturgeons are susceptible to viral, parasitic, and bacterial Various types of texts, such as abstracts, reviews, and original research articles, were examined and evaluated individually to determine their eligibility based on specific criteria.These included recording information about the sturgeon species, the parasite species, the site of infection, and the country of origin.

Protozoa, Monogenea and Crustaceans
Protozoa comprise a diverse group of predominantly single-celled eukaryotic organisms [75].Depending on their species, protozoa can be either ectoparasites or endoparasites.Among cultured fish, ectoparasitic protozoa are the most commonly encountered parasites [88].These parasites induce a reactive hyperplasia of the fish epithelium, and excessive mucus infestation can lead to gill hyperplasia, including epithelial hyperplasia of the entire gill filament, inflammation, hemorrhage, and necrosis [89].Protozoa pose a significant threat to fish health, causing diseases in both farmed and wild populations [90].Within fish populations, parasitic protozoa can rapidly spread, particularly those with direct life cycles and broad host specificity [91].Some protozoa act as ectoparasites, residing on the skin, fins, and gills, while others invade internal organs, such as the intestine [92].Parasite invasion can impede fish development, cause weight loss, and disrupt reproductive processes.In severe cases, infections can lead to long-term mortality and substantial damage to fish populations [93].
In a study conducted by Vasile et al. (2019) [20], the protozoan parasite Ichthyophthirius multifiliis was identified in Acipenser stellatus at a research hatchery in Romania.Ichthyophthirius multifiliis is a parasitic ciliate that was initially described by the French parasitologist Fouquet in 1876.This parasite has the ability to infect a wide range of freshwater fish species, including sturgeon.Upon infecting sturgeon, the parasite attaches itself to the skin and gills, where it feeds on bodily fluids, resulting in the formation of visible white spots on the outer layer of the fish, commonly referred to as "white spot disease".
Ichthyophthirius multifiliis can cause significant harm to the fish, including irritation, inflammation, tissue damage, reduced growth, weakened immune function, and even death [94,95].The disease caused by this tissue-feeding parasite is referred to as ichthyophthiriasis [96].Outbreaks of I. multifiliis occur when conditions are favorable for rapid multiplication, making it a major concern in aquaculture settings [97].
In another study conducted by Popielarczyk and Kolman (2013) [21] with Acipenser oxyrinchus oxyrinchus specimens obtained from an open system pond in Kuźniczka, Poland, protozoa, monogenean, and crustacean parasites were identified.The protozoa Trichodina sp. and Apiosoma sp., as well as the monogenean Gyrodactylus sp. and the crustaceans Ergasilus sieboldi and Argulus coregoni, were observed in specimens from various water habitats.A high number of Trichodina sp.parasites with varying morphology and size were found.These parasites resemble caps and range in size from 18 to 50 µm, with some specimens measuring up to 80 µm.They possess partial ciliation and have a saucer-shaped body, which enables them to move along the skin, fins, and gills of fish.Trichodina sp.parasites reproduce through binary fission; after reproduction they can either reattach to the same host or seek a new host in the water column.
The parasite possesses cilia arrangements on its body, which include a distinctive ring of denticles, morphological features that are crucial for species identification.Additionally, this parasite is classified as an ectoparasite that exhibits rapid movement on the gills, fins, and body surface of its host (in certain species, it can even inhabit the urinary tract).The Trichodinidae family, to which this parasite belongs, is known to cause trichodinosis [98] (also known as trichodinads), characterized by hyperplasia of the epithelium [99].
Apiosoma sp.parasites are not typically considered highly dangerous, but they can still inflict damage on sturgeons by attaching to their fins, gills, or skin surface, which leads to the destruction of the epithelial tissue and impairment of organ function.These ciliates are ectocommensals, living on the gills and body surface of aquatic organisms, particularly the fry of freshwater fish [100].They are large, bell-shaped organisms measuring approximately 50-70 µm in length and 18-40 µm in width.The species have a free-living lifestyle but frequently attach themselves to various organisms in the water, including fish [98].When sturgeons become infected with Trichodina sp. and Apiosoma sp., mucus accumulates on the skin surface, especially around the pectoral fin, gills, and gastrointestinal tract, as well as the oviduct and urinary bladder [96].
In aquaculture-related studies conducted in Romania, a total of 22 species of Gyrodactylus sp.within the monogenea group have been identified [101].However, it should be noted that some sources report 145 species for the Gyrodactylus genus [102], while others mention up to 400 species [103].The exact number remains uncertain due to synonyms and variations in taxonomic interpretation [103].Gyrodactylus sp. is an ectoparasitic flatworm with a length of less than 1 mm and a body width of approximately 0.1 mm.It is characterized by a four-lobed head and an opisthaptor, which includes one prominent pair of large hooks and up to 12 smaller hooks.Infections caused by Gyrodactylus sp. can result in skin irritation and tissue damage.Additionally, in a study conducted by Choudhury (1997) [71], the monogenean species D. atriatum and the trematode Skrjabinopsolus sp. were identified in the gill of Acipenser fulvescens in Canada.
The copepod crustacea Ergasilus sieboldi, commonly known as "fish lice" [104], has been reported to infect sturgeons [21].This parasite can have detrimental effects on the gills, as it attaches to the skin or gills and can cause physical damage, potentially leading to suffocation.Pazooki and Msoumian (2018) [22] identified the protozoa Haemogregarina acipenseris and Cryptobia acipenseris in Acipenser persicus and Acipenser guldenstadti in the southern part of the Caspian Sea.Haemogregarina acipenseris has an oval body shape, measuring 6.5-8.2 × 2.2-3.0 µm, with two rounded ends or one rounded and one sharpened end.The nucleus typically consists of a few chromatin granules, and it is commonly found in erythrocytes.Haemogregarina acipenseris has been previously recorded in sturgeons in the Caspian and Black seas, and it has been found in sterlet in the Volga and Danube rivers [30].Cryptobia acipenseris is a parasitic protozoan measuring 11-16.4µm in size [105].The vegetative and sexual stages of this protozoan have been found in the blood of various sturgeon species [22].While the majority of Cryptobia acipenseris live in the host's blood, some can also be found in the intestines and gills.Infections caused by Haemogregarina acipenseris and Cryptobia acipenseris can lead to severe consequences, including anemia and, finally, death [106].Mohler et al. (2000) [23] identified the protozoan Chilodonella sp. in Acipenser oxyrinchus oxyrinchus in the eastern side of Esopus Island in the Hudson River, New York.Chilodonella sp. is a single-celled organism belonging to the ciliate class of Alveolata.It is covered in cilia and possesses a dual nuclear structure.Chilodonella sp. is the causative agent of Chilodonelloza, a disease that affects the gills and skin of freshwater fish [107].
In the study conducted by Kayiş et al. (2017) [24], the protozoan Trichodina reticulata was identified in Acipenser gueldenstaedtii and Acipenser baerii in the Black Sea region of Turkey.This parasite infects the gill, skin, and fins, as mentioned in the previous reference [21].Furthermore, Baska (1999) [28] discovered the presence of the protozoan Ichthyophthirius multifiliis and the nematode Goussia acipenseris in Acipenser ruthenus specimens in Hungary.Dobson and May (1987) [74] identified the monogenea Nitzschia sturionis in Acipenser stellatus specimens in the USA.Chebanov [27] identified the protozoa Nitzschia sturionis in Acipenser oxyrinchus oxyrinchus.

Cestode, Trematode and Nematode
Fish-borne cestodes that can infect humans primarily belong to the order Diphyllobothriidea and are commonly referred to as broad tapeworms.These tapeworms have a three-host life cycle, with teleost fishes (excluding spirometra) serving as the second intermediate hosts and a source of human infection [27].The larval form of the cestode penetrates the tissue of a crustacean host and undergoes metamorphosis into a proceroid.The fish becomes infected by consuming the crustacean.Once inside the fish, the adult cestodes gradually migrate to body organs and intestines, causing diseases and reducing the fish's lifespan [79].
The trematode Diplostomum spathaceum is responsible for a disease called diplostomatosis, or eye fluke disease [108].This parasite has been found to be widespread among fish in Utah [109].Diplostomum spathaceum has a complex life cycle involving multiple hosts and can cause significant harm.It attaches to the eye tissue of the fish and feeds on blood, leading to inflammation, swelling, and the formation of dark spots on the eye's surface [110].Choudhury (2009) [31] identified the trematoda Pristicola bruchi in Acipenser fulvescens in Wisconsin, USA.Pristicola bruchi is smaller in size (ranging from 1.660 to 2.110 µm) than Pristicola sturionis.It possesses a single row of prominent peg-like oral spines instead of two rows, and its vitelline follicles dorsally converge over a small region without extending beyond the posterior testes.This is the first recorded occurrence of this genus in North America and appears to be the first report of the genus in sturgeon since the description of Pristicola sturionis in 1930 [111].Warren et al. (2017) [32] identified the trematoda Acipensericola glacialis in Acipenser fulvescens during a survey of the Great Lakes Basin, specifically the Lake Winnebago system in the USA.Acipensericola glacialis derives its name from the Latin-specific epithet "glacialis" (glacier).The impact of this parasite on sturgeon can vary depending on the severity of the infestation and the overall health of the fish.

Copepods
Small crustaceans called copepods are commonly found in freshwater and marine habitats [42].The calanoid copepod is the most common form of copepod found in sturgeon fish.It is a tiny planktonic creature that is an important food source for many fish species, including sturgeon.Cyclopoid copepods, Harpacticoid copepods, and Poecilostomatoid are other copepod species that can be found in sturgeon fish.In addition, copepod parasites have been shown to affect the physiological health of the sturgeon and cause anemia.In particular, these ectoparasites can reduce host osmotic competence both directly by damaging and necrosing the epithelium and indirectly by increasing host stress hormone levels [40].
Vasilean et al. (2012) [42] identified the copepoda Argulus sp. in Huso huso in Romania.The parasite is popularly called "fish lice" and is shaped like a pear, wide at the front and narrow at the end.Its length is about 3.7 mm and it has a pair of tentacles and hooks that are the size of the parasite's body.These crustaceans have bodies adapted to parasitic life in general.Andres et al. (2019) [43] found the copepoda Argulus flavescens in Acipenser oxyrinchus in the Pascagoula river, USA.The Argulus flavescens attaches itself to the gills and skin using its sharp claws and proboscis, causing irritation and inflammation of the skin and feeding on the blood, which can lead to anemia if the infestation is severe [116].
Ergasilus sieboldi, Paraergasilus rylovi, Lernaea cyprinacea, L. elegans, Caligus lacustris and Argulus foliaceus are also copepods that occur on different fishes and are well known to be pathogenic to fishes in aquaculture.Three species are specific to sturgeons, but only one of them, Pseudotracheliastes stellatus, is pathogenic.A rather high infection of A. stellatus and A. gueldenstaedtii by Pseudotracheliastes stellatus was noted in the Azov sea.Infection by these species results in quantitative and qualitative changes in white and red blood cells, as diseased fish present anemia [117].Bauman et al. (2011) [47] identified the copepoda Argulus sp. on the gills and skin of Acipenser fulvescens in the Marys river, USA. Brown (2010) [48] identified the copepoda Dichelesthium oblongum on the gills of Acipenser oxyrinchus oxyrinchus in New York.Munroe et al. (2011) [49] identified the copepoda Caligus elongatus and Dichelesthiumoblongum, the Hirudinea Calliobdella vivida, the Crustacea Argulus stizostethii, and the Monogenea Nitzschia sturionis in Acipenser oxyrinchus in Canada.Bozorgnia (2018) [118] identified the Copepoda Lernaea cyprinacea in the gills of Acipenser stellatus in the Caspian sea, Iran.

Hirudinea and Polypodiozoa
The Hirudinea Caspiobdella fadejewi was identified in wild Acipenser oxyrinchus specimens in the Drwêca river, Poland, by Bielecki et al. (2011) [49].Caspiobdella fadejewi can cause physical harm to fish, particularly sturgeon.These leeches attach themselves to the skin of sturgeons and feed on their blood, which can lead to irritation, inflammation, and tissue damage.In severe cases, a large number of leeches can weaken the fish, making it more vulnerable to other predators or diseases.Additionally, leeches can transmit diseases or parasites to the fish, as they can carry a range of harmful pathogens [119].Bolotov et al. (2022) [60] identified the Hirudinea Acipenserobdella volgensis in the pectoral fin of Acipenseridae in the Volga river basin in Russia.This species was also found on Acipenser baerii, A. gueldenstaedtii, and A. nudiventris [120].Raikova (2002) [50] identified the polypodiozoa Polypodium hydriforme in Acipenseriformes in the Volga river as well.This is the only cnidarian species adapted to intracellular parasitism in fish oocytes.It is a diploblastic animal that possesses stinging cells known as cnidocytes, with a life cycle that consists of two stages: a parasitic stage and a free-living phase.The parasitic stage occurs within host oocytes throughout oogenesis, starting from early previtellogenesis until the hatching stage.The parasite reproduces through longitudinal fission, with the number of tentacles doubling before each division [121].Polypodium hydriforme can affect the reproductive health of the sturgeon in particular, with the infected female sturgeon experiencing reduced egg production and poor egg quality [122,123].

Hyperoartia
Hyperoartia, commonly known as lampreys, are parasitic jawless fish that feed by attaching themselves to the body of fish and sucking their blood and body fluids [84].When lampreys attach themselves to sturgeons, they create open wounds that can become infected and weaken the fish.This makes the fish more susceptible to predation and disease and can also impair their ability to swim and reproduce.Lampreys can also compete with sturgeons for food and habitat, further contributing to population reduction [81].Petromyzon marinus lampreys have been identified by Briggs et al. [81] 2022) [125] identified the lamprey Petromyzon marinus in Acipenser fulvescens in Lake Sturgeon, Canada.

Discussion
According to the literature, sturgeon fish are infected with various ecto-and endoparasite species that live in freshwater, marine areas, lakes, and fish farms.The most commonly reported microhabitats of fish hosts were external organs such as the gills, skin, and the surface of fins.The skin surface, gills, blood, eggs, intestines, gut, and digestive system were the most commonly infected sites (Table 2).Overall, the literature has recognized sturgeon parasite species to include Protozoa, Trematoda, Crustacea, Nematodes, Monogenea, Hirudinea, Copepoda, Acanthocephala, Cestoda, Polypodiozoa, and Hyperoartia (Lamprey).

Parasites
Infected Organs By considering all taxonomic groups of parasites (Table 3) that have been the subject of studies concerning the occurrence and absence of parasites in different organs, it is presented in Figure 1 that the intestines are the most susceptible to infestation (30.49%).This is followed by the skin (21.95%), gills (18.29%), and fins (16.46%), while eggs (4.27%), blood (1.83%), and heart (0.61%) are the least susceptible to infestation.
G gill, S skin, F fin, I intestine, E eye, SP Spleen, H heart, N nose, Eg eggs, B body, BL blood T testes, GU gut, Ga gastrointestinal, Ds digestive system.
Considering the extent of infestation manifested by various organs of sturgeons in accordance with each taxonomic group of parasites, the scientific literature provides the subsequent data, also presented in the chart in Figure 3: Protozoa affects the skin the most (48.57%),followed by the fins (22.86%), gills (20%), and blood (8.57%).No species of this group were identified in the intestines, heart, or eggs of sturgeons.
Monogenea affects the skin the most (36%), followed equally by the gills and fins (32%).No species of this group were documented in other organs in sturgeons.
Crustacea affects the skin, gills and fins equally (31.25%), followed by the intestines (6.25%).There were no species of this taxonomic group documented or identified in the blood, heart, or eggs of sturgeons.
Trematoda affects mostly the intestines (92.86%), followed by the heart (7.14%).No species of this group were identified in the gills, fins, skin, blood, or eggs of sturgeons.
Copepoda affects the gills the most (37.5%),followed by the fins and skin equally (25%).The rest of the studies document the infestation of the body as a whole by this group of parasites, while there are no studies about the recurrence of infestation in the blood, intestines, heart, or eggs of sturgeon species.and polypodiozoa (4%).The Hyperoartia group is recorded as having the lowest percentage of identified infestations, at 1%.However, these statistics do not reflect the real in situ scenario, where percentages can vary substantially; rather, they indicate the level of parasite identification based on the literature.Considering the extent of infestation manifested by various organs of sturgeons in accordance with each taxonomic group of parasites, the scientific literature provides the subsequent data, also presented in the chart in Figure 3: Protozoa affects the skin the most (48.57%),followed by the fins (22.86%), gills (20%), and blood (8.57%).No species of this group were identified in the intestines, heart, or eggs of sturgeons.
Monogenea affects the skin the most (36%), followed equally by the gills and fins (32%).No species of this group were documented in other organs in sturgeons.
Crustacea affects the skin, gills and fins equally (31.25%), followed by the intestines (6.25%).There were no species of this taxonomic group documented or identified in the blood, heart, or eggs of sturgeons.
Trematoda affects mostly the intestines (92.86%), followed by the heart (7.14%).No species of this group were identified in the gills, fins, skin, blood, or eggs of sturgeons.
Copepoda affects the gills the most (37.5%),followed by the fins and skin equally (25%).The rest of the studies document the infestation of the body as a whole by this group of parasites, while there are no studies about the recurrence of infestation in the blood, intestines, heart, or eggs of sturgeon species.
Polypodiozoa species were only identified and documented in the eggs of sturgeons.Hirudinea species were mostly documented to affect the body as a whole (60%), while 20% of studies identify these parasites in either the gills or fins of sturgeons.
Nematoda species were only identified in the intestines of sturgeon species.Acanthocephala species were only documented in the intestines of sturgeons.Cestoda species were only identified in the intestines of sturgeons.Hyperoartia species were only documented in the body of sturgeons as a whole, with no particular specifications.

Conclusions
According to the studies, it may be concluded that among the organs of the sturgeon, the intestines are the most prone to parasite infestation, while the blood seems to be the least affected by parasites.
Considering the scientific community's present understanding, most recorded instances of infestation are attributed to protozoa, whereas the group Hyperoartia has the least amount of evidence available.
Furthermore, according to current research, each taxonomic group of parasites exhibits selectivity in terms of the sturgeon organs they target.Nevertheless, the provided statistics are based on the existing level of knowledge, and further research is necessary to gain a more thorough understanding of the impact of each parasite group on sturgeons, which are currently in a critical conservation status globally.Polypodiozoa species were only identified and documented in the eggs of sturgeons.Hirudinea species were mostly documented to affect the body as a whole (60%), while 20% of studies identify these parasites in either the gills or fins of sturgeons.
Nematoda species were only identified in the intestines of sturgeon species.Acanthocephala species were only documented in the intestines of sturgeons.Cestoda species were only identified in the intestines of sturgeons.
species were only documented in the body of sturgeons as a whole, with no particular specifications.

Conclusions
According to the studies, it may be concluded that among the organs of the sturgeon, the intestines are the most prone to parasite infestation, while the blood seems to be the least affected by parasites.
Considering the scientific community's present understanding, most recorded instances of infestation are attributed to protozoa, whereas the group Hyperoartia has the least amount of evidence available.
Furthermore, according to current research, each taxonomic group of parasites exhibits selectivity in terms of the sturgeon organs they target.Nevertheless, the provided statistics are based on the existing level of knowledge, and further research is necessary to gain a more thorough understanding of the impact of each parasite group on sturgeons, which are currently in a critical conservation status globally.
Despite the incomplete understanding of the diversity of parasite species that affect sturgeons, there is less research regarding their ecology, distribution, and prevalence.It is striking that there is currently a lack of scientific focus on understanding the biology and ecology of potentially harmful parasites.Despite a few comprehensive studies on the topic, which have relied solely on the enthusiasm and research efforts of individual scientists, there has been minimal motivation to structure these studies in a more systematic manner.
It is recommended that national and international organizations facilitate more structured research programs regarding fish parasites, especially regarding endangered fish species.These should be designed to allow trend analysis of changes in the parasitic fauna of fishes, such as sturgeons, in the face of environmental changes.
Furthermore, in aquaculture, diseases will continue to play an important role in the economic performance of the industry.Therefore, it is highly recommended that studies be supported and systematically organized to assist in preventing the loss of cultured stock while also preventing aquaculture from becoming a potential reservoir for parasites and disease agents affecting natural stocks.
Time and resources are required to better address the study of parasites that influence sturgeon species from the standpoints of biodiversity monitoring and reducing the risk of disease transmission in natural habitats and aquaculture farms.

Figure 1 .
Figure 1.Percentage of parasite recurrence by affected organs (all taxonomic groups).

Figure 1 .
Figure 1.Percentage of parasite recurrence by affected organs (all taxonomic groups).

Figure 2 .
Figure 2. Percentage of parasite taxonomic group identification in sturgeon species, based on the reviewed scientific literature.

Figure 2 .
Figure 2. Percentage of parasite taxonomic group identification in sturgeon species, based on the reviewed scientific literature.

Figure 3 .
Figure 3. Percentage of infestation of each parasite taxonomic group on different organs.

Figure 3 .
Figure 3. Percentage of infestation of each parasite taxonomic group on different organs.

Table 2 .
Parasites sites of infection.

Table 3 .
The taxonomy of parasites hosted by sturgeons.

Table 3 .
The taxonomy of parasites hosted by sturgeons.