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Review

Ecological Interdependence of Pollution, Fish Parasites, and Fish in Freshwater Ecosystems of Turkey

by
Ahmet Öktener
1,*,† and
Doru Bănăduc
2,*,†
1
Atalar Neighborhood, 927th Street, Ergul Site, A Blok No. 1/9, 20150 Denizli, Turkey
2
Applied Ecology Research Center, Lucian Blaga University of Sibiu, 550024 Sibiu, Romania
*
Authors to whom correspondence should be addressed.
†
These authors contributed equally to this work.
Water 2023, 15(7), 1385; https://doi.org/10.3390/w15071385
Submission received: 11 February 2023 / Revised: 29 March 2023 / Accepted: 1 April 2023 / Published: 3 April 2023
(This article belongs to the Section Biodiversity and Functionality of Aquatic Ecosystems)
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Abstract

:
Records of mass fish deaths were found in different data sources for this study. A map of mass fish deaths in Turkey was also realized for the first time. We aimed to present a review of the distribution of mass fish deaths in the freshwater ecosystems of Turkey, mostly present in the Marmara Region and Aegean Sea Region, where there are intensive industrial and agricultural activities. Fish parasites generally occur in equilibrium with their hosts in natural environments. In the freshwater ecosystems of Turkey, which are highly affected by human activities and have extremely rich natural ichthyofauna, the negative effects of pollution on environmental parameters, which can directly affect the fish, and the emergence and overextension of fish parasites can cause a supplementary synergic direct negative effect transposition in mass fish deaths due to the deterioration of host immunity and to the wounds induced in fish where bacterial, viral, and fungal pathogens can be effective. Finally, these factors can influence the fish rate of survival and skew the structure of fish populations. Mass fish deaths have been frequently reported in Turkey, but are usually only explained by pollution as a single accepted anthropogenic stressor. Together with pollution, a supplementary induced bioecological stressor, the qualitative and quantitative characteristics of the fish parasites’ association variations should be assessed and monitored as potential complex precursor indicators of fish communities’ structural degradation and freshwater ecosystems’ dreadful conditions. Fish parasites as biomonitor species should be used to identify the effects of pollution in Turkish ecosystems, and not only in freshwater ecosystems, in the future. An optimum management plan for freshwater ecosystems should include all the physico-chemical factors, fish parasites, and fish elements involved in permanent assessment and monitoring activities.

1. Introduction and Background

Biodiversity changes and declining tendencies under human impact represent a planetary process influencing most taxonomical groups and their natural habitats [1,2,3]. In the context of 21st-century global concern about freshwater as a strategic sustainable natural resource and generator of secondary resources, among increasing stressors, threats, and risks, pollution is a major stressor impacting aquatic ecosystems [4,5,6,7,8,9,10,11,12]. The directly and indirectly associated freshwater biodiversity is an essential component of the biosphere, without which its proper functioning is impossible. There are a relatively large number of studies on the impacts of pollution, with a high variety of negative effects on different freshwater ecosystem taxa, including fish, revealing the significance and magnitude of the topic worldwide [13,14,15,16,17,18,19,20,21]. The relatively new climate change context amplifies the human-induced stressors’ effects in an accelerated rhythm [22,23,24]. Although the negative effects of direct pollution on fish have been studied in different circumstances, the possibility of indirect impact through a pollution–parasites–risk interrelation still needs to be addressed, which is the main purpose of this study.
A good ecological status for the protection and conservation of the aquatic environment is of vital importance around the world for the well-being of the related habitats, species, and human societies [23,25,26,27,28,29,30,31,32]. Aquatic environment protection activities have to deal with variable human-induced environmental stressors worldwide, including domestic, industrial, agricultural, water-body hydro-morphological changes, climate change, and natural disasters, which are significantly affecting these ecosystems [20,33,34]. All these human-induced situations and cases are present in Turkey, too [30,35,36,37].
Fish parasites have been used by various scientists as a biological indicator to determine fish population dynamics and stock trends [38,39,40]. Fish parasites are ubiquitous, primarily surviving in dynamic equilibrium with their host(s), and they are often overlooked in fish health assessments [41]. Pollution can affect the susceptibility and immune response of fish, exposing them to parasite infection [42,43]. Pollutants can also affect the free-living stages of parasites, directly or indirectly, through the intermediate hosts of the parasite. Hence, it is easier to monitor the changes in the infection values of the parasite in the host than to use the routine methods to determine the pollution [44].
Classical methods used to verify the accumulation of pollutants provide exact quantification but do not reflect the environmental impact on the ecosystem’s key end taxa. Moreover, they are not cheaper than biological monitoring [45].
Pollution studies have generally been carried out on the short-term effects of chemicals, namely their acute toxicity [46]. In nature, aquatic organisms are exposed to low concentrations of pollutants over long periods [44]. Therefore, working on bio-indicator species can provide clearer results for the accumulative and synergetic effects of pollution.
There have been many environmental impact studies that aim to understand interactions between parasites and ecological problems such as pollution [44,47,48,49,50,51].
The Middle East is extremely rich in fish diversity. It is a transitional area between three main biogeographical units: the Palearctic, the Afrotropical, and the Oriental regions. However, it is also subject to a major human impact effect [18]. Turkey shows a notable diversity of habitats, with significant variations in altitude, precipitations, temperature, topography, and geological history, which is reflected in its rich biodiversity [25]. Its territory lies at the nexus of Europe, the Middle East, Central Asia, and Africa [26]. It is a hotspot of freshwater fish diversity and also includes endemic species, possessing unique and rich ichthyofauna containing distinct Euro–Asian–African elements. Currently, among the 368 freshwater fish species, 3 are globally extinct, 5 are extinct in Turkey, and 153 species are recognized as endemic, 65 of which are classified as Critically Endangered and Endangered [27]. All of them are affected by high and variable human stressors, which have induced habitat degradation [28,29]. Many stressors plague the Turkish waters, and the contribution of each stressor is difficult to quantify [30]. It is much more difficult to highlight indirect the influence of complex stressor on fish.
A total of 199 parasite species have been reported in freshwater fish in Turkey. In total, 131 of these species (Monogenea—85 species, Digenea—23 species, Cestoda—23 species) belong to Platyhelminthes; 15 species belong to Nematoda; 10 species belong to Acanthocephala; 7 species belong to Annelida; 14 species belong to Ciliophora; 3 species belong to Euglenozoa; 1 species belongs to each of Myzozoa, Metamonada, Choanozoa, and Mollusca; 4 species belong to Cnidaria; and 11 species belong to Arthropoda [52,53,54,55,56,57].
There are a few published studies on using fish parasites as a bioindicator species in freshwater ecosystems in pollution-related studies in Turkey [58,59,60]. One of the most visible direct effects of pollution in freshwater is mass fish deaths. This study aims to reveal the role of fish parasites as aquatic ecosystem bioindicators for the freshwater ecosystems’ key driving pollution-related stressors in these types of habitats, and to stress the interdependencies among Turkey’s freshwater ecosystems’ pollution, fish parasites, and fish.
The main aim of this article is to review reports of pollution-related fish deaths in Turkey and to examine the ecological relationships between fish, parasites, and pollutants. This is the first such review to be conducted in Turkey, so it could be a potentially important contribution to the literature in this field. The study draws attention to the pollution situation by associating it with the reported bioindication parasites in the freshwater where mass fish deaths have occurred. The study also highlights a potential interrelation between pollution and the decrease in fish resilience, the facilitation of fish parasites by the reduced biological status of fish, and the decrease in fish ecological status because of pollution and parasite synergistic effects.

2. Material and Methods

The literature on the parasites of freshwater fish in Turkey was prepared from significant specific publications, such as articles, theses, projects, proceedings, and checklists, from 1964 to 2022. Data from 44 water bodies were compiled, and the collected data come from all years of research, regardless of the date of fish death. The names of parasites were checked on databases such as the World Register of Marine Species [61] and FishBase [21]. Reports in several media materials were also used to track these incidents with related information and compile a map of mass fish deaths.
For this study, a map was produced of the localities where mass fish deaths occurred in the freshwaters of Turkey. We also listed fish parasite studies in freshwaters where mass fish deaths occurred. As a result, we interpreted the usability of the related fish parasites as bioindicator species based on current pollution where mass fish deaths occurred and highlighted the pollution–fish and parasites–fish interrelations.

3. Results

3.1. Types of Pollutants

Mass fish deaths are a common disaster in freshwaters. Natural causes, such as oxygen depletion, cyanobacterial blooms, storms, hail, waves, and currents cause mass fish deaths [62]. Infectious agents (viral, bacterial, fungal, parasitic agents, etc.) can also cause mass fish deaths. These agents are present at low levels in equilibrium in fish in natural environments and farms. However, they cause mass deaths in fish because of the deterioration of environmental conditions in the aquatic ecosystem [63].
However, mostly anthropogenic causes are more responsible for mass fish deaths. These causes are: agricultural (manure, pesticides, irrigation, etc.); industrial (mining, petroleum, wood products, chemicals, food, metal, etc.); municipal (sewage, power generation, water supply, etc.); transportation (pipeline, truck, rail, etc.); other (construction, well drilling, etc.); and tourism (thermal spas, boats, etc.) [64].
Mass fish deaths are also seen frequently in the freshwaters of Turkey, such as in the agricultural irrigation pond in Yeni Ziraatli Village of Manyas District, in 2014. These deaths occurred because of the wastewater containing animal pesticides and natural fertilizers released from the cattle farms in the region reaching the pond, as well as a large amount of water being drawn from the pond for irrigation. In the analysis, ammonia and phosphorus values in the waters were found to be relatively high. As a result, wels catfish and carp died there due to lack of oxygen (Figure 1, https://www.youtube.com/watch?v=6FTqOUIrXWg (accessed on 11 August 2022)).

3.2. Indicator Parasites

There are various reviews in which studies are compiled on the determination of the differences in the parasite community and infection values based on changes in water-quality parameters related to pollution, as well as the determination of the pollutant bioaccumulation in the parasites according to the pollution type in the aquatic ecosystems [47,48,50,51,65,66,67,68,69,70].

3.3. Region

For this review, a distribution map of the localities where mass fish deaths occur in the freshwaters of Turkey was prepared based on the public information available (Figure 2). A fish parasite list was also prepared according to parasite surveys carried out in freshwaters where mass fish deaths occurred (Table 1). In addition, the existing pollution types and causes in these freshwaters where mass fish deaths occurred were examined with reference to the subject. As a result, we interpreted the usability of the related parasites as bioindicator species based on the current pollution in freshwaters where mass fish deaths occurred, and stressed the potential interrelations among the aquatic ecosystems’ pollution, fish parasites, and fish.
Turkey territory is geographically divided into seven main regions: Central Anatolia, Marmara, Black Sea, Eastern Anatolia, Southeastern Anatolia, Aegean, and Mediterranean [71]. In all of these freshwater ecosystems, one of the most obvious evidence of the presence of pollution is mass fish death events. The existence of 200 natural lakes [72] and 2.214 dam lakes and ponds [73] has been determined in Turkey. In this research, 56 ecosystems containing lakes, streams, and rivers were identified and recognized as places where mass fish deaths occurred, and parasitological studies were carried out in these regions of Turkey.
According to the identified type of pollution, there are domestic wastes and wastewaters in almost all of these freshwaters. Domestic pollutants are followed by pollutants originating from industrial and agricultural activities. There are also pollutants from mining, thermal or spa facilities, fish farms, and tourism sectors in some ecosystems.

4. Discussion

Several studies have shown that the prevalence of Paradiplozoon homoion increases in waters where eutrophication and thermal pollution are in effect [74,75,76]. Nevertheless, it has been found by various researchers that the prevalence of the parasite decreases in lakes where there is effluent and thermal pollution [67,75,77,78]. The prevalence of Paradiplozoon homoion was low in various fish, for example, 3.5% on Squalius cephalus in Büyükçekmece Dam Lake [79]; 0.8% on Rutilus rutilus in Manyas Lake [80]; and 10.4% on R. rutilus in Uluabat Lake [81]. Paradiplozoon megan was also found in low amounts (22.8%) on S. cephalus in Susurluk Stream [82].
Özdemir [83] showed that Büyükçekmece Lake has a mesotrophic character and that nitrogen and phosphorus loads from agricultural and industrial sources increased considerably from 1990 to 2000. Arı [84] emphasized the intensity of excessive eutrophication and showed that the pollution in Manyas Lake is of industrial origin. Kurtoglu et al. [85] determined that the high nitrogen and phosphorus pollution in Uluabat Lake was caused by agricultural, animal, and industrial wastewater carried from Mustafa Kemalpaşa Stream. Manyas, Uluabat Lakes, Büyükçekmece Dam Lake, and Susurluk Stream are mostly threatened by domestic, industrial, and agricultural pollution. Therefore, this may be the main cause of low infection.
The prevalence was reported to be high when examining the ecosystems where Dactylogyrus crucifer has been reported in Turkey. Selver [86] reported a 59.3% prevalence on R. rutilus from Kocadere Stream; 44% prevalence from Manyas Lake by Öztürk [80]; 87.6% prevalence from Sapanca Lake by Karabiber [87]; 90.6% prevalence from Uluabat Lake by Öztürk [81]; and 100% prevalence on Blicca bjoerkna from Sapanca Lake by Soylu [88].
Crafford et al. [89] detected an increase in the prevalence of Dactylogyrus with rising temperature. The reason for the high prevalence of Dactylogyrus crucifer in Turkey may be the increase in water temperature. Bagge and Valtonen [77] found an increase in prevalence in waters with effluent pollution, while Dušek et al. [90] found a decrease in the prevalence of Dactylogyrus in waters with eutrophication and organic pollution. The presence of pollution caused by domestic, industrial, and agricultural effluents in the ecosystems where Dactylogyrus has been reported has been demonstrated by various studies of, for example, Manyas Lake [84], Sapanca Lake [91], Kocadere Stream [92], and Uluabat Lake [85].
In contrast to Dactylogyrus crucifer, the prevalence values of Dactylogyrus vistulae are low. Gürkan and Tekin Özan [82] reported Dactylogyrus vistulae with 30.7% prevalence on S. cephalus from Susurluk Stream; 42.7% from Örenler Dam Lake by Kurupınar [93]; and 27.7% on Squalius carinus from Işıklı Dam Lake by Halmetoja et al. [94]. In these ecosystems, the decrease in the prevalence of Dactylogyrus vistulae may be explained by the presence of eutrophication and organic contamination [93].
Various researchers have shown that there is a decrease in the infection values in the monitoring studies of Tylodelphys clavata according to pollution type. Karvonen et al. [78] determined that the T. clavata tends to decrease in Carassius carassius where organic pollution is high; Valtonen et al. have shown that it tends to decrease in R. rutilus in waters where effluent is mixed [67]; and Halmetoja et al. have shown that it tends to decrease in Perca fluviatilis in waters with high acidification [94]. This digenea has been reported with infection rates of 6.6% in B. bjoerkna, 7.40% in R. rutilus, 13% in S. carinus, and 1% in Sander lucioperca in Turkey, by Altan and Soylu [95], Karabiber [87], and Soylu et al. [94], respectively.
Durmaz [96] determined that heavy metals such as arsenic, mercury, and selenium are at critical levels in Büyük Akgöl Lake due to industrial activities and pesticides. Altuğ [91] found higher levels of zinc, lead, copper, mercury, and cadmium in mussels than in fish samples in Sapanca Lake. She determined that heavy metal levels in fish in Sapanca Lake do not pose a danger to human health. However, she also emphasized that heavy metal pollution started in the lake. Bulut et al. [97] attributed the low dissolved oxygen data in Işıklı Lake to the presence of domestic, industrial, and agricultural wastes. Akbulut et al. [98] explained that eutrophication is very heavy in Bafra Fish Lakes and attributed it to the discharge of agricultural and domestic discharge waters into the lakes without any treatment.
As can be seen, Sapanca Lake and Büyük Akgöl Lakes, where the parasite is reported, are threatened by domestic and industrial pollution, while Işıklı Lake and Bafra Lake are mostly threatened by domestic and agricultural pollution. Therefore, the reason for the low rate of infection in these lakes is compatible with the findings of Valtonen et al. [67] and Altan and Soylu [95].
It has been found that Rhipidocotyle fennica in R. rutilus show a greater prevalence against pollution in ecosystems where wastewater is mixed [67,99]. Öztürk et al. [100] stated that Rhipidocotyle fennica (94%) is one of the dominant parasites in the seasonal distribution of parasites in Esox lucius in Uluabat Lake. As mentioned above [84], the mixing of the wastewater of Uluabat Lake has a possible effect on increasing the infection rate of this parasite.
Baruš et al. [101] reported low prevalence of Bathybothrium rectangulum in Barbus barbus from water containing heavy metals. Işıklı Dam Lake, where Dişçi [102] reported the parasite, is especially affected by agricultural activities including pesticides and fertilization. The detection of such low infection may be due to the heavy metal content of these pesticides.
It has been determined that, while pollution causes a decrease in the prevalence of Caryophyllaeus laticeps in lakes polluted by effluent [67,103], it causes an increase in lakes where metal and thermal pollution are present [79,103,104]. Prevalence of Caryophyllaeus laticeps was low in various fish; for example, it was 1.9% on R. rutilus in Büyükçekmece Dam Lake [79]; 8.3% on Abramis brama in Sakarya River [105]; 4.6% on R. rutilus in Uluabat Lake [81]; and 42.1% on Cyprinus carpio in Bendimahi River [106]. Pollution of wastewater is effective in Büyükçekmece Dam Lake [83], Sakarya River [107], Uluabat Lake [85], and Bendimahi Brook [108,109]. Therefore, these findings agree with those of Valtonen et al. [67] and Jirsa et al. [103]. The reason for the high level of parasite infection in Iznik Lake may be the wastes from industrial activities and from agricultural fertilizers and pesticides [110].
It has been found that pollution events causes a decrease in the prevalence of Ligula intestinalis in waters with heavy metal pollution [111], while it causes an increase in waters with waste pollution [67]. L. intestinalis from different ecosystems of Turkey were generally detected at low prevalence. It is reported that the prevalence was 0.8% from Manyas Lake [80], 6.9% from Çayırhan Stream [112], 1.5% from Eymir Lake and Sarıyar Dam Lake [113], 52.2% from Porsuk Stream [114], 6.9% from Demirköprü Dam Lake [112], 10.6% from Enne Dam Lake [115], 22% from Karacaören I. Dam Lake [116], 1.5% and 43.8% from Kars Stream in different years [117], and 18.7% and 7% from Devegecidi Dam Lake in different years [118]. When we compared with the prevalence of Ligula intestinalis in Turkey, it is consistent with the research findings of Gabrashanska and Nedeva [111] and Oyoo-Okoth et al. [112]. In these aquatic ecosystems, the pollution caused by the mixing of domestic and industrial wastes has been determined by various researchers, for example, in Manyas Lake [84], Çayırhan Stream [119], Eymir Lake [120], Sarıyar Dam Lake [121], Porsuk Creek [122], Demirköprü Dam Lake [123], Enne Dam Lake [124], Karacaören I. Dam Lake [125], Kars Stream [126], and Devegeçidi Dam Lake [127]. However, these findings do not agree with those of Valtonen et al. [67]. This may be because the distribution of L. intestinalis in fish was not examined seasonally, which is the reason for the low infection values of L. intestinalis in most of the studies conducted in Turkey.
Shah et al. [128] found an increase in the prevalence of Bothriocephalus acheilognathi in waters with organic pollution, while Khalil et al. [129] found a decrease in experimental studies of cadmium toxicity. When examining ecosystems where the parasite have been reported in Turkey, various researchers have shown that wastewaters from domestic, industrial, and agricultural activities negatively affect these ecosystems in such waterbodies as Mustafakemalpaşa Stream [130], Bendimahi Brook and Zernek Dam Lake [131], Hazar Lake [132], Karakaya Dam Lake [133], Keban Dam Lake [134], and Bafra Fish Lakes [98].
When the infection values of this parasite have been examined in Turkey, they have generally been found to be low. The prevalence of Bothriocephalus acheilognathi was low in various fish, such as 8.3% on Alburnus alburnus in Mustafakemalpaşa Stream [135]; 14% on C. carpio in Bendimahi Brook and Zernek Dam Lake [106]; 0.8% on Capoeta umbla in Hazar Lake [136]; 1.6 % on C. umbla and 20% on Acanthobrama marmid in Karakaya Dam Lake [137]; and 23% on A. marmid and 10.8 % on Chondrostoma regium in Keban Dam Lake [138].
For waters with metal contamination, Morley et al. [139] determined an increase in the prevalence of Proteocephalus torulosus, while Valtonen et al. [67] found a decrease in waters where the wastes were mixed. Low prevalence values of Proteocephalus torulosus were determined in studies conducted in Beyşehir Lake (3%) and Akşehir Lake (2.8%) [140,141]. According to [142], there are three main types of pollution affecting Akşehir Lake: agricultural fertilizers, medicines, and household wastes, which are wastes from a canned fruit factory. The pollution present in Beyşehir Lake is generated by the streams of domestic waste, pesticides and fertilizers, and factory waste (textiles, rifle factories, fish businesses, etc.) [143]. Therefore, the low prevalence of parasite infection is in line with Valtonen et al.’s [67] findings.
Valtonen et al. [67] and Karvonen et al. [78] determined a decrease in the prevalence of Neoechinorhynchus rutili in lakes where waste and organic pollution are present. When the studies conducted in Turkey were examined, generally low infection rates were also found, for example, 6.2% prevalence by Kavak and Şeker [144], 21% prevalence by Topçu [106], 29.2% prevalence by Aydoğdu et al. [145], and 4% prevalence by Öztürk et al. [146]. These lakes are especially threatened by domestic and industrial pollution. When the pollution types of the ecosystems where the parasite is reported were examined, the presence of domestic, agricultural, and industrial wastes was identified by various researchers, for example, in Bendimahi River [131], Keban Dam Lake [134], İznik Lake [110], and Sarıkum Lagoon [147].
A decrease in the prevalence values of Pomphorhynchus laevis was determined in the lakes and the experimental studies of heavy metal pollution [103,148,149,150]. Low infection rates were also reported in the ecosystems where this parasite was reported in Turkey. Burgu et al. [113] reported this parasite from Eymir Lake (0.3%), from Sarıyar Dam Lake (0.3%), and from Örenler Dam Lake (32.7%) by Kurupınar [93]. These lakes are in affected by heavy metal pollutants originating from pesticides and fertilizers from agricultural and animal activities. Soylu [151] reported this parasite with 83.3% prevalence from Karasu Stream, while 61.8% prevalence from Akşehir Lake was reported by Buhurcu [152]. Although both studies found a high percentage of infections, this could be attributed to the lack of seasonal study of parasites.
Filipović Marijić et al. [150] determined that the infection value decreased for Acanthocephalus anguillae in S. cephalus in the case of heavy metal contamination. Infection values of Acanthocephalus anguillae are low: 0.7% on E. lucius in Uluabat Lake [100] and 1% on Tinca tinca in Beyşehir Lake [140] in Turkey.
While an increase was found in the prevalence of Raphidascaris acus in waters with thermal and waste pollution [67,104], a decrease was found in waters with organic pollution [78]. There has been an increase in the infection values of the parasite in Sapanca and Uluabat Lakes, while waste pollution has been found in these lakes [91,153]. Soylu et al. [88] reported this parasite with 65.2% prevalence, while 96.2% prevalence was reported by Öztürk et al. [100]. There is intense organic pollution in Sakarya River and Karacabey Lagoon [107,154]. There was a decrease in the infection values in these ecosystems. This parasite was recorded with 15.7% and 18.1% prevalence by Öztürk et al. [100] and Akmırza and Yardımcı [105], respectively.
It has been determined that ergasilids tend to decrease in waters with eutrophication and organic pollution [75,78,155], effluent pollution [155], acidification [95], and thermal pollution [104]. A similar decrease has been observed in the infection values of ergasilids, even in some lakes in Turkey (Ömerli Dam Lake, Keban Dam Lake, Bafra Fish Lakes, Sarıkum Lagoon Lake). Ergasilus briani was recorded with 9.5% prevalence on Alburnus mossulensis by Sağlam [156], Ergasilus sieboldi with 13.5% prevalence on Alburnus istanbulensis by Şimşek [157], and 6.2% prevalence on C. regium and 0.5% prevalence on Capoeta trutta by Sağlam [156]. Considering the ecosystems where ergasilids have been reported in Turkey, there is the presence of the above-mentioned contaminants, for example, in Ömerli Dam Lake [158], Keban Dam Lake [134], Bafra Fish Lakes [98], and Sarıkum Lagoon [147].
Tuuha et al. [155] determined that the infection value of Paraergasilus longidigitus increased in waters with eutrophication and effluent pollution. The infection rate of the parasite in A. alburnus in Enne Dam Lake in Turkey was found to be higher (56.7%) than that of other ergasilids. In the Enne Dam Lake, where the parasite is reported, there is thermal pollution in addition to waste pollution [126].
Infection values of the parasitic copepods were generally found to be significantly low. Lernaea cyprinacea was reported with 6.4% prevalence on C. carpio (Tahtalı Dam Lake) by Karakişi and Demir [159]; 5% on Cyprinion macrostomum from Murat River by Koyun et al. [160]; 31.3% on Pseudophoxinus egridiri from Egirdir Lake by Akçimen et al. [161]; and Lamproglena pulchella was reported with 28.5% on C. trutta from Keban Dam Lake by Sağlam [156].
In Tóro et al.’s [162] laboratory study, it was determined that oil and petroleum waste caused a decrease in the prevalence of Lernaea cyprinacea, while Galli et al.’s [66] field study determined the limiting effect of pollution on Lamproglena pulchella.
When the pollution status of the lakes where Lernaea cyprinacea are reported was examined, pollution from industrial, mining, and oil exploration activities was found [163,164,165]. Similarly, domestic and agricultural contamination has been identified in Keban Dam Lake, where Lamproglena pulchella was previously reported.
A decrease in the prevalence of Argulus foliaceus was found in a lake where organic pollution was present, by Karvonen et al. [78], and in an experiment on metal pollution by Pettersen et al. [166]. When the infection values of the parasite were examined in Turkey, low infection rates were observed. Öztürk [167] reported argulus with 6.5% prevalence on C. carpio, while 10.7% was reported on C. carassius by Tekin Özan and Kır [141]; 1.3% on Planiza abu and 14.3% on Mastacembelus mastacembelus by Öktener et al. [168]; and 19.1% on C. carpio and 11.1% on Carasobarbus luteus by Öktener and Alaş [169]. These lakes are under the influence of both organic pollution and metal pollution.
Altan and Soylu [95] found a decrease in the infection values of Piscicola geometra in inland waters with acidification, and Jirsa et al. found the same in waters with effluent pollution [103]. When the ecosystems where Piscicola geometra has been reported were examined, the infection values of the parasite were reported to be low. A prevalence of 4.9% on B. bjoerkna was reported by Altan and Soylu [95]; 1.2% on R. rutilus was found by Karabiber [87]; 2.1% on Barbus rajanorum was found by Sağlam [156]; and 1.4% on T. tinca was reported by Öztürk [80]. The presence of wastewater pollution in the mentioned lakes (Büyük Akgöl, Sapanca, Keban Dam, Uluabat) has been identified by the researchers mentioned above. Therefore, these findings from Turkey overlap with those of Altan and Soylu [95] and Jirsa et al. [103].
Karvonen et al. [78] reported that the prevalence value of glochid in fish tends to decrease in waters with eutrophication and organic pollution, and Pettersen et al. [166] found the same in waters with metal pollution. In these aquatic environments, where glochids are reported in Turkey, there is intense pollution, as stated above. Altan and Soylu [95] reported glochid prevalence with 21.3% on B. bjoerkna; 18.1% on A. brama was reported by Akmırza and Yardımcı [105]; and 8.8% on T. tinca was found by Akbeniz [170].
There are few studies on the accumulation of pollutants in parasites in determining the pollution in freshwaters in Turkey. Tekin Özan and Kır [58] pointed out that Ligula intestinalis (Cestoda) might be a suitable biomonitor species in the determination of heavy metal pollution in their study of Kovada Lake, while, in two studies conducted in Beyşehir Lake, it was stated that it was not useful as a biomonitor species [60]. Tekin Özan and Kır’s [59] study on pike reported that Raphidascaris acus (Nematoda) is a reliable species in the determination of heavy metal pollution in Işıklı Lake. Genç et al. [60] described Anguillicola crassus (Nematoda) as a useful species in the determination of heavy metal pollution in their study on parasites of European eel in the Asi River.

5. Conclusions

Fish parasites generally occur in equilibrium with their hosts in natural environments. In the freshwater ecosystems of Turkey, which are highly affected by human activities and which have extremely rich natural ichthyofauna, the negative effects of pollution on environmental parameters, which can directly affect fish, and the emergence and overextension of fish parasites can cause a supplementary synergic direct negative effect transposition in mass fish deaths due to the deterioration of host immunity and to the induced wounds in fish where bacterial, viral, and fungal pathogens can be effective. Finally, they can influence the fish rate of survival and skew the structure of fish populations.
Mass fish deaths have been frequently reported in Turkey, but are usually explained only by pollution as a single accepted anthropogenic stressor. Together with pollution, a supplementary induced bioecological stressor, the qualitative and quantitative characteristics of the fish parasites’ association variations should be assessed and monitored as potential complex precursor indicators of fish communities’ structural degradation and freshwater ecosystems’ dreadful conditions.
There are many studies across the world on the use of fish parasites as biomonitors in the determination of pollution in aquatic ecosystems. Classical laboratory methods are generally used to determine the pollution in freshwaters in Turkey. Fish parasites as biomonitor species should be used to identify pollution in freshwaters in the future. An optimum freshwater ecosystem management plan should contain all the physico-chemical factors, and fish parasite and fish elements should be involved in permanent monitoring, analysis, and management activities.
This type of research approach is inchoate, opening a new research field of interest. What is required in the future is to be able to identify and indicate individually which parasites and which ecological circumstances are good indicators of a specific or complex case of contamination. It should also be stressed that the interrelated causes and effects should create synergic situations, and one cause should not be attributed to one specific contamination effect.

Author Contributions

Conceptualization, A.Ö. and D.B.; methodology, A.Ö. and D.B.; software, A.Ö. and D.B.; validation, D.B.; formal analysis, A.Ö. and D.B.; investigation, A.Ö.; data curation, A.Ö.; writing—original draft preparation, A.Ö. and D.B.; writing—review and editing, A.Ö. and D.B.; visualization, A.Ö. and D.B.; supervision D.B.; project administration, A.Ö.; funding acquisition, A.Ö. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding. The APC of the paper was funded by Ecotur Sibiu Associon.

Informed Consent Statement

All the co-authors have checked and approved this form of the accepted research paper.

Data Availability Statement

There are no supplementary data, and no part of any publicly archived datasets were analyzed or generated during the study.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Bradley, J.; Cardinale, A.G.; Allington, G.R.H.; Loreau, M. Is local biodiversity declining or not? A summary of the debate over analysis of species richness time trends. Biol. Conserv. 2018, 219, 175–183. [Google Scholar]
  2. Ceballos, G.; Ehrlich, P.R.; Barnosky, A.D.; García, A.; Pringle, R.M.; Palmer, T.M. Accelerated modern human–induced species losses: Entering the sixth mass extinction. Sci. Adv. 2015, 1, e1400253. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  3. SCBD. Global Biodiversity Outlook 4, Secretariat of the Convention on Biological Diversity, Montreal. 2014. Available online: http://www.emdashdesign.ca (accessed on 22 September 2022).
  4. Perujo, N.; Van den Brink, P.J.; Segner, H.; Mantyka-Pringle, C.; Sabater, S.; Birk, S.; Bruder, A.; Romero, F.; Acuña, V. A guideline to frame stressor effects in freshwater ecosystems. Sci. Total Environ. 2021, 777, 146112. [Google Scholar] [CrossRef] [PubMed]
  5. Bănăduc, D.; Barinova, S.; Cianfaglione, K.; Curtean-Bănăduc, A. Editorial: Multiple freshwater stressors—Key drivers for the future of freshwater environments. Front. Environ. Sci. 2023, in press. [Google Scholar] [CrossRef]
  6. Bănăduc, D.; Simić, V.; Cianfaglione, K.; Barinova, S.; Afanasyev, S.; Öktener, A.; McCall, G.; Simić, S.; Curtean-Bănăduc, A. Freshwater as a Sustainable Resource and Generator of Secondary Resources in the 21st Century: Stressors, Threats, Risks, Management and Protection Strategies, and Conservation Approaches. Int. J. Environ. Res. Public Health 2022, 19, 16570. [Google Scholar] [CrossRef]
  7. Stark, J.S. Heavy metal pollution and macrobenthic assemblages in soft sediments in two Sydney estuaries, Australia. Mar. Freshw. Res. 1998, 49, 533–540. [Google Scholar] [CrossRef]
  8. Curtean-Bănăduc, A.; Olosutean, H.; Bănăduc, D. Influence of environmental variables on the structure and diversity of ephemeropteran communities: A case study of the Timiş River, Romania. Acta Zool. Bulg. 2016, 68, 215–224. [Google Scholar]
  9. Barletta, M.; Lima, A.R.; Costa, M.F. Distribution, sources and consequences of nutrients, persistent organic pollutants, metals and microplastics in South American estuaries. Sci. Total Environ. 2019, 651, 1199–1218. [Google Scholar] [CrossRef]
  10. Curtean-Bănăduc, A.; Burcea, A.; Mihuţ, C.-M.; Bănăduc, D. The Benthic Trophic Corner Stone Compartment in POPs Transfer from Abiotic Environment to Higher Trophic Levels—Trichoptera and Ephemeroptera Pre-Alert Indicator Role. Water 2021, 13, 1778. [Google Scholar] [CrossRef]
  11. Horak, I.; Horn, S.; Pieters, R. Agrochemicals in freshwater systems and their potential as endocrine disrupting chemicals: A South African context. Environ. Pollut. 2021, 268, 115718. [Google Scholar] [CrossRef]
  12. Chen, H.L.; Selvam, S.B.; Ting, K.N.; Gibbins, C.N. Microplastic pollution in freshwater systems in Southeast Asia: Contamination levels, sources, and ecological impacts. Environ. Sci. Pollut. Res. 2021, 28, 54222–54237. [Google Scholar] [CrossRef] [PubMed]
  13. Bănăduc, A. Data concerning the benthic communities of the Cibin River (Olt River Basin) Transylv. Transylv. Rev. Syst. Ecol. Res. 1999, 1, 99–110. [Google Scholar]
  14. Barinova, S.; Dyadichko, V. Zoological Water Quality Indicators for Assessment of Organic Pollution and Trophic Status of Continental Water Bodies. Transylv. Rev. Syst. Ecol. Res. 2022, 24, 65–106. [Google Scholar] [CrossRef]
  15. Curtean-Bănăduc, A.; Burcea, A.; Mihuţ, C.-M.; Berg, V.; Lyche, J.L.; Bănăduc, D. Bioaccumulation of persistent organic pollutants in the gonads of Barbus barbus (Linnaeus, 1758). Ecotoxicol. Environ. Saf. 2020, 201, 110852. [Google Scholar] [CrossRef] [PubMed]
  16. Bănăduc, D.; Marić, S.; Cianfaglione, K.; Afanasyev, S.; Somogyi, D.; Nyeste, K.; Antal, L.; Koščo, J.; Ćaleta, M.; Wanzenböck, J.; et al. Stepping Stone Wetlands, Last Sanctuaries for European Mudminnow: How Can the Human Impact, Climate Change, and Non-Native Species Drive a Fish to the Edge of Extinction? Sustainability 2022, 14, 13493. [Google Scholar] [CrossRef]
  17. Boeraș, I.; Curtean-Bănăduc, A.; Bănăduc, D.; Cioca, G. Anthropogenic Sewage Water Circuit as Vector for SARS-CoV-2 Viral ARN Transport and Public Health Assessment, Monitoring and Forecasting—Sibiu Metropolitan Area (Transylvania/Romania) Study Case. Int. J. Environ. Res. Public Health 2022, 19, 11725. [Google Scholar] [CrossRef]
  18. Bănăduc, D.; Oprean, L.; Bogdan, A. Fish Species Community Interest Management Issues in Natura 2000 Site Sighișoara-Târnava Mare (Transylvania, Romania). In Proceedings of the 18th International Economic Conference on Crisis After the Crisis—Inquiries from a National European and Global Perspective, Sibiu, Romania, 19–20 May 2011; pp. 23–27. [Google Scholar]
  19. Bănăduc, D.; Curtean-Bănăduc, A.; Cianfaglione, K.; Akeroyd, J.R.; Cioca, L.-I. Proposed Environmental Risk Management Elements in a Carpathian Valley Basin, within the Roşia Montană European Historical Mining Area. Int. J. Environ. Res. Public Health 2021, 18, 4565. [Google Scholar] [CrossRef]
  20. Simić, V.; Bănăduc, D.; Curtean-Bănăduc, A.; Petrović, A.; Veličković, T.; Stojković-Piperac, M.; Simić, S. Assessment of the ecological sustainability of river basins based on the modified the ESHIPPOfish model on the example of the Velika Morava basin (Serbia, Central Balkans). Front. Environ. Sci. 2022, 10, 1125. [Google Scholar] [CrossRef]
  21. Bănăduc, D.; Joy, M.; Olosutean, H.; Afanasyev, S.; Curtean-Bănăduc, A. Natural and anthropogenic driving forces as key elements in the Lower Danube Basin–South-Eastern Carpathians–North-Western Black Sea coast area lakes: A broken stepping stones for fish in a climatic change scenario? Environ. Sci. Eur. 2020, 32, 73. [Google Scholar] [CrossRef]
  22. Virga, G.; Arnieri, F.; Costantino, M. Differences in Growth Pattern in Two Freshwater Fish Species (Leuciscidae) during Summer Drought in North-West Italy, Transylv. Rev. Syst. Ecol. Res. 2023, 25, 55–64. [Google Scholar]
  23. Bănăduc, D.; Sas, A.; Cianfaglione, K.; Barinova, S.; Curtean-Bănăduc, A. The Role of Aquatic Refuge Habitats for Fish, and Threats in the Context of Climate Change and Human Impact, during Seasonal Hydrological Drought in the Saxon Villages Area (Transylvania, Romania). Atmosphere 2021, 12, 1209. [Google Scholar] [CrossRef]
  24. Zare-Shahraki, M.; Ebrahimi-Dorche, E.; Bruder, A.; Flotemersch, J.; Blocksom, K.; Bănăduc, D. Fish Species Composition, Distribution and Community Structure in Relation to Environmental Variation in a Semi-Arid Mountainous River Basin, Iran. Water 2022, 14, 2226. [Google Scholar] [CrossRef] [PubMed]
  25. Çiçek, E.; Fricke, R.; Sungur, S.; Eagderi, S. Endemic freshwater fishes of Turkey. FishTaxa 2018, 3, 1–39. [Google Scholar]
  26. Şekercioğlu, Ç.H.; Anderson, S.; Akçay, E.; Bilgin, R.; Can, Ö.E.; Semiz, G.; Tavşanoğlu, Ç.; Yokeş, M.B.; Soyumert, A.; Ipekdal, K.; et al. Turkey’s globally important biodiversity in crisis. Biol. Conserv. 2011, 144, 2752–2769. [Google Scholar] [CrossRef]
  27. FishBase. World Wide Web Electronic Publication. Version (08/2021). Froese, R.; Pauly, D. (Eds.) 2021. Available online: www.fishbase.org (accessed on 1 August 2021).
  28. Içek, E.; Birecikligil, S.S.; Ronald, F. Freshwater fishes of Turkey: A revised and updated annotated checklist. Biharean Biol. 2015, 9, 141–157. [Google Scholar]
  29. Tarkan, A.S.; Marr, S.M.; Ekmekçi, F.G. Non-native and translocated freshwater fish species in Turkey. FiSHMED Fishes Mediterr. Environ. 2015, 3, 1–28. [Google Scholar] [CrossRef]
  30. Ulman, A.; Zengin, M.; Demirel, N.; Pauly, D. The Lost Fish of Turkey: A Recent History of Disappeared Species and Commercial Fishery Extinctions for the Turkish Marmara and Black Seas. Front. Mar. Sci. 2020, 7, 650. [Google Scholar] [CrossRef]
  31. Curtean-Bănăduc, A.; Bănăduc, D.; Bucşa, C. Watersheds management (Transylvania/ Romania): Implications, risks, solutions, Strategies to enhance environmental security in transition countries. In NATO Science for Peace and Security Series C: Environmental Security; Springer: Dordrecht, The Netherlands, 2007; p. 225. [Google Scholar] [CrossRef]
  32. Costea, G.; Pusch, M.T.; Bănăduc, D.; Cosmoiu, D.; Curtean-Bănăduc, A. A review of hydropower plants in Romania: Distribution, current knowledge, and their effects on fish in headwater streams. Renew. Sustain. Energy Rev. 2021, 145, 111003. [Google Scholar] [CrossRef]
  33. Curtean-Bănăduc, A.; Marić, S.; Gábor, G.; Didenko, A.; Planellas, S.R.; Bănăduc, D. Hucho hucho (Linnaeus, 1758): Last natural viable population in the Eastern Carpathians—Conservation elements. Turk. J. Zool. 2019, 43, 215–223. [Google Scholar] [CrossRef]
  34. Burcea, A.; Boeraş, I.; Mihuţ, C.-M.; Bănăduc, D.; Matei, C.; Curtean-Bănăduc, A. Adding the Mureş River Basin (Transylvania, Romania) to the List of Hotspots with High Contamination with Pharmaceuticals. Sustainability 2020, 12, 10197. [Google Scholar] [CrossRef]
  35. Ktener, A.; Eğribaş, E.; Başusta, N. A preliminary investigation on serious mortalities of fish in Balıklıgöl (Halil-ür Rahman Gölü, Şanlıurfa). Gazi Univ. J. Sci. 2008, 21, 9–13. [Google Scholar]
  36. Yabanlı, M.; Türk, N.; Tenekecioğlu, E.; Uludağ, R. A Research for Massive Fish Kills in Lake Bafa (Turkey). Sakarya Univ. J. Sci. 2011, 15, 36–40. [Google Scholar]
  37. Pekmezci, G.Z.; Yardimci, B.; Bolukbas, C.S.; Beyhan, Y.E.; Umur, S. Mortality Due to Heavy Infestation of Argulus foliaceus (Linnaeus, 1758) (Branchiura) in Pond-Reared Carp, Cyprinus carpio L., 1758 (Pisces). Crustaceana 2011, 84, 553–557. [Google Scholar] [CrossRef]
  38. MacKenzie, K. Parasites as biological tags in population studies of marine organisms: An update. Parasitology 2002, 124, S153–S163. [Google Scholar] [CrossRef] [PubMed]
  39. Mackenzie, K.; Hemmingsen, W. Parasites as biological tags in marine fisheries research: European Atlantic waters. Parasitology 2015, 142, 54–67. [Google Scholar] [CrossRef] [PubMed]
  40. Del Monte-Luna, P.; Brook, B.W.; Zetina-Rejón, M.J.; Cruz-Escalona, V.H. The carrying capacity of ecosystems. Glob. Ecol. Biogeogr. 2004, 13, 485–495. [Google Scholar] [CrossRef]
  41. Iwanowicz, D.D. Overview on the effects of parasites on fish health. In Proceedings of the Third Bilateral Conference between Russia and the United States. Bridging America and Russia with Shared Perspectives on Aquatic Animal Health, USGS Organization, Leetown Science Center, USA; 2011; pp. 176–184. Available online: https://citeseerx.ist.psu.edu/document?repid=rep1&type=pdf&doi=464af280b7778724425654fe3f557768b1fc0846 (accessed on 10 February 2023).
  42. Zeeman, M.G.; Brindley, W.A. Effects of toxic agents upon fish immune systems: A review. Immunol. Consid. Toxicol. 1981, 2, 1–60. [Google Scholar]
  43. Wojdani, A.; Alfred, L.J. Alterations in cell-mediated immune functions induced in mouse splenic lymphocytes by polycyclic aromatic hydrocarbons. Cancer Res. 1984, 44, 942–945. [Google Scholar] [PubMed]
  44. Poulin, R. Toxic pollution and parasitism in freshwater fish. Parasitol. Today 1992, 8, 58–61. [Google Scholar] [CrossRef] [PubMed]
  45. Karr, J.R. Biological Monitoring cf Aquatic Systems; Loeb, S.L., Spacie, S., Eds.; Kerr Center for Sustainable Agriculture (USA), 1994; pp. 357–373. Available online: https://kerrcenter.com/ (accessed on 10 February 2023).
  46. Sprague, J.B. Measurement of pollutant toxicity to fish I. Bioassay methods for acute toxicity. Water Res. 1969, 3, 793–821. [Google Scholar] [CrossRef]
  47. Khan, R.A.; Thulin, J. Influence of Pollution on Parasites of Aquatic Animals. Adv. Parasitol. 1991, 30, 201–238. [Google Scholar] [CrossRef] [PubMed]
  48. MacKenzie, K.; Williams, H.H.; Williams, B.; McVicar, A.H.; Siddall, R. Parasites as Indicators of Water Quality and the Potential Use of Helminth Transmission in Marine Pollution Studies. Adv. Parasitol. 1995, 35, 85–144. [Google Scholar] [CrossRef] [PubMed]
  49. Lafferty, K.D. Environmental parasitology: What can parasites tell us about human impacts on the environment? Parasitol. Today 1997, 13, 251–255. [Google Scholar] [CrossRef] [PubMed]
  50. Sures, B. The use of fish parasites as bioindicators of heavy metals in aquatic ecosystems: A review. Aquat. Ecol. 2001, 35, 245–255. [Google Scholar] [CrossRef]
  51. Gilbert, B.M.; Avenant-Oldewage, A. Parasites and pollution: The effectiveness of tiny organisms in assessing the quality of aquatic ecosystems, with a focus on Africa. Environ. Sci. Pollut. Res. Int. 2017, 24, 18742–18769. [Google Scholar] [CrossRef]
  52. Öktener, A. A checklist of metazoan parasites recorded in freshwater fish from Turkey. Zootaxa 2003, 394, 1–28. [Google Scholar] [CrossRef]
  53. Öktener, A. A checklist of parasitic helminths reported from sixty-five species of marine fish from Turkey including two new records of monogeneans. Zootaxa 2005, 1063, 33–52. [Google Scholar] [CrossRef]
  54. Öktener, A. Revision of Parasitic Helminths Reported in Freshwater Fish from Turkey with New Records. Transylv. Rev. Syst. Ecol. Res. 2014, 16, 1–56. [Google Scholar] [CrossRef] [Green Version]
  55. Öktener, A. An Updated Checklist of Parasitic Helminths of Marine Fish from Turkey. Transylv. Rev. Syst. Ecol. Res. 2015, 16, 55–96. [Google Scholar] [CrossRef] [Green Version]
  56. Alaş, A.; Öktener, A.; Türker, D.Ç. Review of Parasitic Copepods Recorded in Fish from Turkey. Transylv. Rev. Syst. Ecol. Res. 2015, 17, 39–62. [Google Scholar] [CrossRef] [Green Version]
  57. Alaş, A.; Öktener, A. Different Parasitic Phyla of Fish from Turkey excluding Helminths and Crustacea. J. Zool. Stud. 2015, 2, 24–41. [Google Scholar]
  58. Tekin Özan, S.; Kır, İ. An investigation of parasites of goldfish (Carassius carassius L., 1758) in Kovada Lake. Turk. Parazitolojii Derg. 2005, 29, 200–203. [Google Scholar]
  59. Tekin-Özan, S.; Kir, I. Accumulation of some heavy metals in Raphidascaris acus (Bloch, 1779) and its host (Esox lucius L., 1758). Türkiye Parazitoloji Derg. 2007, 31, 327–329. [Google Scholar]
  60. Genc, E.; Sangun, M.K.; Dural, M.; Can, M.F.; Altunhan, C. Element concentrations in the swimbladder parasite Anguillicola crassus (nematoda) and its host the European eel, Anguilla anguilla from Asi River (Hatay-Turkey). Environ. Monit. Assess. 2008, 141, 59–65. [Google Scholar] [CrossRef] [PubMed]
  61. WoRMS Editorial Board. World Register of Marine Species. 2022. Available online: https://www.marinespecies.org (accessed on 3 April 2022).
  62. Grant, B.; Huchzermeyer, D.; Hohls, B. Manual for Fish Kill Investigations in South Africa (WRC Report No. TT 589/14); Research Commission of South Africa: Report to the Water Research Commission; 2014; 135p, ISBN 978-1-4312-0531-8. Available online: https://www.coastkzn.co.za/wp-content/uploads/2019/02/TT589-14-WEB.pdf (accessed on 22 September 2022).
  63. Helfrich, L.A.; Smith, S.A. Fish Kills: Their Causes and Prevention; Communications and Marketing, College of Agriculture and Life Sciences, Virginia Polytechnic Institute State University: Blacksburg, VA, USA, 2009; pp. 252–420. [Google Scholar]
  64. Meyer, F.P.; Barclay, L.A. (Eds.) Field Manual for the Investigation of Fish Kills; Resource Publication 177; U.S. Fish and Wildlife Service: Washington, DC, USA, 1990; 120p.
  65. Mackenzie, K. Parasites as Pollution Indicators in Marine Ecosystems: A Proposed Early Warning System. Mar. Pollut. Bull. 1999, 38, 955–959. [Google Scholar] [CrossRef]
  66. Galli, P.; Crosa, G.; Mariniello, L.; Ortis, M.; D’Amelio, S. Water quality as a determinant of the composition of fish parasite communities. Hydrobiologia 2001, 452, 173–179. [Google Scholar] [CrossRef]
  67. Valtonen, E.T.; Holmes, J.C.; Aronen, J.; Rautalahti, I. Parasite communities as indicators of recovery from pollution: Parasites of roach (Rutilus rutilus) and perch (Perca fluviatilis) in Central Finland. Parasitology 2003, 126, S43–S52. [Google Scholar] [CrossRef]
  68. Marcogliese, D.J. Parasites: Small Players with Crucial Roles in the Ecological Theater. EcoHealth 2004, 1, 151–164. [Google Scholar] [CrossRef]
  69. Sures, B. Environmental parasitology: Relevancy of parasites in monitoring environmental pollution. Trends Parasitol. 2004, 20, 170–177. [Google Scholar] [CrossRef]
  70. Sures, B.; Nachev, M.; Selbach, C.; Marcogliese, D.J. Parasite responses to pollution: What we know and where we go in ‘Environmental Parasitology’. Parasites Vectors 2017, 10, 65. [Google Scholar] [CrossRef] [Green Version]
  71. Gezici, F. Bölge Sınırlarının Saptanmasında Yararlanılacak Ölçütler; Türkiye’de Bölgesel Yönetim—Bir Model Önerisi; Toksöz, F., Gezici, F., Eds.; Türkiye Ekonomik ve Sosyal Etüdler Vakfı, 2014; pp. 17–30. Available online: https://www.google.ca/search?q=T%C3%BCrkiye+Ekonomik+ve+Sosyal+Et%C3%BCdler+Vakf%C4%B1&ei=E5wqZP_6Arax2roPm7CUiAc&ved=0ahUKEwi_0Ibgso3-AhW2mFYBHRsYBXEQ4dUDCA4&uact=5&oq=T%C3%BCrkiye+Ekonomik+ve+Sosyal+Et%C3%BCdler+Vakf%C4%B1&gs_lcp=Cgxnd3Mtd2l6LXNlcnAQAzIQCC4QgAQQxwEQ0QMQExDqBDIGCAAQHhATMggIABAeEA8QEzoKCAAQRxDWBBCwA0oECEEYAFDPA1jPA2DRC2gBcAF4AIABzAGIAcwBkgEDMi0xmAEAoAECoAEByAECwAEB&sclient=gws-wiz-serp (accessed on 10 February 2023).
  72. Anonymous. Ramsar Sites Assessment Report in Turkey; WWF-Turkey, Wildlife Conservation Foundation: Ankara, Turkey, 2008; 129p. [Google Scholar]
  73. Anonymous. State Hydraulic Works 2020 Annual Report; Ministry of Agriculture and Forestry, General Directorate of State Hydraulic Works: Ankara, Turkey, 2020; 159p.
  74. Höglund, J.; Thulin, J. Thermal effects on the seasonal dynamics of Paradiplozoon homoion (Bychowsky & Nagibina, 1959) parasitizing roach, Rutilus rutilus (L.). J. Helminthol. 1989, 63, 93–101. [Google Scholar] [CrossRef]
  75. Koskivaara, M.; Valtonen, E.T. Paradiplozoon homoion (Monogenea) and some other gill parasites on roach Rutilus rutilus in Finland. Aqua Fenn. 1991, 21, 137–143. [Google Scholar]
  76. Šebelová, Š.; Kuperman, B.; Gelnar, M. Abnormalities of the attachment clamps of representatives of the family Diplozoidae. J. Helminthol. 2002, 76, 249–259. [Google Scholar] [CrossRef] [PubMed]
  77. Bagge, A.M.; Valtonen, E.T. Experimental study on the influence of paper and pulp mill effluent on the gill parasite communities of roach (Rutilus rutilus). Parasitology 1996, 112, 499–508. [Google Scholar] [CrossRef]
  78. Karvonen, A.; Bagge, A.M.; Valtonen, E.T. Parasite assemblages of crucian carp (Carassius carassius)—Is depauperate composition explained by lack of parasite exchange, extreme environmental conditions or host unsuitability? Parasitology 2005, 131, 273–278. [Google Scholar] [CrossRef]
  79. Yardımcı, R.E.; Ürkü, Ç.; Yardımcı, C.H. Parasite fauna of fish in Büyükçekmece Dam Lake. Erzincan Univ. J. Sci. Technol. 2018, 11, 158–167. [Google Scholar] [CrossRef]
  80. Öztürk, M.O. Helminth Fauna of Fishes in Manyas (Kuş) Lake. Ph.D. Thesis, Uludag University, Bursa, Turkey, 2000. [Google Scholar]
  81. Öztürk, M.O. Helminth Fauna of Two Cyprinid Fish Species (Chalcalburnus chalcoides Güldenstadt, 1972, Rutilus rutilus L.) from lake Uluabat, Turkey. Hacet. J. Biol. Chem. 2005, 34, 77–91. [Google Scholar]
  82. Gürkan, Ü.; Tekin Özan, S. Helminth fauna of chub (Squalius cephalus L.) in Susurluk Creek (Bursa-Balıkesir). S.D.U. J. Nat. Appl. Sci. 2012, 7, 77–85. [Google Scholar]
  83. Özdemir, A.C. Impacts of Land Use on Water Quality in Istanbul Watersheds. Master’s Thesis, İstanbul Teknik University, İstanbul, Turkey, 2010. [Google Scholar]
  84. Arı, Y. Cultural Ecology of Lake Manyas: Adaptation and Change in Historical Perspective. Turk. Geogr. Rev. 2014, 40, 75–97. [Google Scholar]
  85. Kurtoglu, S.; Ozengin, N.; Elmaci, A.; Baskaya, H.S. Monitoring of Sediment Quality and Nutrients Dynamics of Lake Uluabat, Turkey. J. Biol. Environ. Sci. 2015, 9, 11–19. [Google Scholar]
  86. Selver, M.M. Helminth Fauna of Some Fish Species Catched from Kocadere Stream. Ph.D. Thesis, Uludag University, Bursa, Turkey, 2008. [Google Scholar]
  87. Karabiber, F.T. Parasite Fauna of Roach (Rutilus rutilus Linnaeus, 1758) in the Lake Sapanca. Master’s Thesis, Marmara University, İstanbul, Turkey, 2006. [Google Scholar]
  88. Soylu, E. Research Studies on the Parasite Fauna of Some Fishes in Sapanca Lake. Ph.D. Thesis, Istanbul University, Istanbul, Turkey, 1990. [Google Scholar]
  89. Crafford, D.; Luus-Powell, W.; Avenant-Oldewage, A. Monogenean parasites from fishes of the Vaal Dam, Gauteng Province, South Africa I. Winter survey versus summer survey comparison from Labeo capensis (Smith 1841) and Labeo umbratus (Smith, 1841) hosts. Acta Parasitol. 2014, 59, 17–24. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  90. Dušek, L.; Gelnar, M.; Šebelová, Š. Biodiversity of parasites in a freshwater environment with respect to pollution: Metazoan parasites of chub (Leuciscus cephalus L.) as a model for statistical evaluation. Int. J. Parasitol. 1998, 28, 1555–1571. [Google Scholar] [CrossRef] [PubMed]
  91. Altuğ, G. Heavy Metal Pollution in Sapanca Lake: Sediment, Fish, Mussel; Sapanca Gölü’ne Bilimsel Açıdan Bakış; Okgerman, H., Aktuğ, G., Eds.; TÜDAV Yayınları, 2008; pp. 149–156. Available online: https://tudav.org/calismalar/yayinlar/ (accessed on 10 February 2023).
  92. lmez, G. Determination of Environmental Objectives for Improvement of Water Quality in Surface Water Resources. Master’s Thesis, Ministry of Forestry and Water Affairs, Ankara, Turkey, 2014. [Google Scholar]
  93. Soylu, E.; Uzmanoğlu, S.; Özesen Çolak, S.; Soylu, M.P. Community Structure of the Parasites of the Endemic Chocolate Chub Squalius carinus Özuluğ & Freyhof, 2011 (Cyprinidae) from Işıklı Lake, Çivril, Turkey. Acta Zool. Bulg. 2017, 69, 405–409. [Google Scholar]
  94. Halmetoja, A.; Valtonen, E.T.; Koskenniemi, E. Perch (Perca fluviatilis L.) parasites reflect ecosystem conditions: A comparison of a natural lake and two acidic reservoirs in Finland. Int. J. Parasitol. 2000, 30, 1437–1444. [Google Scholar] [CrossRef]
  95. Altan, A.; Soylu, E. Composition and structure of parasite communities in white bream Blicca bjoerkna from Lake Büyük Akgöl, Sakarya-Turkey. Ege J. Fish. Aquat. Sci. 2018, 35, 199–206. [Google Scholar] [CrossRef]
  96. Durmaz, A. Evaluation of Heavy Metal Pollution and Sources in Shallow Lakes. Master’s Thesis, Sakarya University, Sakarya, Turkey, 2019. [Google Scholar]
  97. Bulut, C.; Atay, R.; Uysal, K.; Köse, E. Evaluation of Surface Water Quality in Çivril Lake. Anadolu Univ. J. Sci. Technol. C-Life Sci. Biotechnol. 2012, 2, 1–8. [Google Scholar]
  98. Akbulut, M.; Bat, L.; Çulha, M.; Satılmış, H. Problems of Kızılırmak Delta and solution methods. In Proceedings of the Aquatic Products Symposium, Sinop, Turkey, 20–22 September 2000; pp. 655–661. [Google Scholar]
  99. Jeney, Z.; Valtonen, E.T.; Jeney, G.; Jokinen, E.I. Effect of pulp and paper mill effluent (BKME) on physiological parameters of roach (Rutilus rutilus) infected by the digenean Rhipidocotyle fennica. Folia Parasitol. 2002, 49, 103–108. [Google Scholar] [CrossRef] [Green Version]
  100. Öztürk, M.O.; Oğuz, M.C.; Altunel, F.N. Metazoon parasites of pike (Esox lucius L.) from Uluabat Lake. Isr. J. Zool. 2000, 46, 119–130. [Google Scholar] [CrossRef]
  101. Baruš, V.; Šimková, A.; Prokeš, M.; Peňáz, M.; Vetešník, L. Heavy metals in two host-parasite systems: Tapeworm vs. fish. Acta Vet. Brno 2012, 81, 313–317. [Google Scholar] [CrossRef] [Green Version]
  102. Dişçi, H. Determination of Endoparasites of Pike-Perch (Esox lucius L., 1758) Inhabiting Işıklı Dam Lake. Master’s Thesis, Süleyman Demirel University, Isparta, Turkey, 2002. [Google Scholar]
  103. Jirsa, F.; Konecny, R.; Frank, C.; Sures, B. The parasite community of the nase Chondrostoma nasus (L. 1758) from Austrian rivers. J. Helminthol. 2011, 85, 255–262. [Google Scholar] [CrossRef]
  104. Pilecka-Rapacz, M.; Piasecki, W.; Czerniawski, R.; Sługocki, Ł.; Krepski, T.; Domagała, J. The effect of warm discharge waters of a power plant on the occurrence of parasitic Metazoa in freshwater bream, Abramis brama (L.). Bull. Eur. Assoc. Fish Pathol. 2015, 35, 94–103. [Google Scholar]
  105. Akmirza, A.; Yardımcı, E.R. Fish parasites of the Sakarya River, Turkey. J. Acad. Doc. Fish. Aquac. 2014, 1, 23–29. [Google Scholar]
  106. Topçu, A. The Helminths of the Digestive Tract of the Carps (Cyprinus carpio) in Van Region. Ph.D. Thesis, Yuzuncu Yıl University, Van, Turkey, 1993. [Google Scholar]
  107. Baştürk, O. Identification of Pollution of Sakarya River by Using Geographical Information (GIS). Master’s Thesis, Sakarya University, Sakarya, Turkey, 2006. [Google Scholar]
  108. Eken, G.; Bozdoğan, M.; İsfendiyaroğlu, S.; Kılıç, S.; Lise, Y. (Eds.) Bendimahi Delta. Important Natural Areas of Turkey; Doğa Derneği: Ankara, Turkey, 2006; pp. 390–391. [Google Scholar]
  109. Anonymous. Van Province 2019 Environmental Status Report; Directorate of Environmental Management and Inspection: Pretoria, South Africa, 2021; 157p. [Google Scholar]
  110. Gabrashanska, M.; Nedeva, I. Content of heavy metals in the system fish-cestodes. Parassitologia 1996, 38, 58. [Google Scholar]
  111. Oyoo-Okoth, E.; Wim, A.; Osano, O.; Kraak, M.H.; Ngure, V.; Makwali, J.; Orina, P.S. Use of the fish endoparasite Ligula intestinalis (L., 1758) in an intermediate cyprinid host (Rastreneobola argentea) for biomonitoring heavy metal contamination in Lake Victoria, Kenya. Lakes Reserv. Res. Manag. 2010, 15, 63–73. [Google Scholar] [CrossRef]
  112. Keskin, N.; Arkan, F.E. Ligulosis in freshwater fishes in Turkey. Hacet. Üniv. J. Sci. Eng. 1987, 8, 57–70. [Google Scholar]
  113. Burgu, A.; Oğuz, T.; Körting, W.; Güralp, N. Parasites of freshwater fishes in some areas of Central Anatolia. Etlik Vet. Mikrobiyoloji Derg. 1988, 6, 143–166. [Google Scholar]
  114. Yılmaz, F.; Solak, K.; Alaş, A. A research on Ligula intestinalis L. from Yukarı Porsuk. In Proceedings of the XIII. Congress of National Biology, İstanbul, Turkey, 17–20 September 1996; pp. 71–79. [Google Scholar]
  115. Koyun, M. Helminth Fauna of Some Fish Species in Enne Dam Lake (Kütahya). Ph.D. Thesis, Uludag University, Bursa, Turkey, 2001. [Google Scholar]
  116. Kır, I. Investigation of Parasites and Growth of Common Carp (Cyprinus carpio l. 1758), Heckel’s Orontes Barbell (Barbus capito pectoralis Heckel, 1843) and Gibel Carp (Carassius carassius L. 1758) in Karacaören I Dam Lake. Ph.D. Thesis, Süleyman Demirel University, Isparta, Turkey, 1998. [Google Scholar]
  117. Arslan, M.Ö.; Yilmaz, M.; Tasçi, G.T. Infections of Ligula intestinalis on Freshwater Fish in Kars Plateau of North-Eastern Anatolia, Turkey. Türkiye Parazitolojii Derg. 2015, 39, 218–221. [Google Scholar] [CrossRef]
  118. Başaran, A.; Kelle, A. Distribution of Ligula intestinalis Some Freshwater Fish Living on the Devegecidi Dam Lake. Hacet. Univ. J. Fac. Sci. 1976, 26, 45–56. [Google Scholar]
  119. Anonymous. Ankara Province Environmental Report in 2019; Provincial Directorate of Environment and Urbanization: Ankara, Turkey, 2019; 296p. [Google Scholar]
  120. Uğurlu, Ö. The Effects of Ankara Urban Development on the Mogan and Eymir Lakes Wetland Ecosystem. Master’s Thesis, Ankara University, Ankara, Turkey, 2020. [Google Scholar]
  121. Çıplakoğlu, G. A Research on the Eutrophication Sensitivity of the Surface Waters and Sakarya River Basin Sample. Master’s Thesis, İstanbul Technical University, İstanbul, Turkey, 2006. [Google Scholar]
  122. Öztürk, R.; Altan, T. Porsuk Creek Envirronmental Problems and Watershed Management Suggestions in Solutions to These Problems. CUNAS 2008, 17, 79–89. [Google Scholar]
  123. Sarıyıldız, A.; Harmancıoğlu, N.; Sılay, A.; Çetin, H.C. Trend Analysis of Water Quality Parameters of Gediz River. In Proceedings of the TMMOB İzmir City Symposium, DSI II, İzmir, Turkey, 11 August 2008; pp. 603–611. [Google Scholar]
  124. Köse, E.; Uysal, K. The comparison of heavy metal accumulation ratios in muscle, skin and gill of non-maturated common carp (Cyprinus carpio L., 1758). J. Sci. Tech. Dumlupınar Univ. 2008, 17, 19–26. [Google Scholar]
  125. Yalım, F.B.; Emre, N.; Gülle, İ.; Emre, Y.; Pak, F.; Aktaş, Ö.; Uysal, R.; Veske, E. Seasonal Change of Microbiological Pollution Level of Karacaören I Dam Lake, Burdur, Turkey. LimnoFish 2020, 6, 120–126. [Google Scholar] [CrossRef]
  126. Anonymous. Kars Province Environmental Report in 2018; Provincial Directorate of Environment and Urbanization: Kars, Turkey, 2018; 124p. [Google Scholar]
  127. Yıldız, H.B. Investigation of Change Water Quality Depending on Period and Space Using Enrichment Factor in the Upper Tigris Basin. Master’s Thesis, Hacettepe University, Ankara, Turkey, 2013. [Google Scholar]
  128. Shah, H.B.; Yousuf, A.R.; Chishti, M.Z.; Ahmad, F. Helminth communities of fish as ecological indicators of lake health. Parasitology 2013, 140, 352–360. [Google Scholar] [CrossRef] [PubMed]
  129. Khalil, M.; Furness, D.N.; Zholobenko, V.; Hoole, D. Effect of tapeworm parasitisation on cadmium toxicity in the bioindicator copepod, Cyclops strenuus. Ecol. Indic. 2014, 37, 21–26. [Google Scholar] [CrossRef]
  130. Dalkıran, N.; Karacaoğlu, D.; Taş, D.; Karabayırlı, G.; Atak, S.; Arda Koşucu, T.N.; Coşkun, F.; Akay, E. Use of Factor Analysis to Evaluate the Water Quality of Mustafakemalpaşa Stream (Bursa). Acta Aquat. Turc. 2020, 16, 124–137. [Google Scholar] [CrossRef]
  131. Deniz, O.; Doğu, A.F. Water Pollution in the Lake Van Basin. 38. In Proceedings of the ICANAS (International Congress of Asian and North African Studies) Congress, Ankara, Turkey, 10–15 September 2007; pp. 299–308. [Google Scholar]
  132. Topal, M. Past and Present Status of Water Quality of Hazar Lake. J. Eng. Sci. Des. 2011, 1, 120–134. [Google Scholar]
  133. Küçükyılmaz, M.; Uslu, G.; Birici, N.; Örnekçi, G.N.; Yıldız, N.; Şeker, T. Examination Water Quality of Karakaya Dam Lake. Yunus Araştırma Bülteni 2017, 2, 145–155. [Google Scholar]
  134. Eliker, M. Hydrogeologıc Assesment of Uluova (Elazığ) by Geographıcal Informatıon Systems. Master’s Thesis, Cukurova University, Adana, Turkey, 2008. [Google Scholar]
  135. Aydoğdu, A.; Selver, M. An investigation of helminth fauna of the bleak (Alburnus alburnus L.) from the Mustafakemalpasa stream, Bursa, Turkey. Turk. Parazitolojii Derg. 2006, 30, 68–71. [Google Scholar]
  136. Aksoy, Ş. Endohelminths Research in Capoeta capoeta umbla from Hazar Lake. Master’s Thesis, Fırat University, Elazığ, Turkey, 1996. [Google Scholar]
  137. rün, İ.; Dörücü, M.; Yazlak, H.; Öztürk, E. A Research Study on the Helminths of Karakaya Dam Lake Fishes and Their Impacts; Project No. 15; İnönü University, Department of Research Project: Malatya, Turkey, 2003. [Google Scholar]
  138. Dörücü, M.; İspir, Ü. Study on endo-parasites of some fish species caught in Keban Dam Lake. Fırat Univ. J. Sci. Eng. 2005, 17, 400–404. [Google Scholar]
  139. Morley, N.J.; Costa, H.H.; Lewis, J.W. Effects of a Chemically Polluted Discharge on the Relationship Between Fecundity and Parasitic Infections in the Chub (Leuciscus cephalus) from a River in Southern England. Arch. Environ. Contam. Toxicol. 2010, 58, 783–792. [Google Scholar] [CrossRef]
  140. Tekin Özan, S. The Investigation of Heavy Metals and Parasites in Carp (Cyprinus carpio L., 1758) and Tench (Tinca tinca L., 1758) Inhabiting Beysehir Lake. Ph.D. Thesis, Süleyman Demirel University, Isparta, Turkey, 2005. [Google Scholar]
  141. Kır, İ.; Tekin Özan, S. Occurrence of helminths in tench (Tinca tinca L., 1758) of Kovada (Isparta) Lake, Turkey. Bull. Eur. Assoc. Fish Pathol. 2005, 25, 75–81. [Google Scholar]
  142. Ateş, H.; Uzer, Y. Attempts at Rural Development on the Success of Wetland Rehabilitation: Akşehir Rehabilitation Project. 38. In Proceedings of the ICANAS (International Congress of Asian and North African Studies) Congress, Istambul, Turkey, 1 August 2011; Volume 1, pp. 85–104. [Google Scholar]
  143. Büber, H.; Bozyurt, O. Environmental Problems of Beyşehir Lake and Basin. Int. Soc. Ment. Res. Think. J. 2020, 38, 2389–2408. [Google Scholar] [CrossRef]
  144. Kavak, M.; Şeker, E. Investigation of endohelminthes in fish caught in Pertek Region of Keban Dam Lake. Fırat Univ. J. Sci. Eng. 2017, 29, 33–40. [Google Scholar]
  145. Aydoğdu, A.; Yıldırımhan, H.S.; Altunel, F.N. The helminth fauna of Adriatic roach (Rutilus rubilio) in İznik Lake. Bull. Eur. Assoc. Fish Pathol. 2000, 20, 170–172. [Google Scholar]
  146. Ztürk, T.; Öter, A.; Çam, A.; Yılmaz, D.; Ünsal, G. Metazoan parasites of pike-perch, Stizostedion lucioperca, L., 1758 collected from Lower Kızılırmak Delta in Turkey. In Proceedings of the 15th International Conference on Diseases of Fish and Shellfish, Split, Croatia, 12–16 September 2011; p. 430. [Google Scholar]
  147. Hasançavuşoğlu, Z.; Gündoğdu, A. Investigation of Anionic Detergent Pollution in Sarıkum Lake (Sinop). TURJAF 2019, 7, 1825–1833. [Google Scholar] [CrossRef] [Green Version]
  148. Sures, B.; Siddall, R.; Taraschewski, H. Parasites as Accumulation Indicators of Heavy Metal Pollution. Parasitol. Today 1999, 15, 16–21. [Google Scholar] [CrossRef]
  149. Sures, B.; Dezfuli, B.S.; Krug, H.F. The intestinal parasite Pomphorhynchus laevis (Acanthocephala) interferes with the uptake and accumulation of lead (210Pb) in its fish host chub (Leuciscus cephalus). Int. J. Parasitol. 2003, 33, 1617–1622. [Google Scholar] [CrossRef]
  150. Marijić, V.F.; Smrzlić, I.V.; Raspor, B. Does fish reproduction and metabolic activity influence metal levels in fish intestinal parasites, acanthocephalans, during fish spawning and post-spawning period? Chemosphere 2014, 112, 449–455. [Google Scholar] [CrossRef]
  151. Soylu, E. Pomphorhynchus laevis (Müller, 1776) (Acanthocephala) in Barbus plebejus escherichi Steindachner 1897 of Büyükcoz Lake, Karasu (Sakarya). Anadolu Univ. J. Sci. 1991, 3, 31–37. [Google Scholar]
  152. Buhurcu, H.İ. An Investigation on Endoparasite Fauna of Some Fish Species (Cyprinus carpio and Alburnus nasreddini) from Lake Akşehir. Master’s Thesis, Afyon Kocatepe University, Afyon, Turkey, 2006. [Google Scholar]
  153. Katip, A. Water Quality Monitoring of Lake Uluabat. Ph.D. Thesis, Uludag University, Bursa, Turkey, 2010. [Google Scholar]
  154. Bebka, B. TR41 Environmental Report; Development Agency of Bursa: Eskişehir, Turkey, 2011; 86p. [Google Scholar]
  155. Tuuha, H.; Valtonen, E.T.; Taskinen, J. Ergasilid copepods as parasites of perch Perca fluviatilis and roach Rutilus rutilus in central Finland: Seasonality, maturity and environmental influence. J. Zool. 1992, 228, 405–422. [Google Scholar] [CrossRef]
  156. Sağlam, N. Investigation of External Parasites of Fish Caught in Keban Dam Lake. Master’s Thesis, Fırat University, Elazığ, Turkey, 1992. [Google Scholar]
  157. imşek, Ö. Parasite Fauna of Fish Species from Ömerli Dam Lake. Master’s Thesis, Marmara University, İstanbul, Turkey, 2013. [Google Scholar]
  158. Tezer, A.; Çetin, N.İ.; Onur, A.C.; Menteşe, E.Y.; Albayrak, İ.; Cengiz, E.C. Project for Development of Integrated Basin Management Plan Based on Ecosystem Services in Ömerli Basin; TR10/14/DFD/0039; Istanbul Development Agency: İstanbul, Turkey, 2015; 177p. [Google Scholar]
  159. Karakişi, H.; Demir, S. Metazoan Parasites of the Common Carp (Cyprinus carpio L., 1758) from Tahtalı Dam Lake (İzmir). Türkiye Parazitolojii Derg. 2012, 36, 174–177. [Google Scholar] [CrossRef]
  160. Koyun, M.; Ulupınar, M.; Mart, A. First record of Lernaea cyprinacea L. 1758 (Copepoda: Cyclopoida) on Cyprinion macrostomus Heckel, 1843 from Eastern Anatolia, Turkey. Biharean Biol. 2015, 9, 44–46. [Google Scholar]
  161. Akçimen, U.; Apaydın Yağcı, M.; Yeğen, V.; Uysal, R.; Bilgin, F.; Yağcı, A. First report of Eustrongylides excisus larvae and Lernaea cyprinacea on Eğirdir minnow (Pseudophoxinus egridiri). In Proceedings of the 13th International Symposium on Fisheries and Aquatic Sciences, Ankara, Turkey, 21–23 October 2018; p. 108. [Google Scholar]
  162. Tóro, R.M.; Gessner, A.A.; Furtado, N.A.; Ceccarelli, P.S.; De Albuquerque, S.; Bastos, J.K. Activity of the Pinus elliottii resin compounds against Lernaea cyprinacea in vitro. Vet. Parasitol. 2003, 118, 143–149. [Google Scholar] [CrossRef] [PubMed]
  163. Ay, Z.K. Determination of Alternative Land Use Policies to Prevent Pollution in the Tahtalı Dam Conservation Area; T.C. General Directorate of Forestry Aegean Forestry Research Institute Technical Report; T.C. General Directorate of Forestry Aegean Forestry Research Institute: İzmir, Turkey, 2001; Volume 4, p. 70. [Google Scholar]
  164. Beyhan, M.; Kaçıkoç, M. Pollution Status and Pollution Sources Modeling Study in Lake Eğirdir. Seven Colored Life to Seven Colored Lake Project; WWF-Türkiye (Doğal Hayatı Koruma Vakfı): İstanbul, Türkiye, 2013; 35p. [Google Scholar]
  165. Demir, A.D.; Şahin, Ü.; Demir, Y. Trend Analysis and Agricultural Perspective Availability of Water Quality Parameters at Murat River. Yuz. Yıl Univ. J. Agric. Sci. 2016, 26, 414–420. [Google Scholar]
  166. Pettersen, R.A.; Vøllestad, L.A.; Flodmark, L.E.; Poléo, A.B. Effects of aqueous aluminium on four fish ectoparasites. Sci. Total Environ. 2006, 369, 129–138. [Google Scholar] [CrossRef] [PubMed]
  167. Oztürk, M.O. An investigation of metazoan parasites of common Carp (Cyprinus carpio L.) in Lake Eber, Afyon, Turkey. Turk. Parazitolojii Derg. 2005, 29, 204–210. [Google Scholar]
  168. Ktener, A.; Ali, A.H.; Gustinelli, A.; Fioravanti, M.L. New host records for fish louse, Argulus foliaceus L., 1758 (Crustacea, Branchiura) in Turkey. Ittiopatologia 2006, 3, 161–167. [Google Scholar]
  169. Ktener, A.; Alaş, A. A parasitological study of fish from the Atatürk Dam Lake, Turkey. Bull. Eur. Assoc. Fish Pathol. 2009, 29, 193–197. [Google Scholar]
  170. Akbeniz, E. Metazoan Parasites of Tench (Tinca tinca L., 1758) in the Lake Sapanca. Master’s Thesis, Marmara University, Istanbul, Turkey, 2006. [Google Scholar]
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Figure 1. A case of mass fish deaths in an irrigation pond used for agricultural purposes in Bandırma.
Figure 1. A case of mass fish deaths in an irrigation pond used for agricultural purposes in Bandırma.
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Figure 2. Ecosystems in Turkey where mass fish deaths occurred and parasite surveys were carried out; 1–44 spots names and characteristics are presented in the below Table 1.
Figure 2. Ecosystems in Turkey where mass fish deaths occurred and parasite surveys were carried out; 1–44 spots names and characteristics are presented in the below Table 1.
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Table
Table 1. Mass fish deaths and parasitology studies in some ecosystems in Turkey.
Table 1. Mass fish deaths and parasitology studies in some ecosystems in Turkey.
LocationHost Fish Species: Parasite SpeciesReferenceFish Deaths DateSource
Marmara Region
1BüyükakgölBlicca bjoerkna: Tylodelphys clavata, Piscicola geometra, GlochidiaAltan and Soylu (2018) 2010https://www.etkihaber.com/akgolde-toplu-balik-olumleri-yasaniyor.-51904h.htm (accessed on 1 November 2022)
2Büyükçekmece Dam LakeSqualius cephalus: Paradiplozoon homoion
Rutilus rutilus: Caryophyllaeus laticeps		Yardımcı et al. (2018)2021https://www.yenisafak.com/video-galeri/gundem/rengi-degisen-buyukcekmece-golunde-olen-baliklar-kiyiya-vurdu-2220804 (accessed on 10 November 2022)
3İznik LakeRutilus frisii: Caryophyllaeus laticeps,
Rutilus rubilio: Neoechinorhynchus rutili		Aydoğdu et al. (1997)
Aydoğdu et al. (2000)		2020https://www.tv100.com/bursanin-iznik-ilcesinde-iznik-golunu-besleyen-en-buyuk-dere-olan-cakirca-deresinde-yasanan-toplu-balik-olumleri-vatandaslari-tedirgin-etti-video-499455 (accessed on 23 November 2022)
4Karacabey Lagoon LakeEsox lucius: Raphidascaris acusÖztürk et al. (2002)2020https://www.bursadabugun.com/haber/bursa-karacabey-deki-balik-olumlerinin-arastirilmasi-istendi-1324902.html (accessed on 23 November 2022)
5Karasu StreamLuciobarbus escherichii: Pomphorhynchus laevisSoylu (1991)2021https://www.hurriyet.com.tr/gundem/karasu-nehrinin-ustunu-tamamen-kapladi-yore-halkini-tedirgin-eden-balik-olumleri-41837035 (accessed on 23 November 2022)
6Kocadere StreamR. rutilus: Dactylogyrus crucifer, Diplostomum spathaecumSelver (2008)2018https://kuzeyormanlari.org/2018/09/16/bursa-inegol-kocadereyi-yine-zehirlediler-baliklar-4-kez-topluca-can-verdi/ (accessed on 24 November 2022)
7Manyas LakeR. rutilus: Dactylogyrus crucifer, Paradiplozoon homoion, Ligula intestinalisÖztürk (2000)2014https://www.mynet.com/manyas-golunde-balik-olumleri-180101621484 (accessed on 23 November 2022)
8Mustafakemalpaşa StreamAlburnus alburnus: Bothriocephalus acheilognathiAydoğdu and Selver (2006)2019https://www.bursadabugun.com/haber/bursa-mustafakemalpasa-daki-balik-olumleri-suruyor-1200184.html (accessed on 27 November 2022)
9Ömerli Dam LakeAlburnus istanbulensis: Ergasilus sieboldiŞimşek (2013)2021https://www.denizhaber.net/omerli-barajindaki-balik-olumleri-korkuttu-haber-102459.htm (accessed on 27 November 2022)
10Sakarya RiverAbramis brama: Caryophyllaeus laticeps, Glochidia
E. lucius: Raphidascaris acus		Akmırza and Yardımcı (2014)2021https://www.halk54.com/gundem/sakarya-nehri-nde-balik-olumleri-goruldu-h53220.html (accessed on 3 December 2022)
11Sapanca LakeB. bjoerkna: Dactylogyrus crucifer, Asymphylodora imitans, Piscicola geometra
R. rutilus: Dactylogyrus crucifer, D. vistulae, Diplostomum spathaecum, Tylodelphys clavata
E. lucius: Raphidascaris acus
Tinca tinca: Glochidia		Soylu (1990), Karabiber (2006), Soylu (2006)2007https://www.hurriyet.com.tr/gundem/sapanca-golunde-balik-olumleri-basladi-7575460 (accessed on 15 December 2022)
12Uluabat LakeR. rutilus: Dactylogyrus crucifer, Paradiplozoon homoion, Caryophyllaeus laticeps
E. lucius: Rhipidocotyle fennica, Raphidascaris acus, Acanthocephalus anguillae
T. tinca: Piscicola geometra		Öztürk et al. (2000), Öztürk (2005), Öztürk (2002)2014https://www.olay.com.tr/yuzlerce-olu-balik-ve-kus-kiyiya-vurdu-337894 (accessed on 15 December 2022)
13Susurluk StreamS. cephalus: D. vistulae, Paradiplozoon meganGürkan and Tekin Özan (2012)2019https://www.denizhaber.net/susurluk-cayinda-toplu-balik-olumleri-yasandi-haber-91537.htm (accessed on 15 December 2022)
Central Anatolia Region
14Akşehir LakeAlburnus nasreddini: Pomphorhynchus laevisBuhurcu (2006)2010https://www.milliyet.com.tr/gundem/aksehir-golunde-kus-olumleri-1287711 (accessed on 15 December 2022)
15Beyşehir LakeT. tinca: Proteocephalus torulosus, Acanthocephalus anguillaeTekin Özan (2005)2020https://www.konhaber.com/haber-beysehir_de_tedirgin_eden_toplu_balik_olumleri-1360411.html (accessed on 15 December 2022)
16Çayırhan StreamAlburnus orontis: Ligula intestinalisKeskin and Erakan (1987)2020https://www.haberler.com/ankara-daki-cayirhan-golu-nde-toplu-balik-olumu-13660519-haberi/ (accessed on 17 December 2022)
17Eymir LakeAlburnus sp: Ligula intestinalis, Pomphorhynchus laevisBurgu et al. (1988)2010https://www.internethaber.com/eymir-golunde-balik-olumleri-247392h.htm (accessed on 17 December 2022)
18Porsuk StreamA. alburnus: Ligula intestinalisYılmaz et al. (1996)2021https://www.gazeteduvar.com.tr/su-akisi-duran-porsuk-cayinda-baliklar-toplu-halde-oldu-haber-1529347 (accessed on 17 December 2022)
19Sarıyar Dam LakeAlburnus sp: Ligula intestinalis, Pomphorhynchus laevisBurgu et al. (1988)2020https://www.cnnturk.com/turkiye/ankarada-barajdaki-balik-olumlerine-inceleme?page=4 (accessed on 17 December 2022)
Aegean Region
20Demirkopru Dam LakeCapoeta capoeta: Ligula intestinalisKeskin and Erakan (1987)2015https://www.salihlisektorgazetesi.com/14823/haber/demirkopru-baraji-nda-balik-olumleri-.aspx (accessed on 17 December 2022)
21Enne Dam LakeA. alburnus: Ligula intestinalis, Paraergasilus longidigitus
Carassius carassius: Argulus foliaceus		Koyun (2001), Koyun et al. (2007)2018https://www.mynet.com/kutahyada-toplu-balik-olumleri-110104353108 (accessed on 10 February 2023)
22Eber LakeCyprinus carpio: Argulus foliaceusÖztürk (2005)2017https://www.sondakika.com/haber/haber-eber-golu-nde-yasanan-toplu-balik-olumleri-9293003/ (accessed on 17 December 2022)
23Işıklı Dam LakeSqualius carinus: Dactylogyrus vistulae, Tylodelphys clavata
E. lucius: Bathybothrium rectangulum		Soylu et al. (2017), Dişçi (2002)2017https://www.denizlihaber.com/denizli/civril/iddialar-cok-vahim-isikliyi-besleyen-kufi-cayi-zirai-ilaclarla-zehirleniyor-balik-olumleri-basladi/ (accessed on 19 December 2022)
24Örenler Dam LakeS. cephalus: Dactylogyrus vistulae, Diplostomum spathaecum, Pomphorhynchus laevisKurupınar (2009)2015https://www.afyonzafer.net/sandikli/sandikli-orenler-barajindaki-baliklar-telef-oldu-h23431.html (accessed on 17 December 2022)
25Tahtalı Dam LakeC. carpio: Lernaea cyprinaceaKarakişi and Demir (2012)2012https://www.etkihaber.com/izmire-icme-suyu-saglayan-tahtali-barajindaki-balik-olumleri-korkuttu-139705h.htm (accessed on 17 December 2022)
Mediterranean Region
26Asi RiverAnguilla anguilla: Anguillicola crassusGenç et al. (2008)2021https://www.trthaber.com/haber/guncel/asi-nehrinde-su-sicakliginin-yukselmesi-ve-kalitesinin-azalmasi-balik-olumlerine-neden-olabilir-601224.html (accessed on 17 December 2022)
27Ceyhan RiverA. anguilla: Anguillicola crassusGenç et al. (2005)2021https://www.ntv.com.tr/galeri/turkiye/kahramanmarasta-meydana-gelen-balik-olumlerinin-nedeni-arastiriliyor,RIt7rfdox0CHT0ljQDDsKA/4_o5u0oyAUWZNHzq4mqVwA (accessed on 10 February 2023)
28Egirdir LakePseudophoxinus egridiri: Lernaea cyprinaceaAkçimen et al. (2018)2012https://www.denizhaber.net/egirdir-golunde-toplu-balik-olumleri-haber-41608.htm (accessed on 17 December 2022)
29Karacaören I. Dam LakeLuciobarbus pectoralis: Ligula intestinalisKır (1998)2013https://www.sondakika.com/haber/haber-ozel-haber-karacaoren-baraji-nda-sazan-olumleri-4798468/ (accessed on 19 December 2022)
30Kovada LakeC. carassius: Argulus foliaceus
T. tinca: Proteocephalus torulosus		Tekin Özan and Kır (2005), Kır and Tekin Özan (2005)2014http://www.egirdirses.com/haber-valimizin-dikkatine-...-7971.html (accessed on 19 December 2022)
Eastern Anatolia Region
31Bendimahi BrookC. carpio: Bothriocephalus acheilognathi, Caryophyllaeus laticeps, Neoechinorhynchus rutiliTopçu (1993)2021https://www.vansiyaseti.com/van/van-baligi-olumleri-arastiriliyor-h73155.html (accessed on 19 December 2022)
32Fırat RiverMastacembellus mastacembelus: Diplostomum spathaecum, Glochidia Koyun and Çelik (2020)2021https://jinepsgazetesi.com/2021/06/milyonlarca-balik-neden-oldu/ (accessed on 19 December 2022)
33Hazar LakeCapoeta umbla: Bothriocephalus acheilognathiAksoy (1996)2020https://www.gunisigigazetesi.net/elazig-guncel/baliklar-neden-oluyor-h78174.html (accessed on 19 December 2022)
34Karakaya Dam LakeC. umbla, Acanthobrama marmid: Bothriocephalus acheilognathiÖrün et al. (2003)2021https://www.ntv.com.tr/galeri/turkiye/karakaya-barajinda-toplu-balik-olumleri,zLDDlyH2lkOtmQZ2sUfj7g/szqvGqbDeUq8xZCOVvluJw (accessed on 19 December 2022)
35Kars StreamC. capoeta, Barbus plebejus: Ligula intestinalisArslan et al. (2015)2021https://www.trthaber.com/haber/turkiye/kars-cayinda-toplu-balik-olumleri-goruldu-600223.html (accessed on 17 December 2022)
36Keban Dam LakeChondrostoma regium: Bothriocephalus acheilognathi, Ergasilus sieboldi
Capoeta trutta: Lamproglena pulchella, Ergasilus sieboldi
Alburnus mossulensis: Neoechinorhynchus rutili, Ergasilus briani
Barbus rajanorum: Piscicola geometra		Sağlam (1992), Dörücü and İspir (2005), Kavak and Şeker (2017)2014https://www.sondakika.com/haber/haber-keban-baraj-golu-nde-balik-olumlerine-inceleme-6504258/ (accessed on 17 December 2022)
37Murat RiverCyprinion macrostomum: Lernaea cyprinaceaKoyun et al. (20152019https://www.denizhaber.net/murat-nehrindeki-balik-olumleri-endiselendirdi-haber-90238.htm (accessed on 17 December 2022)
South Easten Anatolia Region
38Dicle RiverM. mastacembelus: GlochidiaKoyun and Çelik (2020)2021https://www.gazeteduvar.com.tr/diclede-baliklar-neden-oluyor-haber-1522077 (accessed on 20 December 2022)
39Atatürk Dam LakePlaniliza abu,
M. mastacembelus, C. carpio, Carasobarbus luteus: Argulus foliaceus		Öktener et al. (2006),
Öktener and Alaş (2009)		2019https://www.haberturk.com/adiyaman-da-kiyiya-vuran-baliklara-inceleme-2526158 (accessed on 20 December 2022)
40Halil-ür Rahman LakeC. luteus: C. umbla, Lamproglena pulchellaÖktener et al. (2008)2021https://www.hurriyet.com.tr/gundem/balikligolde-balik-olumleri-raporlastiriliyor-41753569 (accessed on 20 December 2022)
41Zernek Dam LakeC. carpio: Bothriocephalus acheilognathiTopçu (1993)2021https://www.rudaw.net/turkish/kurdistan/1709202114 (accessed on 20 December 2022)
42Devegecidi Dam LakeA. marmid, A. mossulensis: Ligula intestinalisBaşaran and Kelle (1976)2021https://www.facebook.com/TigrisHaber/videos/diyarbak%C4%B1r-devege%C3%A7idi-baraj%C4%B1nda-toplu-bal%C4%B1k-%C3%B6l%C3%BCmleri/895500778037894/ (accessed on 20 December 2022)
Black Sea
Region
43Bafra Fish LakesSander lucioperca: Tylodelphys clavata, Bothriocephalus acheilognathi
C. carpio: Ergasilus sieboldi		Öztürk et al. (2011),
Öztürk et al. (2012)		2014https://www.haberler.com/kizilirmak-deltasi-nda-balik-ve-sulun-olumleri-6450737-haberi/ (accessed on 20 December 2022)
44Sarıkum Lagoon LakeAphanius chantrei: Neoechinorhynchus rutili, Ergasilus sieboldiÖztürk (2005)2018https://www.ajanssinop.com/koruma-alaninda-balik-katliami-iddiasi/3877/ (accessed on 20 December 2022)
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Öktener, A.; Bănăduc, D. Ecological Interdependence of Pollution, Fish Parasites, and Fish in Freshwater Ecosystems of Turkey. Water 2023, 15, 1385. https://doi.org/10.3390/w15071385

AMA Style

Öktener A, Bănăduc D. Ecological Interdependence of Pollution, Fish Parasites, and Fish in Freshwater Ecosystems of Turkey. Water. 2023; 15(7):1385. https://doi.org/10.3390/w15071385

Chicago/Turabian Style

Öktener, Ahmet, and Doru Bănăduc. 2023. "Ecological Interdependence of Pollution, Fish Parasites, and Fish in Freshwater Ecosystems of Turkey" Water 15, no. 7: 1385. https://doi.org/10.3390/w15071385

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