Ichthyophthirius multifiliis, Fouquet, 1876, Fouquet, 1876

Qin, Tian, Hu, Guangran, Cheng, Jiangwen, Chen, Fanglin, Fu, Peipei, Zhao, Weishan, Bu, Xialian, Cheng, Houda, Zou, Hong, Li, Wenxiang, Wu, Shangong, Wang, Guitang & Li, Ming, 2024, Investigation of Ichthyophthirius multifiliis infection in fish from natural water bodies in the Lhasa and Nagqu regions of Tibet, International Journal for Parasitology: Parasites and Wildlife 23, pp. 100894-100894 : 100894-

3.1. Infection status of I. multifiliis in Tibetan fishes

A total of 866 fish of 19 species were examined in Tibet ( Table 1 ), including two Cobitidae , ten Cyprinidae , six Nemacheilidae , and one Siluridae species. With C. auratus , S. selincuoensis and S. thermalis being collected in the highest numbers.

The fish from the subfamily Schizothoracinae , such as the genus Schizopygopsis , and the family Nemacheilidae , such as the genus Triplophysa , exhibited a relatively higher prevalence of I. multifiliis than the other fish examined ( Table 1 ). Schizopygopsis selincuoensis (33.73%) exhibited the highest prevalence, followed by Triplophysa tibetana (30.00%) and Triplophysa brevicauda (27.91%). The other two species of Schizopygopsis , Schizopygopsis thermalis and Schizopygopsis younghusbandi , were also found to be infected but at a lower level. In terms of parasite infection intensity and abundance ( Table 2 ), the mean intensity and mean abundance in fish in the Boqu Zangbo (river), such as S. selincuoensis (MA = 24.94, MI = 50.96) and T. brevicauda (MA = 25.17, MI = 100.67), were relatively high. Conversely, the mean intensity and mean abundance in fish in Selincuo Lake and Lhasa River, such as S. selincuoensis (MA =1.76, MI =22.0), T. stenura (MA =4.0, MI = 20.0), and S. younghusbandi (MA = 1.03, MI = 8.0), were comparatively low. In addition, varying degrees of infection were also observed in Cuona Lake, Cuoe Lake, and Za’ gya Zangbo (river). This indicates that I. multifiliis is widespread in Cuoe Lake, Cuona Lake, Za’ gya Zangbo (river) and Boqu Zangbo (river) in the Nagqu region and more inclined to parasitize the genera Schizopygopsis and Triplophysa . No instances of infection were observed in exotic species, such as C. auratus , C. carpio , P. parva , M. anguillicaudatus , and S. asotus .

Each row tests the null hypothesis that the Sample 1 and Sample 2 distributions are the same. Asymptotic significances (2-sided tests) are displayed. The significance level is 0.050.

*: Indicates a significant difference between sample 1 and sample 2.

3.2. I. multifiliis infection from different localities

The prevalences of I. multifiliis in Selincuo Lake, Boqu Zangbo (river) and Cuona Lake in the Nagqu region were significantly higher than those in Lalu Wetland and Chabalang Wetland in Lhasa (P <0.05) ( Table 6 ; Fig. 2 ). In addition, the prevalence in Lhasa River was significantly different from that in Cuona Lake (P <0.05). The highest prevalence in Boqu Zangbo (river) was found in S. selincuoensis (48.94%; Table 2 ). In Cuona Lake, S. thermalis and T. brevicauda had high prevalences (36.51% and 56.25%, respectively). In Cuoe Lake, the highest prevalence was also found in S. thermalis (17.95%). In Za’ gya Zangbo (river), high prevalences were observed in T. tibetana (35.29%) and S. selincuoensis (32.98%). The other species of Triplophysa and Schizopygopsis were not infected. Moreover, I. multifiliis infection was rare or absent in fish from Lalu Wetland and Chabalang Wetland.

3.3. Correlation analysis of salinity and I. multifiliis prevalence

The prevalence of I. multifiliis in the genus Schizopygopsis varied depending on the salinity of the sampling sites in Za’ gya Zangbo (river), Boqu Zangbo (river), and Selincuo Lake. The prevalence was higher in areas with low salinity, such as the upper reaches of Za’ gya Zangbo, Boqu Zangbo and Cuona Lake ( Table 7 ; Fig. 3 ), and significantly lower in high salinity areas, such as the north and south shores of Selincuo Lake (Boqu Estuary) and Cuoe Lake. However, it is noteworthy that there was still a relatively high prevalence (17.95%) in Cuoe Lake, where the salinity was 4.01 ±0.02 ppt. The Pearson correlation analysis revealed a significant negative association between prevalence and salinity (P <0.05; Table 8 ).

Codes: IH, number of infected hosts by each species; P (%), prevalence; FN, number of examined fishes; MS, mean salinity. SD, standard deviation.

4. Discussion

Studies on fish parasites in Tibet are still in a nascent phase ( Chen, 2022), with only a few works published to date ( Kuang, 1964; Li et al., 2008; Pan et al., 2022). Prior to this study, no information was available on the prevalence of I. multifiliis in natural water bodies in Tibet, with only two cases of mass infection reported in S. macropogon ( Li et al., 2022) and O. stewartii ( Yang et al., 2020) under artificial breeding conditions. Considering the enormous harm that I. multifiliis inflicts on fish populations in other parts of the world, and for the purpose of protecting the indigenous fish resources of Tibet, we conducted the present survey of the prevalence of I. multifiliis in natural water bodies in Tibet. This is the first systematic investigation of I. multifiliis infection in natural fish populations in the Tibetan region.

The introduced fish species examined in this study, including C. auratus , C. carpio , P. parva , M. anguillicaudatus , and S. asotus , did not exhibit any signs of parasitism by I. multifiliis . The potential reason for this phenomenon may be the limited sampling number of certain species, such as carp ( Cyprinus carpio ) and catfish ( Silurus asotus ), resulting in no diseased fish being captured. Introduced fish are primarily found in regions characterized by high levels of human activity, such as the middle reaches of the Yarlung Zangbo River ( Yang et al., 2010), Chabalang Wetland, and Lalu Wetland in the Lhasa River basin ( Zhu et al., 2022; Chen and Chen, 2010). Among them, C. auratus , P. parva , and other dominant species have successfully established natural populations ( Hu et al., 2019; Zhu et al., 2022). In these particular localities, ichthyophthiriasis among indigenous fish is infrequent, with lower infection intensity and abundance than in the Nagqu region. The possible reason for this could be that the fish residing in the Lhasa River basin have developed a survival mechanism to adapt to coexistence with I. multifiliis to some extent. This mechanism may involve the activation of both innate and adaptive immune responses ( Teixeira Alves and Taylor, 2020) and may have ultimately led, over time, to a reduction in overall infection prevalence. In contrast, the fish species in the rivers and lakes of the Nagqu region in the northern Tibetan Plateau are predominantly native Tibetan fish ( Chen et al., 2001), mainly the genus Schizopygopsis and Triplophysa . The response mechanisms of these fishes to infection with I. multifiliis appear to be either underdeveloped or in the process of gradual development and the fish appear to lack an evolutionary co-adaptation process with the parasite ( Honka and Sures, 2021), leaving them vulnerable to severe damage by the parasite. It is therefore evident that I. multifiliis presents a significant potential hazard to indigenous fish species.

When sampling in Za’ gya Zangbo (river), Boqu Zangbo (river) and Selincuo Lake, we noticed that the salinity changed according to the flow direction of the river. Elevated salinity levels in natural aquatic environments are known to impede the survival of I. multifiliis ( David, 2012) and our correlation analysis supports this assertion. Previous studies have shown that a salinity of 5 ppt will completely inhibit the normal development of I. multifiliis ( Aihua and Buchmann, 2001) , so this could potentially account for the low intensity and abundance of I. multifiliis observed in Cuoe Lake and Selincuo Lake. However, I. multifiliis infections could still be observed in Boqu Estuary with salinity levels above 4 ppt. This could be attributed to two possible factors. Firstly, the genus Schizopygopsis has been found to have high salt tolerance and migratory characteristics ( Chen et al., 2002; Huang et al., 2022). After being infected by I. multifiliis in low salinity areas, these fish could therefore have migrated to high salinity areas, where they were subsequently captured prior to the detachment of the trophonts from their body surface. Secondly, it is possible that the I. multifiliis commonly found in these areas has become adapted to high salinity environments. If the latter is the case, this will pose a potential threat to the preservation of native fish species in Tibet. Further studies will therefore be carried out to investigate whether I. multifiliis in these regions can indeed withstand high salinities.

Figures

Fig. 2. Pairwise comparisons of locality. Localities: BZ, Boqu Zangbo (river); CEL, Cuoe lake; CNL, Cuona lake; CW, Chabalang Wetland; LR, Lhasa River; LW, Lalu Wetland; SL, Selincuo Lake ZZ, Za’gya Zangbo (river). *: Indicates a significant difference between location 1 and location 2.

Fig. 3. Prevalence of I. mutlifillis infection in Schizopygopsis at locations of differing salinity.