Register      Login
Marine and Freshwater Research Marine and Freshwater Research Society
Advances in the aquatic sciences
RESEARCH ARTICLE (Open Access)

Gill parasites of Schizocypris altidorsalis (Pisces: Cyprinidae), a threatened freshwater fish in Iran

Shokoofeh Shamsi https://orcid.org/0000-0002-8606-6400 A * , Javad Khedri B , Hassan Borji B , Jaydipbhai Suthar A and Nidhish Francis A
+ Author Affiliations
- Author Affiliations

A Gulbali Institute, School of Agricultural, Environmental and Veterinary Sciences, Charles Sturt University, Wagga Wagga, NSW 2678, Australia.

B Department of Pathobiology, Faculty of Veterinary Medicine, Ferdowsi University of Mashhad, Mashhad, Iran.

* Correspondence to: sshamsi@csu.edu.au

Handling Editor: Max Finlayson

Marine and Freshwater Research 75, MF23251 https://doi.org/10.1071/MF23251
Submitted: 19 December 2023  Accepted: 16 February 2024  Published: 28 March 2024

© 2024 The Author(s) (or their employer(s)). Published by CSIRO Publishing. This is an open access article distributed under the Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License (CC BY-NC-ND)

Abstract

Context

Schizocypris altidorsalis is a fish of very restricted distribution, with its populations being known only from few water reservoirs on the border of Iran and Afghanistan.

Aims

The aim was to investigate the occurrence and diversity of host-specific Monogenea on this fish.

Methods

In total, 400 fish were purchased from the market and examined for the presence of Monogenea. Specimens were characterised morphologically and genetically.

Key results

In total, 26.5% of fish were found to be infected with Monogenea. Further morphological and molecular studies based on the sequences of the 18S, 28S and ITS2 regions suggested that they all belong to a new species, herein named as Paradiplozoon jalalii. Our results suggest that this monogenean is a highly specific parasite of Schizocypris altidorsalis.

Conclusions

Monogeneans are highly specialised host-specific parasites infecting fish gill. They can adversely affect respiration and excretory functions in fish, making them more vulnerable to illness, leading to population declines.

Implications

Determining effective strategies for safeguarding endangered fish can be challenging in conflict zones, such as the area studied here. Additionally, the parasite identified in our study, with its blood-feeding habits, could contribute to the extinction of its fish host, subsequently leading to its own extinction. An unanswered question lingers regarding the potential extinction of other symbionts of Schizocypris altidorsalis if the fish faces extinction.

Keywords: conservation, Diplozoidae, fish, freshwater fish, Iran, Monogenea, new species, threatened species.

References

Acosta AA, Smit NJ (2021) A first for Southern Africa: description of a new Heterobothrium (Monogenea: Diclidophoridae) parasitizing the evileye pufferfish Amblyrhynchotes honckenii (Tetraodontiformes: Tetraodontidae). Parasitology Research 120(3), 819-830.
| Crossref | Google Scholar | PubMed |

Arken K, Hao C-L, Guo A-M, Zhang W-R, Rong M-J, Kamal W, Tian S-L, Kadir M, Yue C (2022) A new species of Paradiplozoon (Monogenea: Diplozoidae), a gill parasite of the Schizothorax fish (Cyprinidae: Schizothoracinae) from the Yarkand River, Xinjiang, China. Acta Parasitologica 67, 330-339.
| Crossref | Google Scholar |

Aydoğdu N, Alemdar A, Koç HT, Erdoğan Z (2020) Susurluk Çayı (Balıkesir)’ndaki Acı Balık, Rhodeus amarus (Pallas, 1782) (Teleostei: Cyprinidae)’un Helmint Parazitleri üzerine bir araştırma: Acı Balık’ta Paradiplozoon homoion’un Türkiye’de ilk kaydı ve Helmint Parazitlerin her biri için yeni lokalite kaydı. Türk Tarım ve Doğa Bilimleri Dergisi 7(4), 1049-1056 [In Turkish].
| Google Scholar |

Badets M, Whittington I, Lalubin F, Allienne J-F, Maspimby J-L, Bentz S, Du Preez LH, Barton D, Hasegawa H, Tandon V (2011) Correlating early evolution of parasitic platyhelminths to Gondwana breakup. Systematic Biology 60(6), 762-781.
| Crossref | Google Scholar | PubMed |

Barton DP, Gherman CM, Zhu X, Shamsi S (2022) Characterization of tongue worms, Linguatula spp. (Pentastomida) in Romania, with the first record of an unknown adult Linguatula from roe deer (Capreolus capreolus Linnaeus). Parasitology Research 121(8), 2379-2388.
| Crossref | Google Scholar | PubMed |

Bazzi H, Ebrahimi H, Aminnejad B (2021) A comprehensive statistical analysis of evaporation rates under climate change in Southern Iran using WEAP (Case study: Chahnimeh Reservoirs of Sistan Plain). Ain Shams Engineering Journal 12(2), 1339-1352.
| Crossref | Google Scholar |

Benovics M, Koubková B, Civáňová K, Rahmouni I, Čermáková K, Šimková A (2021) Diversity and phylogeny of Paradiplozoon species (Monogenea: Diplozoidae) parasitising endemic cyprinoids in the peri-Mediterranean area, with a description of three new Paradiplozoon species. Parasitology Research 120, 481-496.
| Crossref | Google Scholar | PubMed |

Bush AO, Lafferty KD, Lotz JM, Shostak AW (1997) Parasitology meets ecology on its own terms: Margolis et al. revisited. The Journal of Parasitology 83(4), 575-583.
| Crossref | Google Scholar |

Cao S, Fu P, Zou H, Li M, Wu S, Wang G, Blazhekovikj-Dimovska D, Li W (2022) Sindiplozoon coreius n. sp. (Monogenea: Diplozoidae) from the gills of Coreius guichenoti (Cyprinidae) in China. Parasitology International 87, 102494.
| Crossref | Google Scholar | PubMed |

Carlson CJ, Hopkins S, Bell KC, Doña J, Godfrey SS, Kwak ML, Lafferty KD, Moir ML, Speer KA, Strona G, Torchin M, Wood CL (2020) A global parasite conservation plan. Biological Conservation 250, 108596.
| Crossref | Google Scholar |

Dos Santos QM, Avenant-Oldewage A (2016) The description of a new diplozoid species, Paradiplozoon krugerense n. sp., from Labeo rosae Steindachner, 1894 and Labeo congoro Peters, 1852 in the Kruger National Park, South Africa with notes on the effect of water quality on its infection variables. Hydrobiologia 777, 225-241.
| Crossref | Google Scholar |

Dos Santos QM, Avenant-Oldewage A (2020) Review on the molecular study of the Diplozoidae: analyses of currently available genetic data, what it tells us, and where to go from here. Parasites & Vectors 13(1), 539.
| Crossref | Google Scholar | PubMed |

Dos Santos QM, Van Vuuren BJ, Avenant-Oldewage A (2015) Paradiplozoon vaalense n. sp. (Monogenea: Diplozoidae) from the gills of moggel, Labeo umbratus (Smith, 1841), in the Vaal River System, South Africa. Journal of Helminthology 89(1), 58-67.
| Crossref | Google Scholar | PubMed |

Durden LA, Keirans JE (1996) Host–parasite coextinction and the plight of tick conservation. American Entomologist 42(2), 87-91.
| Crossref | Google Scholar |

Fernando CH, Furtado JI, Gussev AV, Hanek G, Kakonge SA (1972) ‘Methods for the study of freshwater fish parasites.’ (University of Waterloo Publishing)

Galli P, Pugachev O, Kritsky D (2010) ‘Guide to Monogenoidea of freshwater fish of Palaearctic and Amur regions.’ (Ledizioni Publishing)

Gao Q, Chen MX, Yao WJ, Gao Y, Song Y, Wang GT, Wang MX, Nie P (2006) Phylogeny of diplozoids in five genera of the subfamily Diplozoinae Palombi, 1949 as inferred from ITS-2 rDNA sequences. Parasitology 134(5), 695-703.
| Crossref | Google Scholar |

Gilbert BM, Avenant-Oldewage A (2016) Seasonal occurrence and microhabitat specificity of Paradiplozoon ichthyoxanthon Avenant-Oldewage in Avenant-Oldewage et al., 2014 (Monogenea: Diplozoidae) infecting Labeobarbus aeneus (Burchell) (Teleostei: Cyprinidae) from the Vaal Dam, South Africa: water quality and host size as determining factors? Folia Parasitologica 63, 2016.004.
| Crossref | Google Scholar |

Gilbert BM, Avenant-Oldewage A (2021) Monogeneans as bioindicators: a meta-analysis of effect size of contaminant exposure toward Monogenea (Platyhelminthes). Ecological Indicators 130, 108062.
| Crossref | Google Scholar |

Gläser H-J, Gläser B (1964) Zur taxonomie der gattung Diplozoon Nordmann, 1832. Zeitschrift für Parasitenkunde 25, 164-192 [In German].
| Crossref | Google Scholar |

Gussev AV (1983) ‘Methods for collection and processing fish parasitic monogenean material’, 1st edn. (Nauka: Leningrad, USSR) [In Russian]

Huang J, Zhou X, Yuan K, Ding X (2023) Paradiplozoon cirrhini n. sp. (Monogenea, Diplozoidae), a gill parasite of Cirrhinus molitorella (Cyprinidae, Labeoninae) in South China. Parasite 30, 20.
| Crossref | Google Scholar | PubMed |

Jalali B, Shamsi S, Molnar K (2000) New Dactylogyrus species (Monogenea, Dactylogyridae) from cyprinid fishes of the Bahu-Kalat River in southeast Iran. Acta Parasitologica 45(4), 289-294.
| Google Scholar |

Jalali B, Shamsi S, Barzegar M (2005) Occurrence of Gyrodactylus spp. (Monogenea: Gyrodactylidae) from Iranian freshwater fishes. Iranian Journal of Fisheries Sciences 4(2), 19-30 [In Persian].
| Google Scholar |

Jirsová D, Ding X, Civáňová K, Jirounková E, Ilgová J, Koubková B, Kašný M, Gelnar M (2018) Redescription of Paradiplozoon hemiculteri (Monogenea, Diplozoidae) from the type host Hemiculter leucisculus, with neotype designation. Parasite 25, 4.
| Crossref | Google Scholar |

Johnsen BO, Jensen AJ (1986) Infestations of Atlantic salmon, Salmo salar, by Gyrodactylus salaris in Norwegian rivers. Journal of Fish Biology 29(2), 233-241.
| Crossref | Google Scholar |

Jørgensen D (2016) Are parasites forever? In ‘EMOP XII: Proceedings of the 12th European Multicolloquium of Parasitology’, 20–24 July 2016, Turku, Finland. (Turku Convention Bureau)

Khotenovsky IA (1985) Подотряд Octomacrinae Khotenovsky [Suborder Octomacrinae Khotenowsky]. In ‘Фауна СССР. Моногенеи [Fauna of the USSR. Monogenea]’. (Ed AV Gussev) pp. 356–384. (USSR Academy of Sciences, Zoological Institute) [In Russian]

Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Molecular Biology and Evolution 33(7), 1870-1874.
| Crossref | Google Scholar | PubMed |

Leis E, Bailey J, Katona R, Standish I, Dziki S, McCann R, Perkins J, Eckert N, Baumgartner W (2023) A mortality event involving endangered pallid sturgeon (Scaphirhynchus albus) associated with Gyrodactylus conei n. sp. (Monogenea: Gyrodactylidae) effectively treated with Parasite-S (formalin). Parasitologia 3(2), 205-214.
| Crossref | Google Scholar |

Lockyer AE, Olson PD, Littlewood DTJ (2003) Utility of complete large and small subunit rRNA genes in resolving the phylogeny of the Neodermata (Platyhelminthes): implications and a review of the cercomer theory. Biological Journal of the Linnean Society 78(2), 155-171.
| Crossref | Google Scholar |

Lymbery AJ, Smit NJ (2023) Conservation of parasites: a primer. International Journal for Parasitology: Parasites and Wildlife 21, 255-263.
| Crossref | Google Scholar |

Matejusová I, Koubková B, D’Amelio S, Cunningham CO (2001) Genetic characterization of six species of diplozoids (Monogenea; Diplozoidae). Parasitology 123(5), 465-474.
| Crossref | Google Scholar |

Matejusová I, Koubková B, Cunningham CO (2004) Identification of European diplozoids (Monogenea, Diplozoinae) by restriction digestion of the ribosomal RNA internal transcribed spacer. Journal of Parasitology 90(4), 817-822.
| Crossref | Google Scholar | PubMed |

Mirnia N, Mirdar Harijani J, Gharaei A, Rigi M (2019) Survey of some metal elements (Cu, Zn, Ni, Pb) accumulation in muscle, liver, kidney and gill of Schizocypris altidorsalis in Chahnimeh reservoirs of Sistan. Iranian Scientific Fisheries Journal 28(5), 157-161.
| Google Scholar |

Moir ML, Brennan KEC (2020) Incorporating coextinction in threat assessments and policy will rapidly improve the accuracy of threatened species lists. Biological Conservation 249, 108715.
| Crossref | Google Scholar |

Moir ML, Vesk PA, Brennan KEC, Poulin R, Hughes L, Keith DA, McCarthy MA, Coates DJ (2012) Considering extinction of dependent species during translocation, ex situ conservation, and assisted migration of threatened hosts. Conservation Biology 26(2), 199-207.
| Crossref | Google Scholar | PubMed |

Moudi Z, Tabatabaei SM, Share Mollashahi S, Zaboli M (2022) Study factors involved in maternal deaths attributed to Covid-19 in a disadvantaged area in southeast of Iran. Journal of Family & Reproductive Health 16(1), 67-77.
| Crossref | Google Scholar | PubMed |

Nejat F, Benovics M, Řehulková E, Vukić J, Šanda R, Kaya C, Tarkan AS, Abdoli A, Aksu S, Šimková A (2023) Diversity, phylogeny and intraspecific variability of Paradiplozoon species (Monogenea: Diplozoidae) parasitizing endemic cyprinoids in the Middle East. Parasitology 150, 705-722.
| Crossref | Google Scholar |

Nitta M, Nagasawa K (2023) Gill monogeneans (Platyhelminthes) parasitic on Gnathopogon elongatus elongatus and G. caerulescens (Cypriniformes: Gobionidae) from Japan, with descriptions of one new species of Dactylogyrus and three new species of Bivaginogyrus (Dactylogyridae). Species Diversity 28(1), 69-97.
| Crossref | Google Scholar |

Obiakezie AI, Taege M (1991) Mortality in hatchery reared fry of the African catfish Clarias gariepinus (Burchell) caused by Gyrodactylus groschafti Ergens, 1973. Bulletin of the European Association of Fish Pathologists 11, 82-85.
| Google Scholar |

Ogawa K, Itoh N (2022) Five new and two known species of Heterobothrium (Monogenea: Diclidophoridae) infecting puffers of the genus Takifugu from Japanese waters. Systematic Parasitology 99(3), 317-340.
| Crossref | Google Scholar | PubMed |

Olson P, Littlewood D (2002) Phylogenetics of the Monogenea: evidence from a medley of molecules. International Journal for Parasitology 32(3), 233-244.
| Crossref | Google Scholar |

Pecínková M, Matejusova I, Koubková B, Gelnar M (2005) Classification and occurrence of abnormally developed Paradiplozoon homoion (Monogenea, Diplozoinae) parasitising gudgeon Gobio gobio. Diseases of Aquatic Organisms 64(1), 63-68.
| Crossref | Google Scholar |

Přikrylová I, Mašová Š, Gelnar M, Matla MM, Tavakol S, Luus-Powell WJ (2018) Redescription of the genus Afrodiplozoon Khotenovski, 1981 and its only known species Afrodiplozoon polycotyleus (Paperna, 1973) (Monogenea: Diplozoidae) using a combined multidisciplinary approach. Parasitology International 67(2), 245-252.
| Crossref | Google Scholar | PubMed |

Rohlenová K, Morand S, Hyršl P, Tolarová S, Flajšhans M, Šimková A (2011) Are fish immune systems really affected by parasites? An immunoecological study of common carp (Cyprinus carpio). Parasites & Vectors 4(1), 120.
| Crossref | Google Scholar |

Roohi JD, Dalimi Asl A, Pourkazemi M, Shamsi S (2019) Occurrence of dactylogyrid and gyrodactylid Monogenea on common carp, Cyprinus carpio, in the southern Caspian Sea Basin. Parasitology International 73, 101977.
| Crossref | Google Scholar |

Rozhkovan KV, Shedko MB (2015) Phylogenetic relationships of Paradiclybothrium pacificum and Diclybothrium armatum (Monogenoidea: Diclybothriidae) inferred from 18S rDNA sequence data. Parasitology International 64(5), 448-452.
| Crossref | Google Scholar | PubMed |

Rubio-Godoy M, Paladini G, Freeman MA, Garcia-Vasquez A, Shinn AP (2012) Morphological and molecular characterisation of Gyrodactylus salmonis (Platyhelminthes, Monogenea) isolates collected in Mexico from rainbow trout (Oncorhynchus mykiss Walbaum). Veterinary Parasitology 186(3–4), 289-300.
| Crossref | Google Scholar | PubMed |

Sayyaf Dezfuli B, Giari L, Bosi G (2021) Chapter Three – Survival of metazoan parasites in fish: putting into context the protective immune responses of teleost fish. In ‘Advances in parasitology. Vol. 112’. (Eds D Rollinson, R Stothard) pp. 77–132. (Academic Press)

Shamsi S, Steller E, Chen Y (2018) New and known zoonotic nematode larvae within selected fish species from Queensland waters in Australia. International Journal of Food Microbiology 272, 73-82.
| Crossref | Google Scholar | PubMed |

Shamsi S, Day S, Zhu X, McLellan M, Barton DP, Dang M, Nowak BF (2021) Wild fish as reservoirs of parasites on Australian Murray cod farms. Aquaculture 539, 736584.
| Crossref | Google Scholar |

Shamsi S, Nelson L, Gordon A, Markham K, Francis N, Suthar J, Zhu X (2024) Multidisciplinary approach to the diagnosis of Contracaecum magnipapillatum infections in Australian black noddies, Anous minutus (Charadriiformes: Laridae). Parasitology Research 123(1), 90.
| Crossref | Google Scholar | PubMed |

Smyth J, Halton D (1983) ‘The physiology of trematodes’, 2nd edn. (Cambridge University Press)

Soler-Jiménez LC, Hernández-Mena DI, Centeno-Chalé OA, Vidal-Martínez VM (2021) A new species of Neoheterobothrium Price, 1943 (Monogenea, Diclidophoridae) from Syacium papillosum (Linnaeus) (Pleuronectiformes, Paralichthyidae) in the Yucatan Shelf, with notes on the validity of the subfamilies in the Diclidophoridae. Parasitology Research 120, 887-897.
| Crossref | Google Scholar | PubMed |

Thoney DA, Hargis W, Jr (1991) Monogenea (Platyhelminthes) as hazards for fish in confinement. Annual Review of Fish Diseases 1, 133-153.
| Crossref | Google Scholar |

Torres-Carrera G, Ruiz-Escobar F, García-Prieto L, Oceguera-Figueroa A (2020) Narcinecotyle longifilamentus n. gen., n. sp. (Monogenea: Hexabothriidae), gill parasite of the numbfish Narcine entemedor (Torpediniformes: Narcinidae) from the Mexican Pacific coast. Parasitology International 76, 102095.
| Crossref | Google Scholar | PubMed |

Verma A, Verma J (2022) Redescription and new host record of Heteraxinoides atlanticus (Monogenea: Heteraxinidae) from the gills of Nemipterus japonicus (Bloch) and its systematics. Agricultural Science Digest – A Research Journal 42(2), 203-209.
| Crossref | Google Scholar |

Víllora-Montero M, Pérez-del-Olmo A, Georgieva S, Raga JA, Montero FE (2020) Considerations on the taxonomy and morphology of Microcotyle spp.: redescription of M. erythrini van Beneden & Hesse, 1863 (sensu stricto) (Monogenea: Microcotylidae) and the description of a new species from Dentex dentex (L.) (Teleostei: Sparidae). Parasites & Vectors 13(1), 45.
| Crossref | Google Scholar |

Whittington ID (2012) Benedenia seriolae and Neobenedenia species. In ‘Fish parasites: pathobiology and protection’. (Eds PTK Woo, K Buchmann) pp. 225–244. (CABI: Wallingford, UK)

Windsor DA (1995) Equal-rights for parasites. Conservation Biology 9(1), 1-2.
| Crossref | Google Scholar |

Zare Abianeh H, Sabziparvar A, Marofi S, Ghiyami F, Mirmasoud SS, Kazemi A (2015) Analyzing and monitoring the meteorological droughts in the region of Sistan and Balouchestan. Environmental Science and Technology Quarterly 17(1), 49-61 [In Persian].
| Google Scholar |