Iranian Journal of Fisheries Sciences 16(2) 537-548 2017
Commensalism and parasitic infestation in crayfish (Astacus leptodactylus Eschscholtz, 1823) of Aras Dam Reservoir, Iran
Yahyazadeh M.Y.1*; Seidgar M.1; Mehrabi M.R.2; Shiri S.1
Received: March 2015 Accepted: February 2016
Abstract The freshwater crayfish of the Aras Reservoir is an important economic fisheries resource of West Azarbaijan, Iran. This study was conducted to evaluate the prevalence of parasitic infestation of Crayfish seasonally in this area in 2010. Among 390 different sizes of Astacus leptodactylus which were examined, a range of ectocommensals or ectosymbionts from a number of different phyla including 9 orders and 11 classes infested the different anatomic units of the surface and appendages such as gills, head, thorax, abdomen, walking legs, uropod, telson, antennae and antennulae of freshwater crayfish. Common groups such as peritrich ciliates, suctorian ciliates, free living nematodes, branchiobdellids, and algae, copepods, rotifers and oligochaetes have also been observed in association with freshwater crayfish.
Keywords: Astacus leptodactylus, Parasitic and commensal infestation, Aras Dam, West Azarbaijan, Iran.
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1- National Artemia Research Center, Iranian Fisheries Science Research Institute (IFSRI), Agricultural Research Education and Extension Organization (AREEO), Urmia, Iran 2- Iranian Fisheries Science Research Institute, Agricultural Research Education and Extension Organization (AREEO), Tehran, Iran * Corresponding author's Email: [email protected] 538 Yahyazadeh et al., Commensalism and parasitic infestation in crayfish (Astacus leptodactylus …
Introduction epicommensal organisms. This study Astacus leptodactylus of Aras Reservoir was performed to determine and is considered as one of the important identify the parasitic organisms in A. economic aquatic animal resources of leptodactylus of Aras Dam. Iran. It provides a luxurious and delicious but expensive meal in most Materials and methods countries. Regarding the increase of 390 samples of A.leptodactylus of resource management and culture of various lengths and weights were freshwater crayfish in the USA and captured randomly with conical traps in European countries, its economic different seasons of 2010. All samples values, health and disease status has were transferred live to the laboratory become of great important recently. of Iranian Artemia Research Center, Though it has received worldwide Urmia in polyurethane boxes containing attention, the health condition and ice. In the laboratory, the samples were pathogen agents of this valuable species weighted, measured and examined. In especially from parasitic infestation order to determine protozoan and have not been studied completely. The metazoan infestations, external parts of complexity, variety and abundance of all samples were examined and wet opportunistic and pathogen factors in mounts from carapace, branch, eye, natural and culture environments of intestine and hepatopancreas were aquatic animals and their impact on prepared and examined by light and survival, growth, reproduction of stereomicroscope. All collected aquatic animals and human being health parasitic agents were isolated, fixed, hazards are among restricting and stained and classified using Moszynsky, hazardous factors including freshwater 1938; Bykhovskyaya-Pavlovskaya et
Downloaded from jifro.ir at 7:55 +0330 on Monday September 27th 2021 crayfish. Parasitic infestations of al., 1964; Alderman and Polglase, freshwater crayfish are varied all over 1988; Hall, 2001. Then some external the world regarding the geographical parts such as branch, telson and distribution, natural habitats and carapace were placed separately in petri parasitic sites. They can cause dishes, NaCl solution was added to infestations and even epidemic diseases them and they were examined for depending on bioenvironmental external metazoan and parasites of conditions. Crayfish has an important internal organs using a role as a co existent among most stereomicroscope. invertebrates and may be a host for a variety of parasites (Lodge and Hill, Results 1994; Edgerton et al., 2002; Evans and Some biometrical characters of sampled Edgerton, 2002). Parasitic infestation A. leptodactylus are shown in Table 1. and diseases of fresh water crayfish are divided into protozoa, metazoans and Iranian Journal of Fisheries Sciences 16(2) 2017 539
Table 1: Some biometrical characters of sampled Astacus leptodactylus. A. leptodactylus Weight (g) Length (mm) Sex Number Maximum Minimum Mean Maximum Minimum Mean M 232 118 4 31.39 155 60 82.9 F 157 78 7 28.97 150 75 36.10
In this study 9 phyla and 11 classes In this study, parasitic infestation of consisting 40 species of various internal organs was not observed. opportunistic and epicommensal Most of these organisms live as protozoa and metazoans were isolated epibiont on cephalothoraxes, branch, from some parts of crayfish body. pereiopods, antennules, rostrum and These included various ciliate (Prêtrich, eyes of A. leptodactylus. Ciliophora and Loricate), free living Nematodes, Arthropoda, Prorodontidae, Annelids, Copepoda, Rotatoria, etc. the Adenophorea, Naviculaceae, list of isolated parasites and commensal Gastrotricha, Tubulinea had the highest organisms’ species were summarized and lowest abundance, respectively. and illustrated in Tables 2-4.
Table2: Isolated parasites and species of commensal organisms from the Aras Dam crayfish.
Kingdom Phylum Class Family Genus/ Species Animalia Rotifera Monogonta lepadelilidae Lepadella patella " " Monogonta Trichocercidae Trichocerca cylindrical " " Monogonta Notommatidae Monommata grandis " " Monogonta Brachionidae Brachionus plicatilis " " Bdelloidea Philodinidae Philodina roseola Downloaded from jifro.ir at 7:55 +0330 on Monday September 27th 2021 " " Monogonta Epiphanidae Epiphanes senta " Annelida Clitellata Branchiobdellidae Branchiobdella sp. " " Oligochaeta Naididae Nais sp. " Gastrotricha Gastrotriches Chaetonotidae Chaetonotus sp. " Arthropoda Maxillopoda Cyclopidae Mesocyclops sp " Nematoda Chromadorea - Nematod sp. protozoa Ciliophora Ciliatea Parameciidae Paramecium sp. " " Ciliatea Vaginicolidae Pyxicola sp. " " Ciliatea Halteriidae Halteria sp. " " Ciliatea Cyclidiidae Cyclidium sp. " " Ciliatea Urostylidae Urostyla sp. " " Ciliatea Amphileptidae Amphileptus sp. " " Ciliatea Dendrosomatidae Tokophrya sp. " " Ciliatea Chilododontidae Chilodonella sp. " " Ciliatea Vorticellidae Vorticella sp 540 Yahyazadeh et al., Commensalism and parasitic infestation in crayfish (Astacus leptodactylus …
Table 2 (continued):
Kingdom Phylum Class Family Genus/ Species " " Ciliatea Vorticellidae Zoothamnium sp.. " " Ciliatea Strombidiidae Strombidium sp. " " Ciliatea Tetrahymenidae Tetrahymena sp. " " Ciliatea Acinetidae Acineta sp. " " Ciliatea Colepidae Coleps sp. " " Ciliatea Operculariidae Opercularia sp. " " Ciliatea Didiniidae Didinium sp. " " Ciliatea Oxytrichidae Stylonychia sp. " " Ciliatea Tracheliidae Trachelius sp. " " Ciliatea Tracheliidae Dileptus sp. " " Ciliatea Euplotidae Euplotes sp. " " ciliatea Podophryidae Paracineta sp. " " Ciliatea Podophryidae Podophrya sp. " " Cciliata Prorodontidae Prorodon sp " " Ciliatea Uronematidae Uronema sp " Protozoa Heliozoa Actinophyridae Actinophrys sp. " " Lobosa Amoebidae Amoebae sp. Chromista Heterokonta Bacillariophyceae Naviculaceae Navicula sp. Chromista " Bacillariophyceae Cymbellaceae Cymbella sp. plantae Chlorophyta Chlorophyceae Chlamydomonadaceae Chlamydomonas sp.
Table 3: Distribution of parasitic and commensal organism infestation on different parts of Astacus leptodactylus captured from Aras Dam.
Branch and Parasitic agents Skin Abdomen cephalothorax Lepadella patella + + +
Downloaded from jifro.ir at 7:55 +0330 on Monday September 27th 2021 Trichocerca cylindrica - + + Monommata grandis - + + Philodina roseola - + + Brachionus plicatilis - + + Epiphanes - + + Paramecium + + + Pyxicola - + + Halteria - - + Cyclidium - + + Urostyla - + + Amphileptus - + + Tokophrya - + + Chiliodenella - + + Vorticella - + + Strombidium - + + Tetrahymena - + + Acineta - - + Coleps - + + Didinium - + + Stylonchia + + + Iranian Journal of Fisheries Sciences 16(2) 2017 541
Table 3 (continued) : Branch and Parasitic agents Skin Abdomen cephalothorax Trachelius - + + Dileptus - + + Euplotes - + + Chlamydomonas + - + Paracineta - - + Podophrya - - + Uronema sp - + + Zoothamnium - + + Navicula - + + Cymbella - - + Nais - + + Branchiobdella + - + Chaetonotus - - + Amoebae - - + Prorodo sp - + + Opercolaria - + + Mesocyclops - - + Actinophrys - - +
Table 4: The presence of parasitic agents on Astacus leptodactylus during different seasons.
Parasitic factors Winter Autumn Summer Spring Lepadella patella * * * * Trichocerca cylindrica * - - * Monommata grandis * - - - Philodina roseola * * - * Coleps * * * * Paramecium caudatum * * * * Pyxicola * * * * Cyclidiidium * * * * Urostyla * * - *
Downloaded from jifro.ir at 7:55 +0330 on Monday September 27th 2021 Amphileptus * * * * Tokophrya * * * * Ciliodenella * * * * Vorticella * * * * Stombidium * - - - Opercularia sp * * - * Tetrahymena Pyriformis * * * * Mesocyclops - - - * Prorodon sp * * - * chlamydomoras * - - - Uronema sp * * * * Navicula - * * * cymbella - * * * Acineta * * - * Amoebae Protcus * * * * Didinium * * * * Branchiobdella - - - * Nais * * - -
542 Yahyazadeh et al., Commensalism and parasitic infestation in crayfish (Astacus leptodactylus …
Table 4 (continued): Parasitic factors Winter Autumn Summer Spring branchiobdella - * * - Chaetonotus - * * * mesocyclops - * * * Actinophrys - * * * Stylonchia - * * * Brachionus plicatilis - * * - Epiphanes - * * - Halteria - * * * Trachelius - * * - Dileptus - * * * Euplotes * * * * Paracineta - * * * Zoothamnium * * * *
Discussion variety and abundance in larger animals Most of the epibionts were distributed and on bucal area and branch was on maxillipods, mandible, maxilla, higher than smaller ones and upon branch, pereiopods, Antennules, uropods and telson which might be rostrum, eyes, uropods and pleopods distributed on larger body surfaces for and telson. organism attachment and lower molting Different species of crustaceans can compared to younger ones (Fernandez– occur as symbionts, commensal and Leborans, 2001, 2009). 15 species of pathogenic parasites. Invading of peritrich ciliates have been isolated opportunistic and commensal parasites from different parts of Capmburcnus such as ciliates, free living nematodes, patzcuarensis of the Michigan Lake Branchiobdla, Rotifer, Copepods have (Mayen-Estrada et al., 2001b). been reported on different crustaceans Distribution and abundance of Downloaded from jifro.ir at 7:55 +0330 on Monday September 27th 2021 (Leborans and Tato-Porto , 2000a, b; parasites is observed more frequently in Mayen - Estrada and Aladro - Lubel , proximal parts rather than distal parts 2001a; Edgerton et al., 2002; Duris et due to nutritional behavior and al., 2006; Quaglio et al., 2006a; morphology of appendices of both Fernandez –Leborans, 2009; Abedian crayfish and organisms. The infestation Amiri et al.,2008) . Different parasitic outbreaks of ciliates in fresh water agents isolated from various parts of A. crayfish were varied probably due to leptodactylus including sessile and water quality, environmental change, suctorian ciliates, free living molting and various species of crayfish nematodes, annelids, Branchiodenella, (Edgerton et al., 2002). Although copepod and rotatoria. The distribution histopathologically, a great deal of of isolated species varied depending on ciliates isolated from branch and parasite type so that some of them were external surfaces of freshwater crayfish restricted to branch carapace or in this study were opportunistic and distributed all over the body. Also, their epicommensal similar to observation of Iranian Journal of Fisheries Sciences 16(2) 2017 543
Brown et al. (1993); Morado and Small et al., 2006; Fernandez–Leborans, (1995); Harlioglu (1999); Edgerton et 2009). Suctorian ciliates such as al. (2002); Huseyin and Selcuk, (2005); Acineta, Tokophrya, Opercolaria, Quaglio et al. (2006b); Fernandez– Coterins, isolated from the Aras Dam Leborans (2009), some of them may A. leptodactylus had no contractile have a negative impact on the host and stalk, sucker organ (antennules) or if they invade branch they can cause pseudo chitin cover and were observed respiratory problems, hypoxia and on branch, and the external surface of susceptibility to microorganisms and body as epicommensal organisms. Their mortality due to environmental factors transmission is via the aquatic especially in culture conditions with environment and they attach to the body poor water quality, increased water surface of motile larvae and grow up to temperature and overcrowding. adult stage and feed on free living Mortality has been reported in penaeid ciliated protozoa. In sever infestations shrimps under poor culture conditions they can cause hypoxia on branch due to severe invading of peritrish (Edgerton et al., 2002). In this study ciliates (Shields and Overstreet, 2003) heavy infestation of branch from and Cherax tenuimanus (Villarreal and Cothurina spp. was observed. The Hutchings, 1986; Brown et al., 1993). metazoan parasites including free living Also, systemic infection of redclaw nematode, Branchiobdella Annelids, crayfish by Tetrahymna peryformis was and Oligocheta that were isolated in this reported from north Queensland and study were reported as epicommensal or Australia (Edgerton et al., 1996). cymbiont which did not cause important Ciliated protozoa are the most common diseases in freshwater crayfish and abundant parasites in different (Alderman and Polglase, 1988;
Downloaded from jifro.ir at 7:55 +0330 on Monday September 27th 2021 crustaceans. Most of them considered Edgerton et al., 2002). Isolated as epibionts in fresh water crayfish the nematodes belonging to free living heavy infestation of which can affect nematodes were observed on external growth, molting, larvae survival, other body surfaces, the bucal area and organ functions such as that of the eyes, branch of A. leptodactylus samples. branch, and appendices, and restrict There may be a close relationship locomotion and cause occlusion of between the nematodes and the host as female genital pores, decrease they need the crayfish to complete their fecundity, feed intake competition and life cycle (Edgerton et al., 2002). mortality specially in culture Isolated Branchiobodella species were environments (Mayen-Estrada and leech like small nematodes from Aladro- Lubel, 2001a; Fernandez– Analidae with a segmented body and Leborans, 2004; Fernandez– Leborans ventral and dorsal sucker to attach to
544 Yahyazadeh et al., Commensalism and parasitic infestation in crayfish (Astacus leptodactylus …
the host. These worms were mentioned They grew up and developed by laying as Ectocommensal and Ectosymbiont eggs in cocoons attached to the external that settled on branch and body surfaces surface of the host. It is believed that especially carapace, and bucal area but transmission was through direct contact some of them were external facultative (Thune, 1994; Edgerton et al., 2002). parasites in freshwater crayfish and Also, Branchiobodella species have crustaceans (Alderman and Polglase, been observed independent and hostless 1988; Gelder et al., 1999). but it is believed that they cannot Branchiobodella were the most continue to live without a host and common organisms existing on the reproduce only when attached to a live freshwater crayfish that included crayfish host. However they have been several genera. It was estimated that up reported on the body surface of isopods to now, nearly 150 species were and crabs (Brown et al., 2002; Edgerton identified from 21 genera the highest et al., 2002; Evans and Edgerton, numbers of which belonged to 2002). Cambricola and Branchiobodella. The There is evidence of branch injury distribution of infestation to these due to accumulation of B. hexodenta organisms in freshwater crayfish in the and B. actasi and feeding from tissue north hemisphere has been reported specially in sever infestations from the north and central parts of (Alderman and Polglase, 1988; Vogt, America, Europe, Asia (Alderman and 1999). On the other hand, there are Polglase, 1988), cultured crayfish of some reports on their positive symbiotic Iran (Asgharnia, 2008) whereas no effects on cleaning and eradication of infestation has been reported from the organisms existing on body surface of southern hemisphere (Edgerton et al., crayfish, increasing growth and
Downloaded from jifro.ir at 7:55 +0330 on Monday September 27th 2021 2002). Also, in this study higher decreasing mortality (Keller, 1992; infestation from Branchiobodella Brown et al., 2002; Lee et al., 2009). species was observed on larger A. The Aras Dam is the only natural leptodactylus from the Aras Dam than and economic harvesting resource for smaller sized ones , especially on the A. leptodactylus in Iran which enjoys a maxillopods and head which could be good stocking capacity. The flowing of related to larger body size to parasite domestic, industrial and agricultural colonization, nutritional richness, and sewages into this reservoir can affect lower molting (Cenni et al., 2002; Mori the water quality and infection of et al., 2002). Also, characterization of aquatic animals.Therefore, preservation, their colonization area could be conservation, monitoring and seasonal and related to the presence of management of this vulnerable and Branchiobodella species (Edgerton et economic resource are very important. al., 2002). The life cycle of It seems that interaction among Branchiobodella is not exactly known. opportunistic or commensally parasitic Iranian Journal of Fisheries Sciences 16(2) 2017 545
agents with their host (crayfish) crayfish—biology, management and depends on environmental conditions, exploitation. Croom Helm, London, immune defense of the host and pp. 167– 212. invasive rate of agents (interaction Asgharnia, M., 2008. The study of among host, parasite and environment). parasitic infestation in Astacus Existence of parasitic agents and effects leptodactylus in culture of anthropogenic factors such as environments of Sefid-Rood overfishing, industrial, domestic and fisheries research center – Astaneh, agricultural pollution on aquatic Guilan Province. Pajhohesh va ecosystems and euthrophic condition of Sazandegi in livestock and aquatics, the Aras Dam (Mohsenpour Azari, N.78P. (in Persian) . 2010) could change this interaction and Brown, B.L., Creed, R.P., Dobson, due to adverse environmental W.E., 2002. Branchiobdellid conditions, weakening of crayfish annelids and their crayfish hosts: are immunity acts as a predisposing factor they engaged in a cleaning for viral, bacterial and fungal diseases symbiosis? Oecologia, 132, 250– of crayfish and other aquatic resources 255. of the Aras Dam Reservoir. Therefore, Brown, P.B., White, M.R., Swann, due to economic and bio-ecological D.L. and Fuller, M.S., 1993. A importance of A. leptodactylus and less severe outbreak of ectoparsitism due information about its health status, to Epistylis sp. Journal of the World continuous monitoring and good Aquaculture Society, 24 (1), 116– management of the Aras Dam is 120. needed. Bykhovskyaya-Pavlovskaya, I.E., Gusev, A.V., Dubinina, M.N.,
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