Parasites of goatfishes (parupeneus spp.) in Khanh Hoa province, Vietnam, preliminary results

We record 9 parasite species infecting goatfishes. The highest prevalence was observed in P. heptacanthus as all fish were infected by Haliotrema sp. and Caligus sp. The mean intensity is also highest for Haliotrema sp. (227.28). Lowest prevalence (3.85) and mean intensity (1) occurred with two digeneans infecting P. multifasciatus. Infection status was recorded differently between species as infection heaviest in fish of the genus Pseudupeneus, while being mild or sporadic in Upeneus and Mulloidichthys (Paperna, 1972). According to Klimpel et al., (2008), the parasite richness among the different areas ranged from 4-10 species. The red mullets from the North Sea harbored the most species rich parasite fauna (10).

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Journal of Fisheries science and Technology Special issue - 2015 10 • NHA TRANG UNIVERSITY PARASITES OF GOATFISHES (PARUPENEUS SPP.) IN KHANH HOA PROVINCE, VIETNAM, PRELIMINARY RESULTS Dang Nguyen Anh Tuan1, Tran Quang Sang1, Dang Thuy Binh1 ABSRACT Coral reefs known as high diversity of fish and other invertebrates provide ecosystem services, food to coastal populations, and potential medicinal products. Currently, research on parasitic infections in goatfishes (Parupeneus spp.) is limited. In this study, 2 goatfish species (P. multifasciatus and P. heptacanthus) were collected at Nha Trang and Cam Ranh Bay (Vietnam), and examined for parasites. So far, based on morphological features, 9 parasite species have been documented: 2 monogeneans (Haliotrema sp., Bothitrema sp.), 3 copepods (Caligus sp., Halectinosoma sp., Caligus quadratus), 1 isopod (Gnathia sp.), 1 nematode (Camallanus sp.) and 2 digeneans (Cholepotes sp. and Carneophallus sp.). The specimens of P. heptacanthus were most heavily infected by Haliotrema sp. and Caligus sp. with a prevalence of 100%. Cholepotes sp. and Carneophallus sp. had the lowest prevalence (3.85%). Haliotrema sp. had the highest intensity (227.28); whereas, Cholepotes sp. and Carneophallus sp., which were found in P. multifasciatus, had the lowest value (1). The highly parasite diversity in goatfish may reflect the habitat use and diet of the fish. As important food fish in Vietnam, an in-depth study on parasite composition in goatfish remains necessary. Keywords: parasite, goatfish, Vietnam, infection 1 Institute for Biotechnology and Environment, Nha Trang University I. INTRODUCTION Coral reefs are, like tropical rainforests, areas of high biodiversity (Reaka-Kudla 1997) and currently threatened (Roberts et al., 2002, Jone et al., 2004). Parasites are typically neglected in numerical evaluation of biodiversity (Whittington and Chisholm, 2003, Poulin 2004, Bouchet 2006). As an integral part of biodiversity studies, parasitology should be considered in any program for biodiversity assessment (Brooks and Hoberg, 2000). Goatfishes (Perciformes: Mullidae) are a major component of reef ecosystem assemblages, including more than 60 species (Uiblein, 2007), distributed in tropical and subtropical seas. Goatfish of Parupeneus and Upeneus were abundant in coral reefs, lower portions of rivers, seagrass beds, and mangrove forests in Vietnam (Nguyen Van Quan, 2013). Although goatfishes are commercially important species, their parasites are scarcely known. Several research projects have focused on parasites of goatfishes of genus Mulus, e.g., Argentine goatfish, Mullus argentinae (see Luque et al., 2002, Di Azevedo et al., 2014), red mullet, Mullus surmuletus (see Bayoumy et al., 2008, Klimpel et al., 2008, Hassani et al., 2015). Paperna (1972) reported 5 monogenean species infecting goatfishes in the Gulf of Eliat. Justine (2010) documented some parasites of New Caledonian coral reef fishes, including Parupeneus multifasciatus. A checklist including 370 parasite species representing infections by species of Turbellaria, Monopisthocotylea, Polyopisthocotylea, Digenea, Cestoda, Nematoda, Copepoda, Isopoda, Acanthocephala, and Hirudine were updated (Justine et al. (2010). Studies on diversity of marine fish parasites in Vietnam has not received adequate attention: only fishes of high economic value such as groupers and seabasses (Vo The Dung et al., Journal of Fisheries science and Technology Special issue - 2015 NHA TRANG UNIVERSITY • 11 2008, Dang Thuy Binh et al., 2010, 2013), have been explored for the presence of parasite infections. There have been no comprehensive studies of parasite diversity on non-commercially valued fishes in Vietnam. The purpose of the present study is to characterize the parasite fauna of 2 goatfishes: manybar goatfish, Parupeneus multifasciatus and cinnabar goatfish, Parupeneus heptacanthus, which both commonly occur in coral reefs of Nha Trang and Cam Ranh Bay, Khanh Hoa Province, Vietnam. This study provides critical baseline information on the incidence and taxonomic identities of parasites that infect ecologically important reef fishes in Vietnam. II. MATERIALS AND METHODS 1. Sampling method Goatfishes were sampled by fishing at Nha Trang and Cam Ranh Bay, Khanh Hoa Province. A total of 40 individuals (30 and 10 specimens of P. multifasciatus and P. heptacanthus, respectively) were collected during February through April 2015, and examined for the presence of parasites within 24 hours of capture. The number and size of goatfish is presented in Table 1. Parasites were collected as per the protocols of Ha Ky et al. (2007) and preserved in non-denatured ethanol (99.8% EtOH). Table 1. Number and size of goatfishes collected at Khanh Hoa Province Species Number (n) Weight (g) Length (cm) Parupeneus multifasciatus 30 95,92 ± 109,2 18,25 ± 8,5 Parupeneus heptacanthus 10 119,93 ± 126,88 20,45 ± 8,3 Presentation value: Mean value ± SD 2. Species identification Parasite species were identified based on morphological features following Yamaguti (1958), Hendrix (2004) (monogenea), Justine et al. (2012) and Justine (2010) (Digenea), Ha Ky et al. (2007) (Nematode), Smit et al. (2003), Grutter et al. (2011) and Alaş et al. (2009) (Isopod), Morales & Reinés (2015), and Boehler & Krieger (2012) (Copepods). 3. Data analysis 3.1. Prevalence (%) Prevalence was calculated as = No. of infected fish * 100 No. of examinde fish 3.2. Mean Intensity (I) Mean intensity was calculated as = No. of parasites * 100 No. of infected fish III. RESULT AND DICUSSION 1. Species identification Based on morphological characters, 9 parasite species were identified: 2 monogeneans (Haliotrema sp., Bothitrema sp.), 3 copepods (Caligus quadratus, Caligus sp., Halectinosoma sp.) 1 isopod (Gnathia sp.), 2 digeneans (Cholepotes sp., Carneophallus sp.), and 1 nematode (Camallanus sp.). Of which, 8 species were still unidentified at the species level, and probably new to science. The preferred site was the gill for ectoparasites (Monogenea, Copepoda, and Isopoda). The 3 endoparasites (Digenea and Nematoda) Journal of Fisheries science and Technology Special issue - 2015 12 • NHA TRANG UNIVERSITY infected the stomach and intestine. A list of parasite species, External morphology, infected organs, and infected status are presented in Table 2 and Figure 1. P. multifasciatus were infected by 2 monogeneans (Haliotrema sp., and Bothitrema sp.), 1 copepod (Halectinosoma sp.), 1 isopod (Gnathia sp.), 2 digeneans (Cholepotes sp., Carneophallus sp.), and 1 nematode (Camallanus sp.). The same 2 monogeneans, isopod, and nematode together with 3 copepods (Caligus quadratus, Caligus sp., Halectinosoma sp.) were detected in P. heptacanthus. For comparison, P. multifasciatus has a higher abundance of endoparasites (Digenea and Nematoda) than P. heptacanthus, which had dominated by ectoparasitic species (Monogenea and Copepoda). Figure 1. Parasite species found on goatfishes (Parupeneus spp.) at Nha Trang and Cam Ranh Bay, Vietnam Journal of Fisheries science and Technology Special issue - 2015 NHA TRANG UNIVERSITY • 13 Paperna (1972) reported 4 species of Haliotrema and Gyrodactylus sp. that infect goatfishes of Pseudupeneus, Upeneus, and Mulloidichthys. Infections by species of Haliotrema were also reported commonly in coral reef fishes, including Parupeneus spp. (Rehulková et al., 2010). The parasitic copepods Irodes parupenei and Caligus pupa have been documented from Parupeneus spilurus and P. multifasciatus in Taiwan and on P. multifasciatus in Japan (Ho and Lin, 2007). Bray & Justine (2014) examined parasite diversity in reef fish in New Caledonia, detecting 4 species of Deretrema (Digenea) in 3 goatfishes (P. multifasciatus, P. pleurostigma, and P. barberinus). Justine (2010) reported juvenile flukes potentially representing several species of Didymozoidae as well as adults of Phyllodistomum sp., Deretrema spp., and Lecithochirium sp. on P. multifasciatus, and Camallanus carangis (Nematoda) on Parupeneus ciliates. The goatfishes we examined in Nha Trang Bay exhibited high parasite diversity. The parasite communities of these fishes may be influenced by the fact that these goatfishes occupy slightly different ecological niches (regarding habitat use and diet/ food habits) within Nha Trang and Cam Ranh Bay. Work et al. (2005) reported ‘protozoan’ and metazoan (monogeneans, trematodes, cestodes, and myxozoans) among goatfishes in Hawaii, with protozoans being the most common parasites. The infected organs differed in different fish, and the protozoans infected spleen, kidney, and muscle; whereas, the metazoans infected gill, heart, kidney, spleen, and gut. 2. Parasite Infestation We record 9 parasite species infecting goatfishes. The highest prevalence was observed in P. heptacanthus as all fish were infected by Haliotrema sp. and Caligus sp. The mean intensity is also highest for Haliotrema sp. (227.28). Lowest prevalence (3.85) and mean intensity (1) occurred with two digeneans infecting P. multifasciatus. Infection status was recorded differently between species as infection heaviest in fish of the genus Pseudupeneus, while being mild or sporadic in Upeneus and Mulloidichthys (Paperna, 1972). According to Klimpel et al., (2008), the parasite richness among the different areas ranged from 4-10 species. The red mullets from the North Sea harbored the most species rich parasite fauna (10). This contrasts the Mediterranean Table 2. Species composition, prevalence and mean intensity of parasites in goatfishes (Parupeneus spp.) Parasite species Fish species Infected organ Prevalence (Mean intensity) P. multifasciatus P. heptacanthus P. multifasciatus P. heptacanthus Haliotrema sp. + + Gill 34.61(13.5) 100 (227.28) Bothitrema sp. + + Gill 3.85(3) 42.86 (2) Caligus quadratus + Gill 14.28 (3) Caligus sp. + Gill 100 (6.57) Halectinosoma sp. + + Gill 11.54(1.33) 57.14 (2.75) Gnathia sp. + + Gill 26.92(3.86) 57.14 (1.75) Cholepotes sp. + Stomach 3.85(1) Carneophallus sp. + Stomach 3.85(1) Camallanus sp. + + Intestine 15.38(5) 42.86 (1.33) Journal of Fisheries science and Technology Special issue - 2015 14 • NHA TRANG UNIVERSITY locations (4 to 7 species). Luque et al. (2002) reported the majority of the fishes (97%) were parasitized by one or more metazoan species. Fifteen species of parasites were collected on Mullus argentinae in Brazil water. IV. CONCLUSION Nine parasite species have now been documented infecting goatfishes (Parupeneus spp.) distribited in Khanh Hoa province. P. heptacanthus was most heavily infected by Haliotrema sp. and Caligus sp., both having the highest prevalence (100%). Cholepotes sp. and Carneophallus sp. had the lowest prevalence (3.85%). Haliotrema sp. had the highest intensity (227.28); whereas, Cholepotes sp. and Carneophallus sp., which infected P. multifasciatus, had the lowest value (1). REFERENCES 1. Alaş, A., Öktener, A., & Yilmaz, M., 2009. Türkiye Deniz Balığı Türlerinde Gnathia sp. (Gnathiidae) İnfestasyonu. Kafkas Universitesi Veteriner Fakultesi Dergisi, 15(2), 201–204. doi:10.9775/kvfd.2008.96-A. 2. Bayoumy E. M., El-Monem S. A., Ammar K. A. E., 2008. Ultrastructural study of some helminth parasites infecting the goatfish, Mullus surmuletus (Osteichthyes: Mullidae) from Syrt Coast, Libya. Life Science Journal, Vol 5, No. 1. 3. Boehler, J.A. and Krieger, K.A., 2012. 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