Prevalence, Morpho-Histopathological Identification, Clinical Picture, and the Role of Lernanthropus kroyeri to Alleviate the Zinc Toxicity in Moron labrax

Prevalence, Morpho-Histopathological Identification, Clinical Picture, and the Role of Lernanthropus kroyeri to Alleviate the Zinc Toxicity in Moron labrax | Research Square window.SnipcartSettings = { analytics: { enabled: false } }; (function() { var accessVector = localStorage.getItem('access_vector') || ''; window.dataLayer = window.dataLayer || []; if (accessVector) { window.dataLayer.push({ user: { profile: { profileInfo: { snid: accessVector } } } }); } })(); (function(w,d,s,l,i){w[l]=w[l]||[];w[l].push({'gtm.start':new Date().getTime(),event:'gtm.js'});var f=d.getElementsByTagName(s)[0],j=d.createElement(s),dl=l!='dataLayer'?'&l='+l:'';j.async=true;j.src='https://www.googletagmanager.com/gtm.js?id='+i+dl;f.parentNode.insertBefore(j,f);})(window,document,'script','dataLayer','GTM-K279D39R'); Browse Preprints In Review Journals COVID-19 Preprints AJE Video Bytes Research Tools Research Promotion AJE Professional Editing AJE Rubriq About Preprint Platform In Review Editorial Policies Our Team Advisory Board Help Center Sign In Submit a Preprint Cite Share Download PDF Research Article Prevalence, Morpho-Histopathological Identification, Clinical Picture, and the Role of Lernanthropus kroyeri to Alleviate the Zinc Toxicity in Moron labrax Attia A. Abou Zaid, Rehab, R. Abd EL Maged, Nesma Rasheed, Dina Mohamed Mansour, and 1 more This is a preprint; it has not been peer reviewed by a journal. https://doi.org/ 10.21203/rs.3.rs-1435215/v1 This work is licensed under a CC BY 4.0 License Status: Posted Version 1 posted You are reading this latest preprint version Abstract The present context is the pioneer attempt to verify the ability of copepod, Lernanthropus kroyeri, L. kroyeri , to uptake and accumulate heavy metals. We primarily assess the prevalence of the parasite in various seasons, clinical signs, and post-mortem changes in sea bass (Moron labrax) . Morphological features of the parasite using a light microscope, bioaccumulation of heavy metals in tissues of both L. kroyeri and M. labrax (gills, muscles) using Flame Atomic Absorption Spectrometry, and histopathological alterations were monitored. Fish (n = 200) were obtained from Ezbet Elborg and examined for the parasite, L. kroyeri . Results revealed that the total infection recorded 86%. The infested fish exhibited excessive mucous and ulceration at the site of attachment. The post-mortem lesion in gills was marbling appearance with destructed filaments. Various heavy metals (Zn, Co, Cu, and Cd) were detected in the tissues of L. kroyeri and M. labrax and surprisingly, L. kroyeri had the ability to uptake and accumulate a high amount of Zn in its tissues. Infested fish accumulated less concentration of Zn in their tissue compared to the non-infested ones. Within the host tissue, the accumulation of Zn was higher in gills compared to muscles. Histopathological findings demonstrated scattered parasitic elements with destruction of gill lamellae. Taken together, we clearly highlight the potential role of L. kroyeri to eliminate Zn and it can be utilized as a bio-indicator for metal monitoring studies for sustaining aquaculture. Moron labra Lernanthropus parasite Histopathology Heavy metals residues Electron microscope. Figures Figure 1 Figure 2 Figure 3 Figure 4 Figure 5 Figure 6 Figure 7 Figure 8 Figure 9 Figure 10 Figure 11 Figure 12 Figure 13 Introduction Recently, parasitic infestations induce serious hazards including higher mortalities and diseases to the freshwater fish in Egypt (Mahboub and Shaheen, 2020 ; Mahboub and Shaheen, 2021 ). Parasitic copepods are commonly present in wild and cultured marine fish (Rameshkumar and Ravichandran, 2013 ). Lernanthropus is the most common genus of copepods and there are more than 100 species isolated from gills of different species of marine fish (Korun and Tepecik, 2005 ; Toksen, 2007 ). Lernanthropus causes erosion and necrosis of gill filaments (Merna and Dezfuli, 2003) with severe desquamation and necrosis of secondary lamellae and leukocytic infiltration (Eissa et al., 2020 ). At the site of parasite attachment, complete superficial tissue erosion with exposure of the primary lamellar cartilage, exposure of blood vessels, and hemorrhage resulting from the grasping action of the mandibles and the maxillae of the parasite (Maurizio and Bahram, 2003). Pollution with heavy metals or toxic pollutants in the aquatic ecosystem is a global problem with potential concern as that negatively affects fish health-inducing physiological, biochemical, molecular, and histopathological alterations for fish (Mbeh et al. 2019 ; Abiona et al. 2019 ; Abu Zeid et al., 2021 ). Fish absorb heavy metals from the surrounding water and accumulate in different tissues in various amounts (Mahmoud et al., 2015 ). The metals can enter the fish bloodstream and gradually accumulate in their tissues (Ismail & Mahboub 2016 ; Mahboub et al., 2021 ), particularly in the hepatic tissue, where they are reach to the consumers through the food chain or bio-transformed and excreted (Amini et al., 2013 ). Hence, parasites, as well as heavy metals, induce serious damage to the biochemical and physiology processes that in return induce severe impairments to the health and physiology status of fish (Sabra and Mehana, 2015 ). Recent reports address various methods for heavy metals chelation such as natural extracts, probiotics, and nanoparticles (El-Bouhy et al., 2021a ; El-Bouhy et al., 2021b ; Mahboub et al., 2021 ). Fish parasites are considered extra sensitive to the pollution with heavy metal, as they not only uptake and accumulate toxicants in their tissues, but they also produce a physiological response to it (Diamant, 1989 ). Parasites can be used either as effective indicators or as accumulation indicators, because of the different ways in which they react to anthropogenic pollution (Sures, 2003 ; Luckenbach et al., 2001 ). There is a relationship between parasitism and pollution and the role of parasites as bio-indicators of heavy metals pollution (Sures, 2006 ; vidal-Martinez, 2007). Previous reports addressed the ability of some parasites to accumulate heavy metal concentrations such as Acanthocephalans, Cestodes (Najm and Fakhar, 2015 ), and parasitic nematodes (Khaleghzadeh-Ahangar et al., 2011 , Nachev et al., 2013 ). Therefore, the current investigation was carried out to assess the impacts of L. kroyeri infestation. We addressed the prevalence of the parasite in the different seasons, clinical signs, and post-mortem changes. The body surface of L. kroyeri using light microscope was illustrated, besides bioaccumulation of heavy metals in tissues of both L. kroyeri and M. labrax . Further, histopathological alterations on the gills and muscles of infected M. labrax were detected. Materials And Methods Research ethics: The protocol of the current study complies with the guidelines and was carried out according to the UK Animals (Scientific Procedures) Act, 1986 and associated guidelines, EU Directive for animal experiments. The experimental procedures were approved by the Animal Health Research Institute, El-Mansoura Branch, Egypt. Fish samples: A total number of 200 Sea bass ( Moron labrax ) fish samples were collected alive or freshly dead from the market of Ezbet-Elborg area, Damietta province, Egypt during the period between March 2019 until February 2020. The collected fish were transported in thick ice polyethylene bags to the laboratory of Animal Health Research Institute, El-Mansoura Branch, where they examined immediately. Clinical examination: Fish were examined for detection of any clinical abnormalities and external parasites according to Eissa ( 2016 ). Parasitological examination: Examination of external surface of the fish body was carried out by naked eyes and hand lens to detect any abnormalities, gill opercula removed by scissors and transferred the gill filaments to slides with some normal saline then cover it by cover slide and examined microscopically (Lucky, 1977 ). The detected crustacean parasites were carefully collected by a fine brush and special needle, and transferred into Petri-dish and washed several times in distilled water then preserved in 70% ethanol and cleared in lactophenol then mounting with polyvol (Raef et al., 2000 ). Heavy metals analysis: The samples were dried at 60°C for 48 hr. Then the samples were ground to a fine powder and stored in plastic bags until analysis. One gram of each sample was dry-ashed in a muffle furnace at 450c for 5 hr, extracted with 20% hydrochloric acid. The samples were measured by Flame Atomic Absorption Spectrometry FAAS (GBC Avanta E, Victoria, Australia; Ser. No. A5616). All the used equipments were calibrated and uncertainties were calculated. Internal and external quality assurance systems were applied in the Central laboratory of Environmental studies in Kafr-Elsheikh University according to ISO/IEC 17025 (2005). All measurements, blanks, triplicate measurements of elements in extracts and analysis of certified reference materials for each metal (Merck) were routinely included for quality control. Histopathological examination: The affected parts of gills were fixed in 10% neutral buffered formalin, then dehydrated in ascending grades of alcohol and cleaned in xylol, then embedded in paraffin wax. Five-micron sections were prepared and then routinely stained with Hematoxlyin and Eosin (H&E) according to Suvarna et al. (2013), then examined microscopically. Results Clinical examination of infected fish: The clinical signs of infected fish were hemorrhagic areas on different parts of the body surface (Fig. 1 , red arrows) and gills showed a marbling appearance (area of redness and paleness) (Fig. 1 , white arrows). Gill tips were attached in some areas with mucous secretion and L. kroyeri was seen macroscopically as black filaments (Fig. 1 , black arrows). Parasitological examination: Morphological description of L. kroyeri Van Beneden, 1851. The parasite was found attached to the gills of M. labrax . It appeared white to yellowish color in fresh samples. The female was easily recognized by the presence of the two egg-sacs which were clearly seen by necked eyes (Fig. 2 ). The bodies of isolated copepods appeared elongated in both sexes. The cephalothorax had a dorsal shield narrower anteriorly, and slightly concave on the posterior margin, rounded posterolateral corners, anterolateral extended ventrally as prominent, rounded lobes. A deep constriction was found between the cephalothorax and pregenital trunk. There were 4 pairs of the thoracic legs, the first one was biramous. (Fig. 3 ) Prevalence of L. kroyeri in infected M. labrax: One hundred sixty-two out of 200 examined M. labrax were infected with L. kroyeri (81%). The highest infection was recorded during Spring (94%) followed by Summer (90%) then Autumn (78%) and the lowest infection were recorded in Winter (31%) as depicted in Table 1 , Fig. 4 . Table 1 Seasonal prevalence of L. kroyeri among examined M. labrax : Winter Spring Summer Autumn Total Nu Ex Nu In % Nu Ex Nu In % Nu Ex Nu In % Nu Ex Nu In % Nu Ex Nu In % 50 31 62 50 47 94 50 45 90 50 39 78 200 162 81 Nu.Ex: Number of examined M. labrax . Nu.In: Number of infected M. labrax . % : Percentage of infection. Heavy metal accumulation by L. kroyeri and fish host: Mean ± SEM of heavy metal concentrations in gills and muscle of both infected and non-infected fish as well as in parasitic tissue are illustrated in Table 2 , Fig. 5 . Zinc was accumulated with higher levels in the gills (374.0 ± 2.51 mg/kg) and muscles (270.5 ± 3.03 mg/kg) of non-infested fish compared to the gills (275.0 ± 3.11 mg/kg) and muscles (124.8 ± 2.15 mg/kg) of infested fish. Surprisingly, the parasite accumulated Zn in its tissue (237.5 ± 2.86 mg/kg). The differential concentration of Zn in gills, muscle, and parasitic tissue was analyzed by unpaired t-test. While the concentrations of other elements were recorded under the detection limit (UDL; <0.3 mg/kg for Co and Cu or < 0.03mg/kg for Cd). Table 2 Mean of heavy metals concentration in fish tissues and parasite: Element Organ Non infected Infected p . value Zn Fish Gills 374.0 ± 2.51 275.0 ± 3.11 < 0.0001 Muscle 270.5 ± 3.03 124.8 ± 2.15 < 0.0001 Parasite 237.5 ± 2.86 Co Fish Gills UDL UDL - Muscle UDL UDL - Parasite UDL Cd Fish Gills UDL UDL - Muscle UDL UDL - Parasite UDL Cu Fish Gills UDL UDL - Muscle UDL UDL - Parasite UDL Histopathological results: Various sections from crustcean parasitic elements randomly distributed in gills were noticed (Fig. 6 ). The adjacent primary filaments were bent, stunted, and disorganized with the partial or complete destruction of the secondary lamellar epithelium (Fig. 7 ). Metaplasia of some surface epithelium to goblet cells was evident. Sometimes intense hemorrhage and excess mucous exudate could be seen in the vicinity of some parasites (Fig. 8 ). Moreover, complete destruction of secondary lamellar epithelium from both sides of gill filaments leaving primary filaments denuded could be seen (Fig. 9 ). Other gill filaments showed compensatory hyperplasia and hypertrophy of secondary lamellar epithelium which results in their fusion (Fig. 10 ). The blood vessels of gill filaments and arches revealed telangectiasis beside edema in the surrounding tissue (Fig. 11 ). Sometimes lymphocytes and eosinophils granular cells besides melanomacrophage cells were focally scattered in gill filaments and arches, sloughing of epidermal tissue of gill arch in addition to metaplasia to mucus secretory cells were common (Fig. 12 ). The gill raker had erosion of their covering epithelium beside hyalinization and necrosis of the muscles (Fig. 13 ). Discussion Lernanthropus is the most common genus of parasitic copepods. There are more than 100 species described from gills of different marine fish (Toksen, 2007 ). The current investigation revealed hemorrhagic areas on the body surface with excessive mucous secretion and marbling appearance of the gills of infected M. labrax with L. kroyeri . These lesions could be attributed to attachment of the parasites by their rigid claws, feeding activity, severe irritation caused by parasitic movement, and mucous increase as a defense mechanism from the host to overcome the infection as reported by Heba Abdel-Mawla and El-Ekiaby (2012). The present study recorded isolation of L. kroyeri from gills of M. labrax . Likewise, Tosken et al. (2008), Henery et al. (2009), and Essa et al. (2012) were isolated the same parasite from the same host and the same site. Meanwhile Noor El-Deen et al., ( 2013 ) and Dawlat Hassanin ( 2016 ) isolated L. kroyeri from the gills of other fish species such as Mugil cephalus and Moolgarda seheli . In the current prospective, the prevalence of L. kroyeri was 81%, Concurrent with a previous study; Aneesh et al. ( 2014 ) recorded 81.4% infection of Strongylura strongylura by L. kroyeri . Additionally, Toksen ( 2007 ) reported a higher infection rate (100%) by L. kroyeri in Dicentrarchus labrax . Nevertheless, Manera and Dezfuli, ( 2003 ) obtained a lower infection rate (35%) with L. kroyeri in D. labrax . Our paper reported that L. kroyeri infection was highest during Spring (94%) followed by Summer (90%) then Autumn (78%) and finally Winter (31%). This sequence is nearly in agreement with Eissa et al. (2017) who also reported that the infection rate with L. kroyeri reached their maximum rate during Spring and Summer, while the lowest infection was recorded during Autumn. These results were inconsistent with Ola Abu Samak and Ashraf ( 2008 ) who reported that the infection rates with the same parasite reached their maximum rates in Autumn and Winter (42.5% and 35%) respectively, while their minimum value was 7.5% in Spring. These variances in the total infection and seasonal dynamics could be returned to the difference of fish species and the difference of locality of fish collection. Certain fish parasites can accumulate heavy metals at concentrations significantly higher than those in host tissues or the environment (Sures, 2001 , 2003 , 2004 ; Sures et al., 2003 ; Schludermann et al., 2003 ; Thielen et al., 2004 ; Tekin-Ozan and Kir, 2005). The data of our study revealed that there was a high concentration of Zn in the collected samples. While the concentrations of Cu, Cd and Co were under detection limit. In general, the accumulation of Zn was significantly higher in the non-infested tissue in comparison to the infested tissue samples. It is opined that L. kroyeri can absorb Zn from the fish tissue through its alimentary canal and accumulates it in the parasite tissue, this finding was verified by analysis of Zn in the parasite tissue. On the same manner, a recent study by Hassanine and Al-Hasawi, ( 2021 ) reported that acanthocephalan accumulates higher concentrations of heavy metals. Concurrent with other study, Szefer et al. ( 1998 ) suggested that the bioaccumulation of parasites may reflect the higher ability of host to clear heavy metals. Also, Sures and Siddall ( 1999 ), Taraschewski (2000) and Malek et al. ( 2007 ) considered the parasites beneficial and might act as a heavy metal sanitizer for the host. Gills were accumulated higher Zn value compared to the edible part of its fish host. The low ratio of Zn concentration in host muscle could be returned to the longer exposure time as metal uptake occurs faster in parasites as opined by Sures ( 2001 ). Considering histopathological findings, we illustrated sections of L. kroyeri distributed in the gills. Similarly, a recent study by Eissa et al. ( 2020 ) reported occurrence of L. kroyeri fragments in the gills of D. labrax . Destruction of secondary lamellar epithelium, goblet cell metaplasia with hemorrhage and excess mucous secretion could be induced as a tissue reaction to decrease the irritation against the infestation. Concurrent with previous studies, Heba et al. ( 2015 ), Lester and Hayward ( 2006 ), Ragias et al. ( 2004 ), and Manera and Dezfuli ( 2003 ) reported extensive hemorrhage duo to the feeding activity of this parasite. Lymphocytes and eosinophils were found in gill filaments and arches, these outcomes were in accordance to Manera and Dezfuli ( 2003 ), Korun and Tepecik ( 2005 ), Toksen ( 2007 ), Jithendran et al. ( 2008 ), Yardimci and Pekmezci ( 2012 ). Also, erosion of gill raker beside necrosis of muscles were seen, likewise, Vinoth et al. ( 2010 ) reported pale gills induced by copepod parasites duo to loss of gill raker. Our investigation concluded that, although L. kroyeri has a bad effect on the infected M. labrax , it also plays an important role in elimination of heavy metals from the tissue of the infected fish through its ability to accumulate heavy metals in its body; and this can be advantageous for the infected hosts, allowing them to tolerate much higher concentrations of certain metals. The present results also confirmed that L. kroyeri seem to be good indicators of environmental pollutions. Conclusion To date, our prospective represents a premier study to report the efficacy of Lernanthropus kroyeri to uptake and accumulate heavy metals (zinc). However, L. kroyeri infests M. labrax with a high prevalence in Spring and Summer and demonstrates excessive mucous secretion, ulceration, marbling appearance of gills, and histopathological changes in the gills and muscles of the infested fish. By detecting various heavy metals (Zn, Co, Cu, and Cd) in the tissues of L. kroyeri and M. labrax , surprisingly, L. kroyeri has the ability to uptake the highest concentration of Zn in its tissues. Conclusively, parasitic infestation is eco-friendly method to uptake heavy metals, L. kroyeri can be utilized as natural antitoxic agent as well as considered a bio-indicator for the toxicity with heavy metals, and to lessen hazardous impacts to the aquatic environment for sustaining aquaculture. Future studies are needed to test the activity of other parasites to chelate heavy metals and also on various fish species. Declarations Author's contributions Conceptualization, A.A.A., R.R.A., N.R., D.M.M., H.H.M.; Methodology, A.A.A., R.R.A., N.R., D.M.M., H.H.M.; Formal analysis, A.A.A., R.R.A., N.R., D.M.M., H.H.M.; Investigation, A.A.A., R.R.A., N.R., D.M.M., H.H.M.; Resources, A.A.A., R.R.A., N.R., D.M.M., H.H.M.; Writing-original draft preparation, A.A.A., R.R.A., N.R., D.M.M., H.H.M.; Editing, H.H.M.; All authors have read and agreed to the published version of the manuscript. Conflict of interest The authors claim that there is no conflict of interest. Data availability All data are available in this manuscript and the supplementary file. Ethical approval This research was reviewed and approved by the Animal Care and Welfare Committee of Animal health Research Institute (AHRI), Giza , Egypt. Consent to participate Not applicable. Consent to publish Not applicable. Funding Not applicable. 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Hung Environ Poll 129:421–429 Tekin-Özan SI, Kir (2005) Comparative study on the accumulation of heavy metals in different organs of tench ( Tinca tinca L. 1758) and plerocercoids of its endoparasite Ligula intestinalis. Parasitol Res 97:156–159 Thielen F, Zimmermann S, Baska F, Taraschewski H, Sures B (2004) The intestinal parasite Pomphorhynchus laevis ( Acanthocephala ) from barbel as a bioindicator for metal pollution in the Danube River near Budapest. Hung Environ Pollution 129:421–429 Tokşen E, Nemli E, Değirmenci U (2008) The morphology of Lernanthropus kroyeri van Beneden, 1851 (Copepoda: Lernanthropidae) parasitic on seabass, Dicentrarchus labrax , 1758, from the Aegean Sea, Turkey. Turk Parazitol Derg 32(4):386–389 Toksen E (2007) Lernanthropus kroyeri van Beneden, 1851 (Crustacea: Copepoda) infections of culturedsea bass ( Dicentrarchus labrax L.) Bull. Eur Ass Fish Pathol 27(2):49–53 Topçu N (1977) Preparation of Biologic Objects for Scanning Electron Microscope. III. National Pathology Congress, (19–21 Eylül), 1977; 276–289 Van Bilsen M (2014) Fatty acids and cardiac diseases: Fuel carrying a message. Acta Physiol (Oxf) 211(3):476–490 Vinoth R, Kumar TT, Ravichandran S, Gopi M, Rameshkumar G (2010) Infestation of copepod parasites in the food fishes of Vellar Estuary, Southeast Cost of India. Acta Parasitol Globalis 1(1):01–05 Yardimci B, Pekmezci GZ (2012) Gill histopathology in cultured sea bass ( Dicentrarchus labrax L.) coinfected by Diplectanum aequans (Wagener, 1857) and Lernanthropus kroyeri (van Beneden, 1851): Ankara Univ. Vet Fak Derg 59:61–64 Cite Share Download PDF Status: Posted Version 1 posted You are reading this latest preprint version Research Square lets you share your work early, gain feedback from the community, and start making changes to your manuscript prior to peer review in a journal. As a division of Research Square Company, we’re committed to making research communication faster, fairer, and more useful. We do this by developing innovative software and high quality services for the global research community. Our growing team is made up of researchers and industry professionals working together to solve the most critical problems facing scientific publishing. Also discoverable on Platform About Our Team In Review Editorial Policies Advisory Board Help Center Resources Author Services Accessibility API Access RSS feed Manage Cookie Preferences © Research Square 2026 | ISSN 2693-5015 (online) Privacy Policy Terms of Service Do Not Sell My Personal Information {"props":{"pageProps":{"initialData":{"identity":"rs-1435215","acceptedTermsAndConditions":true,"allowDirectSubmit":true,"archivedVersions":[],"articleType":"Research Article","associatedPublications":[],"authors":[{"id":117322420,"identity":"63a988cc-52ec-4836-83c0-e72d3a22e566","order_by":0,"name":"Attia A. Abou Zaid","email":"","orcid":"","institution":"Kafrelsheikh University Faculty of Veterinary Medicine","correspondingAuthor":false,"submittingAuthor":false,"prefix":"","firstName":"Attia","middleName":"A. Abou","lastName":"Zaid","suffix":""},{"id":117322421,"identity":"96e19203-4a30-4744-93d1-c653cc33520a","order_by":1,"name":"Rehab, R. Abd EL Maged","email":"","orcid":"","institution":"Animal Health Research Institute","correspondingAuthor":false,"submittingAuthor":false,"prefix":"","firstName":"R.","middleName":"Abd EL Maged","lastName":"Rehab","suffix":""},{"id":117322422,"identity":"1e65990b-45b1-4e85-9226-fd5c6b3a7ccf","order_by":2,"name":"Nesma Rasheed","email":"","orcid":"","institution":"Animal Health Research Institute","correspondingAuthor":false,"submittingAuthor":false,"prefix":"","firstName":"Nesma","middleName":"","lastName":"Rasheed","suffix":""},{"id":117322423,"identity":"5ae14e2c-bfa1-499b-8850-f0cb140bc688","order_by":3,"name":"Dina Mohamed Mansour","email":"","orcid":"","institution":"Animal Health Research Institute","correspondingAuthor":false,"submittingAuthor":false,"prefix":"","firstName":"Dina","middleName":"Mohamed","lastName":"Mansour","suffix":""},{"id":117322424,"identity":"458834a4-6977-4977-bf99-5e7e98923e97","order_by":4,"name":"Heba Mahboub","email":"data:image/png;base64,iVBORw0KGgoAAAANSUhEUgAAAZAAAAAyAQMAAABI0h/eAAAABlBMVEX///8AAABVwtN+AAAACXBIWXMAAA7EAAAOxAGVKw4bAAAAl0lEQVRIiWNgGAWjYBACAwkeBmaGCiCDRC1nSNbC2EaKFnPp3qObC+cdljdnbz7A8KNiG2EtlnPOpd2eue2w4c6eYwmMPWduE+GwGzlmt3m3HWbccCPHAOhCorXMOWxPqpaGw4kkaplxLD15w5ljCQeJ90tBjbXthuPNBx/8qCBCCxQ0g8kDRKsHgjpSFI+CUTAKRsFIAwBbvEH2z0Y73gAAAABJRU5ErkJggg==","orcid":"https://orcid.org/0000-0003-1938-9135","institution":"Zagazig University Faculty of Veterinary Medicine","correspondingAuthor":true,"submittingAuthor":false,"prefix":"","firstName":"Heba","middleName":"","lastName":"Mahboub","suffix":""}],"badges":[],"createdAt":"2022-03-09 14:44:24","currentVersionCode":1,"declarations":"","doi":"10.21203/rs.3.rs-1435215/v1","doiUrl":"https://doi.org/10.21203/rs.3.rs-1435215/v1","draftVersion":[],"editorialEvents":[],"editorialNote":"","failedWorkflow":false,"files":[{"id":23542956,"identity":"c28f7004-7428-47ed-b15d-51aa27e4732e","added_by":"auto","created_at":"2022-07-06 17:10:42","extension":"jpg","order_by":1,"title":"Figure 1","display":"","copyAsset":false,"role":"figure","size":106451,"visible":true,"origin":"","legend":"\u003cp\u003e\u003cem\u003eMoron labrax\u003c/em\u003e showing hemorrhagic areas on different parts of the body surface (red arrows), a marbling appearance (white arrows), and gill tips were attached in some areas with mucous secretion and the parasites were seen by necked eyes as black filaments (black arrows).\u003c/p\u003e","description":"","filename":"1.jpg","url":"https://assets-eu.researchsquare.com/files/rs-1435215/v1/79f52da46a55231d26ae5856.jpg"},{"id":23542957,"identity":"0f3c1751-7a40-44e5-9a4b-1cc010f76998","added_by":"auto","created_at":"2022-07-06 17:10:42","extension":"jpg","order_by":2,"title":"Figure 2","display":"","copyAsset":false,"role":"figure","size":112620,"visible":true,"origin":"","legend":"\u003cp\u003eFresh samples of the parasite, \u003cem\u003eL. kroyeri\u003c/em\u003e, appeared in petri dish white to yellowish color. The female was easily recognized by the presence of the two egg-sacs.\u0026nbsp;\u003c/p\u003e\u003cp\u003e\u003cbr\u003e\u003c/p\u003e","description":"","filename":"2.jpg","url":"https://assets-eu.researchsquare.com/files/rs-1435215/v1/d507a4a45afa219f1cfd8992.jpg"},{"id":23543934,"identity":"daacd875-8e44-4a80-9377-ac17ab8c2ca8","added_by":"auto","created_at":"2022-07-06 17:15:42","extension":"jpg","order_by":3,"title":"Figure 3","display":"","copyAsset":false,"role":"figure","size":47205,"visible":true,"origin":"","legend":"\u003cp\u003eA; \u003cem\u003eL. kroyeri\u003c/em\u003e premature stage. B; male \u003cem\u003eL. kroyeri\u003c/em\u003e. C; female \u003cem\u003eL. kroyeri\u003c/em\u003e. a1;1st antenna. a2; 2nd antenna. L1; 1st thoracic leg. L2; 2nd thoracic leg. L3; 3rd thoracic leg. L4; 4th thoracic leg. m; maxilliped. mt; mouth tube. es; egg sac. ss; spermatophore sac. up; uropod. Scale bars:\u0026nbsp;500 μm.\u003c/p\u003e\u003cp\u003e\u003cbr\u003e\u003c/p\u003e","description":"","filename":"3.jpg","url":"https://assets-eu.researchsquare.com/files/rs-1435215/v1/a9206571fc62f54fabf1f034.jpg"},{"id":23544728,"identity":"242502fc-071e-4314-b6c9-75985ebe7144","added_by":"auto","created_at":"2022-07-06 17:20:42","extension":"jpg","order_by":4,"title":"Figure 4","display":"","copyAsset":false,"role":"figure","size":29985,"visible":true,"origin":"","legend":"\u003cp\u003eSeasonal prevalence of \u003cem\u003eL. kroyeri\u003c/em\u003e among examined \u003cem\u003eM. labrax\u003c/em\u003e.\u003c/p\u003e\u003cp\u003e\u003cbr\u003e\u003c/p\u003e","description":"","filename":"4.jpg","url":"https://assets-eu.researchsquare.com/files/rs-1435215/v1/1ce28f20e121775843776dca.jpg"},{"id":23544993,"identity":"9f2af7df-2065-41bb-b1a9-368827bc4a1b","added_by":"auto","created_at":"2022-07-06 17:25:42","extension":"jpg","order_by":5,"title":"Figure 5","display":"","copyAsset":false,"role":"figure","size":32214,"visible":true,"origin":"","legend":"\u003cp\u003eMean ± SEM concentration of Zn in gills, muscle and parasitic tissue.\u003c/p\u003e\u003cp\u003eSuperscript (****) indicates a significant differences at P value \u0026gt; 0.0001 as reported via t-test.\u003c/p\u003e\u003cp\u003e\u003cbr\u003e\u003c/p\u003e","description":"","filename":"5.jpg","url":"https://assets-eu.researchsquare.com/files/rs-1435215/v1/d099f4c7d6d1c3010f293218.jpg"},{"id":23544725,"identity":"c645bbac-ebc2-40df-b223-4eda303543da","added_by":"auto","created_at":"2022-07-06 17:20:42","extension":"jpg","order_by":6,"title":"Figure 6","display":"","copyAsset":false,"role":"figure","size":60500,"visible":true,"origin":"","legend":"\u003cp\u003eGills showing parasitic elements embedded between gill filaments (arrow) with stunted, bented and disorganized primary filaments (arrowhead).\u003c/p\u003e\u003cp\u003e\u003cbr\u003e\u003c/p\u003e","description":"","filename":"6.jpg","url":"https://assets-eu.researchsquare.com/files/rs-1435215/v1/37f6130f6d1f7d1f04bee09d.jpg"},{"id":23543935,"identity":"f735683b-a66f-4b9b-bff0-1cd0086e0ac7","added_by":"auto","created_at":"2022-07-06 17:15:42","extension":"jpg","order_by":7,"title":"Figure 7","display":"","copyAsset":false,"role":"figure","size":74992,"visible":true,"origin":"","legend":"\u003cp\u003eHigh power of the previous picture showing parasitic sections (arrow) with partial destruction of lamellar epithelium (arrowhead) or metaplasia to mucus secreting cells.\u003c/p\u003e\u003cp\u003e\u003cbr\u003e\u003c/p\u003e","description":"","filename":"7.jpg","url":"https://assets-eu.researchsquare.com/files/rs-1435215/v1/7dd8aef21443ed2288372535.jpg"},{"id":23542960,"identity":"13c7c707-69ce-4c03-ae61-1716cb9bbc4d","added_by":"auto","created_at":"2022-07-06 17:10:42","extension":"jpg","order_by":8,"title":"Figure 8","display":"","copyAsset":false,"role":"figure","size":87651,"visible":true,"origin":"","legend":"\u003cp\u003eGills showing parasitic sections (arrow) intense hemorrhage on gill surface (arrow head) and mucous exudate (thick arrow).\u003c/p\u003e\u003cp\u003e\u003cbr\u003e\u003c/p\u003e","description":"","filename":"8.jpg","url":"https://assets-eu.researchsquare.com/files/rs-1435215/v1/6f538cbeab438f062b1396fb.jpg"},{"id":23542958,"identity":"c4f2fa00-0d9a-49c3-b3ef-a8f808ea83c5","added_by":"auto","created_at":"2022-07-06 17:10:42","extension":"jpg","order_by":9,"title":"Figure 9","display":"","copyAsset":false,"role":"figure","size":86017,"visible":true,"origin":"","legend":"\u003cp\u003eGills showing denuded of primary filaments (arrow) with complete destruction of secondary lamellae of some filaments.\u003c/p\u003e\u003cp\u003e\u003cbr\u003e\u003c/p\u003e","description":"","filename":"9.jpg","url":"https://assets-eu.researchsquare.com/files/rs-1435215/v1/bbc60d52fe717b75a721433e.jpg"},{"id":23542964,"identity":"897c22d3-21fb-4005-bd1e-7b80f6da644d","added_by":"auto","created_at":"2022-07-06 17:10:42","extension":"jpg","order_by":10,"title":"Figure 10","display":"","copyAsset":false,"role":"figure","size":93825,"visible":true,"origin":"","legend":"\u003cp\u003eGills showing compensatory hyperplasia and hypertrophy of secondary lamellar epithelium (arrow) of some adjacent gill filaments.\u003c/p\u003e\u003cp\u003e\u003cbr\u003e\u003c/p\u003e","description":"","filename":"10.jpg","url":"https://assets-eu.researchsquare.com/files/rs-1435215/v1/4809b9074b489d309fe62d00.jpg"},{"id":23543941,"identity":"ac7993b4-012b-407e-92c6-013a39685286","added_by":"auto","created_at":"2022-07-06 17:15:42","extension":"jpg","order_by":11,"title":"Figure 11","display":"","copyAsset":false,"role":"figure","size":79123,"visible":true,"origin":"","legend":"\u003cp\u003eGill arch showing telanjectiasis of blood vessels (arrow) and edema (arrowhead).\u003c/p\u003e\u003cp\u003e\u003cbr\u003e\u003c/p\u003e","description":"","filename":"11.jpg","url":"https://assets-eu.researchsquare.com/files/rs-1435215/v1/3117d2eaecf55d1fc884279d.jpg"},{"id":23544994,"identity":"0d738367-2959-4aae-b7b9-284ec155cd51","added_by":"auto","created_at":"2022-07-06 17:25:42","extension":"jpg","order_by":12,"title":"Figure 12","display":"","copyAsset":false,"role":"figure","size":70277,"visible":true,"origin":"","legend":"\u003cp\u003eGill arch showing partial sloughing of epidermal covering (arrowhead) and metaplasia of mucus secretory cells (goblet cells) in superficial cells (arrow).\u003c/p\u003e\u003cp\u003e\u003cbr\u003e\u003c/p\u003e","description":"","filename":"12.jpg","url":"https://assets-eu.researchsquare.com/files/rs-1435215/v1/9b668e5ad2096e8f6920c79c.jpg"},{"id":23543938,"identity":"c0559929-dda8-4952-b67d-dcdb52e95500","added_by":"auto","created_at":"2022-07-06 17:15:42","extension":"jpg","order_by":13,"title":"Figure 13","display":"","copyAsset":false,"role":"figure","size":86507,"visible":true,"origin":"","legend":"\u003cp\u003eGill raker showing erosion of epidermis (arrow) with partial hyalinization and necrosis of muscles (arrow head).\u003c/p\u003e","description":"","filename":"13.jpg","url":"https://assets-eu.researchsquare.com/files/rs-1435215/v1/5dc49a568f89967a0a5b9c1d.jpg"},{"id":26260191,"identity":"bc4533c3-f6e6-4a15-b5a2-8550f01e5a60","added_by":"auto","created_at":"2022-09-09 14:22:18","extension":"pdf","order_by":0,"title":"","display":"","copyAsset":false,"role":"manuscript-pdf","size":884057,"visible":true,"origin":"","legend":"","description":"","filename":"manuscript.pdf","url":"https://assets-eu.researchsquare.com/files/rs-1435215/v1/3b5c9da2-2906-415c-b882-fc0c3130bb79.pdf"}],"financialInterests":"","formattedTitle":"Prevalence, Morpho-Histopathological Identification, Clinical Picture, and the Role of Lernanthropus kroyeri to Alleviate the Zinc Toxicity in Moron labrax","fulltext":[{"header":"Introduction","content":"\u003cp\u003eRecently, parasitic infestations induce serious hazards including higher mortalities and diseases to the freshwater fish in Egypt (Mahboub and Shaheen, \u003cspan citationid=\"CR25\" class=\"CitationRef\"\u003e2020\u003c/span\u003e; Mahboub and Shaheen, \u003cspan citationid=\"CR26\" class=\"CitationRef\"\u003e2021\u003c/span\u003e). Parasitic copepods are commonly present in wild and cultured marine fish (Rameshkumar and Ravichandran, \u003cspan citationid=\"CR39\" class=\"CitationRef\"\u003e2013\u003c/span\u003e). Lernanthropus is the most common genus of copepods and there are more than 100 species isolated from gills of different species of marine fish (Korun and Tepecik, \u003cspan citationid=\"CR20\" class=\"CitationRef\"\u003e2005\u003c/span\u003e; Toksen, \u003cspan citationid=\"CR54\" class=\"CitationRef\"\u003e2007\u003c/span\u003e). Lernanthropus causes erosion and necrosis of gill filaments (Merna and Dezfuli, 2003) with severe desquamation and necrosis of secondary lamellae and leukocytic infiltration (Eissa et al., \u003cspan citationid=\"CR9\" class=\"CitationRef\"\u003e2020\u003c/span\u003e). At the site of parasite attachment, complete superficial tissue erosion with exposure of the primary lamellar cartilage, exposure of blood vessels, and hemorrhage resulting from the grasping action of the mandibles and the maxillae of the parasite (Maurizio and Bahram, 2003).\u003c/p\u003e \u003cp\u003ePollution with heavy metals or toxic pollutants in the aquatic ecosystem is a global problem with potential concern as that negatively affects fish health-inducing physiological, biochemical, molecular, and histopathological alterations for fish (Mbeh et al. \u003cspan citationid=\"CR31\" class=\"CitationRef\"\u003e2019\u003c/span\u003e; Abiona et al. \u003cspan citationid=\"CR1\" class=\"CitationRef\"\u003e2019\u003c/span\u003e; Abu Zeid et al., \u003cspan citationid=\"CR2\" class=\"CitationRef\"\u003e2021\u003c/span\u003e). Fish absorb heavy metals from the surrounding water and accumulate in different tissues in various amounts (Mahmoud et al., \u003cspan citationid=\"CR27\" class=\"CitationRef\"\u003e2015\u003c/span\u003e). The metals can enter the fish bloodstream and gradually accumulate in their tissues (Ismail \u0026amp; Mahboub \u003cspan citationid=\"CR16\" class=\"CitationRef\"\u003e2016\u003c/span\u003e; Mahboub et al., \u003cspan citationid=\"CR24\" class=\"CitationRef\"\u003e2021\u003c/span\u003e), particularly in the hepatic tissue, where they are reach to the consumers through the food chain or bio-transformed and excreted (Amini et al., \u003cspan citationid=\"CR3\" class=\"CitationRef\"\u003e2013\u003c/span\u003e).\u003c/p\u003e \u003cp\u003eHence, parasites, as well as heavy metals, induce serious damage to the biochemical and physiology processes that in return induce severe impairments to the health and physiology status of fish (Sabra and Mehana, \u003cspan citationid=\"CR40\" class=\"CitationRef\"\u003e2015\u003c/span\u003e). Recent reports address various methods for heavy metals chelation such as natural extracts, probiotics, and nanoparticles (El-Bouhy et al., \u003cspan citationid=\"CR10\" class=\"CitationRef\"\u003e2021a\u003c/span\u003e; El-Bouhy et al., \u003cspan citationid=\"CR11\" class=\"CitationRef\"\u003e2021b\u003c/span\u003e; Mahboub et al., \u003cspan citationid=\"CR24\" class=\"CitationRef\"\u003e2021\u003c/span\u003e). Fish parasites are considered extra sensitive to the pollution with heavy metal, as they not only uptake and accumulate toxicants in their tissues, but they also produce a physiological response to it (Diamant, \u003cspan citationid=\"CR6\" class=\"CitationRef\"\u003e1989\u003c/span\u003e). Parasites can be used either as effective indicators or as accumulation indicators, because of the different ways in which they react to anthropogenic pollution (Sures, \u003cspan citationid=\"CR45\" class=\"CitationRef\"\u003e2003\u003c/span\u003e; Luckenbach et al., \u003cspan citationid=\"CR22\" class=\"CitationRef\"\u003e2001\u003c/span\u003e). There is a relationship between parasitism and pollution and the role of parasites as bio-indicators of heavy metals pollution (Sures, \u003cspan citationid=\"CR42\" class=\"CitationRef\"\u003e2006\u003c/span\u003e; vidal-Martinez, 2007). Previous reports addressed the ability of some parasites to accumulate heavy metal concentrations such as Acanthocephalans, Cestodes (Najm and Fakhar, \u003cspan citationid=\"CR33\" class=\"CitationRef\"\u003e2015\u003c/span\u003e), and parasitic nematodes (Khaleghzadeh-Ahangar et al., \u003cspan citationid=\"CR19\" class=\"CitationRef\"\u003e2011\u003c/span\u003e, Nachev et al., \u003cspan citationid=\"CR32\" class=\"CitationRef\"\u003e2013\u003c/span\u003e).\u003c/p\u003e \u003cp\u003eTherefore, the current investigation was carried out to assess the impacts of \u003cem\u003eL. kroyeri\u003c/em\u003e infestation. We addressed the prevalence of the parasite in the different seasons, clinical signs, and post-mortem changes. The body surface of \u003cem\u003eL. kroyeri\u003c/em\u003e using light microscope was illustrated, besides bioaccumulation of heavy metals in tissues of both \u003cem\u003eL. kroyeri\u003c/em\u003e and \u003cem\u003eM. labrax\u003c/em\u003e. Further, histopathological alterations on the gills and muscles of infected \u003cem\u003eM. labrax\u003c/em\u003e were detected.\u003c/p\u003e"},{"header":"Materials And Methods","content":"\u003cdiv id=\"Sec3\" class=\"Section2\"\u003e \u003ch2\u003eResearch ethics:\u003c/h2\u003e \u003cp\u003e The protocol of the current study complies with the guidelines and was carried out according to the UK Animals (Scientific Procedures) Act, 1986 and associated guidelines, EU Directive for animal experiments. The experimental procedures were approved by the Animal Health Research Institute, El-Mansoura Branch, Egypt.\u003c/p\u003e \u003c/div\u003e \u003cdiv id=\"Sec4\" class=\"Section2\"\u003e \u003ch2\u003eFish samples:\u003c/h2\u003e \u003cp\u003eA total number of 200 Sea bass (\u003cem\u003eMoron labrax\u003c/em\u003e) fish samples were collected alive or freshly dead from the market of Ezbet-Elborg area, Damietta province, Egypt during the period between March 2019 until February 2020. The collected fish were transported in thick ice polyethylene bags to the laboratory of Animal Health Research Institute, El-Mansoura Branch, where they examined immediately.\u003c/p\u003e \u003c/div\u003e \u003cdiv id=\"Sec5\" class=\"Section2\"\u003e \u003ch2\u003eClinical examination:\u003c/h2\u003e \u003cp\u003eFish were examined for detection of any clinical abnormalities and external parasites according to Eissa (\u003cspan citationid=\"CR8\" class=\"CitationRef\"\u003e2016\u003c/span\u003e).\u003c/p\u003e \u003c/div\u003e \u003cdiv id=\"Sec6\" class=\"Section2\"\u003e \u003ch2\u003eParasitological examination:\u003c/h2\u003e \u003cp\u003eExamination of external surface of the fish body was carried out by naked eyes and hand lens to detect any abnormalities, gill opercula removed by scissors and transferred the gill filaments to slides with some normal saline then cover it by cover slide and examined microscopically (Lucky, \u003cspan citationid=\"CR23\" class=\"CitationRef\"\u003e1977\u003c/span\u003e). The detected crustacean parasites were carefully collected by a fine brush and special needle, and transferred into Petri-dish and washed several times in distilled water then preserved in 70% ethanol and cleared in lactophenol then mounting with polyvol (Raef et al., \u003cspan citationid=\"CR37\" class=\"CitationRef\"\u003e2000\u003c/span\u003e).\u003c/p\u003e \u003c/div\u003e \u003cdiv id=\"Sec7\" class=\"Section2\"\u003e \u003ch2\u003eHeavy metals analysis:\u003c/h2\u003e \u003cp\u003eThe samples were dried at 60\u0026deg;C for 48 hr. Then the samples were ground to a fine powder and stored in plastic bags until analysis. One gram of each sample was dry-ashed in a muffle furnace at 450c for 5 hr, extracted with 20% hydrochloric acid. The samples were measured by Flame Atomic Absorption Spectrometry FAAS (GBC Avanta E, Victoria, Australia; Ser. No. A5616). All the used equipments were calibrated and uncertainties were calculated. Internal and external quality assurance systems were applied in the Central laboratory of Environmental studies in Kafr-Elsheikh University according to ISO/IEC 17025 (2005). All measurements, blanks, triplicate measurements of elements in extracts and analysis of certified reference materials for each metal (Merck) were routinely included for quality control.\u003c/p\u003e \u003c/div\u003e \u003cdiv id=\"Sec8\" class=\"Section2\"\u003e \u003ch2\u003eHistopathological examination:\u003c/h2\u003e \u003cp\u003eThe affected parts of gills were fixed in 10% neutral buffered formalin, then dehydrated in ascending grades of alcohol and cleaned in xylol, then embedded in paraffin wax. Five-micron sections were prepared and then routinely stained with Hematoxlyin and Eosin (H\u0026amp;E) according to Suvarna et al. (2013), then examined microscopically.\u003c/p\u003e \u003c/div\u003e"},{"header":"Results","content":"\u003cdiv id=\"Sec10\" class=\"Section2\"\u003e \u003ch2\u003eClinical examination of infected fish:\u003c/h2\u003e \u003cp\u003eThe clinical signs of infected fish were hemorrhagic areas on different parts of the body surface (Fig.\u0026nbsp;\u003cspan refid=\"Fig1\" class=\"InternalRef\"\u003e1\u003c/span\u003e, red arrows) and gills showed a marbling appearance (area of redness and paleness) (Fig.\u0026nbsp;\u003cspan refid=\"Fig1\" class=\"InternalRef\"\u003e1\u003c/span\u003e, white arrows). Gill tips were attached in some areas with mucous secretion and \u003cem\u003eL. kroyeri\u003c/em\u003e was seen macroscopically as black filaments (Fig.\u0026nbsp;\u003cspan refid=\"Fig1\" class=\"InternalRef\"\u003e1\u003c/span\u003e, black arrows).\u003c/p\u003e \u003c/div\u003e \u003cdiv id=\"Sec11\" class=\"Section2\"\u003e \u003ch2\u003eParasitological examination:\u003c/h2\u003e \u003cp\u003e \u003cem\u003eMorphological description of L. kroyeri Van Beneden, 1851.\u003c/em\u003e \u003c/p\u003e \u003cp\u003eThe parasite was found attached to the gills of \u003cem\u003eM. labrax\u003c/em\u003e. It appeared white to yellowish color in fresh samples. The female was easily recognized by the presence of the two egg-sacs which were clearly seen by necked eyes (Fig.\u0026nbsp;\u003cspan refid=\"Fig2\" class=\"InternalRef\"\u003e2\u003c/span\u003e). The bodies of isolated copepods appeared elongated in both sexes. The cephalothorax had a dorsal shield narrower anteriorly, and slightly concave on the posterior margin, rounded posterolateral corners, anterolateral extended ventrally as prominent, rounded lobes. A deep constriction was found between the cephalothorax and pregenital trunk. There were 4 pairs of the thoracic legs, the first one was biramous. (Fig.\u0026nbsp;\u003cspan refid=\"Fig3\" class=\"InternalRef\"\u003e3\u003c/span\u003e)\u003c/p\u003e \u003c/div\u003e \u003cdiv id=\"Sec12\" class=\"Section2\"\u003e \u003ch2\u003ePrevalence of L. kroyeri in infected M. labrax:\u003c/h2\u003e \u003cp\u003eOne hundred sixty-two out of 200 examined \u003cem\u003eM. labrax\u003c/em\u003e were infected with \u003cem\u003eL. kroyeri\u003c/em\u003e (81%). The highest infection was recorded during Spring (94%) followed by Summer (90%) then Autumn (78%) and the lowest infection were recorded in Winter (31%) as depicted in Table\u0026nbsp;\u003cspan refid=\"Tab1\" class=\"InternalRef\"\u003e1\u003c/span\u003e, Fig.\u0026nbsp;\u003cspan refid=\"Fig4\" class=\"InternalRef\"\u003e4\u003c/span\u003e.\u003c/p\u003e \u003cp\u003e \u003cdiv class=\"gridtable\"\u003e\u003ctable float=\"Yes\" id=\"Tab1\" border=\"1\"\u003e \u003ccaption language=\"En\"\u003e \u003cdiv class=\"CaptionNumber\"\u003eTable 1\u003c/div\u003e \u003cdiv class=\"CaptionContent\"\u003e \u003cp\u003eSeasonal prevalence of \u003cem\u003eL. kroyeri\u003c/em\u003e among examined \u003cem\u003eM. labrax\u003c/em\u003e:\u003c/p\u003e \u003c/div\u003e \u003c/caption\u003e \u003ccolgroup cols=\"15\"\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c1\" colnum=\"1\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c2\" colnum=\"2\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c3\" colnum=\"3\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c4\" colnum=\"4\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c5\" colnum=\"5\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c6\" colnum=\"6\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c7\" colnum=\"7\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c8\" colnum=\"8\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c9\" colnum=\"9\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c10\" colnum=\"10\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c11\" colnum=\"11\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c12\" colnum=\"12\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c13\" colnum=\"13\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c14\" colnum=\"14\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c15\" colnum=\"15\"\u003e\u003c/div\u003e \u003cthead\u003e \u003ctr\u003e \u003cth align=\"left\" colspan=\"3\" nameend=\"c3\" namest=\"c1\"\u003e \u003cp\u003eWinter\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colspan=\"3\" nameend=\"c6\" namest=\"c4\"\u003e \u003cp\u003eSpring\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colspan=\"3\" nameend=\"c9\" namest=\"c7\"\u003e \u003cp\u003eSummer\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colspan=\"3\" nameend=\"c12\" namest=\"c10\"\u003e \u003cp\u003eAutumn\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colspan=\"3\" nameend=\"c15\" namest=\"c13\"\u003e \u003cp\u003eTotal\u003c/p\u003e \u003c/th\u003e \u003c/tr\u003e \u003c/thead\u003e \u003ctbody\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eNu\u003c/p\u003e \u003cp\u003eEx\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003eNu\u003c/p\u003e \u003cp\u003eIn\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e%\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003eNu\u003c/p\u003e \u003cp\u003eEx\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003eNu\u003c/p\u003e \u003cp\u003eIn\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e \u003cp\u003e%\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c7\"\u003e \u003cp\u003eNu\u003c/p\u003e \u003cp\u003eEx\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c8\"\u003e \u003cp\u003eNu\u003c/p\u003e \u003cp\u003eIn\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c9\"\u003e \u003cp\u003e%\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c10\"\u003e \u003cp\u003eNu\u003c/p\u003e \u003cp\u003eEx\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c11\"\u003e \u003cp\u003eNu\u003c/p\u003e \u003cp\u003eIn\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c12\"\u003e \u003cp\u003e%\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c13\"\u003e \u003cp\u003eNu\u003c/p\u003e \u003cp\u003eEx\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c14\"\u003e \u003cp\u003eNu\u003c/p\u003e \u003cp\u003eIn\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c15\"\u003e \u003cp\u003e%\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e50\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e31\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e62\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e50\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003e47\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e \u003cp\u003e94\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c7\"\u003e \u003cp\u003e50\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c8\"\u003e \u003cp\u003e45\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c9\"\u003e \u003cp\u003e90\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c10\"\u003e \u003cp\u003e50\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c11\"\u003e \u003cp\u003e39\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c12\"\u003e \u003cp\u003e78\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c13\"\u003e \u003cp\u003e200\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c14\"\u003e \u003cp\u003e162\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c15\"\u003e \u003cp\u003e81\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003c/tbody\u003e \u003c/colgroup\u003e \u003ctfoot\u003e \u003ctr\u003e\u003ctd colspan=\"15\"\u003eNu.Ex: Number of examined \u003cem\u003eM. labrax\u003c/em\u003e.\u003c/td\u003e\u003c/tr\u003e \u003ctr\u003e\u003ctd colspan=\"15\"\u003eNu.In: Number of infected \u003cem\u003eM. labrax\u003c/em\u003e.\u003c/td\u003e\u003c/tr\u003e \u003ctr\u003e\u003ctd colspan=\"15\"\u003e% : Percentage of infection.\u003c/td\u003e\u003c/tr\u003e \u003c/tfoot\u003e \u003c/table\u003e\u003c/div\u003e \u003c/p\u003e \u003c/div\u003e \u003cdiv id=\"Sec13\" class=\"Section2\"\u003e \u003ch2\u003eHeavy metal accumulation by L. kroyeri and fish host:\u003c/h2\u003e \u003cp\u003eMean\u0026thinsp;\u0026plusmn;\u0026thinsp;SEM of heavy metal concentrations in gills and muscle of both infected and non-infected fish as well as in parasitic tissue are illustrated in Table\u0026nbsp;\u003cspan refid=\"Tab2\" class=\"InternalRef\"\u003e2\u003c/span\u003e, Fig.\u0026nbsp;\u003cspan refid=\"Fig5\" class=\"InternalRef\"\u003e5\u003c/span\u003e. Zinc was accumulated with higher levels in the gills (374.0\u0026thinsp;\u0026plusmn;\u0026thinsp;2.51 mg/kg) and muscles (270.5\u0026thinsp;\u0026plusmn;\u0026thinsp;3.03 mg/kg) of non-infested fish compared to the gills (275.0\u0026thinsp;\u0026plusmn;\u0026thinsp;3.11 mg/kg) and muscles (124.8\u0026thinsp;\u0026plusmn;\u0026thinsp;2.15 mg/kg) of infested fish. Surprisingly, the parasite accumulated Zn in its tissue (237.5\u0026thinsp;\u0026plusmn;\u0026thinsp;2.86 mg/kg). The differential concentration of Zn in gills, muscle, and parasitic tissue was analyzed by unpaired t-test. While the concentrations of other elements were recorded under the detection limit (UDL; \u0026lt;0.3 mg/kg for Co and Cu or \u0026lt;\u0026thinsp;0.03mg/kg for Cd).\u003c/p\u003e \u003cp\u003e \u003cdiv class=\"gridtable\"\u003e\u003ctable float=\"Yes\" id=\"Tab2\" border=\"1\"\u003e \u003ccaption language=\"En\"\u003e \u003cdiv class=\"CaptionNumber\"\u003eTable 2\u003c/div\u003e \u003cdiv class=\"CaptionContent\"\u003e \u003cp\u003eMean of heavy metals concentration in fish tissues and parasite:\u003c/p\u003e \u003c/div\u003e \u003c/caption\u003e \u003ccolgroup cols=\"6\"\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c1\" colnum=\"1\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c2\" colnum=\"2\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c3\" colnum=\"3\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c4\" colnum=\"4\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c5\" colnum=\"5\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c6\" colnum=\"6\"\u003e\u003c/div\u003e \u003cthead\u003e \u003ctr\u003e \u003cth align=\"left\" colname=\"c1\"\u003e \u003cp\u003eElement\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c2\"\u003e\u0026nbsp;\u003c/th\u003e \u003cth align=\"left\" colname=\"c3\"\u003e \u003cp\u003eOrgan\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c4\"\u003e \u003cp\u003eNon infected\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c5\"\u003e \u003cp\u003eInfected\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c6\"\u003e \u003cp\u003e\u003cem\u003ep\u003c/em\u003e. value\u003c/p\u003e \u003c/th\u003e \u003c/tr\u003e \u003c/thead\u003e \u003ctbody\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\" morerows=\"2\" rowspan=\"3\"\u003e \u003cp\u003e\u003cb\u003eZn\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\" morerows=\"1\" rowspan=\"2\"\u003e \u003cp\u003eFish\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003eGills\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e374.0\u0026thinsp;\u0026plusmn;\u0026thinsp;2.51\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003e275.0\u0026thinsp;\u0026plusmn;\u0026thinsp;3.11\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e \u003cp\u003e\u0026lt;\u0026thinsp;0.0001\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003eMuscle\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e270.5\u0026thinsp;\u0026plusmn;\u0026thinsp;3.03\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003e124.8\u0026thinsp;\u0026plusmn;\u0026thinsp;2.15\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e \u003cp\u003e\u0026lt;\u0026thinsp;0.0001\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003eParasite\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colspan=\"3\" nameend=\"c5\" namest=\"c3\"\u003e \u003cp\u003e237.5\u0026thinsp;\u0026plusmn;\u0026thinsp;2.86\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e\u0026nbsp;\u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\" morerows=\"2\" rowspan=\"3\"\u003e \u003cp\u003e\u003cb\u003eCo\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\" morerows=\"1\" rowspan=\"2\"\u003e \u003cp\u003eFish\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003eGills\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003eUDL\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003eUDL\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e \u003cp\u003e-\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003eMuscle\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003eUDL\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003eUDL\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e \u003cp\u003e-\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003eParasite\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colspan=\"3\" nameend=\"c5\" namest=\"c3\"\u003e \u003cp\u003eUDL\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e\u0026nbsp;\u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\" morerows=\"2\" rowspan=\"3\"\u003e \u003cp\u003e\u003cb\u003eCd\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\" morerows=\"1\" rowspan=\"2\"\u003e \u003cp\u003eFish\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003eGills\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003eUDL\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003eUDL\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e \u003cp\u003e-\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003eMuscle\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003eUDL\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003eUDL\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e \u003cp\u003e-\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003eParasite\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colspan=\"3\" nameend=\"c5\" namest=\"c3\"\u003e \u003cp\u003eUDL\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e\u0026nbsp;\u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\" morerows=\"2\" rowspan=\"3\"\u003e \u003cp\u003e\u003cb\u003eCu\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\" morerows=\"1\" rowspan=\"2\"\u003e \u003cp\u003eFish\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003eGills\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003eUDL\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003eUDL\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e \u003cp\u003e-\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003eMuscle\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003eUDL\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003eUDL\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e \u003cp\u003e-\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003eParasite\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colspan=\"3\" nameend=\"c5\" namest=\"c3\"\u003e \u003cp\u003eUDL\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e\u0026nbsp;\u003c/td\u003e \u003c/tr\u003e \u003c/tbody\u003e \u003c/colgroup\u003e \u003c/table\u003e\u003c/div\u003e \u003c/p\u003e \u003c/div\u003e \u003cdiv id=\"Sec14\" class=\"Section2\"\u003e \u003ch2\u003eHistopathological results:\u003c/h2\u003e \u003cp\u003eVarious sections from crustcean parasitic elements randomly distributed in gills were noticed (Fig.\u0026nbsp;\u003cspan refid=\"Fig6\" class=\"InternalRef\"\u003e6\u003c/span\u003e). The adjacent primary filaments were bent, stunted, and disorganized with the partial or complete destruction of the secondary lamellar epithelium (Fig.\u0026nbsp;\u003cspan refid=\"Fig7\" class=\"InternalRef\"\u003e7\u003c/span\u003e). Metaplasia of some surface epithelium to goblet cells was evident. Sometimes intense hemorrhage and excess mucous exudate could be seen in the vicinity of some parasites (Fig.\u0026nbsp;\u003cspan refid=\"Fig8\" class=\"InternalRef\"\u003e8\u003c/span\u003e). Moreover, complete destruction of secondary lamellar epithelium from both sides of gill filaments leaving primary filaments denuded could be seen (Fig.\u0026nbsp;\u003cspan refid=\"Fig9\" class=\"InternalRef\"\u003e9\u003c/span\u003e).\u003c/p\u003e \u003cp\u003eOther gill filaments showed compensatory hyperplasia and hypertrophy of secondary lamellar epithelium which results in their fusion (Fig.\u0026nbsp;\u003cspan refid=\"Fig10\" class=\"InternalRef\"\u003e10\u003c/span\u003e). The blood vessels of gill filaments and arches revealed telangectiasis beside edema in the surrounding tissue (Fig.\u0026nbsp;\u003cspan refid=\"Fig11\" class=\"InternalRef\"\u003e11\u003c/span\u003e). Sometimes lymphocytes and eosinophils granular cells besides melanomacrophage cells were focally scattered in gill filaments and arches, sloughing of epidermal tissue of gill arch in addition to metaplasia to mucus secretory cells were common (Fig.\u0026nbsp;\u003cspan refid=\"Fig12\" class=\"InternalRef\"\u003e12\u003c/span\u003e). The gill raker had erosion of their covering epithelium beside hyalinization and necrosis of the muscles (Fig.\u0026nbsp;\u003cspan refid=\"Fig13\" class=\"InternalRef\"\u003e13\u003c/span\u003e).\u003c/p\u003e \u003c/div\u003e"},{"header":"Discussion","content":"\u003cp\u003e\u003cem\u003eLernanthropus\u003c/em\u003e is the most common genus of parasitic copepods. There are more than 100 species described from gills of different marine fish (Toksen, \u003cspan citationid=\"CR54\" class=\"CitationRef\"\u003e2007\u003c/span\u003e). The current investigation revealed hemorrhagic areas on the body surface with excessive mucous secretion and marbling appearance of the gills of infected \u003cem\u003eM. labrax\u003c/em\u003e with \u003cem\u003eL. kroyeri\u003c/em\u003e. These lesions could be attributed to attachment of the parasites by their rigid claws, feeding activity, severe irritation caused by parasitic movement, and mucous increase as a defense mechanism from the host to overcome the infection as reported by Heba Abdel-Mawla and El-Ekiaby (2012).\u003c/p\u003e \u003cp\u003eThe present study recorded isolation of \u003cem\u003eL. kroyeri\u003c/em\u003e from gills of \u003cem\u003eM. labrax\u003c/em\u003e. Likewise, Tosken et al. (2008), Henery et al. (2009), and Essa et al. (2012) were isolated the same parasite from the same host and the same site. Meanwhile Noor El-Deen et al., (\u003cspan citationid=\"CR34\" class=\"CitationRef\"\u003e2013\u003c/span\u003e) and Dawlat Hassanin (\u003cspan citationid=\"CR5\" class=\"CitationRef\"\u003e2016\u003c/span\u003e) isolated \u003cem\u003eL. kroyeri\u003c/em\u003e from the gills of other fish species such as \u003cem\u003eMugil cephalus\u003c/em\u003e and \u003cem\u003eMoolgarda seheli\u003c/em\u003e.\u003c/p\u003e \u003cp\u003eIn the current prospective, the prevalence of \u003cem\u003eL. kroyeri\u003c/em\u003e was 81%, Concurrent with a previous study; Aneesh et al. (\u003cspan citationid=\"CR4\" class=\"CitationRef\"\u003e2014\u003c/span\u003e) recorded 81.4% infection of \u003cem\u003eStrongylura strongylura by L. kroyeri\u003c/em\u003e. Additionally, Toksen (\u003cspan citationid=\"CR54\" class=\"CitationRef\"\u003e2007\u003c/span\u003e) reported a higher infection rate (100%) by \u003cem\u003eL. kroyeri\u003c/em\u003e in \u003cem\u003eDicentrarchus labrax\u003c/em\u003e. Nevertheless, Manera and Dezfuli, (\u003cspan citationid=\"CR29\" class=\"CitationRef\"\u003e2003\u003c/span\u003e) obtained a lower infection rate (35%) with \u003cem\u003eL. kroyeri\u003c/em\u003e in \u003cem\u003eD. labrax\u003c/em\u003e. Our paper reported that \u003cem\u003eL. kroyeri\u003c/em\u003e infection was highest during Spring (94%) followed by Summer (90%) then Autumn (78%) and finally Winter (31%). This sequence is nearly in agreement with Eissa et al. (2017) who also reported that the infection rate with \u003cem\u003eL. kroyeri\u003c/em\u003e reached their maximum rate during Spring and Summer, while the lowest infection was recorded during Autumn. These results were inconsistent with Ola Abu Samak and Ashraf (\u003cspan citationid=\"CR35\" class=\"CitationRef\"\u003e2008\u003c/span\u003e) who reported that the infection rates with the same parasite reached their maximum rates in Autumn and Winter (42.5% and 35%) respectively, while their minimum value was 7.5% in Spring. These variances in the total infection and seasonal dynamics could be returned to the difference of fish species and the difference of locality of fish collection.\u003c/p\u003e \u003cp\u003eCertain fish parasites can accumulate heavy metals at concentrations significantly higher than those in host tissues or the environment (Sures, \u003cspan citationid=\"CR44\" class=\"CitationRef\"\u003e2001\u003c/span\u003e, \u003cspan citationid=\"CR45\" class=\"CitationRef\"\u003e2003\u003c/span\u003e, \u003cspan citationid=\"CR46\" class=\"CitationRef\"\u003e2004\u003c/span\u003e; Sures et al., \u003cspan citationid=\"CR47\" class=\"CitationRef\"\u003e2003\u003c/span\u003e; Schludermann et al., \u003cspan citationid=\"CR41\" class=\"CitationRef\"\u003e2003\u003c/span\u003e; Thielen et al., \u003cspan citationid=\"CR52\" class=\"CitationRef\"\u003e2004\u003c/span\u003e; Tekin-Ozan and Kir, 2005). The data of our study revealed that there was a high concentration of Zn in the collected samples. While the concentrations of Cu, Cd and Co were under detection limit. In general, the accumulation of Zn was significantly higher in the non-infested tissue in comparison to the infested tissue samples. It is opined that \u003cem\u003eL. kroyeri\u003c/em\u003e can absorb Zn from the fish tissue through its alimentary canal and accumulates it in the parasite tissue, this finding was verified by analysis of Zn in the parasite tissue. On the same manner, a recent study by Hassanine and Al-Hasawi, (\u003cspan citationid=\"CR12\" class=\"CitationRef\"\u003e2021\u003c/span\u003e) reported that acanthocephalan accumulates higher concentrations of heavy metals. Concurrent with other study, Szefer et al. (\u003cspan citationid=\"CR49\" class=\"CitationRef\"\u003e1998\u003c/span\u003e) suggested that the bioaccumulation of parasites may reflect the higher ability of host to clear heavy metals. Also, Sures and Siddall (\u003cspan citationid=\"CR43\" class=\"CitationRef\"\u003e1999\u003c/span\u003e), Taraschewski (2000) and Malek et al. (\u003cspan citationid=\"CR28\" class=\"CitationRef\"\u003e2007\u003c/span\u003e) considered the parasites beneficial and might act as a heavy metal sanitizer for the host. Gills were accumulated higher Zn value compared to the edible part of its fish host. The low ratio of Zn concentration in host muscle could be returned to the longer exposure time as metal uptake occurs faster in parasites as opined by Sures (\u003cspan citationid=\"CR44\" class=\"CitationRef\"\u003e2001\u003c/span\u003e).\u003c/p\u003e \u003cp\u003eConsidering histopathological findings, we illustrated sections of \u003cem\u003eL. kroyeri\u003c/em\u003e distributed in the gills. Similarly, a recent study by Eissa et al. (\u003cspan citationid=\"CR9\" class=\"CitationRef\"\u003e2020\u003c/span\u003e) reported occurrence of \u003cem\u003eL. kroyeri\u003c/em\u003e fragments in the gills of \u003cem\u003eD. labrax\u003c/em\u003e. Destruction of secondary lamellar epithelium, goblet cell metaplasia with hemorrhage and excess mucous secretion could be induced as a tissue reaction to decrease the irritation against the infestation. Concurrent with previous studies, Heba et al. (\u003cspan citationid=\"CR14\" class=\"CitationRef\"\u003e2015\u003c/span\u003e), Lester and Hayward (\u003cspan citationid=\"CR21\" class=\"CitationRef\"\u003e2006\u003c/span\u003e), Ragias et al. (\u003cspan citationid=\"CR38\" class=\"CitationRef\"\u003e2004\u003c/span\u003e), and Manera and Dezfuli (\u003cspan citationid=\"CR29\" class=\"CitationRef\"\u003e2003\u003c/span\u003e) reported extensive hemorrhage duo to the feeding activity of this parasite. Lymphocytes and eosinophils were found in gill filaments and arches, these outcomes were in accordance to Manera and Dezfuli (\u003cspan citationid=\"CR29\" class=\"CitationRef\"\u003e2003\u003c/span\u003e), Korun and Tepecik (\u003cspan citationid=\"CR20\" class=\"CitationRef\"\u003e2005\u003c/span\u003e), Toksen (\u003cspan citationid=\"CR54\" class=\"CitationRef\"\u003e2007\u003c/span\u003e), Jithendran et al. (\u003cspan citationid=\"CR17\" class=\"CitationRef\"\u003e2008\u003c/span\u003e), Yardimci and Pekmezci (\u003cspan citationid=\"CR58\" class=\"CitationRef\"\u003e2012\u003c/span\u003e). Also, erosion of gill raker beside necrosis of muscles were seen, likewise, Vinoth et al. (\u003cspan citationid=\"CR57\" class=\"CitationRef\"\u003e2010\u003c/span\u003e) reported pale gills induced by copepod parasites duo to loss of gill raker.\u003c/p\u003e \u003cp\u003eOur investigation concluded that, although \u003cem\u003eL. kroyeri\u003c/em\u003e has a bad effect on the infected \u003cem\u003eM. labrax\u003c/em\u003e, it also plays an important role in elimination of heavy metals from the tissue of the infected fish through its ability to accumulate heavy metals in its body; and this can be advantageous for the infected hosts, allowing them to tolerate much higher concentrations of certain metals. The present results also confirmed that \u003cem\u003eL. kroyeri\u003c/em\u003e seem to be good indicators of environmental pollutions.\u003c/p\u003e"},{"header":"Conclusion","content":"\u003cp\u003eTo date, our prospective represents a premier study to report the efficacy of \u003cem\u003eLernanthropus kroyeri\u003c/em\u003e to uptake and accumulate heavy metals (zinc). However, \u003cem\u003eL. kroyeri\u003c/em\u003e infests \u003cem\u003eM. labrax\u003c/em\u003e with a high prevalence in Spring and Summer and demonstrates excessive mucous secretion, ulceration, marbling appearance of gills, and histopathological changes in the gills and muscles of the infested fish. By detecting various heavy metals (Zn, Co, Cu, and Cd) in the tissues of \u003cem\u003eL. kroyeri\u003c/em\u003e and \u003cem\u003eM. labrax\u003c/em\u003e, surprisingly, \u003cem\u003eL. kroyeri\u003c/em\u003e has the ability to uptake the highest concentration of Zn in its tissues. Conclusively, parasitic infestation is eco-friendly method to uptake heavy metals, \u003cem\u003eL. kroyeri\u003c/em\u003e can be utilized as natural antitoxic agent as well as considered a bio-indicator for the toxicity with heavy metals, and to lessen hazardous impacts to the aquatic environment for sustaining aquaculture. Future studies are needed to test the activity of other parasites to chelate heavy metals and also on various fish species.\u003c/p\u003e"},{"header":"Declarations","content":"\u003cp\u003e\u003cstrong\u003eAuthor\u0026apos;s contributions\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eConceptualization, A.A.A., R.R.A., N.R., D.M.M., H.H.M.; Methodology, A.A.A., R.R.A., N.R., D.M.M., H.H.M.; Formal analysis, A.A.A., R.R.A., N.R., D.M.M., H.H.M.; Investigation, A.A.A., R.R.A., N.R., D.M.M., H.H.M.; Resources, A.A.A., R.R.A., N.R., D.M.M., H.H.M.; Writing-original draft preparation, A.A.A., R.R.A., N.R., D.M.M., H.H.M.; Editing, H.H.M.;\u0026nbsp;All authors have read and agreed to the published version of the manuscript.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eConflict of interest\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eThe authors claim that there is no conflict of interest.\u0026nbsp;\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eData availability\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eAll data are available in this manuscript and the supplementary file.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eEthical approval\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eThis research was reviewed and approved by the Animal Care and Welfare Committee of\u0026nbsp;Animal health Research Institute (AHRI), Giza\u003cstrong\u003e,\u003c/strong\u003e Egypt.\u003c/p\u003e\n\n\u003cp\u003e\u003cstrong\u003eConsent to participate\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eNot applicable.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eConsent to publish\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eNot applicable.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eFunding\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eNot applicable.\u003c/p\u003e"},{"header":"References","content":"\u003col\u003e\u003cli\u003e\u003cspan\u003eAbiona OO, Anifowoe AJ, Awojide SH, Adebisi OC, Adesina BT, Ipinmoroti MO (2019) Histopathological biomarking changes in the internal organs of Tilapia (\u003cem\u003eOreochromis niloticus\u003c/em\u003e) and catfish (\u003cem\u003eClarias gariepinus\u003c/em\u003e) exposed to heavy metals contamination from Dandaru pond, Ibadan. 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Vet Fak Derg 59:61\u0026ndash;64\u003c/span\u003e\u003c/li\u003e\u003c/ol\u003e"}],"fulltextSource":"","fullText":"","funders":[],"hasAdminPriorityOnWorkflow":false,"hasManuscriptDocX":true,"hasOptedInToPreprint":true,"hasPassedJournalQc":"","hasAnyPriority":false,"hideJournal":true,"highlight":"","institution":"","isAcceptedByJournal":false,"isAuthorSuppliedPdf":false,"isDeskRejected":"","isHiddenFromSearch":false,"isInQc":false,"isInWorkflow":false,"isPdf":false,"isPdfUpToDate":true,"isWithdrawnOrRetracted":false,"journal":{"display":true,"email":"[email protected]","identity":"researchsquare","isNatureJournal":false,"hasQc":true,"allowDirectSubmit":true,"externalIdentity":"","sideBox":"","snPcode":"","submissionUrl":"/submission","title":"Research Square","twitterHandle":"researchsquare","acdcEnabled":true,"dfaEnabled":false,"editorialSystem":"","reportingPortfolio":"","inReviewEnabled":false,"inReviewRevisionsEnabled":true},"keywords":"Moron labra, Lernanthropus parasite, Histopathology, Heavy metals residues, Electron microscope.","lastPublishedDoi":"10.21203/rs.3.rs-1435215/v1","lastPublishedDoiUrl":"https://doi.org/10.21203/rs.3.rs-1435215/v1","license":{"name":"CC BY 4.0","url":"https://creativecommons.org/licenses/by/4.0/"},"manuscriptAbstract":"\u003cp\u003eThe present context is the pioneer attempt to verify the ability of copepod, \u003cem\u003eLernanthropus kroyeri, L. kroyeri\u003c/em\u003e, to uptake and accumulate heavy metals. We primarily assess the prevalence of the parasite in various seasons, clinical signs, and post-mortem changes in sea bass \u003cem\u003e(Moron labrax)\u003c/em\u003e. Morphological features of the parasite using a light microscope, bioaccumulation of heavy metals in tissues of both \u003cem\u003eL. kroyeri\u003c/em\u003e and \u003cem\u003eM. labrax\u003c/em\u003e (gills, muscles) using Flame Atomic Absorption Spectrometry, and histopathological alterations were monitored. Fish (n\u0026thinsp;=\u0026thinsp;200) were obtained from Ezbet Elborg and examined for the parasite, \u003cem\u003eL. kroyeri\u003c/em\u003e. Results revealed that the total infection recorded 86%. The infested fish exhibited excessive mucous and ulceration at the site of attachment. The post-mortem lesion in gills was marbling appearance with destructed filaments. Various heavy metals (Zn, Co, Cu, and Cd) were detected in the tissues of \u003cem\u003eL. kroyeri\u003c/em\u003e and \u003cem\u003eM. labrax\u003c/em\u003e and surprisingly, \u003cem\u003eL. kroyeri\u003c/em\u003e had the ability to uptake and accumulate a high amount of Zn in its tissues. Infested fish accumulated less concentration of Zn in their tissue compared to the non-infested ones. Within the host tissue, the accumulation of Zn was higher in gills compared to muscles. Histopathological findings demonstrated scattered parasitic elements with destruction of gill lamellae. Taken together, we clearly highlight the potential role of \u003cem\u003eL. kroyeri\u003c/em\u003e to eliminate Zn and it can be utilized as a bio-indicator for metal monitoring studies for sustaining aquaculture.\u003c/p\u003e","manuscriptTitle":"Prevalence, Morpho-Histopathological Identification, Clinical Picture, and the Role of Lernanthropus kroyeri to Alleviate the Zinc Toxicity in Moron labrax","msid":"","msnumber":"","nonDraftVersions":[{"code":1,"date":"2022-07-06 17:10:40","doi":"10.21203/rs.3.rs-1435215/v1","editorialEvents":[{"type":"communityComments","content":0}],"status":"published","journal":{"display":true,"email":"[email protected]","identity":"researchsquare","isNatureJournal":false,"hasQc":true,"allowDirectSubmit":true,"externalIdentity":"","sideBox":"","snPcode":"","submissionUrl":"/submission","title":"Research Square","twitterHandle":"researchsquare","acdcEnabled":true,"dfaEnabled":false,"editorialSystem":"","reportingPortfolio":"","inReviewEnabled":false,"inReviewRevisionsEnabled":true}}],"origin":"","ownerIdentity":"25f5e4da-18c3-4c9a-9e06-2a2d18b12d0c","owner":[],"postedDate":"July 6th, 2022","published":true,"recentEditorialEvents":[],"rejectedJournal":[],"revision":"","amendment":"","status":"posted","subjectAreas":[],"tags":[],"updatedAt":"2022-09-09T14:22:08+00:00","versionOfRecord":[],"versionCreatedAt":"2022-07-06 17:10:40","video":"","vorDoi":"","vorDoiUrl":"","workflowStages":[]},"version":"v1","identity":"rs-1435215","journalConfig":"researchsquare"},"__N_SSP":true},"page":"/article/[identity]/[[...version]]","query":{"redirect":"/article/rs-1435215","identity":"rs-1435215","version":["v1"]},"buildId":"WrCJVZZCHTDjtuVLN7oU0","isFallback":false,"isExperimentalCompile":false,"dynamicIds":[84888],"gssp":true,"scriptLoader":[]}